Here we report a novel regulatory mechanism for autophagy-mediated degradation of Mycobacterium tuberculosis (Mtb) and specific strategy exploited by the virulent Mtb to evade it. We show while both avirulent (H37Ra) and virulent (H37Rv) mycobacteria could readily localize to autophagosomes, their maturation into autolysosomes (flux) was significantly inhibited by the latter strain. The inhibition of autophagy flux by the virulent strain was highly selective, as it did not perturb the basal autophagy flux in the macrophages. Selective inhibition of flux of Mtb-containing autophagosomes required virulence regulators PhoP and ESAT-6. We show that the maturation of Mtb-containing autophagosomes into autolysosomes required recruitment of the late endosome marker RAB7, forming the intermediate compartment amphisomes. Virulent Mtb selectively evaded their targeting to the amphisomes. Thus we report a crosstalk between autophagy and phagosome maturation pathway and highlight the adaptability of Mtb, manifested by selective regulation of autophagy flux.
Here we report a novel regulatory mechanism for autophagy-mediated degradation of Mycobacterium tuberculosis (Mtb) and specific strategy exploited by the virulent Mtb to evade it. We show while both avirulent (H37Ra) and virulent (H37Rv) mycobacteria could readily localize to autophagosomes, their maturation into autolysosomes (flux) was significantly inhibited by the latter strain. The inhibition of autophagy flux by the virulent strain was highly selective, as it did not perturb the basal autophagy flux in the macrophages. Selective inhibition of flux of Mtb-containing autophagosomes required virulence regulators PhoP and ESAT-6. We show that the maturation of Mtb-containing autophagosomes into autolysosomes required recruitment of the late endosome marker RAB7, forming the intermediate compartment amphisomes. Virulent Mtb selectively evaded their targeting to the amphisomes. Thus we report a crosstalk between autophagy and phagosome maturation pathway and highlight the adaptability of Mtb, manifested by selective regulation of autophagy flux.
Autophagy is a degradation process where cellular cargos are delivered to the lysosomes. Initially considered as a response activated under stress conditions, specifically nutrient stress, autophagy now is known to impact on diverse patho-physiological conditions like aging, neurodegenaration, inflammation and infection12. Recently the new paradigm of selective autophagy has emerged through which damaged cellular organelles or intracellular bacterial pathogens could be selectively targeted to autophagy for degradation. The ability to selectively recognize and target its cargo towards degradation has essentially led to the recognition of the autophagy pathway as an innate defense mechanism3. The autophagy of intracellular pathogen is termed as xenophagy while those of damaged organelle or other cellular cargo as macro-autophagy or simply autophagy4. Not surprisingly therefore, many intracellular pathogens including Listeria, Legionella, Shigella, Salmonella, Coxiella, Group A Streptococcus and Mycobacteria are known to specifically evade autophagy5.Upon infection of macrophages with Mycobacterium tuberculosis (Mtb), the role of phagosome maturation pathway has been well elucidated6. Also known are the mechanisms leading to phagosome maturation arrest that help virulent Mtb escape from being targeted to lysosomes and killing78. For instance it has been convincingly shown that virulent Mtb-containing phagosomes do not acquire late endosome marker RAB7, leading to phagosomal maturation arrest78. Interestingly autophagy is yet another mechanism which can influence the targeting of Mtb to the lysosomes and subsequent killing. Despite several reports on the involvement of autophagy in regulation of Mtb killing91011, how these two processes (autophagy and phagosome maturation) interact with each other and get perturbed by Mtb remains poorly understood.Autophagy involves sequestration of cellular cargo in a double-membrane structure called autophagosomes. Autophagy induction is conventionally monitored as MAP1LC3B (LC3) puncta formation through microscopy. It emerges now, autophagy induction does not always lead to degradation of the cargo. Degradation typically involves fusion of autophagosomes with the lysosomes thereby forming autolysosomes and subsequent action of lysosomal hydrolases. However during the degradation process, LC3 on the inner membrane of autophagosomes too gets degraded due to the activity of lysosomal hydrolase12. Therefore when active autophagic degradation is taking place, LC3 would be constantly degraded leaving only the outer membrane associated LC3 intact and thereby making it difficult to accurately assess autophagy induction. The degradation of LC3 however can be blocked by vacuolar ATPase inhibitors like bafilomycin A1 or lysosomal protease inhibitors like E64-d and pepstatin A12. Strangely several studies in the past, which showed an important role for autophagy in case of Mtb infections, did not monitor autophagy flux91314. In some studies however, in case of Mtb infections autophagy flux as a means of bacterial degradation were monitored151617. One such report suggests strain dependent variations in autophagy induction which also correlated with the autophagic degradation17. Yet another study identified the immunity regulator molecule TBK1 as key regulator of autophagy maturation15.In the present study we aimed to investigate the autophagy flux in THP-1 macrophages upon Mtb infection in detail using laboratory strains H37Ra (avirulent) and H37Rv (virulent). Interestingly both the virulent and avirulent strains localized to the autophagosomes. Later in the infection, the flux of Mtb-containing autophagosomes was specifically inhibited by the virulent Mtb. We then show that the inhibition of autophagy flux by H37Rv was the result of its ability to block recruitment of RAB7 on Mtb-containing autophagosomes. Therefore through this study we report a RAB7-dependent autophagy pathway of mycobacterial killing in macrophages.
The laboratory strains H37Rv and H37Ra of Mtb, consistent with previous reports, showed distinct survival ability within the macrophages (Fig. S1A)181920. To check how autophagy gets regulated under the two conditions, we monitored targeting of H37Ra or H37Rv to LC3 positive autophagosomes by immuno-staining followed by confocal microscopy. THP-1 macrophages were infected with H37Ra or H37Rv at 1:10 MOI following the protocol described previously10. We monitored autophagosome targeting of the two strains at 6, 12, 24, 48 and 72 hours post-infection. Throughout the course of infection, both H37Ra and H37Rv efficiently co-localized with LC3 containing compartments (Fig. 1A). The antibody used to stain endogenous LC3 was highly specific and did not show any cross-reactivity with the Mtb (Fig. S1B and S1C). We calculated the M1 Coefficient with respect to Mtb (herein after referred to as co-localization coefficient, see methods) to measure co-localization of both the strains to autophagosomes. In parallel we also had groups where samples were treated with vacuolar ATPase inhibitor Bafilomycin A1 (BafA1, 100 nM) for three hours before the end of each of the time points. Treatment with BafA1 inhibits LC3 degradation upon maturation by blocking the acidification of autolysosomes. We observed a significant increase in the co-localization coefficient of H37Ra with LC3 in BafA1 treated samples relative to the untreated ones from 24 hours post infection (Fig. 1B). Importantly no such increase was observed in case of H37Rv across all time points (Fig. 1C).
PMA differentiated (20 ng/ml, 24 hours) THP-1 macrophages were infected with PKH67 (green) labelled H37Ra or H37Rv at MOI of 1:10 (methods). Autophagosomes were visualized by LC3 immuno-staining at 6, 12, 24, 48 and 72 hours post infection with and without BafA1 treatment (100 nM, 3 hr). (A) Representative images showing co-localization of both H37Ra and H37Rv (green) to autophagosomes (LC3, red) at 48 hours post infection. Panels (B,C) show Co-localization Coefficient M1 of Mtb and LC3 for H37Ra and H37Rv infection, respectively with and without BafA1 treatment (Mean ± Standard Error Measurements, *p < 0.05). Panel (D) shows representative images of Mtb-infected mouse BMDMs with LC3 (red) at 48 hours post infection with and without BafA1. Panel E shows the corresponding quantification of the dataset (mean ± SEM, **p < 0.01). Panel (F) shows LC3 immunoblots from the cell lysates of H37Ra or H37Rv infected macrophages as well as uninfected control macrophages at 6 and 48 hours post infection. Cells were treated with BafA1 (100 nM, 3 hr) to assess autophagy flux. Panel (G) shows representative images of Mtb in autolysosomes (LC3:LysoTracker; (blue:red)) at 48 hours post infection. The plot for the same at 6, 12, 24, 48 and 72 hours post infection is depicted in Panel (F) (Mean ± Standard Error Measurements, *p < 0.05).
We also tested these results in mouse bone marrow derived primary macrophages (BMDMs). Consistent with the results above, BafA1 treatment in BMDMs led to an increase in the co-localization coefficient of H37Ra and LC3, while there was no effect of BafA1 treatment in the case of H37Rv (Fig. 1D,E). Interestingly, Western blot analysis of LC3 in the whole cell lysates from H37Ra or H37Rv infected as well as uninfected THP-1 macrophages showed increased levels of lipidated LC3 (LC3II, Fig. 1F) upon BafA1 treatment, implying maturation of autophagosomes at certain basal state in these cells. We also noted both in THP-1 macrophages and in BMDMs, presence of autophagosomes that did not contain either H37Ra or H37Rv (arrows in Fig. 1A,D).Differential flux of H37Ra and H37Rv containing autophagosomes was also confirmed by monitoring co-localization of Mtb with autolysosomes (Fig. 1G,H). Since BafA1 treatment diminishes LysoTracker staining of lysosomes, we used lysosomal protease inhibitors E64-d and pepstatin A to monitor H37Ra or H37Rv in LC3:LysoTracker double positive compartments representing autolysosomes. We observed a significantly higher percentage of H37Ra in autolysosomes, as compared to H37Rv, from 24 hour post infection (Fig. 1H). We also noted, in both the cases, presence of LC3:LysoTracker double positive compartments that did not contain any Mtb (Fig. 1G, arrows).
Mycobacterium tuberculosis PhoP and ESAT-6 help H37Rv inhibit autophagy flux
The strain H37Ra differs from H37Rv mainly due to a point mutation in the master regulator gene PhoP21 and expression of wild-type (WT) PhoP (from H37Rv) in H37Ra is shown to revert the virulent phenotype2122. We asked whether PhoP, a known Mtb virulence regulator, could help H37Rv modulate host xenophagy flux. We monitored co-localization of WT-PhoP complemented H37Ra strain (H37Ra:PhoP) with LC3 in THP-1 macrophages. PhoP complementation of H37Ra was confirmed by real-time analysis of several genes known to be regulated by PhoP (Fig. S2). The co-localization coefficient of H37Ra:PhoP with LC3 did not show any increase upon BafA1 treatment at 48 hours post infection (Fig. 2A). This response was similar to that of H37Rv at 48 hours post infection (Fig. 1A,C). Subsequently, H37Ra:PhoP had significantly higher intracellular survival with respect to H37Ra at 48 hours post infection (Fig. 2B). Partial rescue of the PhoP complemented strain further confirmed the association of autophagic flux with Mtb killing.
Figure 2
Mycobacterium tuberculosis PhoP and ESAT-6 help H37Rv inhibit autophagy flux.
H37Ra was complemented with wild type phoP (called as H37Ra:PhoP strain). Panel A shows M1 co-localization coefficient of H37Ra:PhoP with LC3 in the presence or absence of BafA1 treatment, 48 hours post infection. Panel (B) shows relative survival percentage in THP-1 macrophages with respect to H37Rv, H37Ra or H37Ra:PhoP at 48 hours post-infection (mean ± SD, *p-value < 0.05). M1 co-localization coefficient of ∆ESAT-6 mutant of H37Rv with LC3 compartment in BafA1 treated and untreated condition is shown in 2C (mean ± SEM, **p < 0.001). In 2D, relative survival was estimated in H37Rv and ∆ESAT-6 infected THP-1 macrophages, 48 hours post-infection. The ∆ESAT-6 strain infected cells were treated with 3-MA (5 mM, 12 hours) to observe their rescue upon autophagy inhibition (mean ± SD, *p-value < 0.05, **p-value < 0.001).
The Mtb PhoP is a global transcriptional factor involved in regulating the expression of RD1 region. H37Ra shows much diminished secretion of ESAT-6, the major antigen on RD1 locus and a well-known mycobacterial virulence effector2123. To test if PhoP mediated block in the autophagy flux was effected by ESAT-6, we used ESAT-6 deleted mutant of H37Rv (∆ESAT-6). BafA1 treatment led to significant increase in the co-localization of ∆ESAT-6 strain with LC3 (Fig. 2C). To note here is that the block in autophagy flux observed in case of H37Rv was released with the deletion of ESAT-6. As expected, ∆ESAT-6 strain showed compromised survival in the THP-1 macrophages compared to the wild type H37Rv (Fig. 2D). Moreover treatment with 3-MA, an autophagy inhibitor, was able to rescue ∆ESAT-6 from killing (Fig. 2D).
H37Rv inhibits amphisome formation
We next wanted to understand the cellular events in the host that gets perturbed by virulent Mtb in order to inhibit autophagy flux. Maturation of autophagosomes involves direct fusion with the lysosome to form auto-lysosome or they can first recruit RAB7 to form amphisomes which eventually fuse with the lysosomes224. It is well known that H37Rv inhibits RAB7 recruitment to escape lysosomal targeting and killing8. Therefore, we tested whether RAB7 recruitment on autophagosomes (amphisomes) could also represent a mechanism of H37Rv to evade lysosomal fusion. Therefore, we monitored co-localization of H37Ra and H37Rv to LC3-RAB7 double positive compartment (hereby defined as amphisomes) at 48 hours post-infection.As expected we observed significantly higher co-localization of H37Ra with either LC3 or RAB7 as compared to H37Rv (Fig. 3A,B). Consistent with that, the percentage of H37Ra was significantly higher in amphisome (LC3:RAB7 double positive) as compared to H37Rv at 48 hours post infection (Fig. 3C). However, LC3-RAB7 co-localization, representing overall amphisome population in the cell, was similar for both the strains. These results clearly suggest that RAB7 recruitment to autophagosomes is significantly higher in H37Ra as compared to H37Rv. Therefore, we next tested whether the inhibition of autophagic flux by virulent Mtb is associated with RAB7 recruitment.
Figure 3
Virulent Mtb inhibits amphisome formation.
Co-localization of H37Ra and H37Rv (green) to LC3 (red) and RAB7 (blue) were examined at 48 hours post-infection. Representative images are shown in panel (A). Panel B shows the plot of Co-localization Coefficient of Mtb to LC3 (Mtb:LC3), Mtb to RAB7 (Mtb:RAB7) and LC3 to RAB7 (LC3:RAB7) at 48 hours post infection (Mean ± SEM, *p < 0.05, **p < 0.001). Panel C shows percentage of Mtb in LC3-RAB7 amphisomes at 48 hours time point (Mean ± SEM, *p-value < 0.05). Panel (D) shows the representative images of H37Ra and H37Rv in amphisomes (white arrow). Scale bar represents 5 μm.
Exclusion of RAB7 from Mtb-containing autophagosome allows H37Rv to escape lysosome targeting
In order to elucidate the role of RAB7 in modulating flux of Mtb-containing autophagosomes, specific siRNA was used to knockdown RAB7 in infected THP-1 macrophages. Specific knockdown of RAB7 was verified by Western blots (Fig S3A). As shown in Fig. 4A, RAB7 knockdown inhibited the flux of H37Ra-containing autophagosomes. There was no effect on flux of H37Rv-containing compartments (Fig. 4A). Intriguingly RAB7 siRNA also led to inhibition of general autophagy flux in THP-1 macrophages (Fig. S3B and S3C). As expected, co-localization of H37Ra to lysosomes was significantly inhibited in the RAB7 knockdown macrophages (Fig. 4B). Moreover RAB7 depletion also resulted in improved intracellular survival of H37Ra (Fig. 4C).
Figure 4
Exclusion of RAB7 from Mtb-containing autophagosome allows H37Rv to escape lysosome targeting.
THP-1 macrophages infected with H37Ra or H37Rv were treated with specific siRNA against RAB7 (50 nM) till 48 hours post infection. Panel (A) shows co-localization coefficient M1 of H37Ra and H37Rv to autophagosomes in BafA1 treated and untreated conditions, with RAB7 siRNA treatment (RAB7) relative to control (SCR, scrambled) (mean ± SEM, *p < 0.05). Panel (B) shows co-localization coefficient M1 of H37Ra and H37Rv to LysoTracker (lysosomes) in the presence or absence of RAB7 siRNA treatment (mean ± SEM, *p < 0.05). Plot in panel C shows Mtb CFU with RAB7 siRNA treatment as compared to scrambled control.
Discussions
Autophagy as a defence mechanism in case of Mtb infection has been shown by several studies in the past91125. Given the fundamental role of autophagy in cells as homeostatic mechanism under various stress conditions, how Mtb could specifically manipulate it, remains poorly understood. There are studies on strain specific regulation of autophagy, suggesting that the virulent strains of Mtb induce autophagy to a lesser extent in contrast to the non-pathogenic, attenuated strains17. Some other reports however suggest while the wild-type strains could induce autophagy, the attenuated ones could not14. Here we exclusively focused on the regulation of maturation of Mtb-containing autophagosomes and observed a distinct pattern of selectivity between the virulent and avirulent strains of Mtb in regulating autophagy flux.We show here that both virulent and avirulent strains of Mtb can readily localize to the autophagosomes. Our experiments with BafA1 revealed a higher co-localization of H37Ra with autophagosomes relative to the untreated set post 24 hours of infection. Since BafA1 inhibits LC3 degradation in the autolysosomes, we believe the increase in co-localization was due to the enhanced signals from the accumulated, undegraded LC3 molecules in the autolysosomes. This result implies flux of H37Ra-containing autophagosomes that were maturing into autolysosomes. On the other hand, we did not observe any increase in the co-localization of H37Rv with autophagosomes upon BafA1 treatment throughout the course of infection, thereby suggesting a block in the flux of H37Rv-containing autophagosomes. This differential flux of Mtb-containing autophagosomes was corroborated by higher localization of H37Ra with the autolysosomes as compared to H37Rv. We found a crucial role of the virulence factors PhoP and ESAT-6 in effecting this maturation block of Mtb-containing autophagosomes. Similar role of ESAT-6 in the regulation of autophagy flux in infected dendritic cells has been shown earlier16.Curiously, we observed several autophagosomes devoid of bacteria in the infected cells. Moreover, several of those autophagosomes were at maturation stage co-localizing with the acidified lysosomes. This observation indicated that the autophagosomes, which did not contain Mtb, could mature without being influenced by infection. The LC3 immunoblots provided additional evidence supporting the selective nature of maturation block brought by the virulent strain. This observation opens up an interesting possibility that non-Mtb-containing autophagosomes and Mtb-containing autophagosomes (xenophagosomes) could have distinct maturation dynamics within the same cell. A blanket inhibition of autophagy, under many circumstances, would lead to induction of apoptosis, which may be detrimental to Mtb survival19. By specifically blocking the maturation of compartments where H37Rv resides, it avoids being killed by lysosomal mechanism. At the same time by allowing cellular autophagy, it ensures extended survival of the host2627. However, this interesting possibility deserves more detailed investigation.Our results on the role of RAB7 in autophagosome maturation provide novel insights into functioning of this small GTPase. Exclusion of RAB7 on phagosomes by virulent Mtb has been classically reported as the mechanism for avoiding lysosomal degradation28. It seems phagosome maturation goes hand-in-hand with autophagosome maturation and that at least Mtb-containing autophagosomes do not mature into autolysosomes without recruiting RAB7 to form an intermediate amphisome. How the resident virulent Mtb could block autophagosome fusion with late endosomes remains unanswered. However in case of phagosome maturation, it was shown that the failure to recruit RAB7 to H37Rv phagosome was contingent on the lipid product phosphatidylinositol 3-phosphate (PtdIns[3]P) and subsequent binding of RAB5 effector EEA129. However it remains unclear if that holds true even in the case of autophagosomes. Interestingly a number of studies propose, in other systems, role of RAB7 in the maturation phase of autophagy303132. The importance of maturation step of autophagy in case of Mtb infections was also supported by the study where TBK1, an innate immunity regulator was shown to regulate autophagy maturation to eliminate BCG infections15. Intriguingly, upon RAB7 depletion in THP-1 macrophages, even the general autophagy flux gets perturbed. That raises another question on how the selectivity in autophagosome maturation could be ensured by resident virulent Mtb if RAB7 is essential for autophagosome maturation in general. One plausible explanation for this may be selective modulation of RAB5 effector function by H37Rv leading to altered autophagosome. Thus even though late endosomes could efficiently fuse with other autophagosomes, H37Rv-containing autophagosomes evade this process. Such mechanisms are studied in case of phagosome maturation29, whether similar mechanism could be functional in case of autophagy needs further investigations. In this study we could not distinguish autophagy from LC3 associated phagocytosis (LAP). Involvement of LAP in Mtb infections remains debatable despite some reports emerging on it, and needs further investigations3334. The crosstalk between the autophagy pathway and the phagosome maturation pathway has been schematically summarized in Fig. 5.
Figure 5
Revisiting Mtb phagosome maturation pathway.
Mtb in the phagosomes could follow many pathways. Mtb, especially the virulent strains, is known to escape from the phagosome. Both phagosome bound and cytosolic Mtb may get trapped in the autophagosomes. Phagosome may also directly recruit LC3 to form a LAP vesicle. Further maturation of phagosomes, LAP or autophagosomes depends on recruitment of RAB7, which facilitates eventual fusion with the lysosome for degradation. Virulent strains of Mtb inhibit RAB7 recruitment on the phagosomes. This study shows, similar inhibition of RAB7 recruitment on autophagosomes and possibly on LAP by the virulent strain.
In conclusion we report here a mechanism whereby virulent Mtb strain could selectively block maturation of the resident autophagosomes. We show that the virulent Mtb could achieve this by avoiding RAB7 recruitment to form the amphisomes. The crucial role of amphisome compartment in the regulation of intracellular Mtb survival has added new dimensions to our understanding of cell autonomous defense mechanisms in case of Mtb infections. Understanding the regulation of autophagy maturation at molecular level could help identify novel and perhaps better host directed drug targets against tuberculosis.
Materials and Methods
Ethics statement
All the experiments with animals were performed in accordance with the approved guidelines and regulations of the Institutional Animal Ethics Committee (IAEC). The experiments were performed upon prior approval from the institutional ethics committee (IAEC) of International Center for Genetic Engineering and Biotechnology (Approval no.: ICGEB/AH/2013/03/IMM-38).
Cells and Infections
THP-1 cells were differentiated with PMA (Sigma, P1269) at a concentration of 20 ng/ml for 24 hours. For infection, Mtb (H37Ra and H37Rv) single-cell suspensions were prepared as described by Kumar et al. and infections were done at an MOI of 1:10 for 4 hours followed by amikacin treatment of 2 hours. The subsequent time points were considered from here on.
Bacterial cultures and media
Bacteria were grown as stationary cultures in Middlebrook 7H9 broth (BD Difco, Becton Dickinson) supplemented with 10% ADC (Becton Dickinson), 0.4% Glycerol and 0.05% Tween-80 until the mid-log phase. The bacteria were then harvested, washed with RPMI and used for suspension preparation.
Bacterial suspension preparation and Infection
Bacterial whole cell suspension was dispersed by aspiration five times each with a 23- and then a 26-gauge needle, followed by an additional dispersion by aspiration 3 times through a 30-gauge needle. The dispersed bacteria were allowed to stand for 5 min to allow the clumps to settle down. The upper half of the suspension was then used for the experiments. Quantitation of bacteria was done by taking absorbance at 600 nm wavelength (0.6 O.D. corresponds to ~100 × 106 bacteria). Complete media containing the required number of bacteria was added to the cultured cells at an MOI of 10, followed by a short spin of the culture plates at 700 rpm for 5 minutes. After 4 hours of infection, the cells were washed twice with warm RPMI and treated with Amikacin (200 μg/ml, HiMedia laboratories) to remove any extracellular bacteria. After two hours of treatment, the cells were washed and maintained in complete media. For microscopy experiments, the desired number of bacteria were stained with PKH67 (green)(Sigma-Aldrich Co. MINI67-1KT), lipophilic fluorescent dye, as per the manufacturer’s protocol. The stained bacteria were passed thrice through a 26-gauge needle and were then used for infection.
Animals and isolation of BMDMs
Bone marrow derived macrophages (BMDMs) were isolated from femurs of BALB/C mice (4-6 weeks old, female). BMDMs were obtained by culturing the marrow cells in the presence of macrophage-colony stimulating factor (M-CSF, eBioscience, 14-8983-80) for 7 days. Fully differentiated macrophages were harvested and seeded for infection with H37Ra or H37Rv. The infection protocol was same as described above for THP-1 macrophages.
Inhibitor treatments
E64-d (Sigma, E8640) and PepstatinA (Sigma, P5318) treatments were given at a concentration of 25 μg/ml and 10 μg/ml, respectively for 2 hours prior to fixation. Autophagy was inhibited by 3-Methyladenine (Sigma, M9281) treatment, added 48 hours post infection, at a concentration of 5 mM. Autophagy flux was monitored using BafilomycinA1 (Invivogen, tlrl-baf1) at 100 nM for 3 hours. LysoTracker Red DND-99 (Molecular Probes, L-7528) was used to monitor acidified lysosomes at 200 nM concentration for one hour.
Construction of PhoP over-expressing Mtb H37Ra strain
For expressing H37Rv PhoP in H37Ra, gene encoding H37Rv PhoP (Rv 0757) was PCR amplified and cloned into E.coli-Mycobacterial shuttle vector, pSD5hsp35. The pSD5-phoP construct was then electroporated into Mtb H37Ra and transformants were selected on 7H11 medium containing kanamycin (25 ug/ml). The expression of phoP was under strong hsp65 gene promoter from M. leprae.
siRNA treatments
We followed established protocols for siRNA treatments of differentiated THP-1 cells as described earlier10. RAB7 siRNA were procured from Dharmacon (M-010388-00-0005). Addition of RAB7 siRNA was done after amikacin wash and treatment was done for 48 hours.
Confocal Microscopy
One hour prior to the termination of the experiment, complete media containing LysoTracker dye at a concentration of 200 nM was added to the cells for staining of acidified lysosomes. Following the required treatments, the cells were fixed with 4% paraformaldehyde (Sigma) for 20 minutes, followed by 3 washes with 1X PBS. The cells were permeabilized using 0.2% (w/v) TritonX-100 in 1X PBS for 20 minutes. Blocking was performed using 3%(w/v) BSA and 0.5%Tween20 in 1X PBS for one hour. This was followed by primary and secondary antibody staining for duration of one hour each. The primary antibodies used in the study are LC3 (Novus, NB100-2220, Cell Signaling Technology, 2775S), RAB7 (Santa Cruz Biotechnology, SC-6563). Commercially available Alexa dye conjugated secondary antibodies (Molecular Probes, A31556 and A11057) were used for immunostaining. Antibody dilutions were made in blocking solution as per the supplier’s protocol. The coverslips were washed thoroughly with 1X PBS and were mounted onto glass slides with Antifade reagent (Invitrogen Molecular Probes). Images were acquired randomly from each set of stained cells with a Nikon EclipseTi-E laser scanning confocal microscope equipped with a 60X/1.4NA PlanApochromat DIC objective. Images were acquired using the softwares EZ-C1 3.80 and NIS-Elements. Image analyses were performed using the software Imaris version 7.6.4 (BitPlane).
Image Capture and analysis
Stained cells were observed with a Nikon Ti-E microscope equipped with 60X /1.4 NA planapochromat DIC objective lens. Samples were excited at 543 nm with He-Neon laser, 488 nm with an Argon ion laser and in the UV range with a blue diode. Images were acquired sequentially to avoid bleed-through signal, with a scanning mode format of 512 × 512 pixels. The transmission and detector gains were set to achieve best signal to noise ratios and the laser powers were tuned to limit bleaching of fluorescence. The refractive index of the immersion oil used was 1.515 (Nikon Corporation). All settings were rigorously maintained for all experiments. All images were qualitatively assessed using Imaris version 7.6.4 (BitPlane). All the images are in the Tiff RGB 24 format. M1 co-localization coefficient of Mtb and various markers were calculated in the software. The percentage of Mtb in autolysosomes and amphisomes were estimated by calculating the percentage of Mtb voxels in LC3:Lysotracker and LC3:RAB7 colocalized channels. The results represent an average of at least three independent sets of experiments.
Statistical analyses
Statistical analyses were performed using Student’s t-tests (two-tailed) with ‘*’ and ‘**’ representing significant difference between the tested group at 95% (p < 0.05) and 99% (p < 0.01) level of confidence.
Additional Information
How to cite this article: Chandra, P. et al.
Mycobacterium tuberculosis Inhibits RAB7 Recruitment to Selectively Modulate Autophagy Flux in Macrophages. Sci. Rep.
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Authors: Lorenzo Galluzzi; Eric H Baehrecke; Andrea Ballabio; Patricia Boya; José Manuel Bravo-San Pedro; Francesco Cecconi; Augustine M Choi; Charleen T Chu; Patrice Codogno; Maria Isabel Colombo; Ana Maria Cuervo; Jayanta Debnath; Vojo Deretic; Ivan Dikic; Eeva-Liisa Eskelinen; Gian Maria Fimia; Simone Fulda; David A Gewirtz; Douglas R Green; Malene Hansen; J Wade Harper; Marja Jäättelä; Terje Johansen; Gabor Juhasz; Alec C Kimmelman; Claudine Kraft; Nicholas T Ktistakis; Sharad Kumar; Beth Levine; Carlos Lopez-Otin; Frank Madeo; Sascha Martens; Jennifer Martinez; Alicia Melendez; Noboru Mizushima; Christian Münz; Leon O Murphy; Josef M Penninger; Mauro Piacentini; Fulvio Reggiori; David C Rubinsztein; Kevin M Ryan; Laura Santambrogio; Luca Scorrano; Anna Katharina Simon; Hans-Uwe Simon; Anne Simonsen; Nektarios Tavernarakis; Sharon A Tooze; Tamotsu Yoshimori; Junying Yuan; Zhenyu Yue; Qing Zhong; Guido Kroemer Journal: EMBO J Date: 2017-06-08 Impact factor: 11.598
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Susanna Ambrosio; Amal O Amer; Veena Ammanathan; Zhenyi An; Stig U Andersen; Shaida A Andrabi; Magaiver Andrade-Silva; Allen M Andres; Sabrina Angelini; David Ann; Uche C Anozie; Mohammad Y Ansari; Pedro Antas; Adam Antebi; Zuriñe Antón; Tahira Anwar; Lionel Apetoh; Nadezda Apostolova; Toshiyuki Araki; Yasuhiro Araki; Kohei Arasaki; Wagner L Araújo; Jun Araya; Catherine Arden; Maria-Angeles Arévalo; Sandro Arguelles; Esperanza Arias; Jyothi Arikkath; Hirokazu Arimoto; Aileen R Ariosa; Darius Armstrong-James; Laetitia Arnauné-Pelloquin; Angeles Aroca; Daniela S Arroyo; Ivica Arsov; Rubén Artero; Dalia Maria Lucia Asaro; Michael Aschner; Milad Ashrafizadeh; Osnat Ashur-Fabian; Atanas G Atanasov; Alicia K Au; Patrick Auberger; Holger W Auner; Laure Aurelian; Riccardo Autelli; Laura Avagliano; Yenniffer Ávalos; Sanja Aveic; Célia Alexandra Aveleira; Tamar Avin-Wittenberg; Yucel Aydin; Scott Ayton; Srinivas Ayyadevara; Maria Azzopardi; Misuzu Baba; Jonathan M Backer; Steven K Backues; Dong-Hun Bae; Ok-Nam Bae; Soo Han Bae; Eric H Baehrecke; Ahruem Baek; Seung-Hoon Baek; Sung Hee Baek; Giacinto Bagetta; Agnieszka Bagniewska-Zadworna; Hua Bai; Jie Bai; Xiyuan Bai; Yidong Bai; Nandadulal Bairagi; Shounak Baksi; Teresa Balbi; Cosima T Baldari; Walter Balduini; Andrea Ballabio; Maria Ballester; Salma Balazadeh; Rena Balzan; Rina Bandopadhyay; Sreeparna Banerjee; Sulagna Banerjee; Ágnes Bánréti; Yan Bao; Mauricio S Baptista; Alessandra Baracca; Cristiana Barbati; Ariadna Bargiela; Daniela Barilà; Peter G Barlow; Sami J Barmada; Esther Barreiro; George E Barreto; Jiri Bartek; Bonnie Bartel; Alberto Bartolome; Gaurav R Barve; Suresh H Basagoudanavar; Diane C Bassham; Robert C Bast; Alakananda Basu; Henri Batoko; Isabella Batten; Etienne E Baulieu; Bradley L Baumgarner; Jagadeesh Bayry; Rupert Beale; Isabelle Beau; Florian Beaumatin; Luiz R G Bechara; George R Beck; Michael F Beers; Jakob Begun; Christian Behrends; Georg M N Behrens; Roberto Bei; Eloy Bejarano; Shai Bel; Christian Behl; Amine Belaid; Naïma Belgareh-Touzé; Cristina Bellarosa; Francesca Belleudi; Melissa Belló Pérez; Raquel Bello-Morales; Jackeline Soares de Oliveira Beltran; Sebastián Beltran; Doris Mangiaracina Benbrook; Mykolas Bendorius; Bruno A Benitez; Irene Benito-Cuesta; Julien Bensalem; Martin W Berchtold; Sabina Berezowska; Daniele Bergamaschi; Matteo Bergami; Andreas Bergmann; Laura Berliocchi; Clarisse Berlioz-Torrent; Amélie Bernard; Lionel Berthoux; Cagri G Besirli; Sebastien Besteiro; Virginie M Betin; Rudi Beyaert; Jelena S Bezbradica; Kiran Bhaskar; Ingrid Bhatia-Kissova; Resham Bhattacharya; Sujoy Bhattacharya; Shalmoli Bhattacharyya; Md Shenuarin Bhuiyan; Sujit Kumar Bhutia; Lanrong Bi; Xiaolin Bi; Trevor J Biden; Krikor Bijian; Viktor A Billes; Nadine Binart; Claudia Bincoletto; Asa B Birgisdottir; Geir Bjorkoy; Gonzalo Blanco; Ana Blas-Garcia; Janusz Blasiak; Robert Blomgran; Klas Blomgren; Janice S Blum; Emilio Boada-Romero; Mirta Boban; Kathleen Boesze-Battaglia; Philippe Boeuf; Barry Boland; Pascale Bomont; Paolo Bonaldo; Srinivasa Reddy Bonam; Laura Bonfili; Juan S Bonifacino; Brian A Boone; Martin D Bootman; Matteo Bordi; Christoph Borner; Beat C Bornhauser; Gautam Borthakur; Jürgen Bosch; Santanu Bose; Luis M Botana; Juan Botas; Chantal M Boulanger; Michael E Boulton; Mathieu Bourdenx; Benjamin Bourgeois; Nollaig M Bourke; Guilhem Bousquet; Patricia Boya; Peter V Bozhkov; Luiz H M Bozi; Tolga O Bozkurt; Doug E Brackney; Christian H Brandts; Ralf J Braun; Gerhard H Braus; Roberto Bravo-Sagua; José M Bravo-San Pedro; Patrick Brest; Marie-Agnès Bringer; Alfredo Briones-Herrera; V Courtney Broaddus; Peter Brodersen; Jeffrey L Brodsky; Steven L Brody; Paola G Bronson; Jeff M Bronstein; Carolyn N Brown; Rhoderick E Brown; Patricia C Brum; John H Brumell; Nicola Brunetti-Pierri; Daniele Bruno; Robert J Bryson-Richardson; Cecilia Bucci; Carmen Buchrieser; Marta Bueno; Laura Elisa Buitrago-Molina; Simone Buraschi; Shilpa Buch; J Ross Buchan; Erin M Buckingham; Hikmet Budak; Mauricio Budini; Geert Bultynck; Florin Burada; Joseph R Burgoyne; M Isabel Burón; Victor Bustos; Sabrina Büttner; Elena Butturini; Aaron Byrd; Isabel Cabas; Sandra Cabrera-Benitez; Ken Cadwell; Jingjing Cai; Lu Cai; Qian Cai; Montserrat Cairó; Jose A Calbet; Guy A Caldwell; Kim A Caldwell; Jarrod A Call; Riccardo Calvani; Ana C Calvo; Miguel Calvo-Rubio Barrera; Niels Os Camara; Jacques H Camonis; Nadine Camougrand; Michelangelo Campanella; Edward M Campbell; François-Xavier Campbell-Valois; Silvia Campello; Ilaria Campesi; Juliane C Campos; Olivier Camuzard; Jorge Cancino; Danilo Candido de Almeida; Laura Canesi; Isabella Caniggia; Barbara Canonico; Carles Cantí; Bin Cao; Michele Caraglia; Beatriz Caramés; Evie H Carchman; Elena Cardenal-Muñoz; Cesar Cardenas; Luis Cardenas; Sandra M Cardoso; Jennifer S Carew; Georges F Carle; Gillian Carleton; Silvia Carloni; Didac Carmona-Gutierrez; Leticia A Carneiro; Oliana Carnevali; Julian M Carosi; Serena Carra; Alice Carrier; Lucie Carrier; Bernadette Carroll; A Brent Carter; Andreia Neves Carvalho; Magali Casanova; Caty Casas; Josefina Casas; Chiara Cassioli; Eliseo F Castillo; Karen Castillo; Sonia Castillo-Lluva; Francesca Castoldi; Marco Castori; Ariel F Castro; Margarida Castro-Caldas; Javier Castro-Hernandez; Susana Castro-Obregon; Sergio D Catz; Claudia Cavadas; Federica Cavaliere; Gabriella Cavallini; Maria Cavinato; Maria L Cayuela; Paula Cebollada Rica; Valentina Cecarini; Francesco Cecconi; Marzanna Cechowska-Pasko; Simone Cenci; Victòria Ceperuelo-Mallafré; João J Cerqueira; Janete M Cerutti; Davide Cervia; Vildan Bozok Cetintas; Silvia Cetrullo; Han-Jung Chae; Andrei S Chagin; Chee-Yin Chai; Gopal Chakrabarti; Oishee Chakrabarti; Tapas Chakraborty; Trinad Chakraborty; Mounia Chami; Georgios Chamilos; David W Chan; Edmond Y W Chan; Edward D Chan; H Y Edwin Chan; Helen H Chan; Hung Chan; Matthew T V Chan; Yau Sang Chan; Partha K Chandra; Chih-Peng Chang; Chunmei Chang; Hao-Chun Chang; Kai Chang; Jie Chao; Tracey Chapman; Nicolas Charlet-Berguerand; Samrat Chatterjee; Shail K Chaube; Anu Chaudhary; Santosh Chauhan; Edward Chaum; Frédéric Checler; Michael E Cheetham; Chang-Shi Chen; Guang-Chao Chen; Jian-Fu Chen; Liam L Chen; Leilei Chen; Lin Chen; Mingliang Chen; Mu-Kuan Chen; Ning Chen; Quan Chen; Ruey-Hwa Chen; Shi Chen; Wei Chen; Weiqiang Chen; Xin-Ming Chen; Xiong-Wen Chen; Xu Chen; Yan Chen; Ye-Guang Chen; Yingyu Chen; Yongqiang Chen; Yu-Jen Chen; Yue-Qin Chen; Zhefan Stephen Chen; Zhi Chen; Zhi-Hua Chen; Zhijian J Chen; Zhixiang Chen; Hanhua Cheng; Jun Cheng; Shi-Yuan Cheng; Wei Cheng; Xiaodong Cheng; Xiu-Tang Cheng; Yiyun Cheng; Zhiyong Cheng; Zhong Chen; Heesun Cheong; Jit Kong Cheong; Boris V Chernyak; Sara Cherry; Chi Fai Randy Cheung; Chun Hei Antonio Cheung; King-Ho Cheung; Eric Chevet; Richard J Chi; Alan Kwok Shing Chiang; Ferdinando Chiaradonna; Roberto Chiarelli; Mario Chiariello; Nathalia Chica; Susanna Chiocca; Mario Chiong; Shih-Hwa Chiou; Abhilash I Chiramel; Valerio Chiurchiù; Dong-Hyung Cho; Seong-Kyu Choe; Augustine M K Choi; Mary E Choi; Kamalika Roy Choudhury; Norman S Chow; Charleen T Chu; Jason P Chua; John Jia En Chua; Hyewon Chung; Kin Pan Chung; Seockhoon Chung; So-Hyang Chung; Yuen-Li Chung; Valentina Cianfanelli; Iwona A Ciechomska; Mariana Cifuentes; Laura Cinque; Sebahattin Cirak; Mara Cirone; Michael J Clague; Robert Clarke; Emilio Clementi; Eliana M Coccia; Patrice Codogno; Ehud Cohen; Mickael M Cohen; Tania Colasanti; Fiorella Colasuonno; Robert A Colbert; Anna Colell; Miodrag Čolić; Nuria S Coll; Mark O Collins; María I Colombo; Daniel A Colón-Ramos; Lydie Combaret; Sergio Comincini; Márcia R Cominetti; Antonella Consiglio; Andrea Conte; Fabrizio Conti; Viorica Raluca Contu; Mark R Cookson; Kevin M Coombs; Isabelle Coppens; Maria Tiziana Corasaniti; Dale P Corkery; Nils Cordes; Katia Cortese; Maria do Carmo Costa; Sarah Costantino; Paola Costelli; Ana Coto-Montes; Peter J Crack; Jose L Crespo; Alfredo Criollo; Valeria Crippa; Riccardo Cristofani; Tamas Csizmadia; Antonio Cuadrado; Bing Cui; Jun Cui; 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; 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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; 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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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Soledad Porte Alcon; Eliana Portilla-Fernandez; Martin Post; Malia B Potts; Joanna Poulton; Ted Powers; Veena Prahlad; Tomasz K Prajsnar; Domenico Praticò; Rosaria Prencipe; Muriel Priault; Tassula Proikas-Cezanne; Vasilis J Promponas; Christopher G Proud; Rosa Puertollano; Luigi Puglielli; Thomas Pulinilkunnil; Deepika Puri; Rajat Puri; Julien Puyal; Xiaopeng Qi; Yongmei Qi; Wenbin Qian; Lei Qiang; Yu Qiu; Joe Quadrilatero; Jorge Quarleri; Nina Raben; Hannah Rabinowich; Debora Ragona; Michael J Ragusa; Nader Rahimi; Marveh Rahmati; Valeria Raia; Nuno Raimundo; Namakkal-Soorappan Rajasekaran; Sriganesh Ramachandra Rao; Abdelhaq Rami; Ignacio Ramírez-Pardo; David B Ramsden; Felix Randow; Pundi N Rangarajan; Danilo Ranieri; Hai Rao; Lang Rao; Rekha Rao; Sumit Rathore; J Arjuna Ratnayaka; Edward A Ratovitski; Palaniyandi Ravanan; Gloria Ravegnini; Swapan K Ray; Babak Razani; Vito Rebecca; Fulvio Reggiori; Anne Régnier-Vigouroux; Andreas S Reichert; David Reigada; Jan H Reiling; Theo Rein; 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Motomasa Tanaka; Daolin Tang; Jingfeng Tang; Tie-Shan Tang; Isei Tanida; Zhipeng Tao; Mohammed Taouis; Lars Tatenhorst; Nektarios Tavernarakis; Allen Taylor; Gregory A Taylor; Joan M Taylor; Elena Tchetina; Andrew R Tee; Irmgard Tegeder; David Teis; Natercia Teixeira; Fatima Teixeira-Clerc; Kumsal A Tekirdag; Tewin Tencomnao; Sandra Tenreiro; Alexei V Tepikin; Pilar S Testillano; Gianluca Tettamanti; Pierre-Louis Tharaux; Kathrin Thedieck; Arvind A Thekkinghat; Stefano Thellung; Josephine W Thinwa; V P Thirumalaikumar; Sufi Mary Thomas; Paul G Thomes; Andrew Thorburn; Lipi Thukral; Thomas Thum; Michael Thumm; Ling Tian; Ales Tichy; Andreas Till; Vincent Timmerman; Vladimir I Titorenko; Sokol V Todi; Krassimira Todorova; Janne M Toivonen; Luana Tomaipitinca; Dhanendra Tomar; Cristina Tomas-Zapico; Sergej Tomić; Benjamin Chun-Kit Tong; Chao Tong; Xin Tong; Sharon A Tooze; Maria L Torgersen; Satoru Torii; Liliana Torres-López; Alicia Torriglia; Christina G Towers; Roberto Towns; Shinya Toyokuni; Vladimir Trajkovic; Donatella Tramontano; Quynh-Giao Tran; Leonardo H Travassos; Charles B Trelford; Shirley Tremel; Ioannis P Trougakos; Betty P Tsao; Mario P Tschan; Hung-Fat Tse; Tak Fu Tse; Hitoshi Tsugawa; Andrey S Tsvetkov; David A Tumbarello; Yasin Tumtas; María J Tuñón; Sandra Turcotte; Boris Turk; Vito Turk; Bradley J Turner; Richard I Tuxworth; Jessica K Tyler; Elena V Tyutereva; Yasuo Uchiyama; Aslihan Ugun-Klusek; Holm H Uhlig; Marzena Ułamek-Kozioł; Ilya V Ulasov; Midori Umekawa; Christian Ungermann; Rei Unno; Sylvie Urbe; Elisabet Uribe-Carretero; Suayib Üstün; Vladimir N Uversky; Thomas Vaccari; Maria I Vaccaro; Björn F Vahsen; Helin Vakifahmetoglu-Norberg; Rut Valdor; Maria J Valente; Ayelén Valko; Richard B Vallee; Angela M Valverde; Greet Van den Berghe; Stijn van der Veen; Luc Van Kaer; Jorg van Loosdregt; Sjoerd J L van Wijk; Wim Vandenberghe; Ilse Vanhorebeek; Marcos A Vannier-Santos; Nicola Vannini; M Cristina Vanrell; Chiara Vantaggiato; Gabriele Varano; Isabel Varela-Nieto; Máté Varga; M Helena Vasconcelos; Somya Vats; Demetrios G Vavvas; Ignacio Vega-Naredo; Silvia Vega-Rubin-de-Celis; Guillermo Velasco; Ariadna P Velázquez; Tibor Vellai; Edo Vellenga; Francesca Velotti; Mireille Verdier; Panayotis Verginis; Isabelle Vergne; Paul Verkade; Manish Verma; Patrik Verstreken; Tim Vervliet; Jörg Vervoorts; Alexandre T Vessoni; Victor M Victor; Michel Vidal; Chiara Vidoni; Otilia V Vieira; Richard D Vierstra; Sonia Viganó; Helena Vihinen; Vinoy Vijayan; Miquel Vila; Marçal Vilar; José M Villalba; Antonio Villalobo; Beatriz Villarejo-Zori; Francesc Villarroya; Joan Villarroya; Olivier Vincent; Cecile Vindis; Christophe Viret; Maria Teresa Viscomi; Dora Visnjic; Ilio Vitale; David J Vocadlo; Olga V Voitsekhovskaja; Cinzia Volonté; Mattia Volta; Marta Vomero; Clarissa Von Haefen; Marc A Vooijs; Wolfgang Voos; Ljubica Vucicevic; Richard Wade-Martins; Satoshi Waguri; Kenrick A Waite; Shuji Wakatsuki; David W Walker; Mark J Walker; Simon A Walker; Jochen Walter; Francisco G Wandosell; Bo Wang; Chao-Yung Wang; Chen Wang; Chenran Wang; Chenwei Wang; Cun-Yu Wang; Dong Wang; Fangyang Wang; Feng Wang; Fengming Wang; Guansong Wang; Han Wang; Hao Wang; Hexiang Wang; Hong-Gang Wang; Jianrong Wang; Jigang Wang; Jiou Wang; Jundong Wang; Kui Wang; Lianrong Wang; Liming Wang; Maggie Haitian Wang; Meiqing Wang; Nanbu Wang; Pengwei Wang; Peipei Wang; Ping Wang; Ping Wang; Qing Jun Wang; Qing Wang; Qing Kenneth Wang; Qiong A Wang; Wen-Tao Wang; Wuyang Wang; Xinnan Wang; Xuejun Wang; Yan Wang; Yanchang Wang; Yanzhuang Wang; Yen-Yun Wang; Yihua Wang; Yipeng Wang; Yu Wang; Yuqi Wang; Zhe Wang; Zhenyu Wang; Zhouguang Wang; Gary Warnes; Verena Warnsmann; Hirotaka Watada; Eizo Watanabe; Maxinne Watchon; Anna Wawrzyńska; Timothy E Weaver; Grzegorz Wegrzyn; Ann M Wehman; Huafeng Wei; Lei Wei; Taotao Wei; Yongjie Wei; Oliver H Weiergräber; Conrad C Weihl; Günther Weindl; Ralf Weiskirchen; Alan Wells; Runxia H Wen; Xin Wen; Antonia Werner; Beatrice Weykopf; Sally P Wheatley; J Lindsay Whitton; 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Vanessa O Zambelli; Isabella Zanella; Qun S Zang; Sara Zanivan; Silvia Zappavigna; Pilar Zaragoza; Konstantinos S Zarbalis; Amir Zarebkohan; Amira Zarrouk; Scott O Zeitlin; Jialiu Zeng; Ju-Deng Zeng; Eva Žerovnik; Lixuan Zhan; Bin Zhang; Donna D Zhang; Hanlin Zhang; Hong Zhang; Hong Zhang; Honghe Zhang; Huafeng Zhang; Huaye Zhang; Hui Zhang; Hui-Ling Zhang; Jianbin Zhang; Jianhua Zhang; Jing-Pu Zhang; Kalin Y B Zhang; Leshuai W Zhang; Lin Zhang; Lisheng Zhang; Lu Zhang; Luoying Zhang; Menghuan Zhang; Peng Zhang; Sheng Zhang; Wei Zhang; Xiangnan Zhang; Xiao-Wei Zhang; Xiaolei Zhang; Xiaoyan Zhang; Xin Zhang; Xinxin Zhang; Xu Dong Zhang; Yang Zhang; Yanjin Zhang; Yi Zhang; Ying-Dong Zhang; Yingmei Zhang; Yuan-Yuan Zhang; Yuchen Zhang; Zhe Zhang; Zhengguang Zhang; Zhibing Zhang; Zhihai Zhang; Zhiyong Zhang; Zili Zhang; Haobin Zhao; Lei Zhao; Shuang Zhao; Tongbiao Zhao; Xiao-Fan Zhao; Ying Zhao; Yongchao Zhao; Yongliang Zhao; Yuting Zhao; Guoping Zheng; Kai Zheng; Ling Zheng; Shizhong Zheng; Xi-Long Zheng; Yi Zheng; Zu-Guo Zheng; Boris Zhivotovsky; Qing Zhong; Ao Zhou; Ben Zhou; Cefan Zhou; Gang Zhou; Hao Zhou; Hong Zhou; Hongbo Zhou; Jie Zhou; Jing Zhou; Jing Zhou; Jiyong Zhou; Kailiang Zhou; Rongjia Zhou; Xu-Jie Zhou; Yanshuang Zhou; Yinghong Zhou; Yubin Zhou; Zheng-Yu Zhou; Zhou Zhou; Binglin Zhu; Changlian Zhu; Guo-Qing Zhu; Haining Zhu; Hongxin Zhu; Hua Zhu; Wei-Guo Zhu; Yanping Zhu; Yushan Zhu; Haixia Zhuang; Xiaohong Zhuang; Katarzyna Zientara-Rytter; Christine M Zimmermann; Elena Ziviani; Teresa Zoladek; Wei-Xing Zong; Dmitry B Zorov; Antonio Zorzano; Weiping Zou; Zhen Zou; Zhengzhi Zou; Steven Zuryn; Werner Zwerschke; Beate Brand-Saberi; X Charlie Dong; Chandra Shekar Kenchappa; Zuguo Li; Yong Lin; Shigeru Oshima; Yueguang Rong; Judith C Sluimer; Christina L Stallings; Chun-Kit Tong Journal: Autophagy Date: 2021-02-08 Impact factor: 13.391
Authors: Blanca I Restrepo; Arshad Khan; Vipul K Singh; Génesis P Aguillón-Durán; Eder Ledezma-Campos; David H Canaday; Chinnaswamy Jagannath Journal: Tuberculosis (Edinb) Date: 2020-12-30 Impact factor: 2.973
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