SDF-9, a protein tyrosine phosphatase-like molecule, regulates the L3/dauer developmental decision through hormonal signaling in C. elegans

Development

Volumn 130, Issue 14, 2003, Pages 3237-3248

  Ohkura, Kiyotaka ^a   Suzuki, Norio ^a,b   Ishihara, Takeshi ^a   Katsura, Isao ^a  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b RIKEN   (Japan)

Author keywords

C. elegans; Cholesterol; Dauer larva; Protein tyrosine phosphatase

Indexed keywords

CAENORHABDITIS ELEGANS PROTEIN; CHOLESTEROL; PROTEIN SDF 9; PROTEIN TYROSINE KINASE; REGULATOR PROTEIN; STEROID; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CELL ASSAY; CELL DEATH; CELL FUNCTION; CONTROLLED STUDY; EMBRYO CELL; EMBRYO DEVELOPMENT; ENVIRONMENTAL FACTOR; GENE ACTIVITY; GENE EXPRESSION; GENE LOCATION; GENE MUTATION; GENETIC EPISTASIS; GROWTH REGULATION; HORMONE ACTION; HORMONE METABOLISM; LARVAL STAGE; MOSAICISM; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SUBCUTANEOUS TISSUE;

ANIMALIA; ARACHNIDA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; HEXAPODA; INVERTEBRATA;

EID: 0042170293     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.00540     Document Type: Article

References (73)

1. Ailion, M., Inoue, T., Weaver, C. I., Holdcraft, R. W. and Thomas, J. H. (1999). Neurosecretory control of aging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 96, 7394-7397.
2. Ailion, M. and Thomas, J. H. (2000). Dauer formation induced by high temperatures in Caenorhabditis elegans. Genetics 156, 1047-1067.
3. Albert, P. S., Brown, S. J. and Riddle, D. L. (1981). Sensory control of dauer larva formation in Caenorhabditis elegans. J. Comp. Neurol. 198, 435-451.
4. Albert, P. S. and Riddle, D. L. (1988). Mutants of Caenorhabditis elegans that form dauer-like larvae. Dev. Biol. 126, 270-293.
5. Antebi, A., Culotti, J. G. and Hedgecock, E. M. (1998). daf-12 regulates developmental age and the dauer alternative in C. elegans. Development 125, 1191-1205.
6. Antebi, A., Yeh, W-H., Tait, D., Hedgecock, E. and Riddle, D. L. (2000). daf-12 encodes a nuclear receptor that regulates the dauer diapause and developmental age in C. elegans. Genes Dev. 14, 1512-1527.
7. Apfeld, J. and Kenyon, C. (1998). Cell nonautonomy of C. elgans DAF-2 function in the regulation of diapause and life span. Cell 95, 199-210.
8. Avery, L. (1993). The genetics of feeding in Caenorhabditis elegans. Genetics 133, 897-917.
9. Bargmann, C. I., Thomas, J. H. and Horvitz, H. R. (1990). Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harbor Symp. Quant. Biol. 55, 529-538.
10. Bargmann, C. I. and Horvitz, H. R. (1991). Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans. Neuron 7, 729-742.
11. Bargmann, C. and Avery, L. (1995). Laser killing of cells in Caenorhabditis elegans. In Methods in Cell Biology. Vol. 48 Caenorhabditis elegans: Modern Biological Analysis of an Organism (ed. H. F. Epstein and D. C. Shakes), pp. 225-250. San Diego: Academic Press.
12. Birnby, D. A., Malone, E., Vowels, J. J., Tian, H., Colacurcio, P. L. and Thomas, J. H. (2000). A transmembrane guanylyl cyclase (DAF- 11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 155, 85-104.
13. Bowers, W. S., Ohta, T., Cleere, J. S. and Marsella, P. A. (1976). Discovery of insect anti-juvenile hormones in plants. Science 193, 542-547.
14. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
15. The C. elegans Sequencing Consortium (1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012-2018.
16. Chitwood, D. J. (1999). Biochemistry and function of nematode steroids. Crit. Rev. Biochem. Mol. Biol. 34, 273-284.
17. Coburn, C. M., Mori, I., Ohshima, Y. and Bargmann, C. I. (1998). A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure. Development 125, 249-258.
18. Conover, D. O. and Kynard, B. E. (1981). Environmental sex determination: Interaction of temperature and genotype in a fish. Science 213, 577-579.
19. Daniels, S. A., Ailion, M., Thomas, J. H. and Sengupta, P. (2000). egl-4 acts through a transforming growth factor-beta/SMAD pathway in Caenorhabditis elegans to regulate multiple neuronal circuits in response to sensory cues. Genetics 156, 123-141.
20. 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.
21. Fujiwara, M., Ishihara, T. and Katsura, I. (1999). A novel WD40 protein, CHE-2, acts cell-autonomously in the formation of C. elegans sensory cilia. Development 126, 4839-4848.
22. Fujiwara, M., Sengupta, P. and McIntire, S. L. (2002). Regulation of body size and behavioral state of C. elegans by sensory perception and the EGL-4 cGMP-dependent protein kinase. Neuron 36, 1091-1102.
23. Georgi, L. L., Albert, P. S. and Riddle, D. L. (1990). daf-1, a C. elegans gene controlling dauer larva development, encodes a novel receptor protein kinase. Cell 61, 635-645.
24. Gerisch, B., Weitzel, C., Kober-Eisermann, C., Rothers, V. and Antebi, A. (2001). A hormonal signaling pathway influencing C. elegans metabolism, reproductive development, and life span. Dev. Cell 1, 841-851.
25. Golden, J. W. and Riddle, D. L. (1982). A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 218, 578-580.
26. Golden, J. W. and Riddle, D. L. (1984a). The Caenorhabditis elegans dauer larva: Developmental effects of pheromone, food and temperature. Dev. Biol. 102, 368-378.
27. Golden, J. W. and Riddle, D. L. (1984b). A pheromone-induced developmental switch in C. elegans: temperature-sensitive mutants reveal a wild-type temperature-dependent process. Proc. Natl. Acad. Sci. USA 81, 819-823.
28. Gottlieb, S. and Ruvkun, G. (1994). daf-2, daf-16 and daf-23: genetically interacting genes controlling dauer formation in Caenorhabditis elegans. Genetics 137, 107-120.
29. Guan, K. L. and Dixon, J. E. (1990). Protein tyrosine phosphatase activity of an essential virulence determinant in Yersinia. Science 249, 553-556.
30. Guan, K. L. and Dixon, J. E. (1991). Evidence for protein-tyrosine-phosphatase catalysis proceeding via a cysteine-phosphate intermediate. J. Biol. Chem. 266, 17026-17030.
31. Hobert, O., Mori, I., Yamashita, Y., Honda, H., Ohshima, Y., Liu, Y. and Ruvkun, G. (1997). Regulation of interneuron function in the C. elegans thermoregulatory pathway by the ttx-3 LIM homeobox gene. Neuron 19, 345-357.
32. Hoekstra, D. and van IJzendoorn, S. C. (2000). Lipid trafficking and sorting: how cholesterol is filling gaps. Curr. Opin. Cell Biol. 12, 496-502.
33. Inoue, T. and Thomas, J. H. (2000). Targets of TGF-β signaling in C. elegans dauer formation. Dev. Biol. 217, 192-204.
34. Ioannou, Y. A. (2001). Multidrug permeases and subcellular cholesterol transport. Nat. Rev. Mol. Cell. Biol. 2, 657-668.
35. Iwasaki, K., Staunton, J., Saifee, O., Nonet, M. and Thomas, J. H. (1997). aex-3 encodes a novel regulator of presynaptic activity in C. elegans. Neuron 18, 613-622.
36. Jansen, G., Thijssen, K. L., Werner, P., van der Horst, M., Hazendonk, E. and Plasterk, R. H. (1999). The complete family of genes encoding G proteins of Caenorhabditis elegans. Nat. Genet. 21, 414-419.
37. Jayanthi, L. D., Apparsundaram, S., Malone, M. D., Ward, E., Miller, D. M., Eppler, M. and Blakely, R. D. (1998). The Caenorhabditis elegans gene T23G5.5 encodes an antidepressant- and cocaine-sensitive dopamine transporter. Mol. Pharmacol. 54, 601-609.
38. Jia, Z., Barford, D., Flint, A. J. and Tonks, N. K. (1995). Structural basis for phosphotyrosine peptide recognition by protein tyrosine phosphatase 1B. Science 268, 1754-1758.
39. Jia, K., Albert, P. S. and Riddle, D. L. (2002). DAF-9, a cytochrome P450 regulating C. elegans larval development and adult longevity. Development 129, 221-231.
40. Katsura, I., Kondo, K., Amano, T., Ishihara, T. and Kawakami, M. (1994). Isolation, characterization and epistasis of fluoride-resistant mutants of Caenorhabditis elegans. Genetics 136, 145-154.
41. Kimura, K. D., Tissenbaum, H. A., Liu, Y. and Ruvkun, G. (1997). daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. Science 277, 942-946.
42. Lanjuin, A. and Sengupta, P. (2002). Regulation of chemosensory receptor expression and sensory signaling by the KIN-29 Ser/Thr kinase. Neuron 33, 369-381.
43. Lin, K., Dorman, J. B., Rodan, A. and Kenyon, C. (1997). daf-16: an HNF-3/Forkhead family member that can function to double the life-span of Caenorhabditis elegans. Science 278, 1319-1322.
44. Malone, E. A. and Thomas, J. H. (1994). A screen for nonconditional dauer-constitutive mutations in Caenorhabditis elegans. Genetics 136, 879-886.
45. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
46. Miller, L. M., Waring, D. A. and Kim, S. K. (1996). Mosaic analysis using a ncl-1(+) extrachromosomal array reveals that lin-31 acts in the Pn.p cells during Caenorhabtitis elegans vulval development. Genetics 143, 1181-1191.
47. Morris, J. Z., Tissenbaum, H. A. and Ruvkun, G. (1996). A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382, 536-539.
48. Ogg, S., Paradis, S., Gottlieb, S., Patterson, G. I., Lee, L., Tissenbaum, H. A. and Ruvkun, G. (1997). The Fork head transcription factor DAF-16 transduces insulin-like metabolic and longevity signals in C. elegans. Nature 389, 994-999.
49. Ogg, S. and Ruvkun, G. (1998). The C. elegans PTEN homolog, DAF-18, acts in the insulin receptor-like metabolic signaling pathway. Mol. Cell 2, 887-893.
50. Patterson, G. I., Koweek, A., Wong, A., Liu, Y. and Ruvkun, G. (1997). The DAF-3 Smad protein antagonizes TGF-β-related receptor signaling in the Caenorhabditis elegans dauer pathway. Genes Dev. 11, 2679-2690.
51. Perkins, L. A., Hedgecock, E. M., Thomson, J. N. and Culotti, J. G. (1986). Mutant sensory cilia in the nematode C. elegans. Dev. Biol. 117, 456-487.
52. Prasad, B. C., Ye, B., Zackhary, R., Schrader, K., Seydoux, G. and Reed, R. R. (1998). unc-3, a gene required for axonal guidance in Caenorhabditis elegans, encodes a member of the O/E family of transcription factors. Development 125, 1561-1568.
53. Ren, P.-f., Lim, C.-S., Johnsen, R., Albert, P. S., Pilgrim, D. and Riddle, D. L. (1996). Control of C. elegans larval development by neuronal expression of a TGF-β homolog. Science 274, 1389-1391.
54. Riddle, D. L., Swanson, M. M. and Albert, P. S. (1981). Interacting genes in nematode dauer larva formation. Nature 290, 668-671.
55. Riddle, D. L. and Albert, P. S. (1997). Genetic and environmental regulation of dauer larva development. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer and J. R. Priess), pp. 739-768. NY: Cold Spring Harbor Laboratory Press.
56. Schackwitz, W. S., Inoue, T. and Thomas, J. H. (1996). Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 17, 719-728.
57. Snow, M. I. and Larsen, P. L. (2000). Structure and expression of daf-12: a nuclear hormone receptor with three isoforms that are involved in development and aging in Caenorhabditis elegans. Biochim Biophys Acta 1494, 104-116.
58. Streuli, M., Krueger, N. X., Tsai, A. Y. and Saito, H. (1989). A family of receptor-linked protein tyrosine phosphatases in humans and Drosophila. Proc. Natl. Acad. Sci. USA 86, 8698-8702.
59. Streuli, M., Krueger, N. X., Thai, T., Tang, M. and Saito, H. (1990). Distinct functional roles of the two intracellular phosphatase like domains of the receptor-linked protein tyrosine phosphatases LCA and LAR. EMBO J. 9, 2399-2407.
60. 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.
61. Sulston, J. and Hodgkin, J. (1988). Methods. In The Nematode Caenorhabditis elegans (ed. W. B. Wood), pp. 587-606. New York: Cold Spring Harbor Laboratory Press.
62. Swanson, M. M. and Riddle, D. L. (1981). Critical periods in the development of the Caenorhabditis elegans dauer larva. Dev. Biol. 84, 27-40.
63. Sym, M., Basson, M. and Johnson, C. (2000). A model for Niemann-Pick type C disease in the nematode Caenorhabditis elegans. Curr. Biol. 10, 527-530.
64. Sze, J. Y., Victor, M., Loer, C., Shi, Y. and Ruvkun, G. (2000). Food and metabolic signaling defects in a C. elegans serotonin-synthesis mutant. Nature 403, 560-564.
65. Take-Uchi, M., Kawakami, M., Ishihara, T., Amano, T., Kondo, K. and Katsura, I. (1998). An ion channel of the degenerin/epithelial sodium channel superfamily controls the defecation rhythm in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 95, 11775-11780.
66. Thomas, J. H., Birnby, D. A. and Vowels, J. J. (1993). Evidence for parallel processing of sensory information controlling dauer formation in Caenorhabditis elegans. Genetics 134, 1105-1117.
67. Tonks, N. K. and Neel, B. G. (2001). Combinatorial control of the specificity of protein tyrosine phosphatases. Curr. Opin. Cell Biol. 13, 182-195.
68. Vowels, J. J. and Thomas, J. H. (1992). Genetic analysis of chemosensory control of dauer formation in Caenorhabditis elegans. Genetics 130, 105-123.
69. White, J. G., Southgate, E., Thomson, J. N. and Brenner, S. (1986). The structure of the nervous system of the nematode C. elegans. Phil. Trans. R. Soc. Lond. B314, 1-340.
70. Wishart, M. J., Denu, J. M., Williams, J. A. and Dixon, J. E. (1995). A single mutation converts a novel phosphotyrosine binding domain into a dual-specificity phosphatase. J. Biol. Chem. 270, 26782-26785.
71. Wishart, M. J. and Dixon, J. E. (1998). Gathering STYX: phosphatase-like form predicts functions for unique protein-interaction domains. Trends Biochem. Sci. 23, 301-306.
72. Yu, S., Avery, L., Baude, E. and Garbers, D. L. (1997). Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc. Natl. Acad. Sci. USA 94, 3384-3387.
73. Zhou, G., Denu, J. M., Wu, L. and Dixon, J. E. (1994). The catalytic role of Cys124 in the dual specificity phosphatase VHR. J. Biol. Chem. 269, 28084-28090.