The TRA-1A sex determination protein of C. elegans regulates sexually dimorphic cell deaths by repressing the egl-1 cell death activator gene

Cell

Volumn 98, Issue 3, 1999, Pages 317-327

  Conradt, Barbara ^a,b   Horvitz, H Robert ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

ARTICLE; BINDING SITE; CAENORHABDITIS ELEGANS; CELL DEATH; GENE EXPRESSION REGULATION; GENE MUTATION; GENE REPRESSION; HERMAPHRODITISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEX DIFFERENCE; TRANSCRIPTION REGULATION;

CAENORHABDITIS ELEGANS; INVERTEBRATA;

EID: 0033529717     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81961-3     Document Type: Article

References (56)

1. Adams, J.M., and Gory, S. (1998). The Bcl-2 protein family: arbiters of cell survival. Science 287, 1322-1326.
2. Alexandre, C., Jacinto, A., and Ingham, P.W. (1996). Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the Cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev. 10, 2003-2013.
3. Benedyk, M.J., Mullen, J.R., and DiNardo, S. (1994). odd-paired: a zinc finger pair-rule protein required for the timely activation of engrailed and wingless in Drosophila embryos. Genes Dev. 8, 105-117.
4. Bloom, L., and Horvitz, H.R. (1997). The Caenorhabditis elegans gene unc-76 and its human homologs define a new gene family involved in axonal outgrowth and fasciculation. Proc. Natl. Acad. Sci. USA 94, 3414-3419.
5. Breedlove, S.M. (1986). Cellular analysis of hormone influence on motoneuronal development and function. J. Neurobiol. 17, 157-176.
6. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
7. elegans Sequencing Consortium (1998). Genome sequencing of the nematode C. elegans: a platform for investigating biology. Science 282, 2012-2018.
8. Clark, S.G., Lu, X., and Horvitz, H.R. (1994). The Caenorhabditis elegans locus lin-15, a negative regulator of a tyrosine kinase signaling pathway, encodes two different proteins. Genetics 137, 987-997.
9. Conradt, B., and Horvitz, H.R. (1998). The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93, 519-529.
10. Davis, E.C., Popper, P., and Gorski, R.A. (1996). The role of apoptosis in sexual differentiation of the rat sexually dimorphic nucleus of the preoptic area. Brain Res. 734, 10-18.
11. de Bono, M., Zarkower, D., and Hodgkin, J. (1995). Dominant feminizing mutations implicate protein-protein interactions as the main mode of regulation of the nematode sex-determining gene tra-1. Genes Dev. 9, 155-167.
12. del Peso, L., Gonzalez, V.M., and Núñez, G. (1998). Caenorhabditis elegans EGL-1 disrupts the interaction of CED-9 with CED-4 and promotes CED-3 activation. J. Biol. Chem. 273, 33495-33500.
13. Desai, C., and Horvitz, H.R. (1989). Caenorhabditis elegans mutants defective in the functioning of the motor neurons responsible for egg laying. Genetics 121, 703-721.
14. Edgar, B.A., Lehmann, D.A., and O'Farrell, P.H. (1994). Transcriptional regulation of string(cdc25): a link between developmental programming and the cell cycle. Development 120, 3131-3143.
15. Ellis, H.M., and Horvitz, H.R. (1986). Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817-829.
16. Ellis, R.E., and Horvitz, H.R. (1991). Two C. elegans genes control the programmed deaths of specific cells in the pharynx. Development 112, 591-603.
17. Ellis, R.E., Yuan, J., and Horvitz, H.R. (1991). Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7, 663-698.
18. Follette, P.J., and O'Farrell, P.H. (1997). Connecting cell behavior to patterning: lessons from the cell cycle. Cell 88, 309-314.
19. Franke, T.F., and Cantley, L.C. (1997). A Bad kinase makes good. Nature 390, 116-117.
20. Hodgkin, J. (1983). Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics 103, 43-64.
21. Hodgkin, J. (1987). A genetic analysis of the sex-determining gene tra-1 in the nematode Caenorhabditis elegans. Genes Dev. 1, 731-745.
22. Hodgkin, J. (1988). Sexual dimorphism and sex determination. In The Nematode Caenorhabditis elegans, W.B. Wood and the Community of C. elegans Researchers, ed. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 243-279.
23. Hunter, C.P., and Wood, W.B. (1990).The tra-1 gene determines sexual phenotype cell-autonomously in C. elegans Cell 63, 1193-1204.
24. Imaizumi, K., Tsuda, M., Imai, Y., Wanaka, A., Takagi, T., and Tohyama, M. (1997). Molecular cloning of a novel polypeptide, DP5, induced during programmed neuronal death. J. Biol. Chem. 272, 18842-18848.
25. Jacobson, M.D., Weil, M., and Raff, M.C. (1997). Programmed cell death in animal development. Cell 88, 347-354.
26. Johnson, R.L., and Scott, M.P. (1998). New players and puzzles in the hedgehog signaling pathway. Curr. Opin. Genet. Dev. 8, 450-456.
27. Kelekar, A., and Thompson, C.B. (1997). Bcl-2 family proteins: the role of the BH3 domain in apoptosis. Trends Cell Biol. 8, 324-330.
28. Kim, R.J., and DeVoogd, T.J. (1989). Genesis and death of vocal control neurons during sexual differentiation in the zebra finch. J. Neurosci. 9, 3176-3187.
29. Konishi, M., and Akutagawa, E. (1985). Neuronal growth, atrophy and death in a sexually dimorphic song nucleus in the zebra finch brain. Nature 375, 145-147.
30. Li, H., Zhu, H., Xu, C.-j., and Yuan, J. (1998). Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501.
31. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998). Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490.
32. Mello, C., and Fire, A. (1995). DNA Transformation. Methods Cell Biol. 48, 451-482.
33. Metzstein, M.M., Hengartner, M.O., Tsung, N., Ellis, R.E., and Horvitz, H.R. (1996). Transcriptional regulator of programmed cell death encoded by Caenorhabditis elegans gene ces-2. Nature 328, 545-547.
34. Metzstein, M.M., Stanfield, G.S., and Horvitz, H.R. (1998). Genetics of programmed cell death in C. elegans: past, present and future. Trends Genet. 14, 410-416.
35. Meyer, B.J. (1997). Sex determination and X chromosome compensation. In C. elegans II. D. L. Riddle et al., eds. (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press), pp. 209-269.
36. Nicholson, D.W., and Thornberry, N.A. (1997). Caspases: killer proteases. Trends Biochem. Sci. 22, 299-306.
37. Nonet, M.L., and Meyer, B.J. (1991). Early aspects of Caenorhabditis elegans sex determination and dosage compensation are regulated by a zinc-finger protein. Nature 351, 65-68.
38. Nordeen, E.J., Nordeen, K.W., Sengelaub, D.R., and Arnold, A.P. (1985). Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science 229, 671-673.
39. Oppenheimer, R.W. (1991). Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501.
40. Perry, M.D., Trent, C., Robertson, B., Chamblin, C., and Wood, W.B. (1994). Sequenced alleles of the Caenorhabditis elegans sex-determining gene her-1 includes a novel class of conditional promoter mutations. Genetics 138, 317-327.
41. Pettmann, B., and Henderson, C.E. (1998). Neuronal cell death. Neuron 20, 633-647.
42. Pollock, R., and Treisman, R. (1990). A sensitive method for the determination of protein-DNA binding specificities. Nucleic Acid Res. 18, 6197-6204.
43. Riddle, D.L., Blumenthal, T., Meyer, B.J., and Priess, J.R., eds. (1997). C. elegans II (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
44. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular cloning: a Laboratory Manual, (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
45. Sasaki, H., Hui, C.-c., Nakafuku, M., and Kondoh, H. (1997). A binding site for Gli proteins is essential for HNF-3-flooi plate enhancer activity in transgenics and can respond to Shh in vitro. Development 124, 1313-1322.
46. Shimell, M.J., Simon, J., Bender, W., and O'Connor, M.B. (1994). Enhancer point mutation results in a homeotic transformation in Drosophila. Science 264, 968-971.
47. Sulston, J.E., and Horvitz, H.R. (1977). Post-embryonic cell lineages of the nematode Caenorhabditis elegans. Dev. Biol. 56, 110-156.
48. 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.
49. Thorn, R.S., and Truman, J.W. (1994). Sexual differentiation in the CNS of the moth Manduca sexta. I. Sex and segment-specificity in production, differentiation, and survival of the imaginai midline neurons. J. Neurobiol. 25, 1039-1053.
50. Trent, C., Tsung, N., and Horvitz, H.R. (1983). Egg-laying defective mutants of the nematode Caenorhabditis elegans. Genetics 104, 619-647.
51. Trent, C., Purnell, B., Gavinski, S., Hageman, J., Chamblin, C., and Wood, W.B. (1991). Sex-specific transcriptional regulation of the C. elegans sex-determining gene her-1. Mech. Dev. 34, 43-56.
52. Truman, J.W. (1984). Cell death in invertebrate nervous systems. Annu. Rev. Neurosci. 7, 171-188.
53. Vaux, D.L. (1997). CED-4 - the third horseman of apoptosis. Cell 90, 389-390.
54. von Ohlen, T., Lessing, D., Nusse, R., and Hooper, J.E. (1997). Hedgehog signaling regulates transcription through cubitus interrupt us, a sequence-specific DNA binding protein. Proc. Natl. Acad. Sci. USA 94, 2404-2409.
55. Zarkower, D., and Hodgkin, J. (1992). Molecular analysis of the C. elegans sex-determination gene tra-1: a gene encoding two zinc finger proteins. Cell 70, 237-249.
56. Zarkower, D., and Hodgkin, J. (1993). Zinc fingers in sex determination: only one of the two C. elegans Tra-1 proteins binds DNA in vitro. Nucleic Acid Res. 21, 3691-3698.