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A pathway for phagosome maturation during engulfment of apoptotic cells
Open accessAbstract
Removal of apoptotic cells is critical for the physiological well-being of the organism and defects in corpse removal have been linked to disease states. Genes regulating corpse recognition and internalization have been identified, but few molecules involved in the processing of internalized corpses are known. Through a combination of targeted and unbiased reverse genetic screens in Caenorhabditis elegans, and studies in mammalian cells, we have identified genes required for maturation of apoptotic-cell-containing phagosomes. We have further ordered these candidates, which include the GTPases RAB-5 and RAB-7 and the HOPS complex, into a coherent linear pathway for the maturation of apoptotic cells within phagosomes. In depth analysis of two additional candidate genes, the phosphatidylinositol 3 kinase (PI(3)K) vps-34 (A001762) and dyn-1/dynamin, showed an accumulation of internalized, but undegraded, corpses within abnormal Rab5-negative phagosomes. We ordered these candidates in our pathway, with DYN-1 functioning upstream of VPS-34 in the recruitment and/or retention of RAB-5 to the phagosome. Finally, we have also identified a previously undescribed biochemical complex containing Vps34, dynamin and Rab5(GDP), thus providing a mechanism for Rab5 recruitment to the nascent phagosome.
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“Efferosomes containing apoptotic material follow a similar succession as phagosomes going from an early to late endosomal to phagolysosomal stages as indicated by differential association with marker proteins such as the small GTPases Rab5 and Rab7, Vsp34 and dynamin, Lamp-1, and finally lysosomal hydrolases (136) (Fig. 1).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [136]
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Cites
THE GENETICS OF CAENORHABDITIS ELEGANS
Brenner, S. (1974) · Genetics · doi:10.1093/genetics/77.1.71 · Cited by 15,220
Systematic functional analysis of the Caenorhabditis elegans genome using RNAi
Kamath, R. S., Fraser, A. G., Yan, D., Poulin, G. B., Durbin, R. M., Gotta, M., Kanapin, A. A., Bot, N. L., Moreno, S., Sohrmann, M., et al. (2003) · Nature · doi:10.1038/nature01278 · Cited by 3,629
Mello, C. C., Kramer, J. M., Stinchcomb, D. T., & Ambros, V. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb04966.x · Cited by 3,095
Rab Conversion as a Mechanism of Progression from Early to Late Endosomes
Rink, J. C., Ghigo, É., Kalaidzidis, Y. L., & Zerial, M. (2005) · Cell · doi:10.1016/j.cell.2005.06.043 · Cited by 1,680
Corpse clearance defines the meaning of cell death
Savill, J., & Fadok, V. A. (2000) · Nature · doi:10.1038/35037722 · Cited by 1,572
Phagocytosis and clearance of apoptotic cells is mediated by MER
Scott, R. S., McMahon, E. J., Pop, S. M., Reap, E. A., Caricchio, R., Cohen, P. L., Earp, H. S., & Matsushima, G. K. (2001) · Nature · doi:10.1038/35075603 · Cited by 1,215
Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells
Gillooly, D. J., Morrow, I. C., Lindsay, M., Gould, R., Bryant, N. J., Gaullier, J., Parton, R. G., & Stenmark, H. (2000) · The EMBO Journal · doi:10.1093/emboj/19.17.4577 · Cited by 1,031
Rabs and their effectors: achieving specificity in membrane traffic
Grosshans, B. L., Ortiz, D., & Novick, P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601617103 · Cited by 1,005
Regulation of Phagosome Maturation by Signals from Toll-Like Receptors
Blander, J. M., & Medzhitov, R. (2004) · Science · doi:10.1126/science.1096158 · Cited by 991
Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG
Liang, C., Feng, P., Ku, B., Dotan, I., Canaani, D., Oh, B.-H., & Jung, J. U. (2006) · Nature Cell Biology · doi:10.1038/ncb1426 · Cited by 919
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The emerging mechanisms of isoform-specific PI3K signalling
Vanhaesebroeck, B., Guillermet-Guibert, J., Graupera, M., & Bilanges, B. (2010) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2882 · Cited by 1,767
Macrophage defense mechanisms against intracellular bacteria
Weiss, G., & Schaible, U. E. (2015) · Immunological Reviews · doi:10.1111/imr.12266 · Cited by 989
Apoptosis and apoptotic body: disease message and therapeutic target potentials
Xu, X., Lai, Y., & Hua, Z. (2018) · Bioscience Reports · doi:10.1042/bsr20180992 · Cited by 953
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Kalra, H., Drummen, G. P. C., & Mathivanan, S. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17020170 · Cited by 906
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
Self-citationRetractedBeginnings of a Good Apoptotic Meal: The Find-Me and Eat-Me Signaling Pathways
Ravichandran, K. S. (2011) · Immunity · doi:10.1016/j.immuni.2011.09.004 · Cited by 559
Self-citationClearance 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 568
Self-citationCORVET and HOPS tethering complexes – coordinators of endosome and lysosome fusion
Balderhaar, H. J. K., & Ungermann, C. (2013) · Journal of Cell Science · doi:10.1242/jcs.107805 · Cited by 527
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
Self-citationClearing the Dead: Apoptotic Cell Sensing, Recognition, Engulfment, and Digestion
Hochreiter-Hufford, A., & Ravichandran, K. S. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008748 · Cited by 503
Self-citationFlorey, O., Kim, S. E., Sandoval, C. P., Haynes, C. M., & Overholtzer, M. (2011) · Nature Cell Biology · doi:10.1038/ncb2363 · Cited by 459
Phospholipase D: Enzymology, Functionality, and Chemical Modulation
Selvy, P. E., Lavieri, R. R., Lindsley, C. W., & Brown, H. A. (2011) · Chemical Reviews · doi:10.1021/cr200296t · Cited by 406
GTPase Networks in Membrane Traffic
Mizuno-Yamasaki, E., Rivera-Molina, F. E., & Novick, P. (2012) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052810-093700 · Cited by 366
Liu, D., Kou, X., Chen, C., Liu, S., Liu, Y., Yu, W., Yu, T., Yang, R., Wang, R., Zhou, Y., et al. (2018) · Cell Research · doi:10.1038/s41422-018-0070-2 · Cited by 298
The life cycle of phagosomes: formation, maturation, and resolution
Levin‐Konigsberg, R., Grinstein, S., & Canton, J. (2016) · Immunological Reviews · doi:10.1111/imr.12439 · Cited by 328
How nascent phagosomes mature to become phagolysosomes
Fairn, G. D., & Grinstein, S. (2012) · Trends in Immunology · doi:10.1016/j.it.2012.03.003 · Cited by 313
Cai, S., Zhao, M., Zhou, B., Yoshii, A., Bugg, D., Villet, O. M., Sahu, A., Olson, G. S., Davis, J., & Tian, R. (2022) · Journal of Clinical Investigation · doi:10.1172/jci159498 · Cited by 290
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Heckmann, B. L., Boada-Romero, E., Cunha, L. D., Magne, J., & Green, D. R. (2017) · Journal of Molecular Biology · doi:10.1016/j.jmb.2017.08.012 · Cited by 276
Legionella and Coxiella effectors: strength in diversity and activity
Qiu, J., & Luo, Z. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.67 · Cited by 266
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The intricate regulation and complex functions of the Class III phosphoinositide 3-kinase Vps34
Backer, J. (2016) · Biochemical Journal · doi:10.1042/bcj20160170 · Cited by 247
How apoptotic cells aid in the removal of their own cold dead bodies
Wickman, G., Julian, L., & Olson, M. F. (2012) · Cell Death and Differentiation · doi:10.1038/cdd.2012.25 · Cited by 241
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Hyenne, V., Apaydin, A., Rodriguez, D., Spiegelhalter, C., Hoff-Yoessle, S., Diem, M., Tak, S., Lefèbvre, O., Schwab, Y., Goetz, J. G., et al. (2015) · The Journal of Cell Biology · doi:10.1083/jcb.201504136 · Cited by 244
Insulin Regulates Adipocyte Lipolysis via an Akt-Independent Signaling Pathway
Choi, S. M., Tucker, D. F., Gross, D. N., Easton, R., DiPilato, L. M., Dean, A. S., Monks, B. R., & Birnbaum, M. J. (2010) · Molecular and Cellular Biology · doi:10.1128/mcb.00797-10 · Cited by 223
Henson, P. M. (2017) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111315-125315 · Cited by 208
Tethering complexes in the endocytic pathway: CORVET and HOPS
Solinger, J. A., & Spang, A. (2013) · FEBS Journal · doi:10.1111/febs.12151 · Cited by 192
Medina, C. B., & Ravichandran, K. S. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2016.13 · Cited by 199
Self-citationGartner, A., Boag, P. R., & Blackwell, T. K. (2008) · WormBook · doi:10.1895/wormbook.1.145.1 · Cited by 192
Beclin 1, an Essential Component and Master Regulator of PI3K-III in Health and Disease
McKnight, N. C., & Yue, Z. (2013) · Current Pathobiology Reports · doi:10.1007/s40139-013-0028-5 · Cited by 168
Cullinane, A. R., Straatman-Iwanowska, A. A., Zaucker, A., Wakabayashi, Y., Bruce, C. K., Luo, G., Rahman, F., Gürakan, F., Ütine, E., Özkan, T., et al. (2010) · Nature Genetics · doi:10.1038/ng.538 · Cited by 184
SLAM is a microbial sensor that regulates bacterial phagosome functions in macrophages
Berger, S. B., Ros, X. R., Ma, C., Wang, G., Faubion, W. A., Liao, G., Compeer, E. B., Keszei, M., Rameh, L. E., Wang, N., et al. (2010) · Nature Immunology · doi:10.1038/ni.1931 · Cited by 184
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 193
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Minciacchi, V. R., Spinelli, C., Reis-Sobreiro, M., Cavallini, L., You, S., Zandian, M., Li, X., Mishra, R., Chiarugi, P., Adam, R. M., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-16-2942 · Cited by 168
Rab7: roles in membrane trafficking and disease
Zhang, M., Chen, L., Wang, S., & Wang, T. (2009) · Bioscience Reports · doi:10.1042/bsr20090032 · Cited by 157
Sun, Q., Zhang, J., Fan, W., Wong, K. N., Ding, X., Chen, S., & Zhong, Q. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.126425 · Cited by 153
Multiple functions of the noncanonical Wnt pathway
Gómez‐Orte, E., Sáenz‐Narciso, B., Moreno, S., & Cabello, J. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.06.003 · Cited by 153
Reiner, D. J. (2016) · WormBook · doi:10.1895/wormbook.1.67.2 · Cited by 164
Wu, Y., Huo, L., Maeder, C. I., Feng, W., & Shen, K. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.035 · Cited by 144
Gratz, N., Hartweger, H., Matt, U., Kratochvill, F., Janos, M., Sigel, S., Drobits, B., Li, X.-D., Knapp, S., & Kovarik, P. (2011) · PLoS Pathogens · doi:10.1371/journal.ppat.1001345 · Cited by 131
Cellular and nuclear degradation during apoptosis
He, B., Lü, N., & Zhou, Z. (2009) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.08.008 · Cited by 131
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Nguyen, J. A., & Yates, R. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.636078 · Cited by 135
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Melcarne, C., Lemaître, B., & Kurant, E. (2019) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2019.04.002 · Cited by 121
Li, Y., Liew, Y. J., Cui, G., Cziesielski, M. J., Zahran, N., Michell, C., Voolstra, C. R., & Aranda, M. (2018) · Science Advances · doi:10.1126/sciadv.aat2142 · Cited by 118
In vivo characterization of microglial engulfment of dying neurons in the zebrafish spinal cord
Morsch, M., Radford, R. A. W., Lee, A., Don, E. K., Badrock, A. P., Hall, T. E., Cole, N. J., & Chung, R. S. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00321 · Cited by 115
Ruck, A., Attonito, J., Garces, K. T., Nuñez, L., Palmisano, N. J., Rubel, Z., Bai, Z., Nguyen, K. C. Q., Sun, L., Grant, B. D., et al. (2011) · Autophagy · doi:10.4161/auto.7.4.14391 · Cited by 115
Maekawa, M., Shimpei, T., Mochizuki, Y., Kawai, K., Ikeda, Y., Araki, N., Skolnik, E. Y., Taguchi, T., & Arai, H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311029111 · Cited by 113
Programmed Cell Death DuringCaenorhabditis elegansDevelopment
Conradt, B., Wu, Y., & Xue, D. (2016) · Genetics · doi:10.1534/genetics.115.186247 · Cited by 116
C. elegans as a model for membrane traffic
Sato, K. (2014) · WormBook · doi:10.1895/wormbook.1.77.2 · Cited by 103
Genetic control of cellular quiescence in S. pombe
Sajiki, K., Hatanaka, M., Nakamura, T., Takeda, K., Shimanuki, M., Yoshida, T., Hanyu, Y., Hayashi, T., Nakaseko, Y., & Yanagida, M. (2009) · Journal of Cell Science · doi:10.1242/jcs.046466 · Cited by 103
Phagosome maturation in polarized macrophages
Canton, J. (2014) · Journal of Leukocyte Biology · doi:10.1189/jlb.1mr0114-021r · Cited by 115
Clearance of Dying Cells by Phagocytes: Mechanisms and Implications for Disease Pathogenesis
Fond, A. M., & Ravichandran, K. S. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-39406-0_2 · Cited by 97
Self-citationWong, D., Chao, J. D., & Av‐Gay, Y. (2012) · Trends in Microbiology · doi:10.1016/j.tim.2012.09.002 · Cited by 96
Hawkins, P. T., Stephens, L., Suire, S., & Wilson, M. I. (2010) · Current topics in microbiology and immunology · doi:10.1007/82_2010_40 · Cited by 102
Wu, M.-Y., Liu, L., Wang, E., Xiao, H., Cai, C.-Z., Wang, J., Su, H., Wang, Y., Tan, J., Zhang, Z., et al. (2020) · Autophagy · doi:10.1080/15548627.2020.1741332 · Cited by 98
Gronski, M. A., Kinchen, J. M., Juncadella, I. J., Franc, N. C., & Ravichandran, K. S. (2009) · Cell Death & Differentiation · doi:10.1038/cdd.2009.55 · Cited by 92
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Yin, C., & Heit, B. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.631714 · Cited by 101
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Chotard, L., Mishra, A. K., Sylvain, M.-A., Tuck, S., Lambright, D. G., & Rocheleau, C. E. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-11-0947 · Cited by 90
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 86
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Wang, S., Zhang, J., Zhou, H., Lu, Y. C., Jin, X., Luo, L., & Jian, Y. (2023) · Journal of Controlled Release · doi:10.1016/j.jconrel.2023.06.014 · Cited by 85
Anti-Inflammatory Neutrophil Functions in the Resolution of Inflammation and Tissue Repair
Loh, W., & Vermeren, S. (2022) · Cells · doi:10.3390/cells11244076 · Cited by 92
Ichino, T., Fuji, K., Ueda, H., Takahashi, H., Koumoto, Y., Takagi, J., Tamura, K., Sasaki, R., Aoki, K., Shimada, T., et al. (2014) · The Plant Journal · doi:10.1111/tpj.12637 · Cited by 83
Kim, S., Wairkar, Y. P., Daniels, R. W., & DiAntonio, A. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200911126 · Cited by 82
Keller, C. W., Sina, C., Kotur, M. B., Ramelli, G., Mundt, S., Quast, I., Ligeon, L.-A., Weber, P., Becher, B., Münz, C., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713664114 · Cited by 81
Vertebrate Epidermal Cells Are Broad-Specificity Phagocytes That Clear Sensory Axon Debris
Rasmussen, J. P., Sack, G. S., Martin, S. M., & Sagasti, A. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3613-14.2015 · Cited by 82
Rab4 Orchestrates a Small GTPase Cascade for Recruitment of Adaptor Proteins to Early Endosomes
D’Souza, R. S., Semus, R., Billings, E. A., Meyer, C. B., Conger, K. K., & Casanova, J. E. (2014) · Current Biology · doi:10.1016/j.cub.2014.04.003 · Cited by 81
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Roy, S., Bag, A. K., Dutta, S., Polavaram, N. S., Islam, R., Schellenburg, S., Banwait, J., Guda, C., Ran, S., Hollingsworth, M. A., et al. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-0562 · Cited by 80
Dynamin‐Actin Cross Talk Contributes to Phagosome Formation and Closure
Marie‐Anaïs, F., Mazzolini, J., Herit, F., & Niedergang, F. (2016) · Traffic · doi:10.1111/tra.12386 · Cited by 78
Cherry, S., Jin, E. J., Özel, M. N., Lu, Z., Agi, E., Wang, D., Jung, W., Epstein, D. J., Meinertzhagen, I. A., Chan, C., et al. (2013) · eLife · doi:10.7554/elife.01064 · Cited by 79
After cell death: the molecular machinery of efferocytosis
Moon, B., Yang, S., Moon, H., Lee, J., & Park, D. (2023) · Experimental & Molecular Medicine · doi:10.1038/s12276-023-01070-5 · Cited by 78
Lü, N., Shen, Q., Mahoney, T. R., Neukomm, L. J., Wang, Y., & Zhou, Z. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001245 · Cited by 76
The full-of-bacteria gene is required for phagosome maturation during immune defense in Drosophila
Akbar, M. A., Tracy, C., Kahr, W. H. A., & Krämer, H. (2011) · The Journal of Cell Biology · doi:10.1083/jcb.201008119 · Cited by 74
Phagosome maturation during the removal of apoptotic cells: receptors lead the way
Zhou, Z., & Yu, X. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.08.002 · Cited by 71
Programmed elimination of cells by caspase-independent cell extrusion in C. elegans
Denning, D. P., Hatch, V., & Horvitz, H. R. (2012) · Nature · doi:10.1038/nature11240 · Cited by 69
Li, W., Zou, W., Zhao, D., Yan, J., Zhu, Z., Lu, J., & Wang, X. (2009) · Development · doi:10.1242/dev.035949 · Cited by 65
Membrane Trafficking and Phagosome Maturation During the Clearance of Apoptotic Cells
Lü, N., & Zhou, Z. (2012) · International review of cytology · doi:10.1016/b978-0-12-394304-0.00013-0 · Cited by 61
Nakae, I., Fujino, T., Kobayashi, T., Sasaki, A., Kikko, Y., Fukuyama, M., Gengyo‐Ando, K., Mitani, S., Kontani, K., & Katada, T. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-12-1010 · Cited by 64
The Vam6-Gtr1/Gtr2 pathway activates TORC1 in response to amino acids in fission yeast
Valbuena, N., Guan, K., & Moreno, S. (2012) · Journal of Cell Science · doi:10.1242/jcs.094219 · Cited by 59
Loss of the RhoGAP SRGP-1 promotes the clearance of dead and injured cells in Caenorhabditis elegans
Neukomm, L. J., Frei, A. P., Cabello, J., Kinchen, J. M., Zaidel‐Bar, R., Ma, Z., Haney, L. B., Hardin, J. D., Ravichandran, K. S., Moreno, S., et al. (2010) · Nature Cell Biology · doi:10.1038/ncb2138 · Cited by 62
Self-citationLi, X., Jiang, Y., Liu, X., Fu, J., Du, J., Luo, Z., Xu, J., BHAWAL, U. K., Liu, Y. F., & Guo, L. (2023) · International Journal of Oral Science · doi:10.1038/s41368-023-00255-y · Cited by 61
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Gray, M. A., & Botelho, R. J. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-6581-6_1 · Cited by 59
PtdIns(4,5)P2 and PtdIns3P coordinate to regulate phagosomal sealing for apoptotic cell clearance
Cheng, S., Wang, K., Zou, W., Miao, R., Huang, Y., Wang, H., & Wang, X. (2015) · The Journal of Cell Biology · doi:10.1083/jcb.201501038 · Cited by 53
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Zou, W., Lu, Q., Zhao, D., Li, W., Mapes, J., Xie, Y., & Wang, X. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000679 · Cited by 63
Three sorting nexins drive the degradation of apoptotic cells in response to PtdIns(3)P signaling
Lü, N., Shen, Q., Mahoney, T. R., Liu, X., & Zhou, Z. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-09-0756 · Cited by 58
mTOR signaling: RAG GTPases transmit the amino acid signal
Shaw, R. J. (2008) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2008.09.005 · Cited by 58
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 59
Gervois, P., & Lambrichts, I. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01668 · Cited by 59
Miettinen, M., Pietilä, T. E., Kekkonen, R. A., Kankainen, M., Latvala, S., Pirhonen, J., Österlund, P., Korpela, R., & Julkunen, I. (2012) · Gut Microbes · doi:10.4161/gmic.21736 · Cited by 56
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
Wang, J., Barr, M. M., & Wehman, A. M. (2024) · Genetics · doi:10.1093/genetics/iyae088 · Cited by 59
Rab17 mediates differential antigen sorting following efferocytosis and phagocytosis
Yin, C., Kim, Y., Argintaru, D., & Heit, B. (2016) · Cell Death and Disease · doi:10.1038/cddis.2016.431 · Cited by 57
Denning, D. P., Hatch, V., & Horvitz, H. R. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003341 · Cited by 54
Lysosome Biogenesis Mediated byvps-18Affects Apoptotic Cell Degradation inCaenorhabditis elegans
Xiao, H., Chen, D., Fang, Z., Xu, J., Sun, X., Song, S., Liu, J., & Yang, C. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-04-0441 · Cited by 53
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Self-citationThe VPS34 PI3K negatively regulates RAB-5 during endosome maturation
Law, F., Seo, J. H., Wang, Z., DeLeon, J. L., Bolis, Y., Brown, A., Zong, W., Du, G., & Rocheleau, C. E. (2017) · Journal of Cell Science · doi:10.1242/jcs.194746 · Cited by 53
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Metadata
- Authors
- Kinchen, J. M., Doukoumetzidis, K., Almendinger, J., Stergiou, L., Tosello-Trampont, A., Sifri, C. D., Hengartner, M. O., & Ravichandran, K. S.
- Affiliations
- University of Virginia (US)
- University of Zurich (CH)
- Corresponding author
- Hengartner, Michael O.
- Ravichandran, Kodi S.
- Venue
- Nature Cell Biology
- Published
- 2008-04-20
- Volume
- 10
- Issue
- 5
- Pages
- 556-566
- ISSN
- 1465-7392 (ISSN-L)
- 1476-4679
- PMC
- PMC2851549
- OpenAlex
- W2136243038
- Cited by
- 284
- References
- 89
- Citations by year
- 2026: 5 · 2025: 14 · 2024: 10 · 2023: 18 · 2022: 16 · 2021: 15 · 2020: 8 · 2019: 6 · 2018: 17 · 2017: 15 · 2016: 24 · 2015: 15 · 2014: 19 · 2013: 21 · 2012: 21
- FWCI
- 8.61
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Cell Biology (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- National Institute of General Medical Sciences (R01GM069998, R01GM064709)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
- Keywords
- phagosome maturation, efferocytosis, corpse removal, Rab5, Rab7, HOPS complex, dynamin, phosphatidylinositol 3-kinase, Caenorhabditis elegans, phagocytosis, reverse genetic screen
- MeSH terms
- rab7 GTP-Binding Proteins, Animals, Humans, Phagocytosis, Phagosomes, Recombinant Fusion Proteins, Caenorhabditis elegans, Apoptosis, Phosphatidylinositol 3-Kinases, rab GTP-Binding Proteins, rab5 GTP-Binding Proteins, Caenorhabditis elegans Proteins, Animals, Genetically Modified, Dynamins, RNA Interference, Multiprotein Complexes
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