Candidate adaptor protein CED-6 promotes the engulfment of apoptotic cells in C. elegans

Cell

Volumn 93, Issue 6, 1998, Pages 961-972

  Liu, Qiong A ^a,b   Hengartner, Michael O ^a  

^a Simons Center for Quantitative Biology   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CED 6 PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CAENORHABDITIS ELEGANS; GENE OVEREXPRESSION; MOLECULAR CLONING; MOSAICISM; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS; NEMATODA;

EID: 0032511234     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81202-7     Document Type: Article

References (65)

1. Asch, A.S., Barnwell, J., Silverstein, R.L., and Nachman, R.L. (1987). Isolation of the thrombospondin membrane receptor. J. Clin. Invest. 79, 1054-1061.
2. Avery, L., and Horvitz, H. (1987). A cell that dies during wild-type C. elegans development can function as a neuron in a ced-3 mutant. Cell 51, 1071-1078.
3. Bianco, C., Griffin, F.M., Jr., and Silverstein, S.C. (1975). Studies of the macrophage complement receptor. Alteration of receptor function upon macrophage activation. J. Exp. Med. 141, 1278-1290.
4. Blaikie, P., Immanuel, D., Wu, J., Li, N., Yajnik, V., and Margolis, B. (1994). A region in Shc distinct from the SH2 domain can bind tyrosine-phosphorylated growth factor receptor. J. Biol. Chem. 269, 32031-32034.
5. Blumenthal, T., and Steward, K. (1997). RNA processing and gene structure. In C. elegans II, D.L. Riddle, T. Blumenthal, B.J. Meyer, and J.R. Priess, eds. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 117-145.
6. Bork, P., and Margolis, B. (1995). A phosphotyrosine interaction domain. Cell 80, 693-694.
7. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
8. Duvall, E., and Wyllie, A.H. (1986). Death and the cell. Immunol. Today 7, 115-119.
9. Duvall, E., Wyllie, A.H., and Morris, R.G. (1985). Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology 56, 351-358.
10. Ellis, R.E., Jacobson, D.M., and Horvitz, H.R. (1991). Genes required for the engulfment of cell corpses during programmed cell death in Caenorhabditis elegans. Genetics 129, 79-94.
11. Estevez, M., Attisano, L., Wrana, J.L., Albert, P.S., Massague, J., and Riddle, D.L. (1993). The daf-4 gene encodes a bone morphogenetic protein receptor controlling C. elegans dauer larva development. Nature 365, 644-649.
12. Fadok, V.A., Savill, J.S., Haslett, C., Bratton, D.L., Doherty, D.E., Campbell, P.A., and Henson, P.M. (1992a). Different populations of macrophages use either the vitronectin receptor or the phosphatidylserine receptor to recognize and remove apoptotic cells. J. Immunol. 149, 4029-4035.
13. Fadok, V.A., Voelker, D.R., Campbell, P.A., Cohen, J.J., Bratton, D.L., and Henson, P.M. (1992b). Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148, 2207-2216.
14. Fire, A., Harrison, S.W., and Dixon, D. (1990). A modular set of lacZ fusion vectors for studying gene expression in Caenorhabditis elegans. Gene 93, 189-198.
15. Feng, S., Chen, J.K., Yu, H., Simon, J.A., and Schreiber, S.L. (1994). Two binding orientations for peptides to the Src SH3 domain: development of a general model for SH3-ligand interactions. Science 266, 1241-1247.
16. Franc, N.C., Dimarcq, J.-L., Lagueux, M., Hoffmann, J., and Ezekowitz, R.A.B. (1996). Croquemort, a novel Drosophila hemocyte/macrophage receptor that recognizes apoptotic cells. Immunity 4, 431-443.
17. Grabs, D., Slepnev, V.I., Songyang, Z., David, C., Lynch, M., Cantley, L.C., and Camilli, P.D. (1997). The SH3 domain of amphiphysin binds the proline-rich domain of dynamin at a single site that defines a new SH3 binding consensus sequence. J. Biol. Chem. 272, 13419-13425.
18. Greenberg, S. (1995). Signal transduction of phagocytosis. Trends Cell Biol. 5, 93-99.
19. Greenberg, S., Chang, P., and Silverstein, S. (1993). Tyrosine phosphorylation is required for Fc receptor-mediated phagocytosis in mouse macrophages. J. Exp. Med. 177, 529-534.
20. Grigg, J., Savill, J., Sarraf, C., Haslett, C., and Silverman, M. (1991). Neutrophil apoptosis and clearance from neonatal lungs. Lancet 338, 720-722.
21. Hedgecock, E.M., and Herman, R.K. (1995). The nuc-1 gene and genetic mosaic of Caenorhabditis elegans. Genetics 141, 989-1006.
22. Hedgecock, E.M., Sulston, J.E., and Thomson, J.N. (1983). Mutations affecting programmed cell deaths in the nematode Caenorhabditis elegans. Science 220, 1277-1279.
23. Hengartner, M.O. (1997). Cell death. In C. elegans II, D.L. Riddle, T. Blumenthal, B.J. Meyer, and J.R. Priess, eds. (Plainview, NY: Cold Spring Harbor Laboratory Press), pp. 383-415.
24. Hengartner, M.O., and Horvitz, H.R. (1994). C. elegans cell survival gene ced-9 encodes a functional homologue of the mammalian proto-oncogene bcl-2. Cell 76, 665-676.
25. Herman, R.K. (1984). Analysis of genetic mosiac of the nematode Caenorhabditis elegans. Genetics 108, 165-180.
26. Higgins, C.F., and Gottesman, M.M. (1992). Is the multidrug transporter a flippase? Trends Biochem. Sci. 17, 18-21.
27. Hodgkin, J. (1997). Genetics. In C. elegans II, D.L. Riddle, T. Blumenthal, B.J. Meyer, and J.R. Priess, eds. (Plainview, NY: Cold Spring Harbor Laboratory Press), pp. 881-1047.
28. Horvitz, H.R, Shaham, S., and Hengartner, M.O. (1994). The genetics of programmed cell death in the nematode Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 59, 377-385.
29. Kavanaugh, W.M., and Williams, L.T. (1994). An alternative to SH2 domains for binding tyrosine-phosphorylated proteins. Science 266, 1862-1865.
30. Kavanaugh, W.M., Turck, C.W., and Williams, L.T. (1995). PTB domain binding to signaling proteins through a sequence motif containing phosphotyrosine. Science 268, 1177-1179.
31. Klass, M., Wolf, N., and Hirsh, D. (1976). Development of the male reproductive system and sexual transformation in the nematode Caenorhabditis elegans. Dev. Biol. 52, 1-18.
32. Koch, C.A., Anderson, D., Moran, M.F., Ellis, C., and Pawson, T. (1991). SH2 and SH3 domains: elements that control interactions of cytoplasmic signaling proteins. Science 252, 252-673.
33. Lockshin, R.A. (1981). Cell death in metamorphosis. In Cell Death in Biology and Pathology, R.A. Lockshin and I.D. Browen, eds. (London: Chapman and Hall), pp. 79-122.
34. Luciani, M.-F., and Chimini, G. (1996). The ATP binding cassette transporter ABC1, is required for the engulfment of corpses generated by apoptotic cell death. EMBO J. 15, 226-235.
35. Mello, C., and Fire, A. (1995). DNA transformation. In Methods in Cell Biology, H.F. Epstein and D.C. Shakes, eds. (San Diego, CA: Academic Press), pp. 452-482.
36. Metchnikoff, E. (1891). Lectures on the comparative pathology of inflammation; delivered at the Pasteur Institute in 1891, 1968 Ed. (New York: Dover Publication).
37. Meyer, B.J., and Casson, L.P. (1986). Caenorhabditis elegans compensates for the difference in X chromosome dosage between the sexes by regulating transcript levels. Cell 47, 871-881.
38. Pawson, T., and Schlessinger, J. (1993). SH2 and SH3 domains. Curr. Biol. 3, 434-442.
39. Pawson, T., and Scott, J.D. (1997). Signaling through scaffold, anchoring, and adaptor proteins. Science 278, 2075-2080.
40. Platt, N., Suzuki, H., Kurihara, Y., Kodama, T., and Gordon, S. (1996). Role for the class A macrophage scavenger receptor in the phagocytosis of apoptotic thymocytes in vitro. Proc. Natl. Acad. Sci. USA 93, 12456-12460.
41. Ravetch, J.V. (1994). Fc receptor: Rubor Redux. Cell 78, 553-560.
42. Ren, R., Mayer, B.J., Cicchetti, P., and Baltimore, D. (1993). Identification of a ten-amino acid proline-rich SH3 binding site. Science 259, 1157-1161.
43. Ren, Y., Silverstein, R.L., Allen, J., and Savill, J. (1995). CD36 Gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J. Exp. Med. 18, 1857-1862.
44. Robertson, A., and Thomson, N. (1982). Morphology of programmed cell death in the ventral nerve cord of Caenorhabditis elegans larvae. J. Embryol. Exp. Morph. 67, 89-100.
45. Rosenbluth, R.E., Cuddeford, C., and Baillie, D.L. (1985). Mutagenesis in Caenorhabditis elegans. II. A spectrum of mutational events induced with 1500 R of γ-radiation. Genetics 109, 493-511.
46. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual (Cold Spring Harbor, NY: Cold Spring Harbor Press).
47. Savill, J., Wyllie, A., Henson, J., Walport, M., Henson, P., and Haslett, C. (1989). Macrophage phagocytosis of aging neutrophils in inflamation. Programmed cell death in the neutrophil leadsto its recognition by macrophages. J. Clin. Invest. 83, 865-875.
48. Savill, J., Dransfield, I., Hogg, N., and Haslett, C. (1990). Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 343, 170-173.
49. Savill, J., Hogg, N., Ren, Y., and Haslett, C. (1992). Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis. J. Clin. Invest. 90, 1513-1522.
50. Savill, J., Fadok, V., Henson, P., and Haslett, C. (1993). Phagocyte recognition of cells undergoing apoptosis. Immunol. Today 14, 131-136.
51. Songyang, Z., Margolis, B., Chaudhuri, M., Shoelson, S.E., and Cantley, L.C. (1995). The phosphotyrosine interaction domain of SHC recognizes tyrosine-phosphorylated NPXY motif. J. Biol. Chem. 270, 14863-14866.
52. Stringham, E.G., Dixon, D.K., Jones, D., and Candido, E.P.M. (1992). Temporal and spatial expression patterns of the small heat shock (hsp-16) genes in transgenic Caenorhabditis elegans. Mol. Biol. Cell 3, 221-233.
53. Sulston, J.E., and Horvitz, H.R. (1977). Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev. Biol. 56, 110-156.
54. Sulston, J.E., Schierenberg, E., White, J.G., and Thomson, J.N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100, 64-119.
55. Sun, A.Y., and Lambie, E.J. (1997). gon-2, a gene required for gonadogenesis in C. elegans. Genetics 147, 1077-1089.
56. van der Geer, P., and Pawson, T. (1995). The PTB domain: a new protein module implicated in signal transduction. Trends Biochem. Sci. 20, 277-280.
57. Vaux, D. (1997), CED-4 the third horseman of apoptosis. Cell 90, 389-390.
58. Wilson, R., Ainscough, R., Anderson, K., Baynes, C., Berks, M., Bonfield, J., Burton, J., Connell, M., Copsey, T., Cooper, J., et al. (1994). 2.2 Mb of contiguous nucleotide sequence from chromosome III of C. elegans. Nature 368, 32-38.
59. Wyllie, A.H., Kerr, J.F.R., and Currie, A.R. (1980). Cell death: the significance of apoptosis. Int. Rev. Cytol. 68, 251-306.
60. Wu, Y.C., and Horvitz, H.R. (1998a). C. elegans phagocytosis and cell-migration protein CED-5 is similar to human Dock180. Nature 392, 501-504.
61. Wu, Y.C., and Horvitz, H.R. (1998b). The C. elegans cell-corpse engulfment gene ced-7 encodes a protein similar to ABC transporters. Cell 93, this issue, 951-960.
62. Yenush, L., and White, M.F. (1997). The IRS-signaling system during insulin and cytokine action. BioEssay 19, 491-500.
63. Yu, H., Chen, J.K., Feng, S., Dalgarno, D.C., Brauer, A.W., and Schreiber, S.L. (1994). Structural basis for the binding of proline-rich peptides to SH3 domains. Cell 76, 933-945.
64. Yuan, J., and Horvitz, R.H. (1990). The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev. Biol. 138, 33-41.
65. Zhou, M.M., Ravichandran, K.S., Olejniczak, E.T., Petros, A.M., Meadows, R.P., Sattler, M., Harlan, J.E., Wade, W.S., Burakoff, S.J., and Fesik, S.W. (1995). Structure and ligand recognition of the phosphotyrosine binding domain of Shc. Nature 378, 584-592.