Engulfment of Apoptotic Cells in C. elegans Is Mediated by Integrin α/SRC Signaling

Current Biology

Volumn 20, Issue 6, 2010, Pages 477-486

  Hsu, Tsung Yuan ^a   Wu, Yi Chun ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

CELLCYCLE; SIGNALING

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CARRIER PROTEIN; CED 12 PROTEIN, C ELEGANS; CED 2 PROTEIN, C ELEGANS; CED 5 PROTEIN, C ELEGANS; CED-12 PROTEIN, C ELEGANS; CED-2 PROTEIN, C ELEGANS; CED-5 PROTEIN, C ELEGANS; CYTOSKELETON PROTEIN; HELMINTH DNA; INA 1 PROTEIN, C ELEGANS; INA-1 PROTEIN, C ELEGANS; INTEGRIN; MEMBRANE PROTEIN; PRIMER DNA; PROTEIN KINASE; PROTEIN SUBUNIT; SRC 1 PROTEIN, C ELEGANS; SRC-1 PROTEIN, C ELEGANS;

ANIMAL; APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; GENE; GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PHYSIOLOGY; PRENATAL DEVELOPMENT; PSEUDOPODIUM; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL; TWO HYBRID SYSTEM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; CYTOSKELETAL PROTEINS; DNA PRIMERS; DNA, HELMINTH; GENES, HELMINTH; INTEGRINS; MEMBRANE PROTEINS; MUTATION; PHAGOCYTOSIS; PROTEIN KINASES; PROTEIN SUBUNITS; PSEUDOPODIA; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

CAENORHABDITIS ELEGANS;

EID: 77949487317     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2010.01.062     Document Type: Article

References (51)

1. Erwig L.P., and Henson P.M. Clearance of apoptotic cells by phagocytes. Cell Death Differ. 15 (2008) 243-250
2. Ravichandran K.S., and Lorenz U. Engulfment of apoptotic cells: Signals for a good meal. Nat. Rev. Immunol. 7 (2007) 964-974
3. Reddien P.W., and Horvitz H.R. The engulfment process of programmed cell death in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 20 (2004) 193-221
4. Darland-Ransom M., Wang X., Sun C.L., Mapes J., Gengyo-Ando K., Mitani S., and Xue D. Role of C. elegans TAT-1 protein in maintaining plasma membrane phosphatidylserine asymmetry. Science 320 (2008) 528-531
5. Galvin B.D., Kim S., and Horvitz H.R. Caenorhabditis elegans genes required for the engulfment of apoptotic corpses function in the cytotoxic cell deaths induced by mutations in lin-24 and lin-33. Genetics 179 (2008) 403-417
6. Fadeel B., and Xue D. The ins and outs of phospholipid asymmetry in the plasma membrane: Roles in health and disease. Crit. Rev. Biochem. Mol. Biol. 44 (2009) 264-277
7. Fadok V.A., Bratton D.L., Rose D.M., Pearson A., Ezekewitz R.A., and Henson P.M. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405 (2000) 85-90
8. Kobayashi N., Karisola P., Peña-Cruz V., Dorfman D.M., Jinushi M., Umetsu S.E., Butte M.J., Nagumo H., Chernova I., Zhu B., et al. TIM-1 and TIM-4 glycoproteins bind phosphatidylserine and mediate uptake of apoptotic cells. Immunity 27 (2007) 927-940
9. Miyanishi M., Tada K., Koike M., Uchiyama Y., Kitamura T., and Nagata S. Identification of Tim4 as a phosphatidylserine receptor. Nature 450 (2007) 435-439
10. Park S.Y., Jung M.Y., Kim H.J., Lee S.J., Kim S.Y., Lee B.H., Kwon T.H., Park R.W., and Kim I.S. Rapid cell corpse clearance by stabilin-2, a membrane phosphatidylserine receptor. Cell Death Differ. 15 (2008) 192-201
11. Park D., Tosello-Trampont A.C., Elliott M.R., Lu M., Haney L.B., Ma Z., Klibanov A.L., Mandell J.W., and Ravichandran K.S. BAI1 is an engulfment receptor for apoptotic cells upstream of the ELMO/Dock180/Rac module. Nature 450 (2007) 430-434
12. Akakura S., Singh S., Spataro M., Akakura R., Kim J.I., Albert M.L., and Birge R.B. The opsonin MFG-E8 is a ligand for the alphavbeta5 integrin and triggers DOCK180-dependent Rac1 activation for the phagocytosis of apoptotic cells. Exp. Cell Res. 292 (2004) 403-416
13. Hanayama R., Tanaka M., Miwa K., Shinohara A., Iwamatsu A., and Nagata S. Identification of a factor that links apoptotic cells to phagocytes. Nature 417 (2002) 182-187
14. Savill J., Dransfield I., Hogg N., and Haslett C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343 (1990) 170-173
15. Ishimoto Y., Ohashi K., Mizuno K., and Nakano T. Promotion of the uptake of PS liposomes and apoptotic cells by a product of growth arrest-specific gene, gas6. J. Biochem. 127 (2000) 411-417
16. Scott R.S., McMahon E.J., Pop S.M., Reap E.A., Caricchio R., Cohen P.L., Earp H.S., and Matsushima G.K. Phagocytosis and clearance of apoptotic cells is mediated by MER. Nature 411 (2001) 207-211
17. Wang X., Wu Y.C., 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. Cell corpse engulfment mediated by C. elegans phosphatidylserine receptor through CED-5 and CED-12. Science 302 (2003) 1563-1566
18. Hong J.R., Lin G.H., Lin C.J., Wang W.P., Lee C.C., Lin T.L., and Wu J.L. Phosphatidylserine receptor is required for the engulfment of dead apoptotic cells and for normal embryonic development in zebrafish. Development 131 (2004) 5417-5427
19. Li W., and Baker N.E. Engulfment is required for cell competition. Cell 129 (2007) 1215-1225
20. Yu X., Odera S., Chuang C.H., Lu N., and Zhou Z. C. elegans Dynamin mediates the signaling of phagocytic receptor CED-1 for the engulfment and degradation of apoptotic cells. Dev. Cell 10 (2006) 743-757
21. 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. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 107 (2001) 27-41
22. Reddien P.W., and Horvitz H.R. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2 (2000) 131-136
23. Wu Y.C., and Horvitz H.R. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 392 (1998) 501-504
24. Wu Y.C., Tsai M.C., Cheng L.C., Chou C.J., and Weng N.Y. C. elegans CED-12 acts in the conserved crkII/DOCK180/Rac pathway to control cell migration and cell corpse engulfment. Dev. Cell 1 (2001) 491-502
25. Zhou Z., Caron E., Hartwieg E., Hall A., and Horvitz H.R. The C. elegans PH domain protein CED-12 regulates cytoskeletal reorganization via a Rho/Rac GTPase signaling pathway. Dev. Cell 1 (2001) 477-489
26. Brugnera E., Haney L., Grimsley C., Lu M., Walk S.F., Tosello-Trampont A.C., Macara I.G., Madhani H., Fink G.R., and Ravichandran K.S. Unconventional Rac-GEF activity is mediated through the Dock180-ELMO complex. Nat. Cell Biol. 4 (2002) 574-582
27. Tosello-Trampont A.C., Kinchen J.M., Brugnera E., Haney L.B., Hengartner M.O., and Ravichandran K.S. Identification of two signaling submodules within the CrkII/ELMO/Dock180 pathway regulating engulfment of apoptotic cells. Cell Death Differ. 14 (2007) 963-972
28. deBakker C.D., Haney L.B., Kinchen J.M., Grimsley C., Lu M., Klingele D., Hsu P.K., Chou B.K., Cheng L.C., Blangy A., et al. Phagocytosis of apoptotic cells is regulated by a UNC-73/TRIO-MIG-2/RhoG signaling module and armadillo repeats of CED-12/ELMO. Curr. Biol. 14 (2004) 2208-2216
29. Kinchen J.M., Cabello J., Klingele D., Wong K., Feichtinger R., Schnabel H., Schnabel R., and Hengartner M.O. Two pathways converge at CED-10 to mediate actin rearrangement and corpse removal in C. elegans. Nature 434 (2005) 93-99
30. Hurwitz M.E., Vanderzalm P.J., Bloom L., Goldman J., Garriga G., and Horvitz H.R. Abl kinase inhibits the engulfment of apoptotic [corrected] cells in Caenorhabditis elegans. PLoS Biol. 7 (2009) e99
31. Zou W., Lu Q., Zhao D., Li W., Mapes J., Xie Y., and Wang X. Caenorhabditis elegans myotubularin MTM-1 negatively regulates the engulfment of apoptotic cells. PLoS Genet. 5 (2009) e1000679
32. Venegas V., and Zhou Z. Two alternative mechanisms that regulate the presentation of apoptotic cell engulfment signal in Caenorhabditis elegans. Mol. Biol. Cell 18 (2007) 3180-3192
33. Wang X., Wang J., Gengyo-Ando K., Gu L., Sun C.L., Yang C., Shi Y., Kobayashi T., Shi Y., Mitani S., et al. C. elegans mitochondrial factor WAH-1 promotes phosphatidylserine externalization in apoptotic cells through phospholipid scramblase SCRM-1. Nat. Cell Biol. 9 (2007) 541-549
34. Baum P.D., and Garriga G. Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron 19 (1997) 51-62
35. Ellis H.M., and Horvitz H.R. Genetic control of programmed cell death in the nematode C. elegans. Cell 44 (1986) 817-829
36. Grossmann J. Molecular mechanisms of "detachment-induced apoptosis-Anoikis". Apoptosis 7 (2002) 247-260
37. Derry W.B., Putzke A.P., and Rothman J.H. Caenorhabditis elegans p53: Role in apoptosis, meiosis, and stress resistance. Science 294 (2001) 591-595
38. Zhou Z., Hartwieg E., and Horvitz H.R. CED-1 is a transmembrane receptor that mediates cell corpse engulfment in C. elegans. Cell 104 (2001) 43-56
39. Conradt B., and Horvitz H.R. The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene. Cell 98 (1999) 317-327
40. Robertson A.G., and Thomson J.N. Morphology of programmed cell death in the ventral nerve cord of Caenorhabiditis elegans larvae. J. Embryol. Exp. Morphol. 67 (1982) 89-100
41. Park D., Hochreiter-Hufford A., and Ravichandran K.S. The phosphatidylserine receptor TIM-4 does not mediate direct signaling. Curr. Biol. 19 (2009) 346-351
42. Kurant E., Axelrod S., Leaman D., and Gaul U. Six-microns-under acts upstream of Draper in the glial phagocytosis of apoptotic neurons. Cell 133 (2008) 498-509
43. Kmiecik T.E., Johnson P.J., and Shalloway D. Regulation by the autophosphorylation site in overexpressed pp60c-src. Mol. Cell. Biol. 8 (1988) 4541-4546
44. Kmiecik T.E., and Shalloway D. Activation and suppression of pp60c-src transforming ability by mutation of its primary sites of tyrosine phosphorylation. Cell 49 (1987) 65-73
45. Savill J., Hogg N., Ren Y., and Haslett C. Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90 (1992) 1513-1522
46. Means T.K., Mylonakis E., Tampakakis E., Colvin R.A., Seung E., Puckett L., Tai M.F., Stewart C.R., Pukkila-Worley R., Hickman S.E., et al. Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J. Exp. Med. 206 (2009) 637-653
47. Franc N.C., Heitzler P., Ezekowitz R.A., and White K. Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284 (1999) 1991-1994
48. Albert M.L., Kim J.I., and Birge R.B. alphavbeta5 integrin recruits the CrkII-Dock180-rac1 complex for phagocytosis of apoptotic cells. Nat. Cell Biol. 2 (2000) 899-905
49. Cram E.J., Fontanez K.M., and Schwarzbauer J.E. Functional characterization of KIN-32, the Caenorhabditis elegans homolog of focal adhesion kinase. Dev. Dyn. 237 (2008) 837-846
50. Hsia D.A., Lim S.T., Bernard-Trifilo J.A., Mitra S.K., Tanaka S., den Hertog J., Streblow D.N., Ilic D., Ginsberg M.H., and Schlaepfer D.D. Integrin alpha4beta1 promotes focal adhesion kinase-independent cell motility via alpha4 cytoplasmic domain-specific activation of c-Src. Mol. Cell. Biol. 25 (2005) 9700-9712
51. Wu L., Bernard-Trifilo J.A., Lim Y., Lim S.T., Mitra S.K., Uryu S., Chen M., Pallen C.J., Cheung N.K., Mikolon D., et al. Distinct FAK-Src activation events promote alpha5beta1 and alpha4beta1 integrin-stimulated neuroblastoma cell motility. Oncogene 27 (2008) 1439-1448