Autophagy genes function sequentially to promote apoptotic cell corpse degradation in the engulfing cell
Open accessAbstract
Apoptotic cell degradation is a fundamental process for organism development, and impaired clearance causes inflammatory or autoimmune disease. Although autophagy genes were reported to be essential for exposing the engulfment signal on apoptotic cells, their roles in phagocytes for apoptotic cell removal are not well understood. In this paper, we develop live-cell imaging techniques to study apoptotic cell clearance in the Caenorhabditis elegans Q neuroblast lineage. We show that the autophagy proteins LGG-1/LC3, ATG-18, and EPG-5 were sequentially recruited to internalized apoptotic Q cells in the phagocyte. In atg-18 or epg-5 mutants, apoptotic Q cells were internalized but not properly degraded; this phenotype was fully rescued by the expression of autophagy genes in the phagocyte. Time-lapse analysis of autophagy mutants revealed that recruitment of the small guanosine triphosphatases RAB-5 and RAB-7 to the phagosome and the formation of phagolysosome were all significantly delayed. Thus, autophagy genes act within the phagocyte to promote apoptotic cell degradation.
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In Caenorhabditis elegans, LGG-1 (homolog of LC3) is recruited to the apoptotic Q neuroblast (Q cell) corpse.
“Similarly, in Caenorhabditis elegans, LGG-1 (homolog of LC3) is recruited to the apoptotic Q neuroblast (Q cell) corpse [34].”
From LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy (2012) · cites this paper as [34]
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1 retracted
Martinez, J., Almendinger, J., Oberst, A., Ness, R., Dillon, C. P., Fitzgerald, P., Hengartner, M. O., & Green, D. R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113421108 · Cited by 655 · cited 4× · see citing works
“…cultures showed that autophagy proteins were recruited from phagocytes to phagosomes, which contain apoptotic or necrotic cells, or to single-membrane entotic vacuoles, which harbor apoptotic cells and facilitated their elimination (Sanjuan et al., 2007; Florey et al., 2011; Martinez et al., 2011).”
BackgroundResultInfluentialRetractedLC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing.
Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., & Yoshimori, T. (2000) · The EMBO Journal · doi:10.1093/emboj/19.21.5720 · Cited by 6,605 · see citing works
Cui, C., Cui, J., Jin, F., Cui, Y., Li, R., Jiang, X., Tian, Y., Wang, R. C., Jiang, P., & Gao, J. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000479571 · Cited by 5,214 · see citing works
Methods in Mammalian Autophagy Research
Mizushima, N., Yoshimori, T., & Levine, B. (2010) · Cell · doi:10.1016/j.cell.2010.01.028 · Cited by 4,497 · see citing works
The embryonic cell lineage of the nematode Caenorhabditis elegans
Sulston, J. E., Schierenberg, E., White, J. G., & Thomson, J. N. (1983) · Developmental Biology · doi:10.1016/0012-1606(83)90201-4 · Cited by 4,199 · see citing works
Antimicrobial Autophagy: A Conserved Innate Immune Response in Drosophila
Moy, R. H., & Cherry, S. R. (2013) · Journal of Innate Immunity · doi:10.1159/000350326 · Cited by 3,549 · see citing works
Post-embryonic cell lineages of the nematode, Caenorhabditis elegans
Sulston, J. E., & Horvitz, H. R. (1977) · Developmental Biology · doi:10.1016/0012-1606(77)90158-0 · Cited by 3,479 · see citing works
Autophagy in immunity and inflammation
Levine, B., Mizushima, N., & Virgin, H. W. (2011) · Nature · doi:10.1038/nature09782 · Cited by 3,289 · see citing works
Cepharanthine potently enhances the sensitivity of anticancer agents in K562 cells
Ikeda, R., Che, X., Yamaguchi, T., Ushiyama, M., Zheng, C., Okumura, H., Takeda, Y., Shibayama, Y., Nakamura, K. T., Jeung, H., et al. (2005) · Cancer Science · doi:10.1111/j.1349-7006.2005.00057.x · Cited by 2,268 · see citing works
Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis
Sanjuan, M. A., Dillon, C. P., Tait, S. W. G., Moshiach, S., Dorsey, F., Connell, S., Komatsu, M., Tanaka, K., Cleveland, J. L., Withoff, S., et al. (2007) · Nature · doi:10.1038/nature06421 · Cited by 1,347 · see citing works
Polson, H. E. J., de Lartigue, J., Rigden, D. J., Reedijk, M., Urbé, S., Clague, M. J., & Tooze, S. A. (2010) · Autophagy · doi:10.4161/auto.6.4.11863 · Cited by 712 · see citing works
Autophagy Gene-Dependent Clearance of Apoptotic Cells during Embryonic Development
Qu, X., Zou, Z., Sun, Q., Luby‐Phelps, K., Cheng, P., Hogan, R. N., Gilpin, C. J., & Levine, B. (2007) · Cell · doi:10.1016/j.cell.2006.12.044 · Cited by 655 · see citing works
CED-1 Is a Transmembrane Receptor that Mediates Cell Corpse Engulfment in C. elegans
Zhou, Z., Hartwieg, E. A., & Horvitz, H. R. (2001) · Cell · doi:10.1016/s0092-8674(01)00190-8 · Cited by 600 · see citing works
Phagosome maturation: going through the acid test
Kinchen, J. M., & Ravichandran, K. S. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2515 · Cited by 555 · see citing works
Clearance of apoptotic cells: implications in health and disease
Elliott, M. R., & Ravichandran, K. S. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201004096 · Cited by 547 · see citing works
Florey, O., Kim, S. E., Sandoval, C. P., Haynes, C. M., & Overholtzer, M. (2011) · Nature Cell Biology · doi:10.1038/ncb2363 · Cited by 459 · see citing works
C. elegans Screen Identifies Autophagy Genes Specific to Multicellular Organisms
Tian, Y., Li, Z., Hu, W., Ren, H., Tian, E., Zhao, Y., Lu, Q., Huang, X., Yang, P., Li, X., et al. (2010) · Cell · doi:10.1016/j.cell.2010.04.034 · Cited by 434 · see citing works
Self-citationHigh-Throughput In Vivo Analysis of Gene Expression in Caenorhabditis elegans
Hunt-Newbury, R., Viveiros, R., Johnsen, R. C., Mah, A. K., Anastas, D., Fang, L. L., Halfnight, E., Lee, D., Lin, J., Lorch, A. H., et al. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050237 · Cited by 372 · see citing works
Developmental apoptosis in C. elegans: a complex CEDnario
Lettre, G., & Hengartner, M. O. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1836 · Cited by 298 · see citing works
Kinchen, J. M., & Ravichandran, K. S. (2010) · Nature · doi:10.1038/nature08853 · Cited by 252 · see citing works
THE ENGULFMENT PROCESS OF PROGRAMMED CELL DEATH INCAENORHABDITIS ELEGANS
Reddien, P. W., & Horvitz, H. R. (2004) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.20.022003.114619 · Cited by 238 · see citing works
Zhang, Y., Yan, L., Zhou, Z., Yang, P., Tian, E., Zhang, K., Zhao, Y., Li, Z., Song, B., Han, J., et al. (2009) · Cell · doi:10.1016/j.cell.2008.12.022 · Cited by 237 · see citing works
Lu, Q., Yang, P., Huang, X., Hu, W., Guo, B., Wu, F., Lin, L., Kovács, A. L., Yu, L., & Zhang, H. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.06.024 · Cited by 236 · see citing works
Genetic Control of Programmed Cell Death During Animal Development
Conradt, B. (2009) · Annual Review of Genetics · doi:10.1146/annurev.genet.42.110807.091533 · Cited by 173 · see citing works
Polarized Myosin Produces Unequal-Size Daughters During Asymmetric Cell Division
Ou, G., Stuurman, N., D’Ambrosio, M. V., & Vale, R. D. (2010) · Science · doi:10.1126/science.1196112 · Cited by 161 · see citing works
Self-citationConradt, B. (2005) · WormBook · doi:10.1895/wormbook.1.32.1 · Cited by 123 · see citing works
Guo, P., Hu, T., Zhang, J., Jiang, S., & Wang, X. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1008946107 · Cited by 88 · see citing works
Self-citationExpression and Imaging of Fluorescent Proteins in the C. elegans Gonad and Early Embryo
Green, R. A., Audhya, A., Pozniakovsky, A., Dammermann, A., Pemble, H., Monen, J., Portier, N., Hyman, A. A., Desai, A. B., & Oegema, K. (2008) · Methods in cell biology · doi:10.1016/s0091-679x(08)85009-1 · Cited by 68 · see citing works
Molecular signatures of cell migration in C. elegans Q neuroblasts
Ou, G., & Vale, R. D. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200812077 · Cited by 51 · see citing works
Self-citationLevine, B., & Ranganathan, R. (2010) · Nature · doi:10.1038/466038a · Cited by 23 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition).
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, M. J., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Autophagy · doi:10.1080/15548627.2015.1100356 · Cited by 5,894 · see citing works
Klionsky, D. J., Abdel-Aziz, A. K., Abdelfatah, S., Abdellatif, M., Abdoli, A., Abel, S., Abeliovich, H., Abildgaard, M. H., Abudu, Y. P., Acevedo-Arozena, A., et al. (2021) · Autophagy · doi:10.1080/15548627.2020.1797280 · Cited by 2,622 · see citing works
Self-citationDoherty, J., & Baehrecke, E. H. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0201-5 · Cited by 626 · see citing works
Regulation of autophagy by the Rab GTPase network
Ao, X., Zou, L., & Wu, Y. (2014) · Cell Death & Differentiation · doi:10.1038/cdd.2013.187 · Cited by 411 · see citing works
Recessive mutations in EPG5 cause Vici syndrome, a multisystem disorder with defective autophagy
Cullup, T., Kho, A. L., Dionisi‐Vici, C., Brandmeier, B., Smith, F., Urry, Z., Simpson, M. A., Yau, S., Bertini, E., McClelland, V. M., et al. (2012) · Nature Genetics · doi:10.1038/ng.2497 · Cited by 282 · see citing works
Life in the balance – a mechanistic view of the crosstalk between autophagy and apoptosis
Rubinstein, A. D., & Kimchi, A. (2012) · Journal of Cell Science · doi:10.1242/jcs.115865 · Cited by 248 · see citing works
Autophagy in stem cells: repair, remodelling and metabolic reprogramming
Boya, P., Codogno, P., & Rodriguez-Muela, N. (2018) · Development · doi:10.1242/dev.146506 · Cited by 197 · see citing works
Macrophages clean up: efferocytosis and microbial control
Martin, C. J., Peters, K. N., & Behar, S. M. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.10.007 · Cited by 177 · see citing works
Reiner, D. J. (2016) · WormBook · doi:10.1895/wormbook.1.67.2 · Cited by 152 · see citing works
Mokarram, P., Albokashy, M., Zarghooni, M., Moosavi, M. A., Sepehri, Z., Chen, Q. M., Hudecki, A., Sargazi, A., Alizadeh, J., Moghadam, A. R., et al. (2017) · Autophagy · doi:10.1080/15548627.2017.1290751 · Cited by 149 · see citing works
Morishita, H., Eguchi, S., Kimura, H., Sasaki, J., Sakamaki, Y., Robinson, M. L., Sasaki, T., & Mizushima, N. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.437103 · Cited by 141 · see citing works
Autophagy is essential for cardiac morphogenesis during vertebrate development
Lee, E., Koo, Y., Ng, A., Wei, Y., Luby‐Phelps, K., Juraszek, A. L., Xavier, R. J., Cleaver, O. B., Levine, B., & Amatruda, J. F. (2014) · Autophagy · doi:10.4161/auto.27649 · Cited by 140 · see citing works
Autophagy proteins in macroendocytic engulfment
Florey, O., & Overholtzer, M. (2012) · Trends in Cell Biology · doi:10.1016/j.tcb.2012.04.005 · Cited by 132 · see citing works
Autophagy in animal development
Allen, E. A., & Baehrecke, E. H. (2020) · Cell Death & Differentiation · doi:10.1038/s41418-020-0497-0 · Cited by 127 · see citing works
Hidden Behind Autophagy: The Unconventional Roles of ATG Proteins
Bestebroer, J., V’kovski, P., Mauthe, M., & Reggiori, F. (2013) · Traffic · doi:10.1111/tra.12091 · Cited by 120 · see citing works
LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy
Lai, S.-C., & Devenish, R. J. (2012) · Cells · doi:10.3390/cells1030396 · Cited by 116 · see citing works
“between PI3P binding at the membrane and recruitment of LC3 in this process [34].”
BackgroundProgrammed Cell Death DuringCaenorhabditis elegansDevelopment
Conradt, B., Wu, Y., & Xue, D. (2016) · Genetics · doi:10.1534/genetics.115.186247 · Cited by 111 · see citing works
Eaten alive: novel insights into autophagy from multicellular model systems
Zhang, H., & Baehrecke, E. H. (2015) · Trends in Cell Biology · doi:10.1016/j.tcb.2015.03.001 · Cited by 102 · see citing works
C. elegans as a model for membrane traffic
Sato, K. (2014) · WormBook · doi:10.1895/wormbook.1.77.2 · Cited by 99 · see citing works
Chen, M., Zhong, G., Liu, M., He, H., Zhou, J., Chen, J., Zhang, M., Liu, Q., Tong, G., Luan, J., et al. (2023) · Pharmacological Research · doi:10.1016/j.phrs.2023.106682 · Cited by 98 · see citing works
Tzelepis, F., Verway, M. J., Daoud, J., Gillard, J., Hassani‐Ardakani, K., Dunn, J. L., Downey, J., Gentile, M., Jaworska, J., Sanchez, A. M. J., et al. (2014) · Journal of Clinical Investigation · doi:10.1172/jci77014 · Cited by 93 · see citing works
Autophagy and its implication in human oral diseases
Tan, Y., Zhang, J., & Zhou, G. (2016) · Autophagy · doi:10.1080/15548627.2016.1234563 · Cited by 88 · see citing works
Autophagy and Intestinal Homeostasis
Patel, K., & Stappenbeck, T. S. (2012) · Annual Review of Physiology · doi:10.1146/annurev-physiol-030212-183658 · Cited by 84 · see citing works
Live imaging of cellular dynamics during Caenorhabditis elegans postembryonic development
Chai, Y., Li, W., Feng, G., Yang, Y., Wang, X., & Ou, G. (2012) · Nature Protocols · doi:10.1038/nprot.2012.128 · Cited by 77 · see citing works
Self-citationGuidelines for the use and interpretation of assays for monitoring autophagy (3rd edition)
Klionsky, D. J., Abdelmohsen, K., Abe, A., Abedin, J., Abeliovich, H., Acevedo‐Arozena, A., Adachi, H., Adams, C. M., Adams, P. D., Adeli, K., et al. (2016) · Kölner Universitäts PublikationsServer (Universität zu Köln) · doi:10.5167/uzh-131237 · Cited by 69 · see citing works
Autophagy genes function in apoptotic cell corpse clearance duringC. elegansembryonic development
Huang, S., Jia, K., Wang, Y., Zhou, Z., & Levine, B. (2012) · Autophagy · doi:10.4161/auto.22352 · Cited by 57 · see citing works
Etchegaray, J. I., Elguero, E. J., Tran, J. A., Sinatra, V., Feany, M. B., & McCall, K. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.1912-15.2016 · Cited by 55 · see citing works
Minnerly, J., Zhang, J., Parker, T., Kaul, T. K., & Jia, K. (2017) · PLoS Genetics · doi:10.1371/journal.pgen.1006764 · Cited by 55 · see citing works
WIPI-Mediated Autophagy and Longevity
Grimmel, M., Backhaus, C., & Proikas‐Cezanne, T. (2015) · Cells · doi:10.3390/cells4020202 · Cited by 51 · see citing works
Development and migration of the C. elegans Q neuroblasts and their descendants
Middelkoop, T. C., & Korswagen, H. C. (2014) · WormBook · doi:10.1895/wormbook.1.173.1 · Cited by 48 · see citing works
Autophagy in C. elegans development
Palmisano, N. J., & Meléndez, A. (2018) · Developmental Biology · doi:10.1016/j.ydbio.2018.04.009 · Cited by 48 · see citing works
Kim, H., Calatayud, C., Guha, S. K., Fernández‐Carasa, I., Berkowitz, L. A., Carballo‐Carbajal, I., Ezquerra, M., Fernández‐Santiago, R., Kapahi, P., Raya, Á., et al. (2018) · Molecular Neurobiology · doi:10.1007/s12035-018-0881-7 · Cited by 46 · see citing works
Autophagy During Vertebrate Development
Aburto, M. R., Hurlé, J. M., Varela‐Nieto, I., & Magariños, M. (2012) · Cells · doi:10.3390/cells1030428 · Cited by 45 · see citing works
Cheng, S., Wu, Y., Lu, Q., Yan, J., Zhang, H., & Wang, X. (2013) · Autophagy · doi:10.4161/auto.26323 · Cited by 44 · see citing works
Self-citationDjeddi, A., Rawi, S. A., Deuve, J. L., Perrois, C., Liu, Y.-Y., Russeau, M., Sachse, M., & Galy, V. (2015) · Development · doi:10.1242/dev.117879 · Cited by 44 · see citing works
Apoptotic regulators promote cytokinetic midbody degradation in C. elegans
Chai, Y., Tian, D., Yang, Y., Feng, G., Cheng, Z., Li, W., & Ou, G. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201209050 · Cited by 41 · see citing works
Self-citationYang, Y., Zhang, Y., Li, W.-J., Jiang, Y., Zhu, Z., Hu, H., Li, W., Wu, J., Wang, Z., Dong, M., et al. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.03.006 · Cited by 39 · see citing works
Self-citationDynamic Regulation of Autophagy and Endocytosis for Cell Remodeling During Early Development
Sato, M., & Sato, K. (2013) · Traffic · doi:10.1111/tra.12050 · Cited by 38 · see citing works
Molecular and cellular mechanisms of macrophage survival in atherosclerosis
Martinet, W., Schrijvers, D. M., & Meyer, G. R. Y. D. (2012) · Basic Research in Cardiology · doi:10.1007/s00395-012-0297-x · Cited by 37 · see citing works
Mortari, E. P., Folgiero, V., Marcellini, V., Romania, P., Bellacchio, E., D’Alicandro, V., Bocci, C., Carrozzo, R., Martinelli, D., Petrini, S., et al. (2017) · Autophagy · doi:10.1080/15548627.2017.1389356 · Cited by 35 · see citing works
Peña-Ramos, O., Chiao, L. J., Liu, X., Yu, X., Yao, T., He, H., & Zhou, Z. (2022) · eLife · doi:10.7554/elife.72466 · Cited by 35 · see citing works
Bu, T., Wang, C., Jin, H., Meng, Q., Huo, X., Sun, H., Sun, P., Wu, J., Ma, X., Liu, Z., et al. (2019) · Journal of Cellular Physiology · doi:10.1002/jcp.29218 · Cited by 34 · see citing works
Common alleles that influence autophagy and the risk for inflammatory bowel disease
Gardet, A., & Xavier, R. J. (2012) · Current Opinion in Immunology · doi:10.1016/j.coi.2012.08.001 · Cited by 32 · see citing works
Detection of Autophagy in Caenorhabditis elegans Using GFP::LGG-1 as an Autophagy MarkerPreprint
Palmisano, N. J., & Meléndez, A. (2016) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot086496 · Cited by 32 · see citing works
Autophagy and lysosomal pathways in nervous system disorders
Bingol, B. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.04.009 · Cited by 31 · see citing works
Autophagy & Phagocytosis in Neurological Disorders and their Possible Cross-talk
Li, G., Sherchan, P., Tang, Z., & Tang, J. (2021) · Current Neuropharmacology · doi:10.2174/1570159x19666210407150632 · Cited by 29 · see citing works
The Presence of Autophagy in Human Periapical Lesions
Zhu, L., Yang, J., Zhang, J., & Peng, B. (2013) · Journal of Endodontics · doi:10.1016/j.joen.2013.07.013 · Cited by 27 · see citing works
Safely removing cell debris with LC3‐associated phagocytosis
Fazeli, G., & Wehman, A. M. (2017) · Biology of the Cell · doi:10.1111/boc.201700028 · Cited by 27 · see citing works
ULK1-mediated phosphorylation regulates the conserved role of YKT6 in autophagy
Sánchez‐Martín, P., Kriegenburg, F., Alves, L. M., Adam, J., Elsaesser, J., Babic, R., Mancilla, H., Licheva, M., Tascher, G., Münch, C., et al. (2023) · Journal of Cell Science · doi:10.1242/jcs.260546 · Cited by 26 · see citing works
Jenzer, C., Simionato, E., Largeau, C., Scarcelli, V., Lefebvre, C., & Legouis, R. (2018) · Autophagy · doi:10.1080/15548627.2018.1512452 · Cited by 26 · see citing works
Cytoprotective effect of autophagy on phagocytosis of apoptotic cells by macrophages
Zhou, P., Tan, Y., Wang, H., Li, T., He, T., Yu, Y., Zhang, J., & Zhang, D. (2016) · Experimental Cell Research · doi:10.1016/j.yexcr.2016.09.011 · Cited by 21 · see citing works
C. elegans CEP-1/p53 and BEC-1 Are Involved in DNA Repair
Hoffman, S., Martin, D., Meléndez, A., & Bargonetti, J. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088828 · Cited by 21 · see citing works
Cleaning up the mess: cell corpse clearance in Caenorhabditis elegans
Pinto, S. M., & Hengartner, M. O. (2012) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2012.11.002 · Cited by 20 · see citing works
Picazarri, K., Nakada‐Tsukui, K., Tsuboi, K., Miyamoto, E., Watanabe, N., Kawakami, E., & Nozaki, T. (2015) · Cellular Microbiology · doi:10.1111/cmi.12453 · Cited by 20 · see citing works
Tools and methods to analyze autophagy in C. elegans
Jenzer, C., Simionato, E., & Legouis, R. (2014) · Methods · doi:10.1016/j.ymeth.2014.11.019 · Cited by 19 · see citing works
CED-10-WASP-Arp2/3 signaling axis regulates apoptotic cell corpse engulfment in C. elegans
Wu, D., Chai, Y., Zhu, Z., Li, W., Ou, G., & Li, W. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.06.005 · Cited by 18 · see citing works
Self-citationChen, M., Huang, F., Chen, B., Kang, J., Yao, Y., Liu, M., Li, Y., Li, Y., Zhou, T., Peng, D., et al. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.115831 · Cited by 15 · see citing works
Self-citationC. elegans to model autophagy-related human disorders
Wong, S. Q., Kumar, A. V., Mills, J., & Lapierre, L. R. (2020) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2020.01.007 · Cited by 14 · see citing works
Detection of Autophagy inCaenorhabditis elegansPreprint
Palmisano, N. J., & Meléndez, A. (2016) · Cold Spring Harbor Protocols · doi:10.1101/pdb.top070466 · Cited by 13 · see citing works
The developmental and physiological roles of phagocytosis in Caenorhabditis elegans
Ghose, P., & Wehman, A. M. (2020) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2020.09.001 · Cited by 11 · see citing works
Lysosome Biogenesis and Autophagy
Reggiori, F., & Klumperman, J. (2016) · Wiley eBooks · doi:10.1002/9781118978320.ch2 · Cited by 11 · see citing works
Conserved components of the macroautophagy machinery in Caenorhabditis elegans
Zhang, H., & Meléndez, A. (2025) · Genetics · doi:10.1093/genetics/iyaf007 · Cited by 10 · see citing works
Lysosomal nucleotide metabolism regulates ER proteostasis through mTOR signalingPreprint
Mak, K. H., Zhao, Q., Hu, P.-W., Au-Yeung, C.-L., Yang, J., Duraine, L., Yu, Y., Abu-Remaileh, M., Sabatini, D. M., Wang, J. D., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.18.048561 · Cited by 10 · see citing works
Fang, J., Wang, J., Wang, Y., Liu, X., Chen, B., & Zou, W. (2023) · Communications Biology · doi:10.1038/s42003-023-05184-4 · Cited by 9 · see citing works
Self-citationThe role of autophagy in odontogenesis, dental implant surgery, periapical and periodontal diseases
İnan, S., & BARIŞ, E. (2024) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.18297 · Cited by 9 · see citing works
Functions of Arp2/3 Complex in the Dynamics of Epithelial Tissues
Martin, E., & Suzanne, M. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.886288 · Cited by 9 · see citing works
Autophagy: New Questions from Recent Answers
Reggiori, F. (2012) · ISRN Molecular Biology · doi:10.5402/2012/738718 · Cited by 8 · see citing works
Methods to Determine the Role of Autophagy Proteins in C. elegans Aging
Henis‐Korenblit, S., & Meléndez, A. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-8873-0_37 · Cited by 4 · see citing works
EPG5 and Vici syndrome: a review of pathogenesis, clinical features, and therapeutic advances
Yang, X., Liu, X., Yang, Y. T., & Lu, Q. (2025) · Genome Instability & Disease · doi:10.1007/s42764-025-00170-y · Cited by 3 · see citing works
Self-citationPhagolysosomes break down the membrane of a non-apoptotic corpse independent of macroautophagy
Kolli, S., Kline, C. J., Rad, K. M., & Wehman, A. M. (2024) · PLoS ONE · doi:10.1371/journal.pone.0306435 · Cited by 4 · see citing works
Les multiples facettes de l’autophagie au cours du développement
Jenzer, C., & Legouis, R. (2017) · médecine/sciences · doi:10.1051/medsci/20173303009 · Cited by 3 · see citing works
Martin, E., Bonnamour, G., & Jenna, S. (2017) · Small GTPases · doi:10.1080/21541248.2017.1372868 · Cited by 2 · see citing works
Nedelsky, N. B., Kuballa, P., Castoreno, A. B., & Xavier, R. J. (2019) · Springer eBooks · doi:10.1007/978-3-030-28703-0_14 · Cited by 2 · see citing works
Target Autophagy as a Novel Therapeutic Strategy in Autoimmune Diseases
Wilhelm, M., & Muller, S. (2016) · Springer eBooks · doi:10.1007/978-3-319-30079-5_13 · Cited by 1 · see citing works
Li, W., Zou, W., Yang, Y., Chai, Y., Chen, B., Cheng, S., Tian, D., Wang, X., Vale, R. D., & Ou, G. (2012) · The Journal of Experimental Medicine · doi:10.1084/jem2094oia5 · Cited by 1 · see citing works
Self-citationBetsuyaku, T., Ito, Y., Peake, N., Al‐Bari, M. A. A., El–Akabawy, G., & Eid, N. A. S. (2024) · PubMed · doi:10.14670/hh-18-729 · Cited by 1 · see citing works
PIKI-1, a class II PI 3-kinase, functions in endocytic trafficking
Reimann, G. R., Edeen, P. T., Conquest, S., Grant, B. D., & Fay, D. S. (2026) · PLoS Genetics · doi:10.1371/journal.pgen.1011740 · Cited by 1 · see citing works
Nedelsky, N. B., Kuballa, P., Castoreno, A. B., & Xavier, R. J. (2013) · Springer eBooks · doi:10.1007/978-1-4614-8256-7_12 · Cited by 1 · see citing works
Autophagy in Model Organisms: Insights into Cancer
Possik, E., & Pause, A. (2016) · InTech eBooks · doi:10.5772/64541 · Cited by 1 · see citing works
Peña-Ramos, O., Chiao, L., Liu, X., Yu, X., Yao, T., He, H., & Zhou, Z. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.07.16.452694 · Cited by 1 · see citing works
Guangshuo Ou: New perspectives on Q cell biology
Sedwick, C. E. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.2072pi
- Authors
- Li, W., Zou, W., Yang, Y., Chai, Y., Chen, B., Cheng, S., Tian, D., Wang, X., Vale, R. D., & Ou, G.
- Affiliations
- Chinese Academy of Sciences (CN)
- National Institute of Biological Sciences, Beijing (CN)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Wang, Xiaochen
- Vale, Ronald D.
- Ou, Guangshuo
- ORCID
- Venue
- Journal of Cell Biology
- Publisher
- Rockefeller University Press
- Published
- 2012-03-26
- Volume
- 197
- Issue
- 1
- Pages
- 27-35
- ISSN
- 0021-9525 (ISSN-L)
- 1540-8140
- PMC
- PMC3317810
- OpenAlex
- W2131771296
- Cited by
- 84
- References
- 30
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 3 · 2023: 4 · 2022: 2 · 2021: 3 · 2020: 5 · 2019: 4 · 2018: 6 · 2017: 8 · 2016: 12 · 2015: 5 · 2014: 8 · 2013: 7 · 2012: 14
- FWCI
- 8.14
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- Locations
- The Journal of Cell Biology (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Keywords
- autophagy, efferocytosis, phagocytosis, phagosome, phagolysosomes, Caenorhabditis elegans, Rab5, Rab7, live-cell imaging
- MeSH terms
- Animals, Autophagy, Lysosomes, Mutation, Phagocytes, Phagocytosis, Phagosomes, Phenotype, Caenorhabditis elegans, Apoptosis, Caenorhabditis elegans Proteins, Vesicular Transport Proteins
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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