The Drosophila Ral GTPase regulates developmental cell shape changes through the Jun NH2-terminal kinase pathway

Journal of Cell Biology

Volumn 146, Issue 2, 1999, Pages 361-372

  Sawamoto, Kazunobu ^a   Winge, Per ^b   Koyama, Shinya ^c   Hirota, Yuki ^a   Yamada, Chiharu ^a   Miyao, Sachiyo ^a   Yoshikawa, Shingo ^d   Jin, Ming Hao ^a   Kikuchi, Akira ^c   Okano, Hideyuki ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c HIROSHIMA UNIV SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

Bristle; Dorsal closure; Hair; Jun NH2 terminal kinase; Ral

Indexed keywords

GLUTATHIONE TRANSFERASE; GUANOSINE TRIPHOSPHATASE; HYBRID PROTEIN; RAL PROTEIN; RAS PROTEIN; RNA; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ADOLESCENT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SHAPE; CONTROLLED STUDY; CUTICLE; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; HAIR GROWTH; IMAGINAL DISC; IN SITU HYBRIDIZATION; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYTENE CHROMOSOME; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS;

ANIMALIA;

EID: 0033606814     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.146.2.361     Document Type: Article

References (83)

1. Adler, P.N. 1992. The genetic control of tissue polarity in Drosophila. BioEssays. 14:735-741.
2. Albright, C.F., B.W. Giddings, J. Liu, M. Vito, and R.A. Weinberg. 1993. Characterization of a guanine nucleotide dissociation stimulator for a ras-related GTPase. EMBO (Eur. Mol. Biol. Organ.) J. 12:339-347.
3. Appel, L.F., M. Prout, R. Abu-Shumays, A. Hammonds, J.C. Garbe, D. Fristrom, and J. Fristrom. 1993. The Drosophila stubble-stubbloid gene encodes an apparent transmembrane serine protease required for epithelial morphologenesis. Proc. Natl. Acad. Sci. USA. 90:4937-4941.
4. Bar Sagi, D., and J.R. Feramisco. 1986. Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by ras proteins. Science. 233: 1061-1068.
5. Barbacid, M. 1987. ras genes. Annu. Rev. Biochem. 56:779-827.
6. Barrett, K., M. Leptin, and J. Settleman. 1997. The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell. 91:905-915.
7. Bos, J.L. 1997. Ras-like GTPases. Biochem. Biophys. Acta 1333:M19-M31.
8. Brand, A.H., and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 118: 401-415.
9. Brunner, D., N. Oellers, J. Szabad, W.H. Biggs III, S.L. Zipursky, and E. Hafen. 1994. A gain-of-function mutation in Drosophila MAP kinase activates multiple receptor tyrosine kinase signaling pathways. Cell. 76:875-888.
10. Cant, K., B.A. Knowles, M.S. Mooseker, and L. Cooley. 1994. Drosophila singed, a facin homolog, is required for actin bundle formation during oogenesis and bristle extension. J. Cell Biol. 125:369-380.
11. Cantor, S.B., T. Urano, and L.A. Feig. 1995. Identification and characterization of Ral-binding protein 1, a potential downstream target of Ral GTPase. Mol. Cell. Biol. 15:4578-4584.
12. Chardin, P., and A. Tavitian. 1989. Coding sequences of human ralA and ralB cDNAs. Nucleic Acid Res. 17:4380.
13. Coso, O.A., M. Chiariello, J.C. Yu, H. Teramoto, P. Crespo, N. Xu, T. Miki, and J.S. Gutkind. 1995. The small GTP-binding proteins Rac and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell. 81:1137-1146.
14. Eaton, S., R. Wept, and K. Simons. 1996. Roles of Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J. Cell Biol. 135: 1277-1289.
15. Emkey, R., S. Freedman, and L.A. Feig. 1991. Characterization of a GTPase-activating protein for the Ras-related Ral protein. J. Biol. Chem. 266:9703-9706.
16. 2+ binding site of Ras blocks its activation by GTP. Mol. Cell. Biol. 11: 4822-4829.
17. Fehon, R.G., T. Oren, D.R. LaJeunesse, T.E. Melby, and B.M. McCartney. 1997. Isolation of mutations in the Drosophila homologues of the human Neurofibromatosis 2 and yeast CDC42 genes using a simple and efficient reverse-genetic method. Genetics. 146:245-252.
18. Feig, L.A., and G.M. Cooper. 1988. Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol. Cell. Biol. 8:3235-3243.
19. Feig, L.A., T. Urano, and S. Cantor. 1996. Evidence for a Ras/Ral signaling cascade. Trends Biochem. Sci. 21:438-441.
20. Fisher-Vize, J.A, G.M. Rubin, and R. Lehmann. 1992. The fat facets gene is required for Drosophila eye and embryo development. Development. 116:985-1000.
21. Fristrom, D., M. Wilcox, and J. Fristrom. 1993. The distribution of PS integrins, laminin A and F-actin during key stages in Drosophila wing development. Development. 117:509-523.
22. Fujita, S.C., S.L. Zipursky, S. Benzer, A. Ferrus, and S.L. Shotwell. 1982. Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. USA. 79:7929-7933.
23. Galcheva-Gargova, Z., B. Derijard, I.H. Wu, and R.J. Davis. 1994. An osmosensing signal transduction pathway in mammalian cells. Science. 265:806-808.
24. Glise, B., and S. Noselli. 1997. Coupling of Jun amino-terminal kinase and decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev. 11:1738-1747.
25. Glise, B., H. Bourbon, and S. Noselli. 1995. hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell. 83:451-461.
26. Goi, T., G. Rusanescu, T. Urano, and L.A. Feig. 1999. Ral-specific guanine nucleotide exchange factor activity opposes other Ras effectors in PC12 cells by inhibiting neurite outgrowth. Mol. Cell. Biol. 19:1731-1741.
27. Hacker. U., and N. Perrimon. 1998. DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila. Genes Dev. 12:274-284.
28. Harden, N., H.Y. Loh, W. Chia, and L. Lim. 1995. A dominant inhibitory version of the small GTP-binding protein Rac disrupts cytoskeletal structures and inhibits developmental cell shape changes in Drosophila. Development. 121:903-914.
29. Harden, N., J. Lee, H.-Y. Loh, Y.M. Ong, I. Tan, T. Leung, E. Manser, and L. Lim. 1996. A Drosophila homolog of the Rac- and Cdc42-activated serine/threonine kinase PAK is a potential focal adhesion and focal complex protein that colocalizes with dynamic actin structures. Mol. Cell. Biol. 16:1896-1908.
30. Hariharan, I.K., R.W. Carthew, and G.M. Rubin. 1991. The Drosophila roughened mutation: activation of a rap homolog disrupts eye development and interferes with cell determination. Cell. 67:717-722.
31. Hariharan, I.K., K.-Q. Hu, H. Asha, A. Quintanilla, R.M. Ezzell, and J. Settleman. 1995. Characterization of rho GTPase family homologues in Drosophila melanogaster: overexpressing Rhol in retinal cells causes a late developmental defect. EMBO (Eur. Mol. Biol. Organ.) J. 14:292-302.
32. Hartenstein, V., and J.W. Posakony. 1989. Development of adult sensilla on the wing and notum of Drosophila melanogaster. Development. 107:389-405.
33. 2+ and the beta gamma-subunit complex on the interactions of guanine nucleotides with G proteins. J. Biol. Chem. 262:757-761.
34. Hinoi, T., S. Kishida, S. Koyama, M. Ikeda, Y. Matsuura, and A. Kikuchi. 1996. Post-translational modifications of Ras and Ral are important for the action of Ral GDP dissociation stimulator. J. Biol. Chem. 271:19710-19716.
35. Hofer, F., S. Fields, C. Schneider, and G.S. Martin. 1994. Activated Ras interacts with the Ral guanine nucleotide dissociation stimulator. Proc. Natl. Acad. Sci. USA. 91:11089-11093.
36. Hopmann, R., J.A. Cooper, and K.G. Miller. 1996. Actin organization, bristle morphology, and viability are affected by actin capping protein mutations in Drosophila. J. Cell Biol. 133:1293-1305.
37. Jiang, H., J.-Q. Luo, T. Urano, P. Frankel, Z. Lu, D.A. Foster, and L.A. Feig. 1995. Involvement of Ral GTPase in v-Src-induced phospholipase D activation. Nature. 378:409-412.
38. Jullien-Flores, V., O. Dorseuil, F. Romero, F. Letourneur, S. Saragosti, R. Berger, A. Tavitian, G. Gacon, and H.J. Camonis. 1995. Bridging Ral GTP-ase to Rho pathways. RL1P76, a Ral defector with CDC42/Rac GTPase-activating protein activity. J. Biol. Chem. 270:22473-22477.
39. Kahn, S., F. Yamamoto, C. Almoguera, E. Winter, K. Forrester, J. Jordano, and M. Perucho. 1987. The c-K-ras gene and human cancer. Anticancer Res. 7:639-652.
40. Kikuchi, A., T. Yamashita, M. Kawata, K. Yamamoto, K. Ikeda, T. Tanimoto, and Y. Takai. 1988. Purification and characterization of a novel GTP-binding protein with a molecular weight of 24,000 from bovine brain membranes. J. Biol. Chem. 263:2897-2904.
41. Kikuchi, A., S.D. Demo, Z.-H. Ye, Y.W. Chen, and L.T. Williams. 1994. ra1-GDS family members interact with the effector domain of ras p21. Mol. Cell. Biol. 14:7483-7491.
42. Kishida, S., S. Koyama, K. Matsubara, M. Kishida, Y. Matsuura, and A. Kikuchi. 1997. Colocalization of Ras and Ral on the membrane is required for Ras-dependent Ral activation through Ral GDP dissociation stimulator. Oncogene. 15:2899-2907.
43. Luo, L, Y.J. Liao, L.Y. Jan, and Y.N. Jan. 1994. Distinct morphogenetic functions of similar small GTPases: Drosophila DRac1 is involved in axonal out-growth and myoblast fusion. Genes Dev. 8:1787-1802.
44. Melzig, J., K.-H. Rein, U. Schafer, H. Pfister, H. Jackle, M. Heisenberg, and T. Raabe. 1998. A protein related to p21-activated kinase (PAK) that is involved in neurogenesis in the Drosophila adult central nervous system. Curr. Biol. 8:1223-1226.
45. Miller, M.J., S. Prigent, E. Kupperman, L. Rioux, S.H. Park, J.R. Feramisco, M.A. White, J.L. Rutkowski, and J.L. Meinkoth. 1997. RalGDS functions in Ras- and cAMP-mediated growth stimulation. J. Biol. Chem. 272:5600-5605.
46. Mitchell, H.K., J. Roach, and N.S. Petersen. 1983. The morphogenesis of cell hairs on Drosophila wings. Dev. Biol. 95:387-398.
47. Moscow, J.A., R. He, J.M. Gudas, and K.H. Cowan. 1994. Utilization of multiple polyadenylation signals in the human RHOA protooncogene. Gene. 144: 229-236.
48. Murai, H., M. Ikeda, S. Kishida, O. Ishda, M. Okazaki-Kishida, Y. Matsuura, and A. Kikuchi. 1997. Characterization of Ral GDP dissociation stimulator-like (RGL) activities to regulate c-fos promoter and the GDP/GTP exchange of Ral. J. Biol. Chem. 272:10483-10490.
49. Neuman-Silberberg, F.S., E. Schejter, P.M. Hoffmann, and B.Z. Shilo. 1984. The Drosophila ras oncogenes: structure and nucleotide sequence. Cell. 37: 1027-1033.
50. Nishida, Y., M. Hata, T. Ayaki, H. Ryo, M. Yamagata, K. Shimizu, and Y. Nishizuka. 1988. Proliferation of both somatic and germ cells is affected in the Drosophila mutants of raf proto-oncogene. EMBO (Eur. Mol. Biol. Organ.) J. 7:775-781.
51. Noselli, S. 1998. JNK signaling and morphogenesis in Drosophila. Trends Genet. 14:33-38.
52. Okazaki, M., S. Kishida, T. Hinoi, T. Hasegawa, M. Tamada, T. Kataoka, and A. Kikuchi. 1997. Synergistic activation of c-fos promoter activity by Raf and RalGDP dissociation stimulator. Oncogene. 14:515-521.
53. Overton, J. 1967. The fine structure of developing bristles in wild-type and mutant Drosophila melanogaster. J. Morphol. 122:367-380.
54. Park, S.H., and R.A. Weinberg. 1995. A putative effector of Ral has homology to Rho/Rac GTPase activating proteins. Oncogene. 11:2349-2355.
55. Petersen, N.S., D.-H. Lankenau, H.K. Mitchell, P. Young, and V.G. Corces. 1994. Forked proteins are components of fiber bundles present in developing bristles of Drosophila melanogaster. Genetics. 136:173-182.
56. Ridley, A.J., and A. Hall. 1992. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70:389-399.
57. Riesgo-Escovar, J.R., M. Jenni, A. Fritz, and E. Hafen. 1996. The Drosophila Jun-N-terminal kinase is required for cell morphogenesis but not for Djun-dependent cell fate specification in the eye. Genes Dev. 10:2759-2768.
58. Rodriguez-Viciana, P., P.H. Warne, A. Khwaja, B.M. Marte, D. Pappin, P. Das, M.D. Waterfield, A. Ridley, and J. Downward. 1997. Role of phosphoinositide 3-OH kinase in cell transformation and control of the actin cytoskeleton by Ras. Cell. 89:457-467.
59. Sawamoto, K., H. Okano, Y. Kobayakawa, S. Hayashi, K. Mikoshiba, and T. Tanimura. 1994. The function of argos in regulating cell fate decisions during the Drosophila eye and wing vein development. Dev. Biol. 164:267-276.
60. Schweighoffer, F., H. Cai, M.C. Chevallier-Multon, I. Path, G. Cooper, and B. Tocque. 1993. The Saccharomyces cerevisiae SDC25 C-domain gene product overcomes the dominant inhibitory activity of Ha-Ras asn-17. Mol. Cell. Biol. 13:39-43.
61. Shoji, I., A. Kikuchi, S. Kuroda, and Y. Takai. 1989. Kinetic analysis of the binding of guanine nucleotide to bovine brain smg p25 A. Biochem. Biophys. Res. Commun. 162:273-281.
62. Simon, M.A., D.D. Bowtell, G.S. Dodson, T.R. Laverty, and G.M. Rubin. 1991. Ras1 and a putative guanine nucleotide exchange factor perform crucial steps in signal transduction by the sevenless protein tyrosine kinase receptor. Cell. 67:701-716.
63. Sluss, H.K., Z. Man, T. Barrett, R.J. Davis, and Y.T. Ip. 1996. A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev. 10:2745-2758.
64. Spaargaren, M., and J.R. Bischoff. 1994. Identification of the guanine nucleotide dissociation stimulator for Ral as a putative effector molecule of R-ras, H-ras, K-ras and rap. Proc. Natl. Acad. Sci. USA 91:12609-12613.
65. Strutt, D.I., U. Weber, and M. Mlodzik. 1997. The role of RhoA in tissue polarity and Frezzled signalling. Nature. 387:292-295.
66. Tautz, D., and C. Pfeifle. 1989. A non-radioactive in situ hybridization method for the localization of specific RNAs in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma. 98:81-85.
67. Tilney, L.G., M.S. Tilney, and G.M. Guild. 1995. Actin bundles in Drosophila bristles. I. Two filament cross-linked are involved in bundling. J. Cell Biol. 130:629-638.
68. Tilney, L.G., P. Connelly, S. Smith, and G.M. Guild. 1996. F-actin bundles in Drosophila bristles are assembled from modules composed of short filaments. J. Cell Biol. 135:1291-1308.
69. Tsuda, L., Y.H. Inoue, M. Yoo, M. Mizuno, M. Hata, Y. Lim, T. Adachi-Yamada, Y. Ryo, Y. Masamune, and Y. Nishida. 1993. A protein kinase similar to MAP kinase activator acts downstream of the raf kinase in Drosophila. Cell. 72:407-414.
70. Turner, C.M., and P.N. Adler. 1998. Distinct roles for the actin and microtubule cytoskeletons in the morphogenesis of epidermal hairs during wing development in Drosophila. Mech. Dev. 70:181-192.
71. Urano, T., R. Emkey, and L.A. Feig. 1996. Ral-GTPases mediates a distinct downstream signaling pathway from Ras that facilitates cellular transformation. EMBO (Eur. Mol. Biol. Organ.) J. 15:810-816.
72. Van Aelst, L., and C. D'Souza-Schorey. 1997. Rho GTPases and signaling networks. Genes Dev. 11:2295-2322.
73. Verheyen, E.M., and L. Cooley. 1994. Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development. 120: 717-728.
74. Vojtek, A.B., and C.J. Der. 1998. Increasing complexity of the Ras signaling pathway. J. Biol. Chem. 273:19925-19928.
75. Wes, P.D., M. Yu, and C. Montell. 1996. RIC, a calmodulin-binding Ras-like GTPase. EMBO (Em. Mol. Biol. Organ.) J. 15:5839-5848.
76. White, M.A., T. Vale, J.H. Camonis, E. Schaefer, and M.H. Wigler. 1996. A role for the Ral guanine nucleotide dissociation stimulator in mediating Ras-induced transformation. J. Biol. Chem. 271:16439-16442.
77. Wieschaus, E., and C. Nusslein-Volhard. 1986. Looking at embryos. In Drosophila, A Practical Approach. D.B. Roberts, editor. IRL Press. Oxford/Washington, D.C. 199-227.
78. Wolthuis, R.M., B. Bauer, L.J. van't Veer, A.M. de Vries-Smits, R.H. Cool, M. Spaargaren, A. Wittinghofer, B.M. Burgering, and J.L. Bos. 1996. RalGDS-like factor (Rlf) is a novel Ras and Rap 1A-associating protein. Oncogene. 13:353-362.
79. Wolthuis, R.M., N.D. de Ruiter, R.H. Cool, and J.L. Bos. 1997. Stimulation of gene induction and cell growth by the Ras effector Rlf. EMBO (Eur. Mol. Biol. Organ.) J. 22:6748-6761.
80. Wolthuis, R.M., F. Zwarlkruis, T.C. Moen, and J.L. Bos. 1998. Ras-dependent activation of the small GTPase Ral. Curr. Biol. 8:471-474.
81. Wong, L.L., and P.N. Adler. 1993. Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J. Cell Biol. 123:209-221.
82. Wulfkuhle, J.D., N.S. Petersen, and J.J. Otto. 1998. Changes in the F-actin cytoskeleton during neurosensory bristle development in Drosophila: the roles of singed and forked proteins. Cell Motil. Cytoskelel. 40:119-132.
83. Zuker, C.S., A.F. Cowman, and G.M. Rubin. 1985. Isolation and structure of a rhodopsin gene from D. melanogaster. Cell. 40:851-858.