Michael Tsabar1, Vinay V Eapen1, Jennifer M Mason2, Gonen Memisoglu1, David P Waterman1, Marcus J Long1, Douglas K Bishop2, James E Haber3. 1. Department of Biology and Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, MA 02454, USA. 2. Department of Radiation and Cellular Oncology and Department of Molecular Genetics and Cell Biology, University of Chicago, Chicago, IL 60637, USA. 3. Department of Biology and Rosenstiel Basic Medical Sciences Research Center, Brandeis University, Waltham, MA 02454, USA haber@brandeis.edu.
Abstract
In response to chromosomal double-strand breaks (DSBs), eukaryotic cells activate the DNA damage checkpoint, which is orchestrated by the PI3 kinase-like protein kinases ATR and ATM (Mec1 and Tel1 in budding yeast). Following DSB formation, Mec1 and Tel1 phosphorylate histone H2A on serine 129 (known as γ-H2AX). We used caffeine to inhibit the checkpoint kinases after DSB induction. We show that prolonged phosphorylation of H2A-S129 does not require continuous Mec1 and Tel1 activity. Unexpectedly, caffeine treatment impaired homologous recombination by inhibiting 5' to 3' end resection, independent of Mec1 and Tel1 inhibition. Caffeine treatment led to the rapid loss, by proteasomal degradation, of both Sae2, a nuclease that plays a role in early steps of resection, and Dna2, a nuclease that facilitates one of two extensive resection pathways. Sae2's instability is evident in the absence of DNA damage. A similar loss is seen when protein synthesis is inhibited by cycloheximide. Caffeine treatment had similar effects on irradiated HeLa cells, blocking the formation of RPA and Rad51 foci that depend on 5' to 3' resection of broken chromosome ends. Our findings provide insight toward the use of caffeine as a DNA damage-sensitizing agent in cancer cells.
In response to chromosomal double-strand breaks (DSBs), eukaryotic cells activate the DNA damage checkpoint, which is orchestrated by the PI3 kinase-like protein kinases ATR and ATM (Mec1 and Tel1 in budding yeast). Following DSB formation, Mec1 and Tel1 phosphorylate histone H2A on serine 129 (known as γ-H2AX). We used caffeine to inhibit the checkpoint kinases after DSB induction. We show that prolonged phosphorylation of H2A-S129 does not require continuous Mec1 and Tel1 activity. Unexpectedly, caffeine treatment impaired homologous recombination by inhibiting 5' to 3' end resection, independent of Mec1 and Tel1 inhibition. Caffeine treatment led to the rapid loss, by proteasomal degradation, of both Sae2, a nuclease that plays a role in early steps of resection, and Dna2, a nuclease that facilitates one of two extensive resection pathways. Sae2's instability is evident in the absence of DNA damage. A similar loss is seen when protein synthesis is inhibited by cycloheximide. Caffeine treatment had similar effects on irradiated HeLa cells, blocking the formation of RPA and Rad51 foci that depend on 5' to 3' resection of broken chromosome ends. Our findings provide insight toward the use of caffeine as a DNA damage-sensitizing agent in cancer cells.
DNA double strand breaks (DSBs) are highly deleterious events that may lead to chromosomal abnormalities, cell death and cancer. Repair of chromosome breaks occurs by several highly conserved pathways. G1 cells predominantly repair DSBs by re-joining the broken ends through nonhomologous end-joining (NHEJ) pathways (1,2). After the cells pass ‘start’ on their way to initiate S phase, the main pathway of repair shifts to homologous recombination (HR) (2–4). An initial and essential step in HR is the 5′ to 3′ resection of the dsDNA at the DSB end, which leaves 3′ single-stranded DNA (ssDNA) tails. Both in vivo and in vitro evidence suggests that resection is initiated by the Mre11-Rad50-Xrs2 complex (MRX) together with Sae2, the budding yeast homolog of CtIP (5–8). Recently, Sae2 has been shown in vitro to facilitate 5′ to 3′ resection by promoting the endonuclease activity of Mre11 (9), although Sae2 itself has been suggested to have nuclease activity (10). More extensive resection depends on two separate nuclease activities, one involving Exo1 and another involving a complex containing Dna2, Sgs1, Top3 and Rmi1 (6,7,11,12). The ssDNA tail created by resection is first coated by replication protein A (RPA) that interacts with Rad52 to facilitate the formation of a filament of the Rad51 recombination protein (13–15). The Rad51 filament catalyzes a search throughout the genome for sequences homologous to the ssDNA within the filament and promotes strand invasion between the ssDNA and homologous double-stranded DNA (dsDNA). Strand invasion is followed by the initiation of DNA synthesis from the 3′ end of the invading strand and eventual repair of the DSB (16,17). When the DSB occurs in sequences that share homology on both ends of the break with a template sequence (a sister chromatid, a homologous chromosome or an ectopic donor) repair occurs by gene conversion (GC). If only one end of the DSB is capable of pairing with homologous sequences, repair proceeds by a recombination-dependent process termed break-induced replication (BIR) (18,19). Repair can also occur in a Rad51-independent fashion by single-strand annealing (SSA) when there are homologous sequences flanking a DSB (20).In order to allow sufficient time for repair, and to prevent mitosis in the presence of a broken chromosome, cells activate the DNA damage checkpoint. Two checkpoint PI3 kinase-like protein kinases, ATM and ATR (Tel1 and Mec1 in yeast, respectively), are recruited to the DSB and phosphorylate a cascade of downstream effectors that, in turn, prevent the cells from dividing until the damage is repaired (21–24). In budding yeast, the scaffolding protein Rad9 is recruited to the DSB, where it is phosphorylated by Mec1 (24). Rad9 then mediates the autophosphorylation of Rad53 (Chk2) and Chk1 (22,25). Rad53 phosphorylates and inhibits Cdc20, an activator of the anaphase-promoting complex. This inhibition, along with activation of Chk1, stabilizes Pds1 (securin) and prevents mitosis (22,26). After repair is complete, the DNA damage checkpoint is turned off to allow the cells to resume cell cycle progression, a process termed recovery. If the damage cannot be repaired, the cells can eventually turn off the checkpoint by a process termed adaptation (27,28).Another target of Mec1 and Tel1 kinase activity is serine 129 of histone H2A. This modification, termed γ-H2AX, is evolutionarily conserved; ATM and ATR rapidly phosphorylate mammalianH2AX-S139 in response to DNA damage (29–32). The modification spreads as far as 100 kb around the DSB in yeast cells, and 1 Mb around a DSB in mammalian cells, and serves to recruit repair factors to the vicinity of the DSB (29,31,33). Cells that lack the ability to phosphorylate H2A-S129 (H2A-S129A) adapt faster than WT cells, suggesting this modification plays a role in determining the length of arrest (34,35). Surprisingly, cells expressing histone H2A-S129A have a rate of 5′ to 3′ resection of the DSB ends greater than that in WT cells (6.8 kb/h versus 4 kb/h), which implies that having more ssDNA or more resection byproducts does not, in and of itself, signal for checkpoint maintenance (36,37). γ-H2AX in yeast is rapidly removed from chromatin after repair by a yet unknown factor and then dephosphorylated by the PP4 phosphatase complex (38).Here we asked if Mec1 and Tel1 are constitutively required to maintain γ-H2AX after its formation. We used caffeine to inhibit Mec1 and Tel1 after the formation of γ-H2AX. Caffeine acts as a PI3K inhibitor and has been shown to inhibit ATM and ATR in mammalian cells, Schizosacchromyces pombe and Saccharomyces cerevisiae (39–45). We find that γ-H2AX is retained around a DSB after caffeine treatment indicating that the modification is stable, and does not depend on continuous Mec1/Tel1 activity.In mammalian cells, the tumor suppressor p53 becomes active following DNA damage in the G1 phase, and maintains a robust G1 checkpoint (46). In contrast, the S phase and G2/M checkpoints are completely dependent on ATM and ATR, and do not require p53 (46). Indeed, caffeine treatment was shown to sensitize p53-deficient tumor cells to ionizing irradiation. This effect was hypothesized to occur due to the caffeine-mediated inhibition of the G2/M checkpoint (47–49). However, caffeine could not further radiosensitize both mammalian and DT-40 cells that are deficient for HR, suggesting that the mechanism of sensitization involves inhibition of HR rather than checkpoint control (50–52). A recent study showed that caffeine treatment interferes with mammalianRad51-mediated joint molecule formation in vitro as well as gene targeting in vivo (53). Here we show that caffeine treatment impairs resection in budding yeast and HeLa cells. We show in budding yeast that inhibition of homologous recombination occurs independently of inhibition of the DNA damage checkpoint, by interfering with the first step in repair: resection of the DSB ends. The impairment of resection correlates with a reduction in the abundance of both Sae2 and Dna2 following caffeine treatment. We show that both nucleases are targeted for proteasomal degradation. In particular, we show that Sae2 is an unstable protein, as it is degraded rapidly following caffeine or cycloheximide (CHX) treatment even in the absence of DNA damage. Taken together, these data suggest that caffeine treatment targets one of the earliest steps in HR, independent of its inhibition of ATM/ATR.
MATERIALS AND METHODS
Yeast strains and plasmids
All yeast strains used in this study are described in Table 1. Deletions of open reading frames (ORFs) were carried out using single-step-PCR-mediated transformation of yeast colonies (54) or introduced by genetic crosses. Primer sequences are available on request.
Chromatin immunoprecipitation (ChIP) was carried out as described in (29). α-γH2AX purchased from Abcam (15083).
Western blotting
Western blotting in S. cerevisiae was carried out using the trichloroacetic acid (TCA) protocol described by Pellicioli et al. (55). α-Rho1 antibody was a generous gift from Satoshi Yoshida (Brandeis, MA, USA). α-GFP (ab290), α-CMyc (ab32) and α-PGK1 (ab113687) antibodies were obtained from Abcam. α-V5 antibody was obtained from Life Technologies. HeLa cells were harvested in lysis buffer containing 1% NP-40, 0.1% SDS, 0.5% sodium-deoxycholate, 1× protease inhibitor cocktail (Roche). Western blotting was performed using antibodies against humanCTIP (kind gift of Richard Baer) and α-Tubulin (Ab-2; Fitzgerald). Signal intensity was measured in Image J. CTIP levels were determined by normalizing signal to Tubulin signal intensity.
qPCR resection assay
qPCR resection assay was carried out as previously described (36). In short, qPCR was used to detect product at varying distances from the DSB. The signal was then normalized to qPCR signal at an uninvolved site (either PHO5 or ARG5,6) and to the signal present before a DSB was induced (0 h). Resection rates were calculated by examining each curve on the plot of distance versus PCR signal and determining the time and distance when the PCR value reached 0.75 (calculated by interpolating between the nearest data points).
Southern blotting
Southern blot analysis was performed as previously described (36). Genomic DNA was purified and digested with the appropriate restriction enzyme (PvuI for YML002, EcoRI for all other Southerns). YML002 probe detected the homologous sequences. All other strains were probed with an MAT distal probe (56). For tGI354 derivatives, the donor signal served as a loading control. Bands were normalized to the loading control and then to the 0 h. JKM179 was cut with StyI prior to hybridization with the MAT distal probe, after which the membrane was stripped and reprobed with ACT1 probe as a loading control.
Mammalian cell culture conditions
HeLa cells were grown in DMEM media (Invitrogen) supplemented with 10% fetal bovine serum, and 1× penicillin/streptomycin (Invitrogen). Cells were cultured at 37°C with 5% CO2.
Immunofluorescence
HeLa cells (1.0 × 105) were plated in 6-well dishes (Corning) containing a 22 × 22 glass coverslip (Fisherbrand) and allowed to adhere overnight. For Rad51 and RPA focus formation, caffeine was added at the indicated doses 1 h prior to irradiation with 6 Gy using a Maxitron generator and allowed to recover for 4 h prior to fixation. Cytosolic proteins were pre-extracted with HEPES/TritonX-100 buffer (20 mM HEPES pH 7.4, 0.5% Triton X-100, 50 mM NaCL, 3 mM MgCl2, 300 mM sucrose in ddH2O) at room temperature for 10 min. Cells were subsequently fixed with 3% paraformaledhyde, 3.4% sucrose in PBS for 10 min at room temperature. Cells were blocked in 1% BSA in PBS for 15 min and stained with humanRAD51 serum (kind gift from Akira Shinohara, Dilution 1:1500) and RPA antibodies (Calbiochem (NA18), Dilution 1:2000) overnight at 4°C. Cells were washed with PBS and stained with Alexa Fluor conjugated secondary antibodies (Invitrogen, Dilution 1:1000) for 1 h at room temperature. Cells were washed with PBS and allowed to air dry. Coverslips were mounted on slides with vectashield containing 4’,6-diamidino-2-phenylindole (DAPI). To image cells, 1 micron sections were acquired on a scanning laser confocal microscope (LSM510, Zeiss) using LSM software. Images were acquired with a 60× objective. Z stacks were compressed into a single image and analyzed using ImageJ software (NIH). The number of RAD51 and RPA foci in at least 75 random nuclei from three independent experiments were counted. Statistical significance was determined using the Wilcoxon rank sum test.
RESULTS
Loss of γ-H2AX after DSB repair occurs in a locus-autonomous fashion
In yeast, histone H2A is phosphorylated by Mec1 and Tel1 in response to DNA damage (29). Following repair, γ-H2AX is removed from the surrounding DNA and then dephosphorylated by the phosphatase Pph3 (38). When the damage cannot be repaired, γ-H2AX is maintained around the DSB, apparently signaling the persistence of damage (40). We first asked if γ-H2AX is removed from the chromatin surrounding a repairable DSB even when an irreparable DSB is present in the same nucleus.To address this question, we designed a system that contains two HO endonuclease recognition sites and a galactose-inducible HO endonuclease gene (34). The recognition site on chromosome 3 (Chr 3) is flanked on each side by identical copies of a 1-kb DNA sequence in the same orientation. Addition of galactose to the media induces HO expression and leads to formation of a DSB that is repaired by single strand annealing (SSA), creating a deletion of one of the two copies of the duplicated sequence and intervening sequences (Figure 1A). An additional HO cleavage site was introduced at the left arm of Chr 6. This cut site does not share homology elsewhere in the genome and thus is irreparable by HR (34). This strain also carries deletions of the HO cleavage site at the MAT locus as well as its two homologous donor sequences HML and HMR. We analyzed γ-H2AX by chromatin immunoprecipitation (ChIP) as described in Materials and Methods (Figure 1B). Repair was assayed by Southern blot hybridization (Figure 1D). γ-H2AX peaks 1–2 h following induction of both DSBs and spreads more than 30 kb on either side of the break. Phosphorylation at the irreparable DSB persists throughout the experiment (Figure 1B), but phosphorylation around the repairable DSB is removed following repair (Figure 1C). Thus, the removal of γ-H2AX is not a global event, but is triggered by the state of repair of each individual damage site.
Figure 1.
γH2AX is stable following caffeine treatment. (A) Schematic of YML002 strain. In a strain lacking MAT, HML and HMR, an irreparable DSB is induced on Chr 6, and a second DSB surrounded by flanking homologies is created on Chr 3. Repair by SSA leads to loss of the centromere. Arrows indicate PvuI restriction sites. (B) ChIP signal for γ-H2AX 30 kb from the irreparable DSB. Fifty micromolar caffeine added to the culture 2 h following HO induction (black). Dashed line marks the time of caffeine addition. (C) ChIP signal for γ-H2AX 22 kb from repairable DSB (bottom graph). Fifty micromolar caffeine added to the culture 2 h following HO induction (black). Dashed line marks the time of caffeine addition. (D) Repair of the SSA event on Chr 3 without treatment and when 50 mM caffeine is added 0.5 h after HO induction.
γH2AX is stable following caffeine treatment. (A) Schematic of YML002 strain. In a strain lacking MAT, HML and HMR, an irreparable DSB is induced on Chr 6, and a second DSB surrounded by flanking homologies is created on Chr 3. Repair by SSA leads to loss of the centromere. Arrows indicate PvuI restriction sites. (B) ChIP signal for γ-H2AX 30 kb from the irreparable DSB. Fifty micromolar caffeine added to the culture 2 h following HO induction (black). Dashed line marks the time of caffeine addition. (C) ChIP signal for γ-H2AX 22 kb from repairable DSB (bottom graph). Fifty micromolar caffeine added to the culture 2 h following HO induction (black). Dashed line marks the time of caffeine addition. (D) Repair of the SSA event on Chr 3 without treatment and when 50 mM caffeine is added 0.5 h after HO induction.
Prolonged phosphorylation of H2AX does not require continuous Mec1 and Tel1 activity
In the presence of persistent damage, γ-H2AX spreads in a Mec1-dependent manner to further distance along the broken chromosome as resection proceeds over many hours (40). Active transcription leads to removal of γ-H2AX from transcribed regions, but after transcription is shut off γ-H2AX is rapidly re-established in a Mec1-dependent fashion (57). Both of these observations indicate that Mec1 is active and able to phosphorylate histone H2A long after a DSB has occurred. It is not yet known, however, if the kinases are continuously required to maintain γ-H2AX after damage.To address this question, we added 50 mM caffeine to inhibit Mec1 and Tel1 2 h after HO induction and γ-H2AX establishment. Previous studies have shown that caffeine at this concentration can efficiently inhibit the DNA damage checkpoint and prevent DNA damage induced γ-H2AX enrichment (39,40). If Mec1 and Tel1 are continuously required for the phosphorylation of H2AX around the break, the inhibition of these two kinases should cause a decrease in phosphorylation around the irreparable break. Caffeine treatment 2 h after HO induction did not result in a significant decrease in γ-H2AX signal at a distance 30 kb from the DSB site at later time points and phosphorylation persisted for at least 5 h (Figure 1B). In the untreated cells, γ-H2AX signal continued to increase until 3 h. This result indicates that caffeine treatment is effective in preventing additional phosphorylation. Inhibition of Mec1 and Tel1 by caffeine led to a slight reduction in γ-H2AX signal but this signal remains more than 30-fold higher than 0 h. Thus maintenance of γ-H2AX around an unrepaired DSB does not require continuous ATM/ATR activity.Surprisingly, γ-H2AX around the repairable DSB also persisted up to 5 h in the presence of caffeine (Figure 1C). This observation raised the possibility that caffeine treatment prevents SSA-dependent repair of the break.
Caffeine treatment inhibits single-strand annealing by impairing resection
To see if caffeine treatment affects repair, we monitored the kinetics of repair of the SSA event in the strain described above by a Southern blot (Figure 1D). Samples were taken at intervals after HO induction, with or without caffeine treatment. In the untreated cells, repair product appeared 1 h after HO induction, and by 5 h the bands representing the original two flanking sequences were lost and only the product band was present, indicating complete repair. When the cells were treated with 50 mM caffeine 30 min after HO induction, repair was completely inhibited. We then tested if lower concentration of caffeine treatment with 10 and 20 mM caffeine 30 min after HO induction also led to a notable reduction in product appearance 5 h after HO induction (Supplementary Figure S1A and S1B). Repair was strongly inhibited by 20 mM treatment and delayed with addition of 10 mM. Notably, caffeine treatment led to the persistence of the 5 kb cut fragment formed after formation of the DSB at all concentrations (Figure 1D and Supplementary Figure S1A). In the untreated cells, this band appeared after DSB formation and disappeared in a resection-dependent manner (11). These observations suggest that caffeine treatment impairs resection.To examine resection more directly, we used strain JKM179 in which an HO-induced DSB at the MAT locus cannot be repaired because both HMLα and HMRa donors have been deleted. We monitored the persistence of the 700 bp StyI fragment created by HO cleavage at MAT. Treatment of cells with 50 mM caffeine 30 min after HO induction had no significant effect on resection of the region immediately adjacent to the DSB (Supplementary Figure S1C and S1D). Moreover, repair by NHEJ, a repair pathway that competes with HR and is preferred when the DSB ends are not resected (3,58), was not elevated following caffeine treatment compared to untreated cells (Supplementary Figure S1E) suggesting that the ends of the DSB are resected sufficiently to interfere with this pathway.In the donorless strain described above, resection can be monitored by a quantitative PCR (qPCR) assay described previously (36). Resection depends on Cdk1 activation and is inhibited in G1-arrested cells (3,4). Because caffeine might impair resection by allowing cells to evade the DNA damage checkpoint and progress to the next G1, we arrested the cells in the G2/M phase of the cell cycle by adding nocodazole 3 h prior to HO induction. At that point, 95% of the cells were at the dumbbell stage characteristic of G2/M arrest. In untreated cells, the resection rate was 4.2 kb/h (Figure 2A and C), which is comparable to the previously published rate of 4 kb/h (36) determined by this method. Fifty micromolar caffeine treatment of nocodazole-arrested cells slowed down resection to 2.4 kb/h (Figure 2A and C). This effect was seen even in lower concentrations of caffeine (10 and 20 mM) although the rate of resection measured at lower concentrations was slightly higher than that seen at 50 mM caffeine (2.7 kb/h at 10 and 20 mM) (Figure 2A and C). Thus, although resection very close to the DSB does not seem to be affected, resection is indeed significantly impaired further from the DSB. This result indicates that caffeine impairs resection directly, rather than by allowing the cells to progress through the cell cycle.
Figure 2.
Caffeine treatment impairs resection independent of Mec1 and Tel1. Cells were arrested in G2/M by nocodazole treatment 3 h prior to HO induction. (A) Resection in strain JKM179 without caffeine treatment (diamonds), or when 10 mM caffeine (squares), 20 mM caffeine (triangles) or 50 mM caffeine (crosses) was added 0.5 h after HO induction. Error bars represent ranges. (B) Resection in JKM179 mec1Δ tel1Δ sml1Δ without caffeine treatment (gray) and when 50 mM caffeine was added 0.5 h after HO induction (black) at different times after HO induction. (C) Rates were calculated by determining the time and distance when the PCR signal fell to 75% of signal at 0 h (36). These values were plotted on time-versus-distance graphs, and the rates were determined by linear regression analysis. Left graph represents resection measurements seen in (A) error bars represent the range. Right graph represents resection measurements seen in (B).
Caffeine treatment impairs resection independent of Mec1 and Tel1. Cells were arrested in G2/M by nocodazole treatment 3 h prior to HO induction. (A) Resection in strain JKM179 without caffeine treatment (diamonds), or when 10 mM caffeine (squares), 20 mM caffeine (triangles) or 50 mM caffeine (crosses) was added 0.5 h after HO induction. Error bars represent ranges. (B) Resection in JKM179 mec1Δ tel1Δ sml1Δ without caffeine treatment (gray) and when 50 mM caffeine was added 0.5 h after HO induction (black) at different times after HO induction. (C) Rates were calculated by determining the time and distance when the PCR signal fell to 75% of signal at 0 h (36). These values were plotted on time-versus-distance graphs, and the rates were determined by linear regression analysis. Left graph represents resection measurements seen in (A) error bars represent the range. Right graph represents resection measurements seen in (B).Next we monitored resection in a mec1Δ tel1Δ sml1Δ donorless strain to see if caffeine impairs resection by inhibiting Mec1 and Tel1. The deletion of SML1 is required to allow viability in the absence of MEC1. In meiosis Mec1 and Tel1-dependent phosphorylation is required for Sae2's function (59); this modification might be important for resection; however in mitosis deletion of MEC1 leads to accelerated resection (60). To allow cells to remain in G2/M following damage, we arrested cells in nocodazole 3 h prior to HO induction. The resection rate in a mec1Δ tel1Δ sml1Δ donorless strain was higher than WT (5.8 kb/h) (Figure 2B and C), most likely due to the inability of these cells to phosphorylate histone H2A (36,37,60). Fifty micromolar caffeine treatment in this mec1Δ tel1Δ sml1Δ strain also impaired resection (2.7 kb/h). We conclude that caffeine slows down resection independently of checkpoint kinase inhibition.
Caffeine treatment leads to degradation of resection enzymes
Caffeine could impair resection by directly blocking the function of resection enzymes or by inhibiting their post-translational modifications, or by an indirect mechanism such as inhibition of protein synthesis. Cdk1-dependent phosphorylation of Dna2 and Sae2 has been shown to be important for resection (61–63), whereas both Mre11 and Exo1 have been shown to be phosphorylated by the checkpoint kinases (63,64). Moreover, a recent study showed that treatment of yeast with the TORC1 inhibitor rapamycin or the histone deacetylase inhibitor valproic acid (VPA) led to the degradation of Sae2 and Exo1 (65).We assayed the abundance of the resection enzymes using western blots. We first arrested cells with nocodazole prior to HO induction and treated the cells with 20 mM caffeine 30 min after HO induction of an irreparable DSB. 20 mM caffeine was used as this concentration showed a more severe repair phenotype by SSA than 10 mM (Supplementary Figure S1A and S1B). Similar to VPA treatment, treatment with 20 mM caffeine markedly reduced Sae2 levels ≥ 3 h after formation of a DSB (Figure 3A and Supplementary Figures S2A and S3A). Sae2 levels were reduced 3-fold compared to the level prior to HO induction and 6-fold compared to untreated cells (Figure 3A and Supplementary Figure S3A).
Figure 3.
Caffeine treatment leads to degradation of resection enzymes. (A) Caffeine leads to degradation of Sae2. WT cells (left six lanes) and atg1Δ (right six lanes) were arrested in nocodazole prior to HO induction, and treated with 20 mM caffeine 0.5 h following HO induction. (B) Caffeine leads to degradation of Dna2. Cells were arrested in nocodazole prior to HO induction, and treated with 20 mM caffeine 0.5 h following HO induction. (C) Deletion of ATG1 does not prevent Dna2 degradation after caffeine treatment. Twenty micromolar caffeine was added to the media 0.5 h after HO induction in atg1Δ cells. (D) Caffeine treatment induces autophagy. A GFP band released from GFP-Atg8 appears 2 h after 10 mM caffeine addition.
Caffeine treatment leads to degradation of resection enzymes. (A) Caffeine leads to degradation of Sae2. WT cells (left six lanes) and atg1Δ (right six lanes) were arrested in nocodazole prior to HO induction, and treated with 20 mM caffeine 0.5 h following HO induction. (B) Caffeine leads to degradation of Dna2. Cells were arrested in nocodazole prior to HO induction, and treated with 20 mM caffeine 0.5 h following HO induction. (C) Deletion of ATG1 does not prevent Dna2 degradation after caffeine treatment. Twenty micromolar caffeine was added to the media 0.5 h after HO induction in atg1Δ cells. (D) Caffeine treatment induces autophagy. A GFP band released from GFP-Atg8 appears 2 h after 10 mM caffeine addition.Phosphorylation of Dna2 by Cdk1 is required for its recruitment to the DSB and subsequent Mec1-dependent phosphorylation (61). Dna2 appears as two bands at 0 h in G2/M arrested cells, the upper band most likely due to the Cdk1 phosphorylation. After DSB formation Dna2 increases in abundance and appears to migrate higher on the gel, probably a result of Mec1-dependent phosphorylation (Figure 3B). Caffeine treatment 0.5 h after DSB formation also reduced Dna2 levels 5-fold compared to untreated cells when compared 4 h after DSB induction (Figure 3B and Supplementary Figure S3C). After caffeine treatment the higher mobility band disappeared, while the lower, presumably unphosphorylated, band persisted, albeit at lower levels than prior to DSB formation (Figure 3B).Unlike VPA treatment (65), caffeine treatment did not significantly alter the abundance of Exo1 (Supplementary Figure S2C). Mre11 levels were slightly reduced following caffeine treatment compared to untreated samples (Supplementary Figure S2A), but remained at the levels detected at G2/M. Levels of Fun30, a chromatin remodeler recently shown to promote resection (36,37), were not affected by either caffeine or VPA treatments (Supplementary Figure S2B).Both VPA and rapamycin have been suggested to cause Sae2 degradation by induction of autophagy (65), and VPA was also shown to decrease the rate of resection of DSB ends. Because rapamycin treatment induces autophagy through inhibition of TORC1 signaling, and caffeine is also a TORC1 inhibitor (66), we hypothesized that caffeine treatment might induce autophagy in yeast, thereby impairing resection. We note that caffeine has been shown to stimulate autophagy in mammalian cells and in the yeastZygosaccharomyces bailii (66–69).A commonly used technique for monitoring autophagy is the cleavage of GFP-Atg8 by vacuolar proteases (70). After the induction of autophagy, the ubiquitin-like protein Atg8 is lipidated and incorporated into autophagosomes. Subsequently, Atg8-containing autophagosomes are transported to the vacuole, where Atg8 is degraded. Tagging Atg8 at the N-terminus with GFP allows monitoring this process by western blotting or fluorescence microscopy. Although GFP-Atg8 is degraded in the vacuole by proteases, the relative resistance of GFP to proteolytic cleavage results in the appearance of a free GFP band upon autophagy induction (70). Treatment of cells with 10 mM caffeine led to the appearance of a free GFP band 1 h after caffeine treatment (Figure 3D). This result is comparable to other autophagy-inducing agents such as rapamycin (71) and VPA (65) and demonstrates that caffeine induces autophagy in S. cerevisiae.Sae2 and Dna2 protein levels were markedly lower after treatment with caffeine. Because deletion of ATG1, a protein kinase required for autophagy (72), was reported to partially rescue of Sae2 degradation after VPA treatment (65), we hypothesized that the same might be true for caffeine. However, caffeine treatment resulted in loss of Sae2 even in atg1Δ cells (Figure 3A and Supplementary Figure S3B). Likewise, treatment of atg1Δ cells with rapamycin resulted in loss of Sae2 (Supplementary Figure S4A). Because deletion of Atg1 did not rescue Sae2 from degradation following either rapamycin or caffeine treatments, we attempted to replicate the rescue of Sae2 following VPA treatment (65). In contrast to the reported result in Roberts et al., we find the deletion of ATG1 failed to rescue Sae2 from VPA-mediated degradation (Supplementary Figure S4B).We also investigated the localization of Sae2 by integrating a C-terminal mCherry tag at the endogenous SAE2 gene. Sae2 is predominantly nuclear localized (Supplementary Figure S4C). As an alternative way to induce autophagy in cells with HO-induced DNA damage, we overexpressed a dominant-active form of the autophagy protein Atg13 (Atg13–8SA), which induces autophagy independently of TORC1 inhibition and without impairing the cell cycle (73). Induction of autophagy has been shown to cause cytoplasmic mislocalization of the nuclear protein Pds1 (74); however, even in cells where Atg13–8SA is overexpressed, Sae2 remains localized to the nucleus and its fluorescence intensity is unchanged (Supplementary Figure S4C). Taken together, these results show that the instability of Sae2 is not predominantly dependent on autophagy.Deletion of ATG1 also failed to prevent the degradation of Dna2 following caffeine treatment, as Dna2 was almost fully degraded by 2.5 h after caffeine treatment (3 h following HO induction) (Figure 3C and Supplementary Figure S3D). As in the WT strains, after caffeine treatment the higher migrating Dna2 was rapidly lost, but the lower migrating forms persisted longer. These data suggest that a pathway other than autophagy, most likely proteasomal degradation, mediates most of the degradation of both Sae2 and Dna2 in response to caffeine treatment.
Sae2 and Dna2 are targets of proteasomal degradation
To determine if Dna2 and Sae2 are substrates of proteasomal degradation following caffeine treatment, we repeated the time-courses in the presence of proteasome inhibitor PS-341 (75). In order to sensitize cells to the inhibitor, we deleted PDR5, a drug transporter and RPN4, a transcriptional regulator of proteasome genes (75–77). After nocodazole arrest, HO was induced, and 45 min later cells were treated with 100 μM of PS-341. Ten min after PS-341 addition (55 min after HO induction), 20 mM caffeine was added to the medium. Treatment with PS-341 prior to caffeine treatment stabilized Sae2 levels when compared to cells not treated with the proteasome inhibitor (Figure 4A). Dna2 was partially stabilized in pdr5Δ rpn4Δ even without addition of PS-341 (compare Figure 4B with Figure 3B), but completely stabilized when the cells were treated with PS-341 prior to caffeine treatment. Such stabilization in rpn4Δ even without PS-341 addition has been shown for other proteasomal targets (76). These data suggest both Sae2 and Dna2 are degraded by the proteasome following caffeine treatment.
Figure 4.
Sae2 and Dna2 are targets of proteasomal degradation. (A) Western blot to detect Sae2 levels in rpn4Δ pdr5Δ cells after caffeine treatment. HO was induced in G2/M-arrested cells. Forty five minutes after HO induction, cells were treated with 100 mM PS-341, and 55 min after HO induction 20 mM caffeine was added to the medium. (B) Western blot to detect Dna2 levels in rpn4Δ pdr5Δ cells after caffeine treatment. HO was induced in G2/- arrested cells. Forty five minutes after HO induction, cells were treated with 100 mM PS-341, and 55 min after HO induction, 20 mM caffeine was added to the medium. (C) Rate of resection after inhibition of proteasomal degradation. Cells were arrested in G2/M by nocodazole treatment for 3 h. HO was induced at 0 h. Resection was measured in JKM179 (WT) or rpn4Δ pdr5Δ (PS341). Following addition of 100 mM PS-341 at the time of HO induction, 20 mM caffeine was added at 0.5 h. Rates were calculated by determining the time and distance when the PCR signal fell to 75% of signal at 0 h (WT rates are as shown in Figure 2A, PS341 rates calculated from graphs shown in Supplementary Figure S5) (36). These values were plotted on time-versus-distance graphs, and the rates were determined by linear regression analysis. Error bars represent the range.
Sae2 and Dna2 are targets of proteasomal degradation. (A) Western blot to detect Sae2 levels in rpn4Δ pdr5Δ cells after caffeine treatment. HO was induced in G2/M-arrested cells. Forty five minutes after HO induction, cells were treated with 100 mM PS-341, and 55 min after HO induction 20 mM caffeine was added to the medium. (B) Western blot to detect Dna2 levels in rpn4Δ pdr5Δ cells after caffeine treatment. HO was induced in G2/- arrested cells. Forty five minutes after HO induction, cells were treated with 100 mM PS-341, and 55 min after HO induction, 20 mM caffeine was added to the medium. (C) Rate of resection after inhibition of proteasomal degradation. Cells were arrested in G2/M by nocodazole treatment for 3 h. HO was induced at 0 h. Resection was measured in JKM179 (WT) or rpn4Δ pdr5Δ (PS341). Following addition of 100 mM PS-341 at the time of HO induction, 20 mM caffeine was added at 0.5 h. Rates were calculated by determining the time and distance when the PCR signal fell to 75% of signal at 0 h (WT rates are as shown in Figure 2A, PS341 rates calculated from graphs shown in Supplementary Figure S5) (36). These values were plotted on time-versus-distance graphs, and the rates were determined by linear regression analysis. Error bars represent the range.We then tested if inhibition of proteasomal degradation would prevent the reduction of resection seen after caffeine treatment. We arrested pdr5Δ rpn4Δ cells in G2/M by nocodazole treatment for 3 h, after which HO was induced and 100 μM PS-341 added to the media. The rate of resection seen after inhibition of proteasomal degradation in this strain was comparable to WT (Figure 4C and Supplementary Figure S5). After inhibition of proteasomal degradation, treatment with 20 mM caffeine at 0.5 h failed to impair resection (Figure 4C and Supplementary Figure S5), strongly suggesting that the proteasomal degradation of Sae2 and Dna2 following caffeine treatment is the main pathway by which caffeine treatment impairs resection.
Sae2 has a short half life that is not dependent on the DNA damage checkpoint
TORC1 regulates protein synthesis by promoting translation initiation, assembly of the translation machinery and regulating mRNA turnover (78). Therefore, inhibition of TORC1 by rapamycin leads to protein synthesis inhibition in both yeast and mammals (79–81). Because caffeine also inhibits TORC1, we hypothesized that the loss of Sae2 could be the result of inhibiting protein synthesis. We therefore tested if Sae2 is lost after inhibiting protein synthesis by CHX. Cells were arrested in G2/M by nocodazole, after which HO was induced. Thirty minutes following HO induction, cells were treated with 100 μg/ml CHX. CHX treatment resulted in complete loss of Sae2 1 h after treatment (Figure 5A).
Figure 5.
Sae2 has a short half-life regardless of DNA damage. (A) The stability of Sae2 was assessed after induction of a DSB. Cells were arrested in nocodazole prior to HO induction and treated with 100 μg/ml CHX 0.5 h after HO induction. (B) The stability of Sae2 was assessed without induction of DSB. Cycling cells were treated with 100 μg/ml CHX. (C) The stability of Sae2 was assessed without induction of DSB. Cycling cells were treated with 20 mM caffeine. (D) The degradation of Sae2 following CHX treatment was assayed in an atg1Δ strain. Cells were arrested in nocodazole prior to HO induction and treated with 100 μg/ml CHX 0.5 h after HO induction. (E) Sae2 is stable up to 9 h following DNA damage. Sae2 was monitored for 9 h following HO induction. (F) Sae2 is degraded after DNA damage dependent induction. Cells were treated with 100 μg/ml CHX 6 h following HO induction. (G) Sae2 is degraded after DNA damage dependent induction. Cells were treated with 20 mM caffeine 6 h following HO induction.
Sae2 has a short half-life regardless of DNA damage. (A) The stability of Sae2 was assessed after induction of a DSB. Cells were arrested in nocodazole prior to HO induction and treated with 100 μg/ml CHX 0.5 h after HO induction. (B) The stability of Sae2 was assessed without induction of DSB. Cycling cells were treated with 100 μg/ml CHX. (C) The stability of Sae2 was assessed without induction of DSB. Cycling cells were treated with 20 mM caffeine. (D) The degradation of Sae2 following CHX treatment was assayed in an atg1Δ strain. Cells were arrested in nocodazole prior to HO induction and treated with 100 μg/ml CHX 0.5 h after HO induction. (E) Sae2 is stable up to 9 h following DNA damage. Sae2 was monitored for 9 h following HO induction. (F) Sae2 is degraded after DNA damage dependent induction. Cells were treated with 100 μg/ml CHX 6 h following HO induction. (G) Sae2 is degraded after DNA damage dependent induction. Cells were treated with 20 mM caffeine 6 h following HO induction.A recent study suggested that Sae2 is degraded following DNA damage in both autophagy- and proteasome-dependent pathways (62). We therefore tested if the rapid loss of Sae2 following treatment with CHX is DNA-damage dependent. We treated cycling cells with 100 μg/ml CHX or 20 mM caffeine. Treatment with CHX resulted in loss of Sae2 as soon as 30 min after treatment (Figure 5B). Caffeine treatment led to a complete loss of Sae2 one h after treatment (Figure 5C). These results demonstrate that Sae2 exhibits a short half-life independent of DNA damage. Furthermore, these results suggest that the instability of Sae2 is not cell cycle dependent.The effect of CHX on autophagy is controversial. While some studies suggest that CHX inhibits starvation-induced autophagy in both yeast and mammals (82,83), others show that CHX cannot inhibit rapamycin-induced autophagy (84). To test if treatment of yeast with CHX leads to loss of Sae2 by stimulating autophagy, we performed a western blot for Sae2 in an atg1Δ strain. As with caffeine, we find that deletion of Atg1 fails to rescue Sae2 from the degradation induced by CHX (Figure 5D).Treatment of Dna2 with 100 μg/ml CHX after HO induction led to a modest decrease in Dna2 levels (Supplementary Figure S6A). Interestingly, the higher migrating band seen after DNA damage was lost after CHX treatment. Unlike Sae2, treatment of cycling cells or G2/M arrested cells with 20 mM caffeine did not result in decrease in Dna2 levels (Supplementary Figure S6B and S6C). These results suggest that DNA damage leads to the susceptibility of Dna2 for degradation following caffeine and CHX treatments.Last we assessed whether CHX and caffeine treatment could lead to loss of Sae2 even after the protein had accumulated significantly after DNA damage. We arrested cells in G2/M with nocodazole, induced HO to create a single unrepaired DSB and treated with either CHX or caffeine 6 h after induction. There was a marked increase in the abundance of Sae2 after DSB induction and the protein remained stable for at least 9 h after DSB induction (Figure 5E). Caffeine or CHX addition resulted in degradation of Sae2 even when the treatment took place 6 h after damage, when the DNA damage checkpoint is fully activated (Figure 5F and G). Treatment with either CHX or caffeine at 6 h led to the appearance of lower migrating bands on the gel. These appear to be degradation intermediates. Taken together, these data show that Sae2 is an intrinsically unstable protein, and that this instability is not a result of post-translational modifications that occur following DNA damage.
Caffeine treatment impairs resection and reduces RPA and Rad51 foci in mammalian cells
In mammalian cells, X-irradiation results in formation of Rad51 foci at sites of DNA damage. When Chinese Hamster Ovary (CHO) cells are treated with caffeine prior to exposure to irradiation, Rad51 foci are greatly diminished (52). While this observation may suggest that Rad51 itself is sensitive to caffeine, it may also be a result of impaired resection in the presence of caffeine.To test if caffeine impairs resection in mammalian cells, we treated HeLa cells with different concentrations of caffeine 1 h prior to irradiation, allowed the cells to recover for 4 h, fixed the cells and immunostained with Rad51 and RPA antibodies. As previously reported (52), the number of Rad51 foci decreased in caffeine-treated cells. We found this decrease to be dose-dependent (Figure 6A and B). However, this reduction was not specific to Rad51, as the number of RPA foci also decreased in a dose-dependent manner. For example, cells treated with 10 mM caffeine resulted in a 3-fold and 7-fold decrease in Rad51 and RPA focus counts, respectively. Furthermore, the intensity of the Rad51 and RPA foci in caffeine-treated cells was weaker than the untreated controls. Given the high level of specificity of RPA for ssDNA tracts, the reduction in staining intensity is very likely to reflect a reduction in the average length of ssDNA tracts in these cells. Taken together with the more direct analysis of ssDNA tract lengths in yeast, these observations suggest that caffeine impairs resection in mammalian cells.
Figure 6.
Caffeine treatment impairs RAD51 and RPA focus formation in HeLa cells. (A) Caffeine treatment impairs resection in HeLA cells. Increasing concentrations of caffeine added to HeLa cells 1 h prior to irradiation (6 Gy). Cells fixed 4 h after irradiation and immunostained with α-Rad51 or α-RPA antibodies. Decrease in RPA and Rad51 foci observed in caffeine-treated cells. (B) Quantification of foci. Brackets show comparisons with the untreated control that revealed statistically significant differences. * P-value<0.05, ** P-value<0.005, *** P-value<0.05, Wilcoxon rank sum test. (C) CtIP steady-state levels in irradiated HeLa cells following caffeine treatment. (D) Quantification of CtIP levels in irradiated HeLa cells following caffeine treatment. Graph depicts average of two independent experiments. Levels are depicted relative to the IR sample without caffeine.
Caffeine treatment impairs RAD51 and RPA focus formation in HeLa cells. (A) Caffeine treatment impairs resection in HeLA cells. Increasing concentrations of caffeine added to HeLa cells 1 h prior to irradiation (6 Gy). Cells fixed 4 h after irradiation and immunostained with α-Rad51 or α-RPA antibodies. Decrease in RPA and Rad51 foci observed in caffeine-treated cells. (B) Quantification of foci. Brackets show comparisons with the untreated control that revealed statistically significant differences. * P-value<0.05, ** P-value<0.005, *** P-value<0.05, Wilcoxon rank sum test. (C) CtIP steady-state levels in irradiated HeLa cells following caffeine treatment. (D) Quantification of CtIP levels in irradiated HeLa cells following caffeine treatment. Graph depicts average of two independent experiments. Levels are depicted relative to the IR sample without caffeine.Next we determined if levels of CtIP, the human homolog of Sae2 (85), were reduced by caffeine treatment. We observed a 2- to 3-fold decrease in the steady-state levels of CtIP in irradiated cells after treatment with increasing amounts of caffeine (Figure 6C and D), similar to the effect of caffeine on Sae2 in budding yeast. These observations suggest that the mechanism through which caffeine limits DNA resection is substantially conserved between budding yeast and human cells.
DISCUSSION
The mechanism by which cells sense DNA damage is of great interest and has important implications for cancer research. γ-H2AX has been proposed to play a role in the maintenance of the DNA damage checkpoint. Here we show that the removal of this modification after DSB repair is locus autonomous. This finding demonstrates that the sensing mechanism for the persistence of a DSB is local and not global, and may suggest that the global DNA damage checkpoint is turned on and off by coordinating many local sensing events.Caffeine's inhibitory effect on the DNA damage checkpoint through the inhibition of ATR and ATM has long been established, though the mechanism of this inhibition remains poorly understood. Evidence from mammalian cells suggests that, apart from inhibiting the DNA damage checkpoint, caffeine treatment also inhibits HR (51,52). Caffeine was also shown to inhibit gene targeting, which requires much of the HR machinery (53). Here we show that caffeine targets one of the earliest processes of HR: 5′ to 3′ resection. Impairment of resection is particularly important as all HR processes depend on resection to create recombinogenic 3′-ended ssDNA. We note that caffeine treatment at lower concentrations (10 and 20 mM) did not completely inhibit SSA. Repair by SSA requires nonhomologous tail clipping that is dependent on Mec1 or Tel1 phosphorylation of Slx4 (86). Caffeine, therefore, affects SSA by two mechanisms; impairing resection and inhibiting nonhomologous tail clipping. It is possible that at lower caffeine concentrations, resection is attenuated but residual Mec1 or Tel1 activity allows nonhomologous tail clipping, therefore SSA is impaired but not abolished. At higher concentrations, Mec1 and Tel1 may be completely inhibited so repair is prevented by both inhibition of tail clipping and attenuation of resection. Yet another possibility is that the slower resection seen after 50 mM caffeine treatment (2.4 kb/h at 50 mM caffeine, 2.7 kb/h at 10 mM and 20 mM caffeine) leads to a more significant inhibition of repair at the higher concentrations.In yeast, caffeine treatment affects enzymes involved both in the initiation of resection and extended resection. Sae2 and its mammalian homolog CtIP together with the MRX complex (MRN in mammalian cells) initiate resection after a DSB (5,85). Cells lacking Sae2 are impaired in resection (8). Here we show that caffeine treatment reduces levels of Sae2. We show that the turnover of Sae2 is very rapid, as inhibiting protein synthesis leads to a complete loss of Sae2 as soon as 30 min after treatment. Surprisingly, caffeine treatment 0.5 h after HO induction did not result in substantial impairment in the resection of the first 700 bp. This result may indicate that Sae2's role in initiation of resection is achieved by that time, and also explains the inability of caffeine treatment to increase NHEJ efficiency. Caffeine also acts as a TORC1 inhibitor, which regulates protein synthesis. Although Robert et. al. showed that Sae2 is degraded by autophagy following VPA treatment, we could not replicate this result. Further we find that abrogation of autophagy by deleting ATG1 failed to rescue Sae2 from degradation following caffeine, rapamycin or CHX treatments. Moreover, the induction of autophagy by Atg13–8SA did not lead to the mislocalization of Sae2. Last, we show that inhibition of proteasomal degradation by PS-341 treatment stabilizes Sae2 levels in cells and prevents the reduction of resection following caffeine treatment. Because CHX led to rapid loss of Sae2 in WT cells both with and without DNA damage, and in atg1Δ cells, we propose that Sae2 has a short half-life independent of DNA damage or chemical treatment.Extensive resection takes place through the Exo1 and Dna2/Sgs1-Top3-Rmi1 pathways. Exo1 levels are not significantly affected by caffeine treatment; however, Dna2 levels decrease in response to caffeine treatment. Interestingly, the rate of resection measured after caffeine treatment (2.4–2.7 kb/h in 10–50 mM caffeine) resembles the rate of resection measured in sgs1Δ cells (3 kb/h) (36). We conclude that caffeine affects resection through the damage-dependent degradation of Dna2 and the rapid turnover of Sae2.We note that caffeine treatment leads to a more rapid loss of the DNA damage dependent phosphorylated form of Dna2 than the unmodified form. It is also possible that the maintenance of the phosphorylated state requires continuous Mec1 and Tel1 activity. In this case, the phosphorylated form of Dna2 would be dephosphorylated by caffeine treatment, leading indirectly to its degradation. Reduction in proteasomal activity by deletion of the transcription factor RPN4 was sufficient to partially stabilize Dna2 levels after caffeine treatment.Caffeine treatment sensitizes mammalian cells to irradiation and other DNA damaging agents. Caffeine was thought to do so through the inhibition of p53, ATM and ATR, although p53-proficient cancer cells are not radiosensitized by caffeine, suggesting that the main pathway by which caffeine acts is inhibition of processes that occur after the cells pass ‘start’ (48). Caffeine-induced radiosensitivity likely results from inhibition of HR because this radiosensitivity is not observed in HR-defective cells (50,51). Recently caffeine was shown in vivo to prevent gene targeting in mammalian cells independently of the DNA damage checkpoint (53). In vitro, caffeine treatment was shown in the same study to interfere with Rad51-mediated joint molecule formation. In an accompanying paper we corroborate these findings, and show that at higher concentrations caffeine fully displaces Rad51 filaments from the ssDNA. However, the findings presented here show that caffeine treatment targets a key step preceding Rad51 filament formation and homology searching. Our studies suggest that the effect of caffeine on resection is conserved from yeast to mammals. The data presented here further our mechanistic understanding of caffeine-mediated radiosensitivity, informing the ongoing effort to develop DNA repair inhibitors for cancer treatment (87–90).
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Yixian Cui; Yong Cui; Emmanuel Culetto; Andrea C Cumino; Andrey V Cybulsky; Mark J Czaja; Stanislaw J Czuczwar; Stefania D'Adamo; Marcello D'Amelio; Daniela D'Arcangelo; Andrew C D'Lugos; Gabriella D'Orazi; James A da Silva; Hormos Salimi Dafsari; Ruben K Dagda; Yasin Dagdas; Maria Daglia; Xiaoxia Dai; Yun Dai; Yuyuan Dai; Jessica Dal Col; Paul Dalhaimer; Luisa Dalla Valle; Tobias Dallenga; Guillaume Dalmasso; Markus Damme; Ilaria Dando; Nico P Dantuma; April L Darling; Hiranmoy Das; Srinivasan Dasarathy; Santosh K Dasari; Srikanta Dash; Oliver Daumke; Adrian N Dauphinee; Jeffrey S Davies; Valeria A Dávila; Roger J Davis; Tanja Davis; Sharadha Dayalan Naidu; Francesca De Amicis; Karolien De Bosscher; Francesca De Felice; Lucia De Franceschi; Chiara De Leonibus; Mayara G de Mattos Barbosa; Guido R Y De Meyer; Angelo De Milito; Cosimo De Nunzio; Clara De Palma; Mauro De Santi; Claudio De Virgilio; Daniela De Zio; Jayanta Debnath; Brian J DeBosch; Jean-Paul Decuypere; Mark A Deehan; Gianluca Deflorian; James DeGregori; Benjamin Dehay; Gabriel Del Rio; Joe R Delaney; Lea M D Delbridge; Elizabeth Delorme-Axford; M Victoria Delpino; Francesca Demarchi; Vilma Dembitz; Nicholas D Demers; Hongbin Deng; Zhiqiang Deng; Joern Dengjel; Paul Dent; Donna Denton; Melvin L DePamphilis; Channing J Der; Vojo Deretic; Albert Descoteaux; Laura Devis; Sushil Devkota; Olivier Devuyst; Grant Dewson; Mahendiran Dharmasivam; Rohan Dhiman; Diego di Bernardo; Manlio Di Cristina; Fabio Di Domenico; Pietro Di Fazio; Alessio Di Fonzo; Giovanni Di Guardo; Gianni M Di Guglielmo; Luca Di Leo; Chiara Di Malta; Alessia Di Nardo; Martina Di Rienzo; Federica Di Sano; George Diallinas; Jiajie Diao; Guillermo Diaz-Araya; Inés Díaz-Laviada; Jared M Dickinson; Marc Diederich; Mélanie Dieudé; Ivan Dikic; Shiping Ding; Wen-Xing Ding; Luciana Dini; Jelena Dinić; Miroslav Dinic; Albena T Dinkova-Kostova; Marc S Dionne; Jörg H W Distler; Abhinav Diwan; Ian M C Dixon; Mojgan Djavaheri-Mergny; Ina Dobrinski; Oxana Dobrovinskaya; Radek Dobrowolski; Renwick C J Dobson; Jelena Đokić; Serap Dokmeci Emre; Massimo Donadelli; Bo Dong; Xiaonan Dong; Zhiwu Dong; Gerald W Dorn Ii; Volker Dotsch; Huan Dou; Juan Dou; Moataz Dowaidar; Sami Dridi; Liat Drucker; Ailian Du; Caigan Du; Guangwei Du; Hai-Ning Du; Li-Lin Du; André du Toit; Shao-Bin Duan; Xiaoqiong Duan; Sónia P Duarte; Anna Dubrovska; Elaine A Dunlop; Nicolas Dupont; Raúl V Durán; Bilikere S Dwarakanath; Sergey A Dyshlovoy; Darius Ebrahimi-Fakhari; Leopold Eckhart; Charles L Edelstein; Thomas Efferth; Eftekhar Eftekharpour; Ludwig Eichinger; Nabil Eid; Tobias Eisenberg; N Tony Eissa; Sanaa Eissa; Miriam Ejarque; Abdeljabar El Andaloussi; Nazira El-Hage; Shahenda El-Naggar; Anna Maria Eleuteri; Eman S El-Shafey; Mohamed Elgendy; Aristides G Eliopoulos; María M Elizalde; Philip M Elks; Hans-Peter Elsasser; Eslam S Elsherbiny; Brooke M Emerling; N C Tolga Emre; Christina H Eng; Nikolai Engedal; Anna-Mart Engelbrecht; Agnete S T Engelsen; Jorrit M Enserink; Ricardo Escalante; Audrey Esclatine; Mafalda Escobar-Henriques; Eeva-Liisa Eskelinen; Lucile Espert; Makandjou-Ola Eusebio; Gemma Fabrias; Cinzia Fabrizi; Antonio Facchiano; Francesco Facchiano; Bengt Fadeel; Claudio Fader; Alex C Faesen; W Douglas Fairlie; Alberto Falcó; Bjorn H Falkenburger; Daping Fan; Jie Fan; Yanbo Fan; Evandro F Fang; Yanshan Fang; Yognqi Fang; Manolis Fanto; Tamar Farfel-Becker; Mathias Faure; Gholamreza Fazeli; Anthony O Fedele; Arthur M Feldman; Du Feng; Jiachun Feng; Lifeng Feng; Yibin Feng; Yuchen Feng; Wei Feng; Thais Fenz Araujo; Thomas A Ferguson; Álvaro F Fernández; Jose C Fernandez-Checa; Sonia Fernández-Veledo; Alisdair R Fernie; Anthony W Ferrante; Alessandra Ferraresi; Merari F Ferrari; Julio C B Ferreira; Susan Ferro-Novick; Antonio Figueras; Riccardo Filadi; Nicoletta Filigheddu; Eduardo Filippi-Chiela; Giuseppe Filomeni; Gian Maria Fimia; Vittorio Fineschi; Francesca Finetti; Steven Finkbeiner; Edward A Fisher; Paul B Fisher; Flavio Flamigni; Steven J Fliesler; Trude H Flo; Ida Florance; Oliver Florey; Tullio Florio; Erika Fodor; Carlo Follo; Edward A Fon; Antonella Forlino; Francesco Fornai; Paola Fortini; Anna Fracassi; Alessandro Fraldi; Brunella Franco; Rodrigo Franco; Flavia Franconi; Lisa B Frankel; Scott L Friedman; Leopold F Fröhlich; Gema Frühbeck; Jose M Fuentes; Yukio Fujiki; Naonobu Fujita; Yuuki Fujiwara; Mitsunori Fukuda; Simone Fulda; Luc Furic; Norihiko Furuya; Carmela Fusco; Michaela U Gack; Lidia Gaffke; Sehamuddin Galadari; Alessia Galasso; Maria F Galindo; Sachith Gallolu Kankanamalage; Lorenzo Galluzzi; Vincent Galy; Noor Gammoh; Boyi Gan; Ian G Ganley; Feng Gao; Hui Gao; Minghui Gao; Ping Gao; Shou-Jiang Gao; Wentao Gao; Xiaobo Gao; Ana Garcera; Maria Noé Garcia; Verónica E Garcia; Francisco García-Del Portillo; Vega Garcia-Escudero; Aracely Garcia-Garcia; Marina Garcia-Macia; Diana García-Moreno; Carmen Garcia-Ruiz; Patricia García-Sanz; Abhishek D Garg; Ricardo Gargini; Tina Garofalo; Robert F Garry; Nils C Gassen; Damian Gatica; Liang Ge; Wanzhong Ge; Ruth Geiss-Friedlander; Cecilia Gelfi; Pascal Genschik; Ian E Gentle; Valeria Gerbino; Christoph Gerhardt; Kyla Germain; Marc Germain; David A Gewirtz; Elham Ghasemipour Afshar; Saeid Ghavami; Alessandra Ghigo; Manosij Ghosh; Georgios Giamas; Claudia Giampietri; Alexandra Giatromanolaki; Gary E Gibson; Spencer B Gibson; Vanessa Ginet; Edward Giniger; Carlotta Giorgi; Henrique Girao; Stephen E Girardin; Mridhula Giridharan; Sandy Giuliano; Cecilia Giulivi; Sylvie Giuriato; Julien Giustiniani; Alexander Gluschko; Veit Goder; Alexander Goginashvili; Jakub Golab; David C Goldstone; Anna Golebiewska; Luciana R Gomes; Rodrigo Gomez; Rubén Gómez-Sánchez; Maria Catalina Gomez-Puerto; Raquel Gomez-Sintes; Qingqiu Gong; Felix M Goni; Javier González-Gallego; Tomas Gonzalez-Hernandez; Rosa A Gonzalez-Polo; Jose A Gonzalez-Reyes; Patricia González-Rodríguez; Ing Swie Goping; Marina S Gorbatyuk; Nikolai V Gorbunov; Kıvanç Görgülü; Roxana M Gorojod; Sharon M Gorski; Sandro Goruppi; Cecilia Gotor; Roberta A Gottlieb; Illana Gozes; Devrim Gozuacik; Martin Graef; Markus H Gräler; Veronica Granatiero; Daniel Grasso; Joshua P Gray; Douglas R Green; Alexander Greenhough; Stephen L Gregory; Edward F Griffin; Mark W Grinstaff; Frederic Gros; Charles Grose; Angelina S Gross; Florian Gruber; Paolo Grumati; Tilman Grune; Xueyan Gu; Jun-Lin Guan; Carlos M Guardia; Kishore Guda; Flora Guerra; Consuelo Guerri; Prasun Guha; Carlos Guillén; Shashi Gujar; Anna Gukovskaya; Ilya Gukovsky; Jan Gunst; Andreas Günther; Anyonya R Guntur; Chuanyong Guo; Chun Guo; Hongqing Guo; Lian-Wang Guo; Ming Guo; Pawan Gupta; Shashi Kumar Gupta; Swapnil Gupta; Veer Bala Gupta; Vivek Gupta; Asa B Gustafsson; David D Gutterman; Ranjitha H B; Annakaisa Haapasalo; James E Haber; Aleksandra Hać; Shinji Hadano; Anders J Hafrén; Mansour Haidar; Belinda S Hall; Gunnel Halldén; Anne Hamacher-Brady; Andrea Hamann; Maho Hamasaki; Weidong Han; Malene Hansen; Phyllis I Hanson; Zijian Hao; Masaru Harada; Ljubica Harhaji-Trajkovic; Nirmala Hariharan; Nigil Haroon; James Harris; Takafumi Hasegawa; Noor Hasima Nagoor; Jeffrey A Haspel; Volker Haucke; Wayne D Hawkins; Bruce A Hay; Cole M Haynes; Soren B Hayrabedyan; Thomas S Hays; Congcong He; Qin He; Rong-Rong He; You-Wen He; Yu-Ying He; Yasser Heakal; Alexander M Heberle; J Fielding Hejtmancik; Gudmundur Vignir Helgason; Vanessa Henkel; Marc Herb; Alexander Hergovich; Anna Herman-Antosiewicz; Agustín Hernández; Carlos Hernandez; Sergio Hernandez-Diaz; Virginia Hernandez-Gea; Amaury Herpin; Judit Herreros; Javier H Hervás; Daniel Hesselson; Claudio Hetz; Volker T Heussler; Yujiro Higuchi; Sabine Hilfiker; Joseph A Hill; William S Hlavacek; Emmanuel A Ho; Idy H T Ho; Philip Wing-Lok Ho; Shu-Leong Ho; Wan Yun Ho; G Aaron Hobbs; Mark Hochstrasser; Peter H M Hoet; Daniel Hofius; Paul Hofman; Annika Höhn; Carina I Holmberg; Jose R Hombrebueno; Chang-Won Hong Yi-Ren Hong; Lora V Hooper; Thorsten Hoppe; Rastislav Horos; Yujin Hoshida; I-Lun Hsin; Hsin-Yun Hsu; Bing Hu; Dong Hu; Li-Fang Hu; Ming Chang Hu; Ronggui Hu; Wei Hu; Yu-Chen Hu; Zhuo-Wei Hu; Fang Hua; Jinlian Hua; Yingqi Hua; Chongmin Huan; Canhua Huang; Chuanshu Huang; Chuanxin Huang; Chunling Huang; Haishan Huang; Kun Huang; Michael L H Huang; Rui Huang; Shan Huang; Tianzhi Huang; Xing Huang; Yuxiang Jack Huang; Tobias B Huber; Virginie Hubert; Christian A Hubner; Stephanie M Hughes; William E Hughes; Magali Humbert; Gerhard Hummer; James H Hurley; Sabah Hussain; Salik Hussain; Patrick J Hussey; Martina Hutabarat; Hui-Yun Hwang; Seungmin Hwang; Antonio Ieni; Fumiyo Ikeda; Yusuke Imagawa; Yuzuru Imai; Carol Imbriano; Masaya Imoto; Denise M Inman; Ken Inoki; Juan Iovanna; Renato V Iozzo; Giuseppe Ippolito; Javier E Irazoqui; Pablo Iribarren; Mohd Ishaq; Makoto Ishikawa; Nestor Ishimwe; Ciro Isidoro; Nahed Ismail; Shohreh Issazadeh-Navikas; Eisuke Itakura; Daisuke Ito; Davor Ivankovic; Saška Ivanova; Anand Krishnan V Iyer; José M Izquierdo; Masanori Izumi; Marja Jäättelä; Majid Sakhi Jabir; William T Jackson; Nadia Jacobo-Herrera; Anne-Claire Jacomin; Elise Jacquin; Pooja Jadiya; Hartmut Jaeschke; Chinnaswamy Jagannath; Arjen J Jakobi; Johan Jakobsson; Bassam Janji; Pidder Jansen-Dürr; Patric J Jansson; Jonathan Jantsch; Sławomir Januszewski; Alagie Jassey; Steve Jean; Hélène Jeltsch-David; Pavla Jendelova; Andreas Jenny; Thomas E Jensen; Niels Jessen; Jenna L Jewell; Jing Ji; Lijun Jia; Rui Jia; Liwen Jiang; Qing Jiang; Richeng Jiang; Teng Jiang; Xuejun Jiang; Yu Jiang; Maria Jimenez-Sanchez; Eun-Jung Jin; Fengyan Jin; Hongchuan Jin; Li Jin; Luqi Jin; Meiyan Jin; Si Jin; Eun-Kyeong Jo; Carine Joffre; Terje Johansen; Gail V W Johnson; Simon A Johnston; Eija Jokitalo; Mohit Kumar Jolly; Leo A B Joosten; Joaquin Jordan; Bertrand Joseph; Dianwen Ju; Jeong-Sun Ju; Jingfang Ju; Esmeralda Juárez; Delphine Judith; Gábor Juhász; Youngsoo Jun; Chang Hwa Jung; Sung-Chul Jung; Yong Keun Jung; Heinz Jungbluth; Johannes Jungverdorben; Steffen Just; Kai Kaarniranta; Allen Kaasik; Tomohiro Kabuta; Daniel Kaganovich; Alon Kahana; Renate Kain; Shinjo Kajimura; Maria Kalamvoki; Manjula Kalia; Danuta S Kalinowski; Nina Kaludercic; Ioanna Kalvari; Joanna Kaminska; Vitaliy O Kaminskyy; Hiromitsu Kanamori; Keizo Kanasaki; Chanhee Kang; Rui Kang; Sang Sun Kang; Senthilvelrajan Kaniyappan; Tomotake Kanki; Thirumala-Devi Kanneganti; Anumantha G Kanthasamy; Arthi Kanthasamy; Marc Kantorow; Orsolya Kapuy; Michalis V Karamouzis; Md Razaul Karim; Parimal Karmakar; Rajesh G Katare; Masaru Kato; Stefan H E Kaufmann; Anu Kauppinen; Gur P Kaushal; Susmita Kaushik; Kiyoshi Kawasaki; Kemal Kazan; Po-Yuan Ke; Damien J Keating; Ursula Keber; John H Kehrl; Kate E Keller; Christian W Keller; Jongsook Kim Kemper; Candia M Kenific; Oliver Kepp; Stephanie Kermorgant; Andreas Kern; Robin Ketteler; Tom G Keulers; Boris Khalfin; Hany Khalil; Bilon Khambu; Shahid Y Khan; Vinoth Kumar Megraj Khandelwal; Rekha Khandia; Widuri Kho; Noopur V Khobrekar; Sataree Khuansuwan; Mukhran Khundadze; Samuel A Killackey; Dasol Kim; Deok Ryong Kim; Do-Hyung Kim; Dong-Eun Kim; Eun Young Kim; Eun-Kyoung Kim; Hak-Rim Kim; Hee-Sik Kim; Jeong Hun Kim; Jin Kyung Kim; Jin-Hoi Kim; Joungmok Kim; Ju Hwan Kim; Keun Il Kim; Peter K Kim; Seong-Jun Kim; Scot R Kimball; Adi Kimchi; Alec C Kimmelman; Tomonori Kimura; Matthew A King; Kerri J Kinghorn; Conan G Kinsey; Vladimir Kirkin; Lorrie A Kirshenbaum; Sergey L Kiselev; Shuji Kishi; Katsuhiko Kitamoto; Yasushi Kitaoka; Kaio Kitazato; Richard N Kitsis; Josef T Kittler; Ole Kjaerulff; Peter S Klein; Thomas Klopstock; Jochen Klucken; Helene Knævelsrud; Roland L Knorr; Ben C B Ko; Fred Ko; Jiunn-Liang Ko; Hotaka Kobayashi; Satoru Kobayashi; Ina Koch; Jan C Koch; Ulrich Koenig; Donat Kögel; Young Ho Koh; Masato Koike; Sepp D Kohlwein; Nur M Kocaturk; Masaaki Komatsu; Jeannette König; Toru Kono; Benjamin T Kopp; Tamas Korcsmaros; Gözde Korkmaz; Viktor I Korolchuk; Mónica Suárez Korsnes; Ali Koskela; Janaiah Kota; Yaichiro Kotake; Monica L Kotler; Yanjun Kou; Michael I Koukourakis; Evangelos Koustas; Attila L Kovacs; Tibor Kovács; Daisuke Koya; Tomohiro Kozako; Claudine Kraft; Dimitri Krainc; Helmut Krämer; Anna D Krasnodembskaya; Carole Kretz-Remy; Guido Kroemer; Nicholas T Ktistakis; Kazuyuki Kuchitsu; Sabine Kuenen; Lars Kuerschner; Thomas Kukar; Ajay Kumar; Ashok Kumar; Deepak Kumar; Dhiraj Kumar; Sharad Kumar; Shinji Kume; Caroline Kumsta; Chanakya N Kundu; Mondira Kundu; Ajaikumar B Kunnumakkara; Lukasz Kurgan; Tatiana G Kutateladze; Ozlem Kutlu; SeongAe Kwak; Ho Jeong Kwon; Taeg Kyu Kwon; Yong Tae Kwon; Irene Kyrmizi; Albert La Spada; Patrick Labonté; Sylvain Ladoire; Ilaria Laface; Frank Lafont; Diane C Lagace; Vikramjit Lahiri; Zhibing Lai; Angela S Laird; Aparna Lakkaraju; Trond Lamark; Sheng-Hui Lan; Ane Landajuela; Darius J R Lane; Jon D Lane; Charles H Lang; Carsten Lange; Ülo Langel; Rupert Langer; Pierre Lapaquette; Jocelyn Laporte; Nicholas F LaRusso; Isabel Lastres-Becker; Wilson Chun Yu Lau; Gordon W Laurie; Sergio Lavandero; Betty Yuen Kwan Law; Helen Ka-Wai Law; Rob Layfield; Weidong Le; Herve Le Stunff; Alexandre Y Leary; Jean-Jacques Lebrun; Lionel Y W Leck; Jean-Philippe Leduc-Gaudet; Changwook Lee; Chung-Pei Lee; Da-Hye Lee; Edward B Lee; Erinna F Lee; Gyun Min Lee; He-Jin Lee; Heung Kyu Lee; Jae Man Lee; Jason S Lee; Jin-A Lee; Joo-Yong Lee; Jun Hee Lee; Michael Lee; Min Goo Lee; Min Jae Lee; Myung-Shik Lee; Sang Yoon Lee; Seung-Jae Lee; Stella Y Lee; Sung Bae Lee; Won Hee Lee; Ying-Ray Lee; Yong-Ho Lee; Youngil Lee; Christophe Lefebvre; Renaud Legouis; Yu L Lei; Yuchen Lei; Sergey Leikin; Gerd Leitinger; Leticia Lemus; Shuilong Leng; Olivia Lenoir; Guido Lenz; Heinz Josef Lenz; Paola Lenzi; Yolanda León; Andréia M Leopoldino; Christoph Leschczyk; Stina Leskelä; Elisabeth Letellier; Chi-Ting Leung; Po Sing Leung; Jeremy S Leventhal; Beth Levine; Patrick A Lewis; Klaus Ley; Bin Li; Da-Qiang Li; Jianming Li; Jing Li; Jiong Li; Ke Li; Liwu Li; Mei Li; Min Li; Min Li; Ming Li; Mingchuan Li; Pin-Lan Li; Ming-Qing Li; Qing Li; Sheng Li; Tiangang Li; Wei Li; Wenming Li; Xue Li; Yi-Ping Li; Yuan Li; Zhiqiang Li; Zhiyong Li; Zhiyuan Li; Jiqin Lian; Chengyu Liang; Qiangrong Liang; Weicheng Liang; Yongheng Liang; YongTian Liang; Guanghong Liao; Lujian Liao; Mingzhi Liao; Yung-Feng Liao; Mariangela Librizzi; Pearl P Y Lie; Mary A Lilly; Hyunjung J Lim; Thania R R Lima; Federica Limana; Chao Lin; Chih-Wen Lin; Dar-Shong Lin; Fu-Cheng Lin; Jiandie D Lin; Kurt M Lin; Kwang-Huei Lin; Liang-Tzung Lin; Pei-Hui Lin; Qiong Lin; Shaofeng Lin; Su-Ju Lin; Wenyu Lin; Xueying Lin; Yao-Xin Lin; Yee-Shin Lin; Rafael Linden; Paula Lindner; Shuo-Chien Ling; Paul Lingor; Amelia K Linnemann; Yih-Cherng Liou; Marta M Lipinski; Saška Lipovšek; Vitor A Lira; Natalia Lisiak; Paloma B Liton; Chao Liu; Ching-Hsuan Liu; Chun-Feng Liu; Cui Hua Liu; Fang Liu; Hao Liu; Hsiao-Sheng Liu; Hua-Feng Liu; Huifang Liu; Jia Liu; Jing Liu; Julia Liu; Leyuan Liu; Longhua Liu; Meilian Liu; Qin Liu; Wei Liu; Wende Liu; Xiao-Hong Liu; Xiaodong Liu; Xingguo Liu; Xu Liu; Xuedong Liu; Yanfen Liu; Yang Liu; Yang Liu; Yueyang Liu; Yule Liu; J Andrew Livingston; Gerard Lizard; Jose M Lizcano; Senka Ljubojevic-Holzer; Matilde E LLeonart; David Llobet-Navàs; Alicia Llorente; Chih Hung Lo; Damián Lobato-Márquez; Qi Long; Yun Chau Long; Ben Loos; Julia A Loos; Manuela G López; Guillermo López-Doménech; José Antonio López-Guerrero; Ana T López-Jiménez; Óscar López-Pérez; Israel López-Valero; Magdalena J Lorenowicz; Mar Lorente; Peter Lorincz; Laura Lossi; Sophie Lotersztajn; Penny E Lovat; Jonathan F Lovell; Alenka Lovy; Péter Lőw; Guang Lu; Haocheng Lu; Jia-Hong Lu; Jin-Jian Lu; Mengji Lu; Shuyan Lu; Alessandro Luciani; John M Lucocq; Paula Ludovico; Micah A Luftig; Morten Luhr; Diego Luis-Ravelo; Julian J Lum; Liany Luna-Dulcey; Anders H Lund; Viktor K Lund; Jan D Lünemann; Patrick Lüningschrör; Honglin Luo; Rongcan Luo; Shouqing Luo; Zhi Luo; Claudio Luparello; Bernhard Lüscher; Luan Luu; Alex Lyakhovich; Konstantin G Lyamzaev; Alf Håkon Lystad; Lyubomyr Lytvynchuk; Alvin C Ma; Changle Ma; Mengxiao Ma; Ning-Fang Ma; Quan-Hong Ma; Xinliang Ma; Yueyun Ma; Zhenyi Ma; Ormond A MacDougald; Fernando Macian; Gustavo C MacIntosh; Jeffrey P MacKeigan; Kay F Macleod; Sandra Maday; Frank Madeo; Muniswamy Madesh; Tobias Madl; Julio Madrigal-Matute; Akiko Maeda; Yasuhiro Maejima; Marta Magarinos; Poornima Mahavadi; Emiliano Maiani; Kenneth Maiese; Panchanan Maiti; Maria Chiara Maiuri; Barbara Majello; Michael B Major; Elena Makareeva; Fayaz Malik; Karthik Mallilankaraman; Walter Malorni; Alina Maloyan; Najiba Mammadova; Gene Chi Wai Man; Federico Manai; Joseph D Mancias; Eva-Maria Mandelkow; Michael A Mandell; Angelo A Manfredi; Masoud H Manjili; Ravi Manjithaya; Patricio Manque; Bella B Manshian; Raquel Manzano; Claudia Manzoni; Kai Mao; Cinzia Marchese; Sandrine Marchetti; Anna Maria Marconi; Fabrizio Marcucci; Stefania Mardente; Olga A Mareninova; Marta Margeta; Muriel Mari; Sara Marinelli; Oliviero Marinelli; Guillermo Mariño; Sofia Mariotto; Richard S Marshall; Mark R Marten; Sascha Martens; Alexandre P J Martin; Katie R Martin; Sara Martin; Shaun Martin; Adrián Martín-Segura; Miguel A Martín-Acebes; Inmaculada Martin-Burriel; Marcos Martin-Rincon; Paloma Martin-Sanz; José A Martina; Wim Martinet; Aitor Martinez; Ana Martinez; Jennifer Martinez; Moises Martinez Velazquez; Nuria Martinez-Lopez; Marta Martinez-Vicente; Daniel O Martins; Joilson O Martins; Waleska K Martins; Tania Martins-Marques; Emanuele Marzetti; Shashank Masaldan; Celine Masclaux-Daubresse; Douglas G Mashek; Valentina Massa; Lourdes Massieu; Glenn R Masson; Laura Masuelli; Anatoliy I Masyuk; Tetyana V Masyuk; Paola Matarrese; Ander Matheu; Satoaki Matoba; Sachiko Matsuzaki; Pamela Mattar; Alessandro Matte; Domenico Mattoscio; José L Mauriz; Mario Mauthe; Caroline Mauvezin; Emanual Maverakis; Paola Maycotte; Johanna Mayer; Gianluigi Mazzoccoli; Cristina Mazzoni; Joseph R Mazzulli; Nami McCarty; Christine McDonald; Mitchell R McGill; Sharon L McKenna; BethAnn McLaughlin; Fionn McLoughlin; Mark A McNiven; 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Taiga Miyazaki; Keisuke Miyazawa; Noboru Mizushima; Trine H Mogensen; Baharia Mograbi; Reza Mohammadinejad; Yasir Mohamud; Abhishek Mohanty; Sipra Mohapatra; Torsten Möhlmann; Asif Mohmmed; Anna Moles; Kelle H Moley; Maurizio Molinari; Vincenzo Mollace; Andreas Buch Møller; Bertrand Mollereau; Faustino Mollinedo; Costanza Montagna; Mervyn J Monteiro; Andrea Montella; L Ruth Montes; Barbara Montico; Vinod K Mony; Giacomo Monzio Compagnoni; Michael N Moore; Mohammad A Moosavi; Ana L Mora; Marina Mora; David Morales-Alamo; Rosario Moratalla; Paula I Moreira; Elena Morelli; Sandra Moreno; Daniel Moreno-Blas; Viviana Moresi; Benjamin Morga; Alwena H Morgan; Fabrice Morin; Hideaki Morishita; Orson L Moritz; Mariko Moriyama; Yuji Moriyasu; Manuela Morleo; Eugenia Morselli; Jose F Moruno-Manchon; Jorge Moscat; Serge Mostowy; Elisa Motori; Andrea Felinto Moura; Naima Moustaid-Moussa; Maria Mrakovcic; Gabriel Muciño-Hernández; Anupam Mukherjee; Subhadip Mukhopadhyay; Jean M Mulcahy Levy; Victoriano Mulero; 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Authors: Michael Tsabar; Jennifer M Mason; Yuen-Ling Chan; Douglas K Bishop; James E Haber Journal: Nucleic Acids Res Date: 2015-05-27 Impact factor: 16.971
Authors: Daniel J Klionsky; Kotb Abdelmohsen; Akihisa Abe; Md Joynal Abedin; Hagai Abeliovich; Abraham Acevedo Arozena; Hiroaki Adachi; Christopher M Adams; Peter D Adams; Khosrow Adeli; Peter J Adhihetty; Sharon G Adler; Galila Agam; Rajesh Agarwal; Manish K Aghi; Maria Agnello; Patrizia Agostinis; Patricia V Aguilar; Julio Aguirre-Ghiso; Edoardo M Airoldi; Slimane Ait-Si-Ali; Takahiko Akematsu; Emmanuel T Akporiaye; Mohamed Al-Rubeai; Guillermo M Albaiceta; Chris Albanese; Diego Albani; Matthew L Albert; Jesus Aldudo; Hana Algül; Mehrdad Alirezaei; Iraide Alloza; Alexandru Almasan; Maylin Almonte-Beceril; Emad S Alnemri; Covadonga Alonso; Nihal Altan-Bonnet; Dario C Altieri; Silvia Alvarez; Lydia Alvarez-Erviti; Sandro Alves; Giuseppina Amadoro; Atsuo Amano; Consuelo Amantini; Santiago Ambrosio; Ivano Amelio; Amal O Amer; Mohamed Amessou; Angelika Amon; Zhenyi An; Frank A Anania; Stig U Andersen; Usha P Andley; Catherine K Andreadi; Nathalie Andrieu-Abadie; Alberto Anel; David K Ann; Shailendra Anoopkumar-Dukie; Manuela Antonioli; Hiroshi Aoki; Nadezda Apostolova; Saveria Aquila; Katia Aquilano; Koichi Araki; Eli Arama; Agustin Aranda; Jun Araya; Alexandre Arcaro; Esperanza Arias; Hirokazu Arimoto; Aileen R Ariosa; Jane L Armstrong; Thierry Arnould; Ivica Arsov; Katsuhiko Asanuma; Valerie Askanas; Eric Asselin; Ryuichiro Atarashi; Sally S Atherton; Julie D Atkin; Laura D Attardi; Patrick Auberger; Georg Auburger; Laure Aurelian; Riccardo Autelli; Laura Avagliano; Maria Laura Avantaggiati; Limor Avrahami; Suresh Awale; Neelam Azad; Tiziana Bachetti; Jonathan M Backer; Dong-Hun Bae; Jae-Sung Bae; Ok-Nam Bae; Soo Han Bae; Eric H Baehrecke; Seung-Hoon Baek; Stephen Baghdiguian; Agnieszka Bagniewska-Zadworna; Hua Bai; Jie Bai; Xue-Yuan Bai; Yannick Bailly; Kithiganahalli Narayanaswamy Balaji; Walter Balduini; Andrea Ballabio; Rena Balzan; Rajkumar Banerjee; Gábor Bánhegyi; Haijun Bao; Benoit Barbeau; Maria D Barrachina; Esther Barreiro; Bonnie Bartel; Alberto Bartolomé; Diane C Bassham; Maria Teresa Bassi; Robert C Bast; Alakananda Basu; Maria Teresa Batista; Henri Batoko; Maurizio Battino; Kyle Bauckman; Bradley L Baumgarner; K Ulrich Bayer; Rupert Beale; Jean-François Beaulieu; George R Beck; Christoph Becker; J David Beckham; Pierre-André Bédard; Patrick J Bednarski; Thomas J Begley; Christian Behl; Christian Behrends; Georg Mn Behrens; Kevin E Behrns; Eloy Bejarano; Amine Belaid; Francesca Belleudi; Giovanni Bénard; Guy Berchem; Daniele Bergamaschi; Matteo Bergami; Ben Berkhout; Laura Berliocchi; Amélie Bernard; Monique Bernard; Francesca Bernassola; Anne Bertolotti; Amanda S Bess; Sébastien Besteiro; Saverio Bettuzzi; Savita Bhalla; Shalmoli Bhattacharyya; Sujit K Bhutia; Caroline Biagosch; Michele Wolfe Bianchi; Martine Biard-Piechaczyk; Viktor Billes; Claudia Bincoletto; Baris Bingol; Sara W Bird; Marc Bitoun; Ivana Bjedov; Craig Blackstone; Lionel Blanc; Guillermo A Blanco; Heidi Kiil Blomhoff; Emilio Boada-Romero; Stefan Böckler; Marianne Boes; Kathleen Boesze-Battaglia; Lawrence H Boise; Alessandra Bolino; Andrea Boman; Paolo Bonaldo; Matteo Bordi; Jürgen Bosch; Luis M Botana; Joelle Botti; German Bou; Marina Bouché; Marion Bouchecareilh; Marie-Josée Boucher; Michael E Boulton; Sebastien G Bouret; Patricia Boya; Michaël Boyer-Guittaut; Peter V Bozhkov; Nathan Brady; Vania Mm Braga; Claudio Brancolini; Gerhard H Braus; José M Bravo-San Pedro; Lisa A Brennan; Emery H Bresnick; Patrick Brest; Dave Bridges; Marie-Agnès Bringer; Marisa Brini; Glauber C Brito; Bertha Brodin; Paul S Brookes; Eric J Brown; Karen Brown; Hal E Broxmeyer; Alain Bruhat; Patricia Chakur Brum; John H Brumell; Nicola Brunetti-Pierri; Robert J Bryson-Richardson; Shilpa Buch; Alastair M Buchan; Hikmet Budak; Dmitry V Bulavin; Scott J Bultman; Geert Bultynck; Vladimir Bumbasirevic; Yan Burelle; Robert E Burke; Margit Burmeister; Peter Bütikofer; Laura Caberlotto; Ken Cadwell; Monika Cahova; Dongsheng Cai; Jingjing Cai; Qian Cai; Sara Calatayud; Nadine Camougrand; Michelangelo Campanella; Grant R Campbell; Matthew Campbell; Silvia Campello; Robin Candau; Isabella Caniggia; Lavinia Cantoni; Lizhi Cao; Allan B Caplan; Michele Caraglia; Claudio Cardinali; Sandra Morais Cardoso; Jennifer S Carew; Laura A Carleton; Cathleen R Carlin; Silvia Carloni; Sven R Carlsson; Didac Carmona-Gutierrez; Leticia Am Carneiro; Oliana Carnevali; Serena Carra; Alice Carrier; Bernadette Carroll; Caty Casas; Josefina Casas; Giuliana Cassinelli; Perrine Castets; Susana Castro-Obregon; Gabriella Cavallini; Isabella Ceccherini; Francesco Cecconi; Arthur I Cederbaum; Valentín Ceña; Simone Cenci; Claudia Cerella; Davide Cervia; Silvia Cetrullo; Hassan Chaachouay; Han-Jung Chae; Andrei S Chagin; Chee-Yin Chai; Gopal Chakrabarti; Georgios Chamilos; Edmond Yw Chan; Matthew Tv Chan; Dhyan Chandra; Pallavi Chandra; Chih-Peng Chang; Raymond Chuen-Chung Chang; Ta Yuan Chang; John C Chatham; Saurabh Chatterjee; Santosh Chauhan; Yongsheng Che; Michael E Cheetham; Rajkumar Cheluvappa; Chun-Jung Chen; Gang Chen; Guang-Chao Chen; Guoqiang Chen; Hongzhuan Chen; Jeff W Chen; Jian-Kang Chen; Min Chen; Mingzhou Chen; Peiwen Chen; Qi Chen; Quan Chen; Shang-Der Chen; Si Chen; Steve S-L Chen; Wei Chen; Wei-Jung Chen; Wen Qiang Chen; Wenli Chen; Xiangmei Chen; Yau-Hung Chen; Ye-Guang Chen; Yin Chen; Yingyu Chen; Yongshun Chen; Yu-Jen Chen; Yue-Qin Chen; Yujie Chen; Zhen Chen; Zhong Chen; Alan Cheng; Christopher Hk Cheng; Hua Cheng; Heesun Cheong; Sara Cherry; Jason Chesney; Chun Hei Antonio Cheung; Eric Chevet; Hsiang Cheng Chi; Sung-Gil Chi; Fulvio Chiacchiera; Hui-Ling Chiang; Roberto Chiarelli; Mario Chiariello; Marcello Chieppa; Lih-Shen Chin; Mario Chiong; Gigi Nc Chiu; Dong-Hyung Cho; Ssang-Goo Cho; William C Cho; Yong-Yeon Cho; Young-Seok Cho; Augustine Mk Choi; Eui-Ju Choi; Eun-Kyoung Choi; Jayoung Choi; Mary E Choi; Seung-Il Choi; Tsui-Fen Chou; Salem Chouaib; Divaker Choubey; Vinay Choubey; Kuan-Chih Chow; Kamal Chowdhury; Charleen T Chu; Tsung-Hsien Chuang; Taehoon Chun; Hyewon Chung; Taijoon Chung; Yuen-Li Chung; Yong-Joon Chwae; Valentina Cianfanelli; Roberto Ciarcia; Iwona A Ciechomska; Maria Rosa Ciriolo; Mara Cirone; Sofie Claerhout; Michael J Clague; Joan Clària; Peter Gh Clarke; Robert Clarke; Emilio Clementi; Cédric Cleyrat; Miriam Cnop; Eliana M Coccia; Tiziana Cocco; Patrice Codogno; Jörn Coers; Ezra Ew Cohen; David Colecchia; Luisa Coletto; Núria S Coll; Emma Colucci-Guyon; Sergio Comincini; Maria Condello; Katherine L Cook; Graham H Coombs; Cynthia D Cooper; J Mark Cooper; Isabelle Coppens; Maria Tiziana Corasaniti; Marco Corazzari; Ramon Corbalan; Elisabeth Corcelle-Termeau; Mario D Cordero; Cristina Corral-Ramos; Olga Corti; Andrea Cossarizza; Paola Costelli; Safia Costes; Susan L Cotman; Ana Coto-Montes; Sandra Cottet; Eduardo Couve; Lori R Covey; L Ashley Cowart; Jeffery S Cox; Fraser P Coxon; Carolyn B Coyne; Mark S Cragg; Rolf J Craven; Tiziana Crepaldi; Jose L Crespo; Alfredo Criollo; Valeria Crippa; Maria Teresa Cruz; Ana Maria Cuervo; Jose M Cuezva; Taixing Cui; Pedro R Cutillas; Mark J Czaja; Maria F Czyzyk-Krzeska; Ruben K Dagda; Uta Dahmen; Chunsun Dai; Wenjie Dai; Yun Dai; Kevin N Dalby; Luisa Dalla Valle; Guillaume Dalmasso; Marcello D'Amelio; Markus Damme; Arlette Darfeuille-Michaud; Catherine Dargemont; Victor M Darley-Usmar; Srinivasan Dasarathy; Biplab Dasgupta; Srikanta Dash; Crispin R Dass; Hazel Marie Davey; Lester M Davids; David Dávila; Roger J Davis; Ted M Dawson; Valina L Dawson; Paula Daza; Jackie de Belleroche; Paul de Figueiredo; Regina Celia Bressan Queiroz de Figueiredo; José de la Fuente; Luisa De Martino; Antonella De Matteis; Guido Ry De Meyer; Angelo De Milito; Mauro De Santi; Wanderley de Souza; Vincenzo De Tata; Daniela De Zio; Jayanta Debnath; Reinhard Dechant; Jean-Paul Decuypere; Shane Deegan; Benjamin Dehay; Barbara Del Bello; Dominic P Del Re; Régis Delage-Mourroux; Lea Md Delbridge; Louise Deldicque; Elizabeth Delorme-Axford; Yizhen Deng; Joern Dengjel; Melanie Denizot; Paul Dent; Channing J Der; Vojo Deretic; Benoît Derrien; Eric Deutsch; Timothy P Devarenne; Rodney J Devenish; Sabrina Di Bartolomeo; Nicola Di Daniele; Fabio Di Domenico; Alessia Di Nardo; Simone Di Paola; Antonio Di Pietro; Livia Di Renzo; Aaron DiAntonio; Guillermo Díaz-Araya; Ines Díaz-Laviada; Maria T Diaz-Meco; Javier Diaz-Nido; Chad A Dickey; Robert C Dickson; Marc Diederich; Paul Digard; Ivan Dikic; Savithrama P Dinesh-Kumar; Chan Ding; Wen-Xing Ding; Zufeng Ding; Luciana Dini; Jörg Hw Distler; Abhinav Diwan; Mojgan Djavaheri-Mergny; Kostyantyn Dmytruk; Renwick Cj Dobson; Volker Doetsch; Karol Dokladny; Svetlana Dokudovskaya; Massimo Donadelli; X Charlie Dong; Xiaonan Dong; Zheng Dong; Terrence M Donohue; Kelly S Doran; Gabriella D'Orazi; Gerald W Dorn; Victor Dosenko; Sami Dridi; Liat Drucker; Jie Du; Li-Lin Du; Lihuan Du; André du Toit; Priyamvada Dua; Lei Duan; Pu Duann; Vikash Kumar Dubey; Michael R Duchen; Michel A Duchosal; Helene Duez; Isabelle Dugail; Verónica I Dumit; Mara C Duncan; Elaine A Dunlop; William A Dunn; Nicolas Dupont; Luc Dupuis; Raúl V Durán; Thomas M Durcan; Stéphane Duvezin-Caubet; Umamaheswar Duvvuri; Vinay Eapen; Darius Ebrahimi-Fakhari; Arnaud Echard; Leopold Eckhart; Charles L Edelstein; Aimee L Edinger; Ludwig Eichinger; Tobias Eisenberg; Avital Eisenberg-Lerner; N Tony Eissa; Wafik S El-Deiry; Victoria El-Khoury; Zvulun Elazar; Hagit Eldar-Finkelman; Chris Jh Elliott; Enzo Emanuele; Urban Emmenegger; Nikolai Engedal; Anna-Mart Engelbrecht; Simone Engelender; Jorrit M Enserink; Ralf Erdmann; Jekaterina Erenpreisa; Rajaraman Eri; Jason L Eriksen; Andreja Erman; Ricardo Escalante; Eeva-Liisa Eskelinen; Lucile Espert; Lorena Esteban-Martínez; Thomas J Evans; Mario Fabri; Gemma Fabrias; Cinzia Fabrizi; Antonio Facchiano; Nils J Færgeman; Alberto Faggioni; W Douglas Fairlie; Chunhai Fan; Daping Fan; Jie Fan; Shengyun Fang; Manolis Fanto; Alessandro Fanzani; Thomas Farkas; Mathias Faure; Francois B Favier; Howard Fearnhead; Massimo Federici; Erkang Fei; Tania C Felizardo; Hua Feng; Yibin Feng; Yuchen Feng; Thomas A Ferguson; Álvaro F Fernández; Maite G Fernandez-Barrena; Jose C Fernandez-Checa; Arsenio Fernández-López; Martin E Fernandez-Zapico; Olivier Feron; Elisabetta Ferraro; Carmen Veríssima Ferreira-Halder; Laszlo Fesus; Ralph Feuer; Fabienne C Fiesel; Eduardo C Filippi-Chiela; Giuseppe Filomeni; Gian Maria Fimia; John H Fingert; Steven Finkbeiner; Toren Finkel; Filomena Fiorito; Paul B Fisher; Marc Flajolet; Flavio Flamigni; Oliver Florey; Salvatore Florio; R Andres Floto; Marco Folini; Carlo Follo; Edward A Fon; Francesco Fornai; Franco Fortunato; Alessandro Fraldi; Rodrigo Franco; Arnaud Francois; Aurélie François; Lisa B Frankel; Iain Dc Fraser; Norbert Frey; Damien G Freyssenet; Christian Frezza; Scott L Friedman; Daniel E Frigo; Dongxu Fu; José M Fuentes; Juan Fueyo; Yoshio Fujitani; Yuuki Fujiwara; Mikihiro Fujiya; Mitsunori Fukuda; Simone Fulda; Carmela Fusco; Bozena Gabryel; Matthias Gaestel; Philippe Gailly; Malgorzata Gajewska; Sehamuddin Galadari; Gad Galili; Inmaculada Galindo; Maria F Galindo; Giovanna Galliciotti; Lorenzo Galluzzi; Luca Galluzzi; Vincent Galy; Noor Gammoh; Sam Gandy; Anand K Ganesan; Swamynathan Ganesan; Ian G Ganley; Monique Gannagé; Fen-Biao Gao; Feng Gao; Jian-Xin Gao; Lorena García Nannig; Eleonora García Véscovi; Marina Garcia-Macía; Carmen Garcia-Ruiz; Abhishek D Garg; Pramod Kumar Garg; Ricardo Gargini; Nils Christian Gassen; Damián Gatica; Evelina Gatti; Julie Gavard; Evripidis Gavathiotis; Liang Ge; Pengfei Ge; Shengfang Ge; Po-Wu Gean; Vania Gelmetti; Armando A Genazzani; Jiefei Geng; Pascal Genschik; Lisa Gerner; Jason E Gestwicki; David A Gewirtz; Saeid Ghavami; Eric Ghigo; Debabrata Ghosh; Anna Maria Giammarioli; Francesca Giampieri; Claudia Giampietri; Alexandra Giatromanolaki; Derrick J Gibbings; Lara Gibellini; Spencer B Gibson; Vanessa Ginet; Antonio Giordano; Flaviano Giorgini; Elisa Giovannetti; Stephen E Girardin; Suzana Gispert; Sandy Giuliano; Candece L Gladson; Alvaro Glavic; Martin Gleave; Nelly Godefroy; Robert M Gogal; Kuppan Gokulan; Gustavo H Goldman; Delia Goletti; Michael S Goligorsky; Aldrin V Gomes; Ligia C Gomes; Hernando Gomez; Candelaria Gomez-Manzano; Rubén Gómez-Sánchez; Dawit Ap Gonçalves; Ebru Goncu; Qingqiu Gong; Céline Gongora; Carlos B Gonzalez; Pedro Gonzalez-Alegre; Pilar Gonzalez-Cabo; Rosa Ana González-Polo; Ing Swie Goping; Carlos Gorbea; Nikolai V Gorbunov; Daphne R Goring; Adrienne M Gorman; Sharon M Gorski; Sandro Goruppi; Shino Goto-Yamada; Cecilia Gotor; Roberta A Gottlieb; Illana Gozes; Devrim Gozuacik; Yacine Graba; Martin Graef; Giovanna E Granato; Gary Dean Grant; Steven Grant; Giovanni Luca Gravina; Douglas R Green; Alexander Greenhough; Michael T Greenwood; Benedetto Grimaldi; Frédéric Gros; Charles Grose; Jean-Francois Groulx; Florian Gruber; Paolo Grumati; Tilman Grune; Jun-Lin Guan; Kun-Liang Guan; Barbara Guerra; Carlos Guillen; Kailash Gulshan; Jan Gunst; Chuanyong Guo; Lei Guo; Ming Guo; Wenjie Guo; Xu-Guang Guo; Andrea A Gust; Åsa B Gustafsson; Elaine Gutierrez; Maximiliano G Gutierrez; Ho-Shin Gwak; Albert Haas; James E Haber; Shinji Hadano; Monica Hagedorn; David R Hahn; Andrew J Halayko; Anne Hamacher-Brady; Kozo Hamada; Ahmed Hamai; Andrea Hamann; Maho Hamasaki; Isabelle Hamer; Qutayba Hamid; Ester M Hammond; Feng Han; Weidong Han; James T Handa; John A Hanover; Malene Hansen; Masaru Harada; Ljubica Harhaji-Trajkovic; J Wade Harper; Abdel Halim Harrath; Adrian L Harris; James Harris; Udo Hasler; Peter Hasselblatt; Kazuhisa Hasui; Robert G Hawley; Teresa S Hawley; Congcong He; Cynthia Y He; Fengtian He; Gu He; Rong-Rong He; Xian-Hui He; You-Wen He; Yu-Ying He; Joan K Heath; Marie-Josée Hébert; Robert A Heinzen; Gudmundur Vignir Helgason; Michael Hensel; Elizabeth P Henske; Chengtao Her; Paul K Herman; Agustín Hernández; Carlos Hernandez; Sonia Hernández-Tiedra; Claudio Hetz; P Robin Hiesinger; Katsumi Higaki; Sabine Hilfiker; Bradford G Hill; Joseph A Hill; William D Hill; Keisuke Hino; Daniel Hofius; Paul Hofman; Günter U Höglinger; Jörg Höhfeld; Marina K Holz; Yonggeun Hong; David A Hood; Jeroen Jm Hoozemans; Thorsten Hoppe; Chin Hsu; Chin-Yuan Hsu; Li-Chung Hsu; Dong Hu; Guochang Hu; Hong-Ming Hu; Hongbo Hu; Ming Chang Hu; Yu-Chen Hu; Zhuo-Wei Hu; Fang Hua; Ya Hua; Canhua Huang; Huey-Lan Huang; Kuo-How Huang; Kuo-Yang Huang; Shile Huang; Shiqian Huang; Wei-Pang Huang; Yi-Ran Huang; Yong Huang; Yunfei Huang; Tobias B Huber; Patricia Huebbe; Won-Ki Huh; Juha J Hulmi; Gang Min Hur; James H Hurley; Zvenyslava Husak; Sabah Na Hussain; Salik Hussain; Jung Jin Hwang; Seungmin Hwang; Thomas Is Hwang; Atsuhiro Ichihara; Yuzuru Imai; Carol Imbriano; Megumi Inomata; Takeshi Into; Valentina Iovane; Juan L Iovanna; Renato V Iozzo; Nancy Y Ip; Javier E Irazoqui; Pablo Iribarren; Yoshitaka Isaka; Aleksandra J Isakovic; Harry Ischiropoulos; Jeffrey S Isenberg; Mohammad Ishaq; Hiroyuki Ishida; Isao Ishii; Jane E Ishmael; Ciro Isidoro; Ken-Ichi Isobe; Erika Isono; Shohreh Issazadeh-Navikas; Koji Itahana; Eisuke Itakura; Andrei I Ivanov; Anand Krishnan V Iyer; José M Izquierdo; Yotaro Izumi; Valentina Izzo; Marja Jäättelä; Nadia Jaber; Daniel John Jackson; William T Jackson; Tony George Jacob; Thomas S Jacques; Chinnaswamy Jagannath; Ashish Jain; Nihar Ranjan Jana; Byoung Kuk Jang; Alkesh Jani; Bassam Janji; Paulo Roberto Jannig; Patric J Jansson; Steve Jean; Marina Jendrach; Ju-Hong Jeon; Niels Jessen; Eui-Bae Jeung; Kailiang Jia; Lijun Jia; Hong Jiang; Hongchi Jiang; Liwen Jiang; Teng Jiang; Xiaoyan Jiang; Xuejun Jiang; Xuejun Jiang; Ying Jiang; Yongjun Jiang; Alberto Jiménez; Cheng Jin; Hongchuan Jin; Lei Jin; Meiyan Jin; Shengkan Jin; Umesh Kumar Jinwal; Eun-Kyeong Jo; Terje Johansen; Daniel E Johnson; Gail Vw Johnson; James D Johnson; Eric Jonasch; Chris Jones; Leo Ab Joosten; Joaquin Jordan; Anna-Maria Joseph; Bertrand Joseph; Annie M Joubert; Dianwen Ju; Jingfang Ju; Hsueh-Fen Juan; Katrin Juenemann; Gábor Juhász; Hye Seung Jung; Jae U Jung; Yong-Keun Jung; Heinz Jungbluth; Matthew J Justice; Barry Jutten; Nadeem O Kaakoush; Kai Kaarniranta; Allen Kaasik; Tomohiro Kabuta; Bertrand Kaeffer; Katarina Kågedal; Alon Kahana; Shingo Kajimura; Or Kakhlon; Manjula Kalia; Dhan V Kalvakolanu; Yoshiaki Kamada; Konstantinos Kambas; Vitaliy O Kaminskyy; Harm H Kampinga; Mustapha Kandouz; Chanhee Kang; Rui Kang; Tae-Cheon Kang; Tomotake Kanki; Thirumala-Devi Kanneganti; Haruo Kanno; Anumantha G Kanthasamy; Marc Kantorow; Maria Kaparakis-Liaskos; Orsolya Kapuy; Vassiliki Karantza; Md Razaul Karim; Parimal Karmakar; Arthur Kaser; Susmita Kaushik; Thomas Kawula; A Murat Kaynar; Po-Yuan Ke; Zun-Ji Ke; John H Kehrl; Kate E Keller; Jongsook Kim Kemper; Anne K Kenworthy; Oliver Kepp; Andreas Kern; Santosh Kesari; David Kessel; Robin Ketteler; Isis do Carmo Kettelhut; Bilon Khambu; Muzamil Majid Khan; Vinoth Km Khandelwal; Sangeeta Khare; Juliann G Kiang; Amy A Kiger; Akio Kihara; Arianna L Kim; Cheol Hyeon Kim; Deok Ryong Kim; Do-Hyung Kim; Eung Kweon Kim; Hye Young Kim; Hyung-Ryong Kim; Jae-Sung Kim; Jeong Hun Kim; Jin Cheon Kim; Jin Hyoung Kim; Kwang Woon Kim; Michael D Kim; Moon-Moo Kim; Peter K Kim; Seong Who Kim; Soo-Youl Kim; Yong-Sun Kim; Yonghyun Kim; Adi Kimchi; Alec C Kimmelman; Tomonori Kimura; Jason S King; Karla Kirkegaard; Vladimir Kirkin; Lorrie A Kirshenbaum; Shuji Kishi; Yasuo Kitajima; Katsuhiko Kitamoto; Yasushi Kitaoka; Kaio Kitazato; Rudolf A Kley; Walter T Klimecki; Michael Klinkenberg; Jochen Klucken; Helene Knævelsrud; Erwin Knecht; Laura Knuppertz; Jiunn-Liang Ko; Satoru Kobayashi; Jan C Koch; Christelle Koechlin-Ramonatxo; Ulrich Koenig; Young Ho Koh; Katja Köhler; Sepp D Kohlwein; Masato Koike; Masaaki Komatsu; Eiki Kominami; Dexin Kong; Hee Jeong Kong; Eumorphia G Konstantakou; Benjamin T Kopp; Tamas Korcsmaros; Laura Korhonen; Viktor I Korolchuk; Nadya V Koshkina; Yanjun Kou; Michael I Koukourakis; Constantinos Koumenis; Attila L Kovács; Tibor Kovács; Werner J Kovacs; Daisuke Koya; Claudine Kraft; Dimitri Krainc; Helmut Kramer; Tamara Kravic-Stevovic; Wilhelm Krek; Carole Kretz-Remy; Roswitha Krick; Malathi Krishnamurthy; Janos Kriston-Vizi; Guido Kroemer; Michael C Kruer; Rejko Kruger; Nicholas T Ktistakis; Kazuyuki Kuchitsu; Christian Kuhn; Addanki Pratap Kumar; Anuj Kumar; Ashok Kumar; Deepak Kumar; Dhiraj Kumar; Rakesh Kumar; Sharad Kumar; Mondira Kundu; Hsing-Jien Kung; Atsushi Kuno; Sheng-Han Kuo; Jeff Kuret; Tino Kurz; Terry Kwok; Taeg Kyu Kwon; Yong Tae Kwon; Irene Kyrmizi; Albert R La Spada; Frank Lafont; Tim Lahm; Aparna Lakkaraju; Truong Lam; Trond Lamark; Steve Lancel; Terry H Landowski; Darius J R Lane; Jon D Lane; Cinzia Lanzi; Pierre Lapaquette; Louis R Lapierre; Jocelyn Laporte; Johanna Laukkarinen; Gordon W Laurie; Sergio Lavandero; Lena Lavie; Matthew J LaVoie; Betty Yuen Kwan Law; Helen Ka-Wai Law; Kelsey B Law; Robert Layfield; Pedro A Lazo; Laurent Le Cam; Karine G Le Roch; Hervé Le Stunff; Vijittra Leardkamolkarn; Marc Lecuit; Byung-Hoon Lee; Che-Hsin Lee; Erinna F Lee; Gyun Min Lee; He-Jin Lee; Hsinyu Lee; Jae Keun Lee; Jongdae Lee; Ju-Hyun Lee; Jun Hee Lee; Michael Lee; Myung-Shik Lee; Patty J Lee; Sam W Lee; Seung-Jae Lee; Shiow-Ju Lee; Stella Y Lee; Sug Hyung Lee; Sung Sik Lee; Sung-Joon Lee; Sunhee Lee; Ying-Ray Lee; Yong J Lee; Young H Lee; Christiaan Leeuwenburgh; Sylvain Lefort; Renaud Legouis; Jinzhi Lei; Qun-Ying Lei; David A Leib; Gil Leibowitz; Istvan Lekli; Stéphane D Lemaire; John J Lemasters; Marius K Lemberg; Antoinette Lemoine; Shuilong Leng; Guido Lenz; Paola Lenzi; Lilach O Lerman; Daniele Lettieri Barbato; Julia I-Ju Leu; Hing Y Leung; Beth Levine; Patrick A Lewis; Frank Lezoualc'h; Chi Li; Faqiang Li; Feng-Jun Li; Jun Li; Ke Li; Lian Li; Min Li; Min Li; Qiang Li; Rui Li; Sheng Li; Wei Li; Wei Li; Xiaotao Li; Yumin Li; Jiqin Lian; Chengyu Liang; Qiangrong Liang; Yulin Liao; Joana Liberal; Pawel P Liberski; Pearl Lie; Andrew P Lieberman; Hyunjung Jade Lim; Kah-Leong Lim; Kyu Lim; Raquel T Lima; Chang-Shen Lin; Chiou-Feng Lin; Fang Lin; Fangming Lin; Fu-Cheng Lin; Kui Lin; Kwang-Huei Lin; Pei-Hui Lin; Tianwei Lin; Wan-Wan Lin; Yee-Shin Lin; Yong Lin; Rafael Linden; Dan Lindholm; Lisa M Lindqvist; Paul Lingor; Andreas Linkermann; Lance A Liotta; Marta M Lipinski; Vitor A Lira; Michael P Lisanti; Paloma B Liton; Bo Liu; Chong Liu; Chun-Feng Liu; Fei Liu; Hung-Jen Liu; Jianxun Liu; Jing-Jing Liu; Jing-Lan Liu; Ke Liu; Leyuan Liu; Liang Liu; Quentin Liu; Rong-Yu Liu; Shiming Liu; Shuwen Liu; Wei Liu; Xian-De Liu; Xiangguo Liu; Xiao-Hong Liu; Xinfeng Liu; Xu Liu; Xueqin Liu; Yang Liu; Yule Liu; Zexian Liu; Zhe Liu; Juan P Liuzzi; Gérard Lizard; Mila Ljujic; Irfan J Lodhi; Susan E Logue; Bal L Lokeshwar; Yun Chau Long; Sagar Lonial; Benjamin Loos; Carlos López-Otín; Cristina López-Vicario; Mar Lorente; Philip L Lorenzi; Péter Lõrincz; Marek Los; Michael T Lotze; Penny E Lovat; Binfeng Lu; Bo Lu; Jiahong Lu; Qing Lu; She-Min Lu; Shuyan Lu; Yingying Lu; Frédéric Luciano; Shirley Luckhart; John Milton Lucocq; Paula Ludovico; Aurelia Lugea; Nicholas W Lukacs; Julian J Lum; Anders H Lund; Honglin Luo; Jia Luo; Shouqing Luo; Claudio Luparello; Timothy Lyons; Jianjie Ma; Yi Ma; Yong Ma; Zhenyi Ma; Juliano Machado; Glaucia M Machado-Santelli; Fernando Macian; Gustavo C MacIntosh; Jeffrey P MacKeigan; Kay F Macleod; John D MacMicking; Lee Ann MacMillan-Crow; Frank Madeo; Muniswamy Madesh; Julio Madrigal-Matute; Akiko Maeda; Tatsuya Maeda; Gustavo Maegawa; Emilia Maellaro; Hannelore Maes; Marta Magariños; Kenneth Maiese; Tapas K Maiti; Luigi Maiuri; Maria Chiara Maiuri; Carl G Maki; Roland Malli; Walter Malorni; Alina Maloyan; Fathia Mami-Chouaib; Na Man; Joseph D Mancias; Eva-Maria Mandelkow; Michael A Mandell; Angelo A Manfredi; Serge N Manié; Claudia Manzoni; Kai Mao; Zixu Mao; Zong-Wan Mao; Philippe Marambaud; Anna Maria Marconi; Zvonimir Marelja; Gabriella Marfe; Marta Margeta; Eva Margittai; Muriel Mari; Francesca V Mariani; Concepcio Marin; Sara Marinelli; Guillermo Mariño; Ivanka Markovic; Rebecca Marquez; Alberto M Martelli; Sascha Martens; Katie R Martin; Seamus J Martin; Shaun Martin; 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