Clearance of apoptotic corpses
Abstract
Apoptotic corpses can be engulfed and cleared by many other cell types in addition to 'professional' phagocytes such as macrophage. Studies of several organisms have contributed to the understanding of apoptotic corpse engulfment. Two partially redundant engulfment pathways have been characterized that act even in non-professional phagocytes to promote corpse engulfment. This review summarizes some recent progress in signaling by these pathways, including the exposure of eat-me-signals on apoptotic cells, and insights from Drosophila on the roles of the bridging receptor Six Microns Under, the non-receptor tyrosine kinase Shark, and store-operated calcium release in the Draper/Ced-1 pathway of corpse recognition and internalization. The mechanism of apoptotic phagosome maturation is outlined, and possible connections between corpse engulfment and proliferation, cell competition, and immunity are discussed.
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Apoptotic cells release 'find me' and expose 'eat me' signals such as PS, lysoPS, cardiolipin, calreticulin, CD31, fractalkine, and small amounts of nucleotides, which are recognized by phagocytes promoting efferocytosis.
“Apoptotic cells release ‘find me’ and expose ‘eat me’ signals such as PS, lysoPS, cardiolipin, calreticulin, and CD31, as well as the chemokine fractalkine (CX3CL1 as recognized by CX3CR1) and small amounts of nucleotides (ATP, UTP). These ligands are recognized by phagocytes promoting efferocytosis (131, 132).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [131]
Both signaling pathways governing apoptotic cell removal converge in activation of Rho GTPases such as Rac1 to promote actin polymerization, membrane ruffling, and phagocytosis.
“Both pathways finally converge in the activation of Rho GTPases such as Rac1 to promote actin polymerization, membrane ruffling, and phagocytosis (131, 132).”
From Macrophage defense mechanisms against intracellular bacteria (2015) · cites this paper as [131]
Cites
Molecular characterization of mitochondrial apoptosis-inducing factor
Susin, S. A., Lorenzo, H. K., Zamzami, N., Marzo, I., Snow, B. E., Brothers, G. M., Mangion, J., Jacotot, E., Costantini, P., Loeffler, M., et al. (1999) · Nature · doi:10.1038/17135 · Cited by 4,060 · see citing works
Fadok, V. A., Voelker, D. R., Campbell, P. A., Cohen, J., Bratton, D. L., & Henson, P. M. (1992) · The Journal of Immunology · doi:10.4049/jimmunol.148.7.2207 · Cited by 3,321 · see citing works
A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function
Feske, S., Gwack, Y., Prakriya, M., Srikanth, S., Puppel, S.-H., Tanasă, B., Hogan, P. G., Lewis, R. S., Daly, M. J., & Rao, A. (2006) · Nature · doi:10.1038/nature04702 · Cited by 2,278 · see citing works
STIM1, an essential and conserved component of store-operated Ca2 + channel function
Roos, J., DiGregorio, P. J., Yeromin, A. V., Ohlsen, K. L., Lioudyno, M., Zhang, S., Safrina, O., Kozak, J. A., Wagner, S. L., Cahalan, M. D., et al. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200502019 · Cited by 1,819 · see citing works
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 · see citing works
Gardai, S. J., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., Bratton, D. L., Oldenborg, P.-A., Michalak, M., & Henson, P. M. (2005) · Cell · doi:10.1016/j.cell.2005.08.032 · Cited by 1,473 · see citing works
Zhang, S. L., Yu, Y., Roos, J., Kozak, J. A., Deerinck, T. J., Ellisman, M. H., Stauderman, K. A., & Cahalan, M. D. (2005) · Nature · doi:10.1038/nature04147 · Cited by 1,374 · see citing works
CRACM1 Is a Plasma Membrane Protein Essential for Store-Operated Ca 2+ Entry
Vig, M., Peinelt, C., Beck, A., Koomoa, D. L., Rabah, D., Koblan‐Huberson, M., Kraft, S., Turner, H. C., Fleig, A., Penner, R., et al. (2006) · Science · doi:10.1126/science.1127883 · Cited by 1,322 · see citing works
Calcium signalling in lymphocyte activation and disease
Feske, S. (2007) · Nature Reviews Immunology · doi:10.1038/nri2152 · Cited by 1,043 · see citing works
Minutes: Mutants of Drosophila autonomously affecting cell division rate
Morata, G., & Ripoll, P. L. (1975) · Developmental Biology · doi:10.1016/0012-1606(75)90330-9 · Cited by 983 · see citing works
BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module
Park, D., Tosello‐Trampont, A., Elliott, M. R., Lu, M., Haney, L. B., Ma, Z., Klibanov, A. L., Mandell, J. W., & Ravichandran, K. S. (2007) · Nature · doi:10.1038/nature06329 · Cited by 848 · see citing works
Surface exposure of phosphatidylserine in pathological cells
Zwaal, R. F. A., Comfurius, P., & Bevers, E. M. (2005) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-005-4527-3 · Cited by 753 · see citing works
Garin, J., Diez, R., Kieffer‐Jaquinod, S., Dermine, J.-F., Duclos, S., Gagnon, É., Sadoul, R., Rondeau, C., & Desjardins, M. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.152.1.165 · Cited by 686 · see citing works
Phagosome maturation: aging gracefully
Vieira, O. V., Botelho, R. J., & Grinstein, S. (2002) · Biochemical Journal · doi:10.1042/bj20020691 · Cited by 675 · see citing works
Desjardins, M., Huber, L., Parton, R., & Griffiths, G. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.5.677 · Cited by 673 · see citing works
Engulfment of apoptotic cells: signals for a good meal
Ravichandran, K. S., & Lorenz, U. M. (2007) · Nature reviews. Immunology · doi:10.1038/nri2214 · Cited by 634 · see citing works
Drosophila Myc Regulates Organ Size by Inducing Cell Competition
de la Cova, C., Abril, M., Bellosta, P., Gallant, P., & Johnston, L. A. (2004) · Cell · doi:10.1016/s0092-8674(04)00214-4 · Cited by 610 · 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
dMyc Transforms Cells into Super-Competitors
Moreno, E., & Basler, K. (2004) · Cell · doi:10.1016/s0092-8674(04)00262-4 · Cited by 597 · see citing works
Gumienny, T. L., Brugnera, E., Tosello-Trampont, A.-C., Kinchen, J. M., Haney, L. B., Nishiwaki, K., Walk, S. F., Nemergut, M. E., Macara, I. G., Francis, R., et al. (2001) · Cell · doi:10.1016/s0092-8674(01)00520-7 · Cited by 568 · 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
The Drosophila Cell Corpse Engulfment Receptor Draper Mediates Glial Clearance of Severed Axons
MacDonald, J. M., Beach, M. G., Porpiglia, E., Sheehan, A. E., Watts, R. J., & Freeman, M. R. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.028 · Cited by 523 · see citing works
Metabolism and functions of phosphatidylserine
VANCE, J., & Steenbergen, R. (2005) · Progress in Lipid Research · doi:10.1016/j.plipres.2005.05.001 · Cited by 506 · see citing works
Bratton, D. L., Fadok, V. A., Richter, D., Kailey, J. M., Guthrie, L. A., & Henson, P. M. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.42.26159 · Cited by 485 · see citing works
Eater, a Transmembrane Protein Mediating Phagocytosis of Bacterial Pathogens in Drosophila
Kocks, C., Cho, J. H., Nehme, N. T., Ulvila, J., Pearson, A. M., Meister, M. F., Strom, C., Conto, S. L., Hétru, C., Stuart, L. M., et al. (2005) · Cell · doi:10.1016/j.cell.2005.08.034 · Cited by 423 · see citing works
Clearance of apoptotic cells by phagocytes
Erwig, L.-P., & Henson, P. M. (2008) · Cell Death & Differentiation · doi:10.1038/sj.cdd.4402184 · Cited by 422 · see citing works
The ribosomal protein genes and Minute loci of Drosophila melanogaster
Marygold, S. J., Roote, J., Reuter, G., Lambertsson, A., Ashburner, M., Millburn, G., Harrison, P. M., Yu, Z., Kenmochi, N., Kaufman, T. C., et al. (2007) · Genome biology · doi:10.1186/gb-2007-8-10-r216 · Cited by 398 · see citing works
Croquemort, A Novel Drosophila Hemocyte/Macrophage Receptor that Recognizes Apoptotic Cells
Franc, N. C., Dimarcq, J., Lagueux, M., Hoffmann, J. A., & Ezekowitz, R. A. B. (1996) · Immunity · doi:10.1016/s1074-7613(00)80410-0 · Cited by 397 · see citing works
Freeman, M. R., Delrow, J. J., Kim, J., Johnson, E. A., & Doe, C. Q. (2003) · Neuron · doi:10.1016/s0896-6273(03)00289-7 · Cited by 388 · see citing works
αvβ5 integrin recruits the CrkII–Dock180–Rac1 complex for phagocytosis of apoptotic cells
Albert, M. L., Kim, J.-I., & Birge, R. B. (2000) · Nature Cell Biology · doi:10.1038/35046549 · Cited by 377 · see citing works
Phagocytosis promotes programmed cell death in C. elegans
Reddien, P. W., Cameron, S., & Horvitz, H. R. (2001) · Nature · doi:10.1038/35084096 · Cited by 348 · see citing works
Nimrod, a Putative Phagocytosis Receptor with EGF Repeats in Drosophila Plasmatocytes
Kurucz, É., Márkus, R., Zsámboki, J., Medzihradszky, K. F., Darula, Z., Vilmos, P., Udvardy, A., Krausz, I., Lukácsovich, T., Gateff, E. A., et al. (2007) · Current Biology · doi:10.1016/j.cub.2007.02.041 · Cited by 347 · see citing works
Modulation of Rab5 and Rab7 Recruitment to Phagosomes by Phosphatidylinositol 3-Kinase
Vieira, O. V., Bucci, C., Harrison, R. E., Trimble, W. S., Lanzetti, L., Gruenberg, J. E., Schreiber, A. D., Stahl, P. D., & Grinstein, S. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.7.2501-2514.2003 · Cited by 347 · see citing works
Phosphatidylserine recognition by phagocytes: a view to a kill
Wu, Y., Tibrewal, N., & Birge, R. B. (2006) · Trends in Cell Biology · doi:10.1016/j.tcb.2006.02.003 · Cited by 341 · see citing works
Function of Rho family proteins in actin dynamics during phagocytosis and engulfment
Chimini, G., & Chavrier, P. (2000) · Nature Cell Biology · doi:10.1038/35036454 · Cited by 329 · see citing works
Apoptosis-inducing factor: vital and lethal
Modjtahedi, N., Giordanetto, F., Madeo, F., & Kroemer, G. (2006) · Trends in Cell Biology · doi:10.1016/j.tcb.2006.03.008 · Cited by 323 · see citing works
Apoptosis-induced compensatory proliferation. The Cell is dead. Long live the Cell!
Fan, Y., & Bergmann, A. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.08.001 · Cited by 309 · see citing works
Engulfment genes cooperate with ced-3 to promote cell death in Caenorhabditis elegans
Hoeppner, D. J., Hengartner, M. O., & Schnabel, R. (2001) · Nature · doi:10.1038/35084103 · Cited by 295 · see citing works
Quantitative and Dynamic Assessment of the Contribution of the ER to Phagosome Formation
Touret, N., Paroutis, P., Terebiznik, M. R., Harrison, R. E., Trombetta, S., Pypaert, M., Chow, A. Y., Jiang, A., Shaw, J. E., Yip, C. M., et al. (2005) · Cell · doi:10.1016/j.cell.2005.08.018 · Cited by 285 · see citing works
Awasaki, T., Tatsumi, R., Takahashi, K., Arai, K., Nakanishi, Y., Ueda, R., & Ito, K. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.027 · Cited by 285 · see citing works
A pathway for phagosome maturation during engulfment of apoptotic cells
Kinchen, J. M., Doukoumetzidis, K., Almendinger, J., Stergiou, L., Tosello-Trampont, A., Sifri, C. D., Hengartner, M. O., & Ravichandran, K. S. (2008) · Nature Cell Biology · doi:10.1038/ncb1718 · Cited by 284 · see citing works
Two pathways converge at CED-10 to mediate actin rearrangement and corpse removal in C. elegans
Kinchen, J. M., Cabello, J., Klingele, D., Wong, K., Feichtinger, R., Schnabel, H., Schnabel, R., & Hengartner, M. O. (2005) · Nature · doi:10.1038/nature03263 · Cited by 266 · see citing works
Rubartelli, A., Poggi, A. D., & Zocchi, M. R. (1997) · European Journal of Immunology · doi:10.1002/eji.1830270812 · Cited by 256 · see citing works
Su, H.-P., Nakada‐Tsukui, K., Tosello‐Trampont, A., Li, Y., Bu, G., Henson, P. M., & Ravichandran, K. S. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m109336200 · Cited by 245 · see citing works
Engulfment Is Required for Cell Competition
Li, W., & Baker, N. E. (2007) · Cell · doi:10.1016/j.cell.2007.03.054 · Cited by 239 · see citing works
Self-citationTHE 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
Recognition ligands on apoptotic cells: a perspective
Gardai, S. J., Bratton, D. L., Ogden, C. A., & Henson, P. M. (2006) · Journal of Leukocyte Biology · doi:10.1189/jlb.1005550 · Cited by 234 · see citing works
A systems biology analysis of the Drosophila phagosome
Stuart, L. M., Boulais, J., Charrière, G. M., Hennessy, E. J., Brunet, S., Jutras, I., Goyette, G., Rondeau, C., Letarte, S., Huang, H., et al. (2006) · Nature · doi:10.1038/nature05380 · Cited by 231 · see citing works
ER-mediated phagocytosis: a new membrane for new functions
Desjardins, M. (2003) · Nature reviews. Immunology · doi:10.1038/nri1053 · Cited by 230 · see citing works
Role of Rab GTPases in Membrane Traffic
Olkkonen, V. M., & Slenmark, H. (1997) · International review of cytology · doi:10.1016/s0074-7696(08)61608-3 · Cited by 216 · see citing works
Identification and purification of aminophospholipid flippases
Daleke, D. L., & Lyles, J. V. (2000) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/s1388-1981(00)00052-4 · Cited by 207 · see citing works
Manaka, J., Kuraishi, T., Shiratsuchi, A., Nakai, Y., Higashida, H., Henson, P. M., & Nakanishi, Y. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m408597200 · Cited by 204 · see citing works
Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling
Ziegenfuss, J. S., Biswas, R., Avery, M. A., Hong, K., Sheehan, A. E., Yeung, Y.-G., Stanley, E. R., & Freeman, M. R. (2008) · Nature · doi:10.1038/nature06901 · Cited by 202 · see citing works
Transbilayer phospholipid movement and the clearance of apoptotic cells
Williamson, P., & Schlegel, R. (2002) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/s1388-1981(02)00324-4 · Cited by 201 · see citing works
Cell Corpse Engulfment Mediated by C. elegans Phosphatidylserine Receptor Through CED-5 and CED-12
Wang, X., Wu, Y., Fadok, V. A., Lee, M.-C., Gengyo‐Ando, K., Cheng, L.-C., Ledwich, D., Hsu, P.-K., Chen, J.-Y., Chou, B.-K., et al. (2003) · Science · doi:10.1126/science.1087641 · Cited by 195 · see citing works
Crozatier, M., & Meister, M. F. (2007) · Cellular Microbiology · doi:10.1111/j.1462-5822.2007.00930.x · Cited by 195 · see citing works
The uniformity of phagosome maturation in macrophages
Henry, R. M., Hoppe, A. D., Joshi, N. S., & Swanson, J. A. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200307080 · Cited by 175 · see citing works
Six-microns-under acts upstream of Draper in the glial phagocytosis of apoptotic neurons.
Kurant, E., Axelrod, S., Leaman, D., & Gaul, U. (2008) · Cell · doi:10.1016/j.cell.2008.02.052 · Cited by 175 · see citing works
Cellular degeneration in the production of some mutant phenotypes in Drosophila melanogaster
Fristrom, D. K. (1969) · Molecular and General Genetics MGG · doi:10.1007/bf00383486 · Cited by 166 · see citing works
Yu, X., Odera, S. L., Chuang, C.-H., Lü, N., & Zhou, Z. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.04.007 · Cited by 148 · see citing works
Cell surface exposure of phosphatidylserine during apoptosis is phylogenetically conserved
van den Eijnde, S. M., Boshart, L., Baehrecke, E. H., Zeeuw, C. I. D., Reutelingsperger, C. P. M., & Vermeij‐Keers, C. (1998) · APOPTOSIS · doi:10.1023/a:1009650917818 · Cited by 135 · see citing works
Undertaker, a Drosophila Junctophilin, Links Draper-Mediated Phagocytosis and Calcium Homeostasis
Cuttell, L., Vaughan, A. N., Silva, E., Escaron, C. J., Lavine, M., Goethem, E. V., Eid, J.-P., Quirin, M., & Franc, N. C. (2008) · Cell · doi:10.1016/j.cell.2008.08.033 · Cited by 134 · see citing works
Role of C. elegans TAT-1 Protein in Maintaining Plasma Membrane Phosphatidylserine Asymmetry
Ransom, M., Wang, X., Sun, C.-L., Mapes, J., Gengyo‐Ando, K., Mitani, S., & Xue, D. (2008) · Science · doi:10.1126/science.1155847 · Cited by 131 · see citing works
PH domain of ELMO functions in trans to regulate Rac activation via Dock180
Lu, M., Kinchen, J. M., Rossman, K. L., Grimsley‐Myers, C. M., deBakker, C. D., Brugnera, E., Tosello‐Trampont, A., Haney, L. B., Klingele, D., Sondek, J., et al. (2004) · Nature Structural & Molecular Biology · doi:10.1038/nsmb800 · Cited by 130 · see citing works
Phagocytic Receptor CED-1 Initiates a Signaling Pathway for Degrading Engulfed Apoptotic Cells
Yu, X., Lü, N., & Zhou, Z. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060061 · Cited by 127 · see citing works
Phagocytosis and development: back to the future
Franc, N. C., White, K., & Ezekowitz, R. A. B. (1999) · Current Opinion in Immunology · doi:10.1016/s0952-7915(99)80009-0 · Cited by 125 · see citing works
Wang, X., Wang, J., Gengyo‐Ando, K., Gu, L., Sun, C.-L., Yang, C., Shi, Y., Kobayashi, T., Shi, Y., Mitani, S., et al. (2007) · Nature Cell Biology · doi:10.1038/ncb1574 · Cited by 123 · see citing works
Identification of cytoskeletal regulatory proteins required for efficient phagocytosis in Drosophila
Pearson, A. M., Baksa, K., Rämet, M., Protas, M. E., McKee, M. L., Brown, D., & Ezekowitz, R. A. B. (2003) · Microbes and Infection · doi:10.1016/s1286-4579(03)00157-6 · Cited by 122 · see citing works
Leverrier, Y., Lorenzi, R., Blundell, M. P., Brickell, P. M., Kinnon, C., Ridley, A. J., & Thrasher, A. J. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.166.8.4831 · Cited by 119 · see citing works
Dewitt, S., & Hallett, M. B. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200206089 · Cited by 117 · see citing works
Russell, M. A. (1974) · Developmental Biology · doi:10.1016/0012-1606(74)90104-3 · Cited by 108 · see citing works
Clearance of apoptotic cells in Caenorhabditis elegans
Mangahas, P. M., & Zhou, Z. (2005) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2004.12.005 · Cited by 104 · see citing works
Senoo‐Matsuda, N., & Johnston, L. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0709021104 · Cited by 101 · see citing works
Venegas, V., & Zhou, Z. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-02-0138 · Cited by 95 · see citing works
Wiskott-Aldrich Syndrome Protein Is a Key Regulator of the Phagocytic Cup Formation in Macrophages
Tsuboi, S., & Meerloo, J. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m705999200 · Cited by 90 · see citing works
Simpson, P., & Schneiderman, H. A. (1975) · Development Genes and Evolution · doi:10.1007/bf00848432 · Cited by 82 · see citing works
Membrane dynamics in phagocytosis
Booth, J. W., Trimble, W. S., & Grinstein, S. (2001) · Seminars in Immunology · doi:10.1006/smim.2001.0332 · Cited by 78 · see citing works
The small GTPase Rab2 functions in the removal of apoptotic cells in Caenorhabditis elegans
Mangahas, P. M., Yu, X., Miller, K. G., & Zhou, Z. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200708130 · Cited by 72 · see citing works
Identification of calreticulin as a marker for phagocytosis of apoptotic cells in Drosophila
Kuraishi, T., Manaka, J., Kono, M., Ishii, H., Yamamoto, N., Koizumi, K., Shiratsuchi, A., Lee, B. L., Higashida, H., & Nakanishi, Y. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.10.027 · Cited by 68 · see citing works
Aminophospholipid Translocase TAT-1 Promotes Phosphatidylserine Exposure during C. elegans Apoptosis
Züllig, S., Neukomm, L. J., Jovanovic, M., Charette, S. J., Lyssenko, N. N., Halleck, M. S., Reutelingsperger, C. P. M., Schlegel, R., & Hengartner, M. O. (2007) · Current Biology · doi:10.1016/j.cub.2007.05.024 · Cited by 68 · see citing works
Dewitt, S., Laffafian, I., & Hallett, M. B. (2003) · Journal of Cell Science · doi:10.1242/jcs.00499 · Cited by 67 · see citing works
The C. elegans P4‐ATPase TAT‐1 Regulates Lysosome Biogenesis and Endocytosis
Ruaud, A., Nilsson, L., Richard, F., Larsen, M. K., Bessereau, J., & Tuck, S. (2008) · Traffic · doi:10.1111/j.1600-0854.2008.00844.x · Cited by 66 · see citing works
Multiple Members of a Third Subfamily of P-Type ATPases Identified by Genomic Sequences and ESTsPreprint
Halleck, M. S., Pradhan, D., Blackman, C., Berkes, C. A., Williamson, P., & Schlegel, R. (1998) · Genome Research · doi:10.1101/gr.8.4.354 · Cited by 60 · see citing works
C. elegansRab GTPase 2 is required for the degradation of apoptotic cells
Lu, Q., Zhang, Y., Hu, T., Guo, P., Li, W., & Wang, X. (2008) · Development · doi:10.1242/dev.016063 · Cited by 56 · see citing works
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 · see citing works
Calreticulin Affects Fibronectin-based Cell-Substratum Adhesion via the Regulation of c-Src Activity
Papp, S., Fadel, M. P., Kim, H., McCulloch, C. A., & Opas, M. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m701011200 · Cited by 52 · see citing works
Phosphoinositide Involvement in Phagocytosis and Phagosome Maturation
Botelho, R. J., Scott, C. C., & Grinstein, S. (2004) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-18805-3_1 · Cited by 50 · see citing works
Engulfment mechanism of apoptotic cells
Krieser, R. J., & White, K. (2002) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(02)00390-3 · Cited by 44 · see citing works
Tejle, K., Magnusson, K., & Rasmusson, B. J. (2002) · Bioscience Reports · doi:10.1023/a:1022025903688 · Cited by 39 · see citing works
TheDrosophilahomolog of the putative phosphatidylserine receptor functions to inhibit apoptosis
Krieser, R. J., Moore, F. E., Dresnek, D., Pellock, B. J., Patel, R. G., Huang, A., Brachmann, C. B., & White, K. (2007) · Development · doi:10.1242/dev.02860 · Cited by 36 · see citing works
The Drosophila Shark tyrosine kinase is required for embryonic dorsal closurePreprint
Fernandez, R. J., Takahashi, F., Liu, Z., Steward, R., Stein, D., & Stanley, E. R. (2000) · Genes & Development · doi:10.1101/gad.14.5.604 · Cited by 35 · see citing works
Intracellular Calcium Dependent Activation of p72syk in Platelets1
Wang, X., Sada, K., Yanagi, S., Yang, C., Rezaul, K., & Yamamura, H. (1994) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a124607 · Cited by 26 · see citing works
Phagocytosis: Dynamin's Dual Role in Phagosome Biogenesis
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Elliott, M. R., & Ravichandran, K. S. (2008) · Cell · doi:10.1016/j.cell.2008.04.014 · Cited by 8 · see citing works
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Rieger, A. M., Konowalchuk, J. D., Grayfer, L., Katzenback, B. A., Havixbeck, J. J., Kiemele, M. D., Belosevic, M., & Barreda, D. R. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047070 · Cited by 57 · see citing works
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Chan, M. S. M., Chen, S.-F., Felizola, S. J. A., Wang, L., Nemoto, N., Tamaki, K., Ishida, T., Chow, L. W. C., Ohuchi, N., & Sasano, H. (2014) · The International Journal of Biological Markers · doi:10.5301/jbm.5000082 · Cited by 6 · see citing works
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Webber, J. L., & Rebay, I. (2013) · Fly · doi:10.4161/fly.24162 · Cited by 2 · see citing works
Wang, M. (2013) · Summit (Simon Fraser University) · Cited by 1 · see citing works
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Bergmann, A. (2018) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733655209.793549319
- Authors
- Fullard, J. F., Kale, A., & Baker, N. E.
- Affiliations
- Albert Einstein College of Medicine (US)
- Corresponding author
- Baker, Nicholas E.
- Venue
- Apoptosis
- Published
- 2009-03-17
- Volume
- 14
- Issue
- 8
- Pages
- 1029-1037
- ISSN
- 1360-8185 (ISSN-L)
- 1573-675X
- OpenAlex
- W2050288158
- Cited by
- 46
- References
- 95
- Citations by year
- 2025: 1 · 2021: 1 · 2019: 1 · 2018: 2 · 2017: 1 · 2016: 6 · 2015: 6 · 2014: 4 · 2013: 3 · 2012: 6
- FWCI
- 3.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- APOPTOSIS (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM061230)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Phagocytosis and Immune Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Cell death mechanisms and regulation
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Keywords
- phagocytosis, eat-me signals, non-professional phagocytes, cell competition, Drosophila
- MeSH terms
- Animals, Humans, Immune System, Phagocytosis, Phagosomes, Signal Transduction, Apoptosis
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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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