Rasputin, the Drosophila homologue of the RasGAP SH3 binding protein, functions in Ras- and Rho-mediated signaling

Development

Volumn 127, Issue 8, 2000, Pages 1715-1725

  Pazman, Cecilia ^a,c   Mayes, Caryl A ^b   Fanto, Manolis ^b   Haynes, Susan R ^a,c   Mlodzik, Marek ^b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

Development; Drosophila; Ommatidial polarity; Ras; RasGAP; Rho

Indexed keywords

BINDING PROTEIN; GUANOSINE TRIPHOSPHATASE; RAS PROTEIN;

ARTICLE; COMPOUND EYE; DROSOPHILA; EYE DEVELOPMENT; GENE MUTATION; NONHUMAN; PHENOTYPE; PHOTORECEPTOR; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CARRIER PROTEINS; CYTOSOL; DNA-BINDING PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; GENE EXPRESSION; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; PHOTORECEPTORS, INVERTEBRATE; RAS PROTEINS; RECEPTORS, STEROID; REPRESSOR PROTEINS; RHOA GTP-BINDING PROTEIN; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION;

EID: 0034090970     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Adler, P. N. (1992). The genetic control of tissue polarity in Drosophila. BioEssays 14, 735-741.
2. Basler, K., Christen, B. and Hafen, E. (1991). Ligand-independent activation of the sevenless receptor tyrosine kinase changes the fate of cells in the developing Drosophila eye. Cell 64, 1069-1081.
3. Basler, K., Siegrist, P. and Hafen, E. (1989). The spatial and temporal expression pattern of sevenless is exclusively controlled by gene-internal elements. EMBO J. 8, 2381-2386.
4. Begemann, G., Michon, A. M., van der Voorn, L., Wepf, R. and Mlodzik, M. (1995). The Drosophila orphan nuclear receptor Seven-up requires the Ras pathway for its function in photoreceptor determination. Development 121, 225-235.
5. Birney, E., Kumar, S. and Krainer, A. R. (1993). Analysis of the RNA-recognition motif and RS and RGG domains: Conservation in metazoan pre-mRNA splicing factors. Nucleic Acids Res. 21, 5803-5816.
6. Boutros, M., Paricio, N., Strutt, D. I. and Mlodzik, M. (1998). Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94, 109-118.
7. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-15.
8. Brunner, D., Oellers, N., Szabad, J., Biggs, W. H., Zipursky, S. L. and Hafen, E. (1994). A gain of function mutation in Drosophila MAP kinase activates multiple receptor tyrosine kinase signaling pathways. Cell 76, 875-888.
9. Cooper, M. T. D. and Bray, S. J. (1999). Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye. Nature 397, 526-529.
10. Diaz-Benjumea., F. J. and Hafen, E. (1994). The sevenless signalling cassette mediates Drosophila EGF receptor function during epidermal development. Development 120, 569-78.
11. Dickson, B., Sprenger, F., Morrison, D. and Hafen, E. (1992). Rat functions downstream of Ras1 in the sevenless signal transduction pathway. Nature 360, 600-603.
12. Duchesne, M., Schweighoffer, F., Parker, F., Clerc, F., Frobert, Y., Thang, M. N. and Tocqué, B. (1993). Identification of the SH3 domain of GAP as an essential sequence for Ras-GAP-mediated signaling. Science 259, 525-528.
13. Ellis, C., Moran, M., McCormick, F. and Pawson, T. (1990). Phosphorylation of GAP and GAP-associated proteins by transforming and mitogenic tyrosine kinases. Nature 343, 377-380.
14. Fanto, M., Mayes, C. A. and Mlodzik, M. (1998). Linking cell-fate specification to planar polarity: determination of the R3/R4 photoreceptors is a prerequisite for the interpretation of the Frizzled mediated polarity signal. Mech. Dev. 74, 51-58.
15. Fanto, M. and Mlodzik, M. (1999). Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397, 523-526.
16. Feldmann, P., Eicher, E. N., Leevers, S. J., Hafen, E. and Hughes, D. A. (1999). Control of growth and differentiation by Drosophila RasGAP, a homolog of p120 Ras-GTPase-Activating protein. Mol. Cell Biol. 19, 1928-1937.
17. Feller, S. M., Ren, R., Hanafusa, H. and Baltimore, D. (1994). SH2 and SH3 domains as molecular adhesives: the interactions of Crk and Ab1. Trends Biochem. Sci. 19, 453-458.
18. Fortini, M. E., Rebay, I., Caron, L. A. and Artavanis-Tsakonas, S. (1993). An activated Notch receptor blocks cell-fate commitment in the developing Drosophila eye. Nature 365, 555-557.
19. Fortini, M. E., Simon, M. A. and Rubin, G. M. (1992). Signalling by the sevenless protein tyrosine kinase is mimicked by Ras1 activation. Nature 355, 559-561.
20. Freeman, M. (1997). Cell determination strategies in the Drosophila eye. Development 124, 261-270.
21. Gallouzi, I. E., Parker, F., Chebli, K., Maurier, F., Labourier, E., Barlat, I., Capony, J. P., Tocque, B. and Tazi, J. (1998). A novel phosphorylation-dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol. Cell Biol. 18, 3956-3965.
22. Gaul, U., Mardon, G. and Rubin, G. M. (1992). A putative Ras GTPase activating protein acts as a negative regulator of signaling by the sevenless receptor tyrosine kinase. Cell 68, 1007-1019.
23. Greenwald, I. and Rubin, G. M. (1992). Making a difference: the role of cell-cell interactions in establishing seperate identities for equivalent cells. Cell 68, 271-282.
24. Guichet, A., Copeland, J. W. R., Erdelyi, M., Hlousek, D., Zavorszky, P., Ho, J., Brown, S., Percival-Smith, A., Krause, H. M. and Ephrussi, A. (1997). The nuclear receptor homologue Ftz-F1 and the homeodomain protein Ftz are mutually dependent cofactors. Nature 385, 548-552.
25. Haynes, S. R., Cooper, M. T., Pype, S. and Stolow, D. T. (1997). Involvement of a tissue-specific RNA recognition motif protein in Drosophila spermatogenesis. Mol. Cell Biol. 17, 2708-2715.
26. Herskowitz, I. (1995). MAP kinase pathways in yeast: for mating and more. Cell 80, 187-197.
27. Hiromi, Y., Mlodzik, M., West, S. R., Rubin, G. M. and Goodman, C. S. (1993). Ectopic expression of seven-up causes cell fate changes during ommatidial assembly. Development 118, 1123-1135.
28. Hobert, O., Jallal, B., Schlessinger, J. and Ullrich, A. (1994). Novel signaling pathway suggested by SH3 domain-mediated p95vav/heterogeneous ribonucleoprotein K interaction. J. Biol. Chem. 269, 20225-20228.
29. Hu, K.-Q. and Settleman, J. (1997). Tandem SH2 binding sites mediate the RasGAP-RhoGAP interaction: a conformational mechanism for SH3 domain regulation. EMBO J. 16, 473-483.
30. Hunter, T. (1995). Protein kinases and phosphatases: the Yin and Yang of protein phosphorylation and signaling. Cell 80, 225-236.
31. John, J., Frech, M. and Wittinghofer, A. (1988). Biochemical properties of Ha-ras encoded p21 mutants and mechanisms of the autophosphorylation reaction. J. Biol. Chem. 263, 11792-11799.
32. Karim, F. D., Chang, H. C., Therrien, M., Wassarman, D. A., Laverty, T. and Rubin, G. M. (1996). A screen for genes that function downstream of Ras1 during Drosophila eye development. Genetics 143, 315-329.
33. Karlovich, C. A., Bonfini, L., Rogge, R. D., Daga, A., Czech, M. P. and Banerjee, U. (1995). In vivo analysis of the Ras exchange factor son of sevenless. Science 268, 576-579.
34. Kazlauskas, A., Ellis, C., Pawson, T. and Cooper, J. A. (1990). Binding of GAP to activated PDGF receptors. Science 247, 1578-1581.
35. Kelley, R. L. (1993). Initial organisation of the Drosophila dorsoventral axis depends on an RNA-binding protein encoded by the squid gene. GenesDev. 7, 948-960.
36. Kiledjian, M. and Dreufuss, G. (1992). Primary structure and binding activity of the hnRNP U protein: binding RNA through RGG box. EMBO J. 7, 2655-2664.
37. Kramer, S., West, S. R. and Hiromi, Y. (1995). Cell fate control in the Drosophila retina by the orphan receptor Seven-up: its role in the decisions mediated by the Ras signaling pathway. Development 121, 1361-1372.
38. Krasnow, R. E., Wong, L. L. and Adler, P. N. (1995). dishevelled is a component of the frizzled signalling pathway in Drosophila. Development 121, 4095-4102.
39. Marshall, C. J. (1994). MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev. 4, 82-89.
40. Marshall, C. J. (1995). Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185.
41. Marx, J. and Kerr, R. A. (1993). Forging a path to the nucleus. Science 260, 1588-1590.
42. Matunis, M. J., Michael, W. M. and Dreyfuss, G. (1992). Characterization and primary structure of the poly(C)-binding heterogeneous nuclear ribonucleoprotein complex K protein. Mol. Cell. Biol. 12, 164-171.
43. McCormick, F. (1989). ras GTPase activating protein: signal transmitter and signal terminator. Cell 56, 5-8.
44. Michelolti, E. F., Michelotti, G. A., Aronsohn, A. I. and Levens, D. (1996). Heterogeneous nuclear ribonucleoprotein K is a transcription factor. Mol. Cell. Biol. 16, 2350-2360.
45. Mlodzik, M., Hiromi, Y., Weber, U., Goodman, C. S. and Rubin, G. M. (1990). The Drosophila seven-up gene, a member of the steroid receptor gene superfamily, controls photoreceptor cell fates. Cell 60, 211-224.
46. Mlodzik, M. (1999). Planar polarity in the Drosophila eye: a multifaceted view of signaling specificity and crosstalk. EMBO J. 18, 6873-6879
47. Moran, M. F., Polakis, P., McCormick, F., Pawson, T. and Ellis, C. (1991). Protein-tyrosine kinases regulate the phosphorylation, protein interactions, subcellular distribution, and activity of p21ras GTPase-activating protein. Mol. Cell Biol. 11, 1804-1812.
48. Olivier, J.-P., Raabe, T., Henkemeyer, M., Dickson, B., Mbamalu, G., Margolis, B., Schlessinger, J., Hafen, E. and Pawson, T. (1993). A Drosophila SH2-SH3 adaptor protein implicated in coupling the sevenless tyrosine kinase to an activator of Ras guanine nucleotide exchange, Sos. Cell 73, 179-191.
49. Parker, F., Maurier, F., Delumeau, I., Duchesne, M., Faucher, D., Debussche, L., Dugue, A. S., F. and Tocque, B. (1996). A Ras-GTPase-activating protein SH3-domain-binding protein. Mol. Cell. Biol. 16, 2561-2569.
50. Patel, N. H. (1994). Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol. 44, 445-487.
51. Pomerance, M., Thang, M. N., Tocque, B. and Pierre, M. (1996). The Ras-GTPase-activating protein SH3 domain is required for Cdc2 activation and Mos induction by oncogenic Ras in Xenopus oocytes independently of mitogen-activated protein kinase activation. Mol. Cell. Biol. 16, 3179-3186.
52. Raabe, T., Riesgo-Escovar, J., Lin, X., Bausenwein, B. S., Deak, P., Maröy, P. and Hafen, E. (1996). DOS, a novel pleckstrin homology domain-containing protein required for signal transduction between sevenless and Ras1 in Drosophila. Cell 85, 911-920.
53. Ready, D. F., Hanson, T. E. and Benzer, S. (1976). Development of the Drosophila retina, a neurocrystalline lattice. Dev. Biol. 53, 217-240.
54. Reifegerste, R. and Moses, K. (1999). The genetics of epithelial polarity and pattern in the Drosophila retina. BioEssays 21, 275-285.
55. Rogge, R. D., Karlovich, C. A. and Banerjee, U. (1991). Genetic dissection of a neurodevelopmental pathway: son of sevenless functions downstream of the sevenless and EGF receptor tyrosine kinases. Cell 64, 39-48.
56. Settleman, J., Narasimhan, V., Foster, L. C. and Weinberg, R. A. (1992). Molecular cloning of cDNAs encoding the GAP-associated protein p190: Implications for a signaling pathway from Ras to the nucleus. Cell 69, 539-549.
57. Simon, M. A., Bowtell, D. D. L., Dudson, G. S., Laverty, T. R. and Rubin, G. M. (1991). Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in the signaling by the sevenless protein tyrosine kinase. Cell 67, 701-716.
58. Spradling, A. C. and Rubin, G. M. (1982). Transposition of cloned P-elements into Drosophila germ line chromosomes. Science 218, 341-347.
59. Steinhauer, W. R., Walsh, R. C. and Kalfayan, L. J. (1989). Sequence and structure of the Drosophila melanogaster ovarian tumor gene and generation of an antibody specific for the ovarian tumor protein. Mol. Cell. Biol. 9, 5726-5732.
60. Strutt, D. I., Weber, U. and Mlodzik, M. (1997). The role of RhoA in tissue polarity and Frizzled signalling. Nature 387, 292-295.
61. Taylor, S. J. and Shalloway, D. (1994). An RNA-binding protein associated with Src through its SH2 and SH3 domains in mitosis. Nature 368, 867-874.
62. Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighing, position specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
63. Tocque, B., Delumeau, I., Parker, F., Maurier, F., Multon, M.-C. and Schweighoffer, F. (1997). Ras-GTPase activating protein (GAP): A putative effector for Ras. Cell. Signal. 9, 153-158.
64. Tomlinson, A. and Ready, D. F. (1987). Cell fate in the Drosophila ommatidium. Dev. Biol. 123, 264-275.
65. Treier, M., Bohmann, D. and Mlodzik, M. (1995). JUN cooperates with the ETS domain protein Pointed to induce photoreceptor R7 fate in the Drosophila eye. Cell 83, 753-760.
66. Wassarman, D. A., Therrien, M. and Rubin, G. M. (1995). The Ras signaling pathway in Drosophila. Curr. Opin. Genet. Dev. 5, 44-50.
67. Zheng, L., Zhang, J. and Carthew, R. W. (1995). frizzled regulates mirror-symmetric pattern formation in the Drosophila eye. Development 121, 3045-3055.
68. Zipursky, S. L. and Rubin, G. M. (1994). Determination of neuronal cell fate: lessons from the R7 neuron of Drosophila. Annu. Rev. Neurosci. 17, 373-397.