V El-Khoury1, S Pierson1, E Szwarcbart1, N H C Brons2, O Roland1, S Cherrier-De Wilde3, L Plawny3, E Van Dyck1, G Berchem4. 1. Laboratory of Experimental Hemato-Oncology, Centre de Recherche Public de la Santé, Luxembourg, Luxembourg. 2. Flow Cytometry Core Facility, Centre de Recherche Public de la Santé, Luxembourg, Luxembourg. 3. Centre Hospitalier de Luxembourg, Luxembourg, Luxembourg. 4. 1] Laboratory of Experimental Hemato-Oncology, Centre de Recherche Public de la Santé, Luxembourg, Luxembourg [2] Centre Hospitalier de Luxembourg, Luxembourg, Luxembourg.
Abstract
Evading apoptosis is a hallmark of B-cell chronic lymphocytic leukemia (CLL) cells and an obstacle to current chemotherapeutic approaches. Inhibiting histone deacetylase (HDAC) has emerged as a promising strategy to induce cell death in malignant cells. We have previously reported that the HDAC inhibitor MGCD0103 induces CLL cell death by activating the intrinsic pathway of apoptosis. Here, we show that MGCD0103 decreases the autophagic flux in primary CLL cells. Activation of the PI3K/AKT/mTOR pathway, together with the activation of caspases, and to a minor extent CAPN1, resulting in cleavage of autophagy components, were involved in MGCD0103-mediated inhibition of autophagy. In addition, MGCD0103 directly modulated the expression of critical autophagy genes at the transcriptional level that may contribute to autophagy impairment. Besides, we demonstrate that autophagy is a pro-survival mechanism in CLL whose disruption potentiates cell death induced by anticancer molecules including HDAC and cyclin-dependent kinase inhibitors. In particular, our data highlight the therapeutic potential of MGCD0103 as not only an inducer of apoptosis but also an autophagy suppressor in both combination regimens with molecules like flavopiridol, known to induce protective autophagy in CLL cells, or as an alternative to circumvent undesired immunomodulatory effects seen in the clinic with conventional autophagy inhibitors.
Evading apoptosis is a hallmark of B-cell chronic lymphocytic leukemia (CLL) cells and an obstacle to current chemotherapeutic approaches. Inhibiting histone deacetylase (HDAC) has emerged as a promising strategy to induce cell death in malignant cells. We have previously reported that the HDAC inhibitor MGCD0103 induces CLL cell death by activating the intrinsic pathway of apoptosis. Here, we show that MGCD0103 decreases the autophagic flux in primary CLL cells. Activation of the PI3K/AKT/mTOR pathway, together with the activation of caspases, and to a minor extent CAPN1, resulting in cleavage of autophagy components, were involved in MGCD0103-mediated inhibition of autophagy. In addition, MGCD0103 directly modulated the expression of critical autophagy genes at the transcriptional level that may contribute to autophagy impairment. Besides, we demonstrate that autophagy is a pro-survival mechanism in CLL whose disruption potentiates cell death induced by anticancer molecules including HDAC and cyclin-dependent kinase inhibitors. In particular, our data highlight the therapeutic potential of MGCD0103 as not only an inducer of apoptosis but also an autophagy suppressor in both combination regimens with molecules like flavopiridol, known to induce protective autophagy in CLL cells, or as an alternative to circumvent undesired immunomodulatory effects seen in the clinic with conventional autophagy inhibitors.
B-cell chronic lymphocytic leukemia (CLL) results from a monoclonal expansion of CD5+/CD19+/CD23+ B lymphocytes that accumulate in lymphatic organs.[1] Circulating CLL cells are mainly arrested in G0/G1 and fail to undergo apoptosis. This pool of malignant cells is fed by a proportion of CLL cells, ranging from 0.1 to 1% per day, that proliferate in the bone marrow and lymph nodes.[2] Despite considerable improvements in CLL chemoimmunotherapy, conventional drugs fail to cure CLL.Histone deacetylase (HDAC) inhibitors have the ability to reverse epigenetic alterations associated with cancer initiation/development and chemoresistance, and to induce tumor cell death.[3, 4] Inhibitors of zinc-dependent HDACs (classes I, II, IV) have emerged as promising cytotoxic agents and are currently being evaluated in several clinical trials for the treatment of cancer.[3]Besides their pro-apoptotic effect, HDAC inhibitors can also induce autophagy,[5, 6, 7] a ‘self-eating' process whereby proteins and organelles are sequestered in autophagosomes, and delivered to lysosomes for digestion.[8] Whereas autophagy operates as a housekeeping process to promote cell survival, autophagy defects have been found in humancancers, suggesting its tumor-suppressive role.[9] Nevertheless, the role of autophagy in cancer remains controversial,[6, 10, 11] and little is known about autophagy in CLL.[12, 13]We have previously shown that MGCD0103, a selective inhibitor of HDACs 1, 2, 3 and 11, triggers in primary CLL cells a death amplification loop involving caspases and calpains.[14]Here, we show that MGCD0103 inhibits autophagy in primary CLL cells while operating at three levels: activation of the phosphatidylinositide 3-kinase/AKT/mammalian target of rapamycin (PI3K/AKT/mTOR) pathway, caspase- and calpain-1-mediated cleavage of autophagy components and downregulation of autophagy gene transcription. Finally, we demonstrate that basal autophagy functions in CLL as a pro-survival mechanism whose disruption potentiates cell death.
Materials and methods
Patients, cell separation and culture conditions
Subjects were CLL patients (n=34) and healthy donors (n=3) seen at the ‘Centre Hospitalier de Luxembourg'. The clinical features of patients are summarized in Supplementary Table 1. The experiments were approved by the ‘Comité National d'Ethique de Recherche' and all subjects signed an informed consent according to the Declaration of Helsinki.Peripheral blood mononuclear cells (PBMCs) were isolated using lymphocyte separation medium (MP Biomedicals, Eindhoven, The Netherlands). PBMCs and Mec-1 cells were cultured in Iscove's modified Dulbecco's medium (Lonza, Verviers, Belgium), MCF-7 cells, JVM-2 and JVM-3 cells in RPMI-1640 medium (Lonza) and HeLa cells in Dulbecco's modified Eagle's medium, all containing 10% fetal bovine serum. The cells were incubated at 37 °C in an atmosphere of 5% CO2.
Reagents and antibodies
MGCD0103 was provided by MethylGene Inc. (Quebec, Canada). Valproic acid (VPA; Depakine IV, Sanofi Aventis) and bortezomib (Velcade IV, Millennium Pharmaceuticals, Inc.) were purchased from the hospital's pharmacy. Q-VD-OPh and Z-VEID-fmk were from R&D Systems (Abingdon, UK). PD151746 and calpeptin were purchased from Merck Chemicals Ltd (Overijse, Belgium). Chloroquine, 3-methyladenine (3-MA), bafilomycin A1, flavopiridol, TRAIL, Actinomycin D and anti-β-actin (ACTB) antibody were from Sigma-Aldrich (Diegem, Belgium). Anti-sequestosome-1 (SQSTM1/p62) antibody was from BD Biosciences (Erembodegem, Belgium). All other antibodies were from Cell Signaling Technology (Leiden, The Netherlands).
Cytotoxicity assay
PBMCs were seeded in 96-well cell culture plates and assays were performed in triplicate. Cell viability was measured after 6 h (when flavopiridol was used) or 48 h of incubation using the Cell Counting Kit-8 (CCK-8) assay (Dojindo Molecular Technologies, Eke, Belgium). Combination experiments done with an autophagy inhibitor and an HDAC inhibitor were carried out at nonconstant ratios, keeping constant the concentration of the former while varying the doses of the latter.MGCD0103 and VPA were used at concentrations that encompass the clinically relevant concentrations.[14, 15, 16] Chloroquine concentrations were fixed to 5 and 10 μmol/l, thus matching plasma concentrations.[17] The 3-MA is not administered in clinic and was used at concentrations that resulted in 70 and 55% of cell viability after a 48- h treatment (0.3 and 0.6 mmol/l, respectively).When flavopiridol was used, human serum was added to the culture medium instead of bovine serum (there is a significant flavopiridol protein binding in human serum, contrarily to bovine serum), and a short treatment time was chosen (6 h) in order to better reproduce the clinical conditions.[18] A combination of flavopiridol and MGCD0103 was done with a constant ratio design.Drug combination analysis was performed following the median-effect method[19] using CompuSyn software (Combosyn, Inc., Paramus, NJ, USA). Combination index (CI)<1, CI=1 and CI>1 indicate synergism, additive effect, and antagonism, respectively. For the 6-h exposure experiments, CI values could not be determined as the LC50 (lethal concentration 50%) of the drugs was not reached. Therefore, the percent of cell viability was used to determine whether drug combination enhanced or decreased cell death, as recommended by Chou.[19]
Immunoblotting analysis
Cells were lysed in RIPA buffer (Merck Chemicals Ltd) supplemented with protease (Roche, Vilvoorde, Belgium) and phosphatase inhibitor (Sigma-Aldrich) cocktails. SDS–polyacrylamide gel electrophoresis and immunoblotting were done using standard procedures. ImageQuant TL 7.0 software (GE Healthcare, Zeist, The Netherlands) was used for protein quantification.
Analysis of autophagy by flow cytometry
Autophagy was monitored with the Cyto-ID Autophagy Detection Kit (Enzo Life Sciences, Antwerpen, Belgium) using a 488-nm excitable fluorescent probe that selectively stains autophagic compartments. Data were acquired on a BD FACSCanto flow cytometer (BD Biosciences) and were analyzed using the BD FACSDiva software (BD Biosciences).
Analysis of cell viability by flow cytometry
PBMC viability was analyzed according to changes in forward and side scatters, or using Annexin V-APC (BD Biosciences) and propidium iodide (Sigma-Aldrich) staining, as previously described.[14]
Autophagy PCR array assay
The Human Autophagy RT2 Profiler PCR Array (SABiosciences, Venlo, The Netherlands) was used for autophagy gene expression profiling in primary CLL cells. Detection was performed using a ViiA 7 Real-Time PCR System (Applied Biosystems, Halle, Belgium). The data were analyzed by the ΔΔCt method, using The PCR Array Data Analysis Web-based software (Qiagen, Venlo, The Netherlands).
siRNA transfections
The 8 × 106 primary CLL cells were transfected with the Amaxa nucleofection system (Lonza) using either Cell Line Nucleofector Kit V and program U016 or Human B Cell Nucleofector Kit and program U015. Small interference RNAs (siRNAs) were from Qiagen. For single and double transfections, 350 and 250 pmol of each siRNA was used, respectively.HeLa cells were transfected with 100 pmol of siRNA using Lipofectamine 2000 (Life Technologies, Gent, Belgium).
Real-time reverse transcription-PCR
Total RNA was extracted using miRNeasy kit (Qiagen), and real-time PCR was performed using Reverse Transcriptase Core kit (Eurogentec, Seraing, Belgium) and Power SYBR Green PCR Master Mix (Applied Biosystems). The primers were purchased from Eurogentec. Detection was performed using a ViiA 7 Real-Time PCR System (Applied Biosystems).
Statistical analysis
Statistical analysis was carried out using a two-sided t-test, with a P-value of <0.05 considered statistically significant.
Results
MGCD0103 decreases the levels of autophagy-related proteins in primary CLL cells
To investigate whether MGCD0103 modulates autophagy in CLL cells, we first analyzed its effect on the levels of SQSTM1 protein, a known autophagy substrate.[20] CLL cells from 14 patients were treated during 24 h with MGCD0103 (3 μmol/l) according to previously described considerations.[14]MGCD0103 considerably reduced SQSTM1 levels in 11 out of 14 CLL samples (Figure 1a). The differences observed were likely because of interindividual variability in patients, as CLL samples were randomly chosen from patients with diverse Rai stages and prognostic factors (Supplementary Table 1).
Figure 1
MGCD0103 decreases the levels of autophagy-related proteins in primary CLL cells. Immunoblotting analysis of protein extracts from PBMCs incubated in the absence or presence of MGCD0103 (0.5 or 3 μmol/l, as indicated) for 24 h. Autophagy-related proteins are indicated, as well as ACTB that was used as a loading control. (a) Shown are representative blots from the samples of 14 patients. The expression levels of SQSTM1 in MGCD0103-treated cells relative to the control and normalized to ACTB levels are indicated. (b, c) Shown are two representative blots from eight independent experiments.
We also assessed the expression levels of the phosphatidylethanolamine-conjugated form of microtubule-associated protein 1 light chain (MAP1LC3-II), required for vesicle elongation and autophagosome formation, the autophagy-related regulator ATG5 (as ATG5-ATG12 conjugate) and beclin-1 (BECN1), required for early steps of autophagy. Similar to SQSTM1, MGCD0103 decreased the levels of above-mentioned proteins (Figures 1b and c). This effect was already apparent at the clinically relevant dose of 0.5 μmol/l and mirrored apoptosis levels (see poly (ADP-ribose) polymerase cleavage).
MGCD0103 decreases the autophagic flux in primary CLL cells
Reduced levels of SQSTM1 and MAP1LC3-II may indicate either an induction or a decrease in the autophagic flux.To assess the autophagic flux, time course analysis of MAP1LC3-II and SQSTM1 expression was performed (Figures 2a and b). When cells were exposed to MGCD0103 (3 μmol/l), the decrease in MAP1LC3-II levels could be observed at early time points (after 2–3 h). This decrease did not result from an increased MAP1LC3 turnover as no accumulation of MAP1LC3-II was detected in the presence of chloroquine that prevents autophagosome–lysosome fusion. At the time points analyzed, MAP1LC3-II levels were lower in MGCD0103-treated cells than in untreated cells, even in the presence of chloroquine. Interestingly, SQSTM1 levels significantly decreased only after 19–48 h, several hours after the drop in MAP1LC3-II, and they were not restored by chloroquine, suggesting that they were reduced by an autophagy-independent mechanism. Similar results were obtained with the autophagosome–lysosome fusion inhibitor, Bafilomycin A1 (Supplementary Figure 1a). These data suggest that MGCD0103 inhibits the autophagic flux in primary CLL cells, an effect that was also observed at the clinically relevant dose of 0.5 μmol/l (Supplementary Figure 1b).
Figure 2
MGCD0103 decreases the autophagic flux in primary CLL cells. (a, b) The effect of MGCD0103 (3 μmol/l) on autophagy was assessed by immunoblotting in the presence of chloroquine in time course experiments. ACTB was used as a loading control. Two representative blots (a and b) from four independent experiments are shown. The expression levels of proteins in treated cells relative to the corresponding untreated control and normalized to ACTB levels are indicated. (c, d) Autophagy was assessed by flow cytometry using the Cyto-ID green autophagy dye. For the left panel in (c), single-cell lymphocyte population was gated in R1 (live and apoptotic cells), whereas apoptotic cells were gated in R2 on the basis of cell shrinkage (decreased in forward scatter (FSC)) and increase in granularity (increase in side scatter (SSC)). Shown on the right panel of (c) are the distributions of the dye green fluorescence (channel FL1) within each R1 population. Dot plots and Cyto-ID green fluorescence intensity from a representative experiment are shown in (c). (d) Results are represented by histograms as mean Cyto-ID green fluorescence of treated cells relative to control cells (dark bars). The percentage of apoptotic cells represents the percentage of cells in R2 (bright bars). The mean values±s.d. (n=8) are shown. Values are compared with the corresponding control value. *P<0.05 and **P<0.01.
Further confirmation of this finding was obtained by flow cytometry using Cyto-ID fluorescent marker of autophagic compartments (Figures 2c and d, and Supplementary Figures 2a and b). As expected, chloroquine generated an increase in fluorescence intensity because of autophagosome accumulation. Either alone or in the presence of chloroquine, MGCD0103 decreased the fluorescence intensity of the dye, suggesting that it reduced autophagosome formation in primary CLL cells. Thus, MGCD0103 decreased the amount of autophagic vacuoles while increasing the percentage of apoptotic cells.
MGCD0103 inhibits autophagy through activation of the PI3K/AKT/mTOR pathway and caspases
To analyze the molecular mechanisms behind MGCD0103-mediated inhibition of autophagy in primary CLL cells, we first investigated the involvement of the PI3K/AKT/mTOR pathway, a major signaling cascade that regulates autophagy.[21] To this end, we examined the phosphorylation of AKT and mTOR, as well as that of the mTORC1 substrate, the eukaryotic translation initiation factor 4E binding protein 1 (EIF4EBP1). Accumulation of p-AKT (Ser473), p-mTOR and p-EIF4EBP1 (Thr37/46) was observed at early time points (between 2 and 6 h depending on the protein) following treatment with 3 μmol/l MGCD0103 (Figure 3a, see also Supplementary Table 2 for blot quantification), thus consistent with MGCD0103 mediating the early activation of the PI3K/AKT/mTOR pathway. Loss of these phosphorylated forms, already observed after 6 h for p-AKT and 4 h for p-EIF4EBP1, is observed in all cases at later time points (21 and 32 h).
Figure 3
MGCD0103 inhibits autophagy in primary CLL cells through activation of the PI3K/AKT/mTOR pathway and caspases. (a, b) The effect of MGCD0103 on the PI3K/AKT/mTOR pathway was assessed in primary CLL cells by immunoblotting through the analysis of the phosphorylation status of key regulators. (a) Time course experiments were performed with 3 μmol/l of MGCD0103 and (b) the effect of the 24-h treatment was analyzed using two concentrations of MGCD0103 (0.5 and 3 μmol/l, as indicated). Relative protein quantification is available in Supplementary Table 2. Blots from three independent experiments are shown. (c, d) MGCD0103 decreases the autophagic flux in primary CLL cells in a caspase-dependent manner. Cells were incubated for 24 h alone or in the presence of MGCD0103 (3 μmol/l) or VPA (4 mmol/l), with or without chloroquine (CQ; 20 μmol/l), bafilomycin A1 (Baf; 20 nmol/l), 3-MA (1 mmol/l), bortezomib (Bort; 2 nmol/l) or Q-VD-OPh (Q-VD; 10 μmol/l). Caspase and proteasome inhibitors were added to PBMCs 1 h before and autophagy inhibitors 1 h after MGCD0103 or VPA. Two representative blots (c and d) from five independent experiments are shown. The levels of indicated proteins were analyzed by immunoblotting, using ACTB as a loading control. The expression levels of proteins in treated cells relative to the untreated control and normalized to ACTB levels are indicated.
To gain more insight into the later-stage impact of MGCD0103 on the PI3K/AKT/mTOR pathway, we next investigated its activation after a 24-h treatment using concentrations of 0.5 and 3 μmol/l. Whereas increased phosphorylation of AKT (Thr308), mTOR, and EIF4EBP1 was still observed in cells treated with 0.5 μmol/l, global dephosphorylation occurred with 3 μmol/l of MGCD0103 (Figure 3b and Supplementary Table 2).Altogether, these results demonstrate that MGCD0103 can induce, in a time and dose-dependent manner, the activation of the PI3K/AKT/mTOR cascade. The early activation of this pathway may explain the rapid MGCD0103-mediated inhibition of autophagy in primary CLL cells (Figures 2a and b). However, prolonged incubation with MGCD0103 (3 μmol/l) amplified autophagy inhibition (Figures 2a and b), whereas the PI3K/AKT/mTOR pathway was by then almost completely inhibited—an event that normally activates autophagy—suggesting that another mechanism impairs autophagy at late time points. We, therefore, analyzed the effects of autophagy blockade, as well as proteasome and caspase inhibition on the levels of SQSTM1 and MAP1LC3-II in primary CLL cells after a 24-h incubation with MGCD0103 (3 μmol/l; Figures 3c and d). As previously shown (Figure 2), MGCD0103 reduced the levels of both proteins even in the presence of chloroquine (compare lanes 1 and 2, and lanes 4 and 5). Besides, the loss of SQSTM1 and MAP1LC3-II bands was not prevented by the proteasome inhibitor, bortezomib. Failure of chloroquine to inhibit MGCD0103-induced decrease in SQSTM1 and MAP1LC3-II levels was also observed with two other autophagy inhibitors, bafilomycin A1 (compare lanes 10 and 11) and 3-MA (autophagy initiation inhibitor; lanes 13 and 14), ruling out a molecule-dependent effect of chloroquine. Similarly, simultaneous inhibition of autophagy and the proteasome did not prevent the loss of SQSTM1 and MAP1LC3-II in response to MGCD0103. In contrast, the pan-caspase inhibitor Q-VD-OPh completely prevented the decrease in protein levels elicited by MGCD0103 (compare lanes 19 and 20). Altogether, these results suggest that MGCD0103-mediated autophagy inhibition results from the activation of the PI3K/AKT/mTOR pathway followed by caspase-mediated degradation of autophagy-related proteins. This effect is not a common property of HDAC inhibitors as VPA, an HDAC I and IIa inhibitor, did not decrease the autophagic flux in primary CLL cells, as assessed by the levels of MAP1LC3-II in the presence of chloroquine and bafilomycin A1 (Figures 3c and d).Contrarily to other autophagy-related proteins, MAP1LC3 has been proposed to be neither a caspase nor a calpain-1 substrate in vitro.[22] Our data show that MAP1LC3-I and MAP1LC3-II levels decrease in MGCD0103-treated primary CLL cells (Figures 1b and c). One mechanism that may contribute to the drop in MAP1LC3-I is the observed reduction in ATG4B amounts, the enzyme that generates MAP1LC3-I (Supplementary Figures 3a and b). The decrease in ATG4B levels was incompletely inhibited by Q-VD-OPh, suggesting that it is partly caspase dependent. The reduced levels of MAP1LC3-II were likely because of the drop in ATG5 levels observed in the presence of MGCD0103 (Figures 1b and 5b).
Figure 5
MGCD0103-induced inhibition of autophagy is specific to primary CLL cells. (a) PBMCs from healthy donors (n=3) were incubated with or without MGCD0103 (0.5 or 3 μmol/l) and/or chloroquine (CQ; 20 μmol/l) for 24 h. (b, c) The effect of MGCD0103 on autophagy was assessed in cell lines. Cells were incubated with or without MGCD0103 (3 μmol/l) and/or Q-VD-OPh (10 μmol/l for CLL patient PBMCs and 20 μmol/l for cell lines) for 24 h (PBMC, JVM-2 and JVM-3) or 48 h (Mec-1 and MCF-7), and/or chloroquine (CQ; 40 μmol/l) for 24 h. The levels of indicated proteins were analyzed by immunoblotting using ACTB as a loading control. Representative blots from at least three independent experiments are shown in each panel.
MGCD0103 modulates the expression of key autophagy regulators at the transcriptional level
To investigate whether modulation of autophagy-related genes could account for the effects of MGCD0103 on autophagy in primary CLL cells, a screening for gene expression was performed using an autophagy PCR array. A 24-h treatment with MGCD0103 (3 μmol/l) reduced the expression of multiple genes involved in autophagy (Figure 4a). In particular, PIK3C3, PIK3R4, BECN1, AMBRA1 and UVRAG, key components of the BECN1–VPS34 complex,[21] were significantly downregulated, as were ATG7, ATG12, GABARAP, BAD, DRAM1 and HDAC6, the positive regulators of autophagy (Figure 4b). Expression levels of mTOR and AKT1 also decreased. MGCD0103 increased the expression of IFNG (interferon-γ), an activator of ‘defense' autophagy,[23] and TGM2 (transglutaminase type 2), previously associated with either autophagy inhibition[24] or completion.[25] Similar trends were observed with MGCD0103 at 0.5 μmol/l (Figure 4b). The decreased mRNA levels did not result from a global RNA degradation, as demonstrated by experiments using the RNA synthesis inhibitor Actinomycin D (Supplementary Figure 4). Altogether, these data demonstrate that MGCD0103 may also operate at the transcriptional level to inhibit autophagy in primary CLL cells.
Figure 4
MGCD0103 modulates autophagy gene expression at the transcriptional level in primary CLL cells. Screening for autophagy gene expression in PBMCs incubated with or without MGCD0103 for 24 h was performed using an autophagy PCR array. Results represent the mean values of four independent experiments. (a) The scatter plot graphs the expression level (2-ΔCt) of each gene in the control sample versus the MGCD0103 (3 μmol/l) sample. The black line indicates fold changes (2-ΔΔCt) of 1. The pink lines indicate a fold change of 2 in gene expression. (b) Histograms represent the fold up- or downregulation of relative gene expression in primary CLL cells incubated with MGCD0103 (0.5 and 3 μmol/l) for 24 h. When fold change values are >1, the fold regulation is equal to the fold change. When fold change values are <1, the fold regulation is the negative inverse of the fold change. *P<0.05, **P<0.01 and ***P<0.001.
MGCD0103-induced inhibition of autophagy is specific to primary CLL cells
We next tested the selectivity of MGCD0103 toward primary CLL cells by comparing its ability to inhibit autophagy in PBMCs from healthy donors, and in the CLL-derived cell lines Mec-1 and JVM-3, the mantle cell lymphoma cell line JVM-2 and the breast cancer cell line MCF-7.In normal PBMCs, a reduction in the levels of MAP1LC3-II upon MGCD0103 treatment was observed that was alleviated by the presence of chloroquine (Figure 5a), suggesting that MGCD0103 did not modulate the autophagic flux.In the cell lines, and in contrast to primary CLL cells, MGCD0103 increased the levels of MAP1LC3-II and failed to decrease ATG5-ATG12 levels (Figure 5b). A slight decrease in SQSTM1 levels was observed in Mec-1 and MCF-7 cells, and MGCD0103 treatment decreased BECN1 expression in all cell lines. However, the impact of MGCD0103 in these cells persisted in the presence of Q-VD-OPh, indicating that it was caspase independent (Figure 5b). Moreover, when treated with MGCD0103+chloroquine, the cell lines showed increased levels of MAP1LC3-II and restoration of SQSTM1 amounts (in JVM-3 and MCF-7; Figure 5c). These results demonstrate that, contrarily to primary CLL cells, MGCD0103 induces autophagy in cell lines.
Activation of CAPN1 is involved in the decreased autophagic flux in MGCD0103-treated cells from some CLL samples
We previously demonstrated that MGCD0103 induces the caspase-mediated activation of calpains in primary CLL cells.[14] Calpains can cleave ATG5, thus provoking a switch from autophagy to apoptotic cell death.[26, 27] To understand the role of calpains in MGCD0103-induced inhibition of autophagy, we used two inhibitors of the major ubiquitous calpains, calpain-1 (CAPN1) and calpain-2 (CAPN2): PD151746 (PD), which specifically inhibits CAPN1, and calpeptin that inhibits both CAPN1 and CAPN2. The effects of these inhibitors on MGCD0103-mediated decrease in autophagy proteins levels varied from one CLL sample to another (Supplementary Figure 5). However, in at least some cases, CAPN1 was involved in the cleavage of autophagy-related proteins in MGCD0103-treated CLL cells (Supplementary Figure 5b). Variations in the levels of CAPN1 and CAPN2 mRNA, as assessed by real-time reverse transcription-PCR (data not shown), could not explain the differences observed between patient samples.We then investigated in more detail the protease-mediated cleavage of SQSTM1, as its degradation has been widely used as a hallmark of autophagy activation. In MGCD0103-treated CLL cells, the pattern of SQSTM1 cleavage products included bands of ca. 30 and 37 KDa (Supplementary Figures 6a and b). Presence of the 30-KDa band was insensitive to PD151746 (Supplementary Figure 6a, lane 3 and Supplementary Figure 6b, lanes 3 and 4), whereas it was considerably blocked by caspase-6 (CASP6) inhibitor Z-VEID-fmk (Supplementary Figure 6b, lanes 5 and 6), consistent with the previously reported role of CASP6 in SQSTM1 cleavage.[22] Besides, Q-VD-OPh significantly reduced the levels of the 30- and the 37-KDa fragments (Supplementary Figures 6a and b), indicating that SQSTM1 cleavage in CLL cells involves not only CAPN1 and CASP6, but also other caspases. Evidence that the observed bands are specific SQSTM1 cleavage products is given in Supplementary Figures 6c and d.A model for MGCD0103-mediated inhibition of autophagy in primary CLL cells is illustrated in Supplementary Figure 7.
Inhibition of autophagy decreases CLL cell viability
Our data suggest that autophagy inhibition might decrease CLL cell survival. To test this hypothesis, we first treated CLL cells with late- or early-stage inhibitors of autophagy (chloroquine and 3-MA, respectively). Both drugs decreased CLL cell viability in a dose-dependent manner (Figure 6a), suggesting that basal autophagy is a survival mechanism in primary CLL cells. To confirm this finding, siRNA-mediated knockdown of key autophagy genes was performed. In agreement with previous reports,[28, 29] primary CLL cells were highly refractory to transfections, probably owing to their quiescent nature. Nevertheless, in three out of seven CLL samples analyzed, introduction of either ATG5, MAP1LC3B, BECN1 or ATG5/BECN1 siRNAs resulted in decreased target gene expression (ranging from 22 to 40% when compared with cells treated with scrambled siRNAs), together with decreased cell viability (Figures 6b–d). These results confirm the prosurvival effect of basal autophagy in primary CLL cells.
Figure 6
Inhibition of autophagy decreases primary CLL cell viability. (a) PBMCs from CLL patients (n=5) were incubated with varying concentrations of chloroquine or 3-MA for 48 h. Viability was determined by a CCK-8 colorimetric assay. Each sample was run in triplicate and was normalized to cells incubated without drug. Data represent the mean values±s.d. (b–d) PBMCs from CLL patients were transfected with autophagy gene-specific or nontargeting scrambled siRNA as indicated. Viability of CLL cells was assessed by flow cytometry following Annexin V-APC/PI staining. Results obtained with three different patient samples at (b) 24 h, (c) 48 h and (d) 72 h after transfection are shown. Viable cells (Annexin V-APC neg/PI neg cells) are represented and expressed relative to scrambled siRNA control, set at 100% viability. Expression levels of targeted genes were analyzed by real-time reverse transcription (RT)-PCR and were normalized to the 28S ribosomal RNA level of the same sample. RT-PCR values are expressed as relative fold change to the scrambled siRNA condition.
The combination of autophagy and HDAC inhibitors potentiates CLL cell death
In order to evaluate the therapeutic potential of regimens combining autophagy and HDAC inhibitors in the treatment of CLL, we tested the cytotoxicity of either MGCD0103 or VPA in combination with chloroquine or 3-MA. Hence, we followed the median-effect method[19] using two concentrations of each of the autophagy inhibitors and various concentrations of the HDAC inhibitors, chosen based on the considerations detailed under Materials and Methods.When MGCD0103 was used at the clinically relevant concentration of 0.4 μmol/l, its association with chloroquine displayed nearly additive effect (0.93-MA led to a clear synergism (0.3MGCD0103 (0.1 and 0.2 μmol/l) (small arrows). Finally, combinations of VPA (at the clinically relevant concentration of 1 mmol/l) with 0.3 and 0.6 mmol/l of 3-MA displayed a slightly synergistic to nearly additive effect (0.85chloroquine was at best nearly additive (arrows in Figure 7c). Supplementary Table 3 recapitulates the CI values of the drug combinations discussed above and their biological description.
Figure 7
The combination of HDAC inhibitors and autophagy inhibitors synergistically/additively kills CLL cells at clinically relevant concentrations. Combination analyses were performed following the median-effect method.[19] PBMCs from CLL patients (n=5) were exposed to an HDAC inhibitor (MGCD0103 (MGCD) or VPA) and an autophagy inhibitor (chloroquine (CQ) or 3-MA) simultaneously for 48 h. Various concentrations of HDAC inhibitors (shown as blue dots or red squares, and increasing from left to right along the x axis) were combined with fixed doses of CQ (5 and 10 μmol/l) or 3-MA (0.3 and 0.6 mmol/l). (a, b) The concentrations of MGCD0103 used for these experiments were (in μmol/l) 0.05, 0.1, 0.2, 0.4, 0.8 and 1.6, and (c, d) those of VPA were (in mmol/l) 0.25, 0.5, 1, 2, 4 and 8. CIs for different levels of cell death (fraction affected) were calculated using the CompuSyn software. CI<1, CI=1 and CI>1 indicate synergism, additive effect and antagonism, respectively.
Collectively, these results demonstrate that inhibition of autophagy may synergize or act additively with HDAC inhibitors at clinically achievable concentrations to kill CLL cells.
The combination of MGCD0103 with flavopiridol considerably enhances CLL cell death
Our data suggest that MGCD0103 could enhance the efficiency of therapeutic molecules, such as the cyclin-dependent kinase (CDK) inhibitor flavopiridol, that induce a protective autophagic response in primary CLL cells.[30]To test this hypothesis, we treated CLL cells with combinations of MGCD0103 and flavopiridol during 6 h—a time period close to the clinically effective schedule of administration of flavopiridol in CLL patients.[18] Although neither drug had a significant effect on cell survival when used at clinically relevant concentrations (0.4 μmol/l (MGCD0103) and 1.5 μmol/l (flavopiridol)), under these conditions, their combination clearly decreased cell viability (Table 1, P(flavopiridol versus flavopiridol+MGCD0103)=0.03; P(MGCD0103 versus flavopiridol+MGCD0103)=0.01).
Table 1
Viability (%) of chronic lymphocytic leukemia (CLL) cells after a 6-h treatment with MGCD0103 and flavopiridol alone or in combination
MGCD0103 (μM)
0
0.05
0.1
0.2
0.4
0.8
Flavopiridol (μM)
0
100
104.12±6.51
96.91±8.16
101.15±10.50
97.33±9.30
86.74±14.42
0.1875
92.90±14.70
78.16±19.59
0.375
96.22±14.51
80.59±20.37
0.75
89.32±16.90
79.88±23.77
1.5
92.89±11.64
70.68±14.71
3
83.42±9.21
68.70±16.50
Peripheral blood mononuclear cells (PBMCs) from CLL patients (n=5) were incubated with various concentrations of MGCD0103 and flavopiridol, either alone or simultaneously, for 6 h. Combination experiments were done using a constant ratio design. Viability was determined by a CCK-8 colorimetric assay. Each sample was run in triplicate and was normalized to cells incubated without drug. Data represent the mean values±s.d.
These data demonstrate that the association of MGCD0103 with the autophagy inducer flavopiridol potentiates CLL cell death.
Discussion
Autophagy may promote either cell survival or cell death; however, its role in CLL remains unclear. In this study, we found that MGCD0103 decreases the autophagic flux in primary CLL cells. In addition, we provided evidence that basal autophagy functions in CLL as a pro-survival mechanism whose disruption potentiates cell death induced by HDAC and CDK inhibitors.We previously reported that MGCD0103 triggers a cell death amplification loop involving caspases and calpains in primary CLL cells.[14] The present report shows that MGCD0103 inhibits autophagy through the activation of the PI3K/AKT/mTOR pathway followed by activation of caspases and CAPN1, leading to the degradation of autophagy-related proteins in primary CLL cells. Besides, our data suggest that MGCD0103-induced autophagy blockade may also result from transcriptional downregulation of key regulators.The existence of an interplay between apoptosis and autophagy has been well documented.[22, 27, 31, 32, 33] Indeed, the caspase-mediated cleavage of BECN1 inhibited BECN1-induced autophagy and generated pro-apoptotic BECN1 fragments that triggered cytochrome c release from mitochondria.[22, 33] Similarly, release of cytochrome c was induced following calpain-mediated generation of an ATG5 fragment.[27] In line with these observations, MGCD0103-induced cleavage of BECN1 and ATG5 observed in the present study may be part of the death amplification loop activated in primary CLL cells.The ATG5 gene product is a crucial proteolytic target for mechanisms aiming to disrupt/modulate autophagy. Using a cell-free system, Yousefi et al.[27] have shown that ATG5 can be cleaved by calpains, but not caspases 3, 6, 7, 8 and 9. However, our results obtained ex vivo suggest that caspases are the major proteases responsible for MGCD0103-induced ATG5 cleavage in primary cells, either directly or, as observed in some CLL patients, through activation of CAPN1. These findings suggest that a caspase different from the aforementioned caspases could cleave ATG5 in a calpain-independent manner.The role of autophagy in CLL has remained controversial. Thus, resistance to dasatinib has been correlated to autophagy induction,[34] and cell death was induced in experimental systems where autophagy was inhibited either by chloroquine or expression of miR-130a.[12] On the other hand, treatment of CLL cells with dexamethasone induced autophagic cell death.[13] More recently, it was shown that many stimuli can induce autophagy in CLL cells; however, only endoplasmic reticulum stress-inducing agents induced protective autophagy.[30] Consistent with previous reports,[12] we found that pharmacological inhibitors of autophagy decreased CLL cell viability in a dose-dependent manner. In addition, the loss of viability observed in cells where partial knockdown of ATG5, BECN1 and MAP1LC3B was achieved by siRNA confirmed the survival-promoting effect of basal autophagy in primary CLL cells. Moreover, we demonstrated that inhibition of autophagy potentiates HDAC inhibitor-induced cell death in CLL cells at clinically relevant concentrations. Although chloroquine and 3-MA may have off-target effects, our data suggest that targeting autophagy may enhance the therapeutic effects of HDAC inhibitors in CLL, consistent with previous findings in other cancer models.[10, 35]Autophagy plays a central role in the immune response to cancer,[11, 36, 37] and the immunomodulatory effects of autophagy inhibitors (chloroquine and hydroxychloroquine) has been exploited in the treatment of autoimmune disorders.[38, 39] Unfortunately, the immunomodulatory properties of these inhibitors have an adverse effect on antitumor immunity.[11, 40] Thus, clinically promising chemotherapeutical strategies based on combinations of autophagy inhibitors with conventional anticancer drugs currently face the limitation that autophagy inhibition is not restricted to cancer cells but also affects immune cells.Chloroquine has previously been shown to neutralize ex vivo the protective autophagy elicited in CLL cells by flavopiridol,[30] a CDK inhibitor that induces high response rates in heavily pretreated CLL patients, including high-risk patients.[41, 42] Unlike chloroquine, we found that the autophagy-inhibiting properties of MGCD0103 specifically target CLL cells but not the other leukemic and nonleukemic cells, including normal PBMCs. Importantly, MGCD0103 counteracted autophagy, a mechanism of resistance to cell death elicited by the CDK inhibitor, and potentiated the cytotoxic effect of flavopiridol. This finding opens new horizons to circumvent the immunomodulatory effects of chloroquine and hydroxychloroquine.Recently, Tenovin-6, an inhibitor of the NAD(+)-dependent class III HDACs, has been shown to inhibit the late stages of autophagy in CLL cells.[43] Suppression of autophagy by inhibitors of zinc-dependent HDACs had hitherto been reported only in cardiomyocytes[44] and, more recently, in myeloid leukemia where the pro-survival role of autophagy was also documented.[45] Instead, HDAC inhibitors have been described to induce autophagy by a variety of mechanisms including transcriptional induction of MAP1LC3[5] and BECN1,[46] inactivation of mTOR signaling,[5, 7] induction of endoplasmic reticulum stress response[7] and production of reactive oxygen species.[47] Although MGCD0103 induced autophagy in cancer cell lines, it decreased the autophagic flux in primary CLL cells. As observed with other anticancer drugs such as metformin,[48, 49] autophagy modulation by HDAC inhibitors appears to be cell type dependent. Moreover, our data underline the well-documented notion that cell lines do not recapitulate all the features of the original primary tumors,[50, 51, 52] a caveat that must be borne in mind when studying the pathology of CLL.Autophagy regulation by HDAC inhibitors can occur at the epigenetic level through modulation of autophagy gene expression, as we and others showed.[5, 53] However, targets of HDACs include nonhistone proteins.[54] In this context, additional mechanisms whereby HDACs may contribute to autophagy include HDAC6-mediated deacetylation of cortactin, enhancing autophagosome-lysosome fusion,[55] or the regulation, by HDAC6, of the transport of aggregates and autophagic machinery components to the aggresome.[56] MGCD0103 is not an HDAC6 inhibitor; however, we cannot rule out that MGCD0103-mediated downregulation of HDAC6 expression (Figure 4b) may contribute to the regulation of autophagy in primary CLL cells.Because SQSTM1 protein is incorporated into autophagosomes and degraded by autophagy,[20, 57, 58] its degradation has been widely used as a hallmark of autophagy activation.[20, 57, 59] Here, we showed that SQSTM1 can be degraded by caspases and CAPN1 independently of autophagy, in agreement with the results of Norman et al.[22] and Pham et al.[60] These findings are in line with the myriad of interacting partners and cellular functions of SQSTM1 beyond its role in autophagy[61] and should prompt researchers to caution in drawing conclusions when interpreting SQSTM1 levels.The contribution of autophagy to microenvironmental signals and CLL progression in the proliferation niches remains to be explored. Similarly, further investigation will be necessary to evaluate whether the role of autophagy in CLL is dependent on the stage of the disease, the genetic aberration profile or the expression of some prognostic markers. Addressing these questions will help understanding how CLL patients may best benefit from a therapeutic strategy involving alteration of autophagy.
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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; Thomas G McWilliams; Fatima Mechta-Grigoriou; Tania Catarina Medeiros; Diego L Medina; Lynn A Megeney; Klara Megyeri; Maryam Mehrpour; Jawahar L Mehta; Alfred J Meijer; Annemarie H Meijer; Jakob Mejlvang; Alicia Meléndez; Annette Melk; Gonen Memisoglu; Alexandrina F Mendes; Delong Meng; Fei Meng; Tian Meng; Rubem Menna-Barreto; Manoj B Menon; Carol Mercer; Anne E Mercier; Jean-Louis Mergny; Adalberto Merighi; Seth D Merkley; Giuseppe Merla; Volker Meske; Ana Cecilia Mestre; Shree Padma Metur; Christian Meyer; Hemmo Meyer; Wenyi Mi; Jeanne Mialet-Perez; Junying Miao; Lucia Micale; Yasuo Miki; Enrico Milan; Małgorzata Milczarek; Dana L Miller; Samuel I Miller; Silke Miller; Steven W Millward; Ira Milosevic; Elena A Minina; Hamed Mirzaei; Hamid Reza Mirzaei; Mehdi Mirzaei; Amit Mishra; Nandita Mishra; Paras Kumar Mishra; Maja Misirkic Marjanovic; Roberta Misasi; Amit Misra; Gabriella Misso; Claire Mitchell; Geraldine Mitou; Tetsuji Miura; Shigeki Miyamoto; Makoto Miyazaki; Mitsunori Miyazaki; 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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Per Nilsson; Shunbin Ning; Rituraj Niranjan; Hiroshi Nishimune; Mireia Niso-Santano; Ralph A Nixon; Annalisa Nobili; Clevio Nobrega; Takeshi Noda; Uxía Nogueira-Recalde; Trevor M Nolan; Ivan Nombela; Ivana Novak; Beatriz Novoa; Takashi Nozawa; Nobuyuki Nukina; Carmen Nussbaum-Krammer; Jesper Nylandsted; Tracey R O'Donovan; Seónadh M O'Leary; Eyleen J O'Rourke; Mary P O'Sullivan; Timothy E O'Sullivan; Salvatore Oddo; Ina Oehme; Michinaga Ogawa; Eric Ogier-Denis; Margret H Ogmundsdottir; Besim Ogretmen; Goo Taeg Oh; Seon-Hee Oh; Young J Oh; Takashi Ohama; Yohei Ohashi; Masaki Ohmuraya; Vasileios Oikonomou; Rani Ojha; Koji Okamoto; Hitoshi Okazawa; Masahide Oku; Sara Oliván; Jorge M A Oliveira; Michael Ollmann; James A Olzmann; Shakib Omari; M Bishr Omary; Gizem Önal; Martin Ondrej; Sang-Bing Ong; Sang-Ging Ong; Anna Onnis; Juan A Orellana; Sara Orellana-Muñoz; Maria Del Mar Ortega-Villaizan; Xilma R Ortiz-Gonzalez; Elena Ortona; Heinz D Osiewacz; Abdel-Hamid K Osman; Rosario Osta; Marisa S Otegui; 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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; Miguel A Martin-Acebes; Paloma Martín-Sanz; Camille Martinand-Mari; Wim Martinet; Jennifer Martinez; Nuria Martinez-Lopez; Ubaldo Martinez-Outschoorn; Moisés Martínez-Velázquez; Marta Martinez-Vicente; Waleska Kerllen Martins; Hirosato Mashima; James A Mastrianni; Giuseppe Matarese; Paola Matarrese; Roberto Mateo; Satoaki Matoba; Naomichi Matsumoto; Takehiko Matsushita; Akira Matsuura; Takeshi Matsuzawa; Mark P Mattson; Soledad Matus; Norma Maugeri; Caroline Mauvezin; Andreas Mayer; Dusica Maysinger; Guillermo D Mazzolini; Mary Kate McBrayer; Kimberly McCall; Craig McCormick; Gerald M McInerney; Skye C McIver; Sharon McKenna; John J McMahon; Iain A McNeish; Fatima Mechta-Grigoriou; Jan Paul Medema; Diego L Medina; Klara Megyeri; Maryam Mehrpour; Jawahar L Mehta; Yide Mei; Ute-Christiane Meier; Alfred J Meijer; Alicia Meléndez; Gerry Melino; Sonia Melino; Edesio Jose Tenorio de Melo; Maria A Mena; Marc D Meneghini; Javier A Menendez; Regina Menezes; Liesu Meng; Ling-Hua Meng; Songshu Meng; Rossella Menghini; A Sue Menko; Rubem Fs Menna-Barreto; Manoj B Menon; Marco A Meraz-Ríos; Giuseppe Merla; Luciano Merlini; Angelica M Merlot; Andreas Meryk; Stefania Meschini; Joel N Meyer; Man-Tian Mi; Chao-Yu Miao; Lucia Micale; Simon Michaeli; Carine Michiels; Anna Rita Migliaccio; Anastasia Susie Mihailidou; Dalibor Mijaljica; Katsuhiko Mikoshiba; Enrico Milan; Leonor Miller-Fleming; Gordon B Mills; Ian G Mills; Georgia Minakaki; Berge A Minassian; Xiu-Fen Ming; Farida Minibayeva; Elena A Minina; Justine D Mintern; Saverio Minucci; Antonio Miranda-Vizuete; Claire H Mitchell; Shigeki Miyamoto; Keisuke Miyazawa; Noboru Mizushima; Katarzyna Mnich; Baharia Mograbi; Simin Mohseni; Luis Ferreira Moita; Marco Molinari; Maurizio Molinari; Andreas Buch Møller; Bertrand Mollereau; Faustino Mollinedo; Marco Mongillo; Martha M Monick; Serena Montagnaro; Craig Montell; Darren J Moore; Michael N Moore; Rodrigo Mora-Rodriguez; Paula I Moreira; Etienne Morel; Maria Beatrice Morelli; Sandra Moreno; Michael J Morgan; Arnaud Moris; Yuji Moriyasu; Janna L Morrison; Lynda A Morrison; Eugenia Morselli; Jorge Moscat; Pope L Moseley; Serge Mostowy; Elisa Motori; Denis Mottet; Jeremy C Mottram; Charbel E-H Moussa; Vassiliki E Mpakou; Hasan Mukhtar; Jean M Mulcahy Levy; Sylviane Muller; Raquel Muñoz-Moreno; Cristina Muñoz-Pinedo; Christian Münz; Maureen E Murphy; James T Murray; Aditya Murthy; Indira U Mysorekar; Ivan R Nabi; Massimo Nabissi; Gustavo A Nader; Yukitoshi Nagahara; Yoshitaka Nagai; Kazuhiro Nagata; Anika Nagelkerke; Péter Nagy; Samisubbu R Naidu; Sreejayan Nair; Hiroyasu Nakano; Hitoshi Nakatogawa; Meera Nanjundan; Gennaro Napolitano; Naweed I Naqvi; Roberta Nardacci; Derek P Narendra; Masashi Narita; Anna Chiara Nascimbeni; Ramesh Natarajan; Luiz C Navegantes; Steffan T Nawrocki; Taras Y Nazarko; Volodymyr Y Nazarko; Thomas Neill; Luca M Neri; Mihai G Netea; Romana T Netea-Maier; Bruno M Neves; Paul A Ney; Ioannis P Nezis; Hang Tt Nguyen; Huu Phuc Nguyen; Anne-Sophie Nicot; Hilde Nilsen; Per Nilsson; Mikio Nishimura; Ichizo Nishino; Mireia Niso-Santano; Hua Niu; Ralph A Nixon; Vincent Co Njar; Takeshi Noda; Angelika A Noegel; Elsie Magdalena Nolte; Erik Norberg; Koenraad K Norga; Sakineh Kazemi Noureini; Shoji Notomi; Lucia Notterpek; Karin Nowikovsky; Nobuyuki Nukina; Thorsten Nürnberger; Valerie B O'Donnell; Tracey O'Donovan; Peter J O'Dwyer; Ina Oehme; Clara L Oeste; Michinaga Ogawa; Besim Ogretmen; Yuji Ogura; Young J Oh; Masaki Ohmuraya; Takayuki Ohshima; Rani Ojha; Koji Okamoto; Toshiro Okazaki; F Javier Oliver; Karin Ollinger; Stefan Olsson; Daniel P Orban; Paulina Ordonez; Idil Orhon; Laszlo Orosz; Eyleen J O'Rourke; Helena Orozco; Angel L Ortega; Elena Ortona; Laura D Osellame; Junko Oshima; Shigeru Oshima; Heinz D Osiewacz; Takanobu Otomo; Kinya Otsu; Jing-Hsiung James Ou; Tiago F Outeiro; Dong-Yun Ouyang; Hongjiao Ouyang; Michael Overholtzer; Michelle A Ozbun; P Hande Ozdinler; Bulent Ozpolat; Consiglia Pacelli; Paolo Paganetti; Guylène Page; Gilles Pages; Ugo Pagnini; Beata Pajak; Stephen C Pak; Karolina Pakos-Zebrucka; Nazzy Pakpour; Zdena Palková; Francesca Palladino; Kathrin Pallauf; Nicolas Pallet; Marta Palmieri; Søren R Paludan; Camilla Palumbo; Silvia Palumbo; Olatz Pampliega; Hongming Pan; Wei Pan; Theocharis Panaretakis; Aseem Pandey; Areti Pantazopoulou; Zuzana Papackova; Daniela L Papademetrio; Issidora Papassideri; Alessio Papini; Nirmala Parajuli; Julian Pardo; Vrajesh V Parekh; Giancarlo Parenti; Jong-In Park; Junsoo Park; Ohkmae K Park; Roy Parker; Rosanna Parlato; Jan B Parys; Katherine R Parzych; Jean-Max Pasquet; Benoit Pasquier; Kishore Bs Pasumarthi; Daniel Patschan; Cam Patterson; Sophie Pattingre; Scott Pattison; Arnim Pause; Hermann Pavenstädt; Flaminia Pavone; Zully Pedrozo; Fernando J Peña; Miguel A Peñalva; Mario Pende; Jianxin Peng; Fabio Penna; Josef M Penninger; Anna Pensalfini; Salvatore Pepe; Gustavo Js Pereira; Paulo C Pereira; Verónica Pérez-de la Cruz; María Esther Pérez-Pérez; Diego Pérez-Rodríguez; Dolores Pérez-Sala; 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