Dcdc42 acts in TGF-β signaling during drosophila morphogenesis: Distinct roles for the Drac1/JNK and Dcdc42/TGF-β cascades in cytoskeletal regulation

Journal of Cell Science

Volumn 112, Issue 8, 1999, Pages 1225-1235

  Ricos, Michael G ^a   Harden, Nicholas ^a,c   Sem, Kai Ping ^a   Lim, Louis ^a,b   Chia, William ^a  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Cdc42; Cytoskeleton; Dorsal closure; DPAK; Drosophila; JNK; Morphogenesis; Rac; Small GTP binding protein; TGF

Indexed keywords

GUANOSINE TRIPHOSPHATASE; PROTEIN KINASE; RAS PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; CYTOSKELETON; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EPIDERMIS; GENE MUTATION; LIGAND BINDING; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; REGULATOR GENE; SIGNAL TRANSDUCTION; SPINAL CORD;

ANIMALIA; HEXAPODA;

EID: 0032891511     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. Affolter, M., Nellen, D., Nussbaumer, U. and Basler, K. (1994). Multiple requirements for the receptor serine/threonine kinase thick veins reveal novel functions of TGFβ homologues during Drosophila embryogenesis. Development 120, 3105-3117.
2. Allen, W. E., Jones G. E., Pollard, J. W. and Ridley, A. J. (1997). Rho, Rac and Cdc42 regulate actin reorganisation and cell adhesion in macrophages. J. Cell Sci. 110, 707-720.
3. Arora, K., Dai, H., Kazuko, S. G., Jamal, J., O'Connor, M., Letsou, A. and Warrior, R. (1995). The Drosophila schnurri gene acts in the Dpp/TGFβ signaling pathway and encodes a transcription factor homologous to the human MBP family. Cell 81, 781-790.
4. Atfi, A., Buisine, M., Mazars, A. and Gespach, C. (1997a). Induction of apoptosis by DPC4, a transcriptional factor regulated by transforming growth factor-β through stress-activated protein kinase/c-Jun N-terminal kinase (SAPK/JNK) signaling pathway. J. Biol. Chem. 272, 24731-24734.
5. Atfi, A., Djellou, S., Chastre, E., Davis, R. and Gespach, C. (1997b). Evidence for a role of Rho-like GTPases and stress-activated protein kinase/c-Jun N-terminal kinase (SAPK/JNK) in transforming growth factor-β mediated signaling. J. Biol. Chem. 272, 1429-1432.
6. Brand, A. H. and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
7. Brown, J. L., Stowers, L., Baer, M., Trejo, J., Coughlin, S. and Chant, J. (1996). Human Ste20 homologue hPAK1 links GTPases to the JNK MAP kinase signaling pathway. Curr. Biol. 6, 598-605.
8. Brummel, T. J., Twombly, V., Marqués, G., Wrana, J. L., Newfeld, S. J., Attisano, L., Massagué, J., O'Connor, M. B. and Gelbart, W. M. (1994). Characterization and relationship of Dpp receptors encoded by the saxophone and thick veins genes in Drosophila. Cell 78, 251-261.
9. Campos-Ortega, J. A. and Hartenstein, V. (1985). The Embryonic Development of Drosophila melanogaster. Berlin: Springer-Verlag.
10. Childs, S. R., Wrana, J. L., Arora, K., Attisano, L., O'Connor, M. and Massague J. (1993). Identification of a Drosophila activin receptor. Proc. Nat. Acad. Sci. USA 90, 9475-9479.
11. Coso, O. A., Chiariello, M., Yu, J.-C., Teramoto, H., Crespo, P., Xu, N., Miki, T. and Gutkind, J. S. (1995). The small GTP-binding proteins Rac 1 and cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146.
12. Derynck, R. and Zhang, Y. (1996). Intracellular signaling: The Mad way to do it. Curr. Biol. 6, 1226-1229.
13. Glise, B., Bourbon, H. and Noselli, S. (1995). hemipterous encodes a novel Drosophila MAP kinase, required for epithelial cell sheet movement. Cell 83, 451-461
14. Glise, B. and Noselli, S. (1997). Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev. 11, 1738-1747.
15. Grieder, N. C., Nellen, D., Burke, R., Basler, K. and Affolter, M. (1995). schnurri is required for Drosophila Dpp signaling and encodes a zinc finger protein similar to the mammalian transcription factor PRDII-BF1. Cell 81, 791-800.
16. Harden, N., Loh, H. Y., Chia, W. and Lim, L. (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.
17. Harden, N., Lee, J., Loh, H.-Y., Ong, Y.-M., Tan, I., Leung, T., Manser, E. and Lim, L. (1996). A Drosophila homologue 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.
18. Harden, N., Ricos, M. G., Ong, Y.-M., Chia, W. and Lim, L. (1999). Participation of small GTPases in dorsal closure: distinct roles for Rho subfamily proteins in epithelial morphogenesis. J. Cell Sci. 112, 273-284.
19. Heitzler, P., Haenlin, M., Ramain, P. and Simpson, P. (1996). A genetic analysis of pannier, a gene necessary for viability of dorsal tissues in Drosophila. Genetics 143, 1271-1286.
20. Hoodless, P. A., Haerry, T., Abdollah, S., Stapelton, M., O'Connor, M. B., Attisano, L. and Wrana, J. L. (1996). MADRI, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500.
21. Hou, X. S., Goldstein, E. S. and Perrimon, N. (1997). Drosophila Jun relays the Jun amino-terminal kinase signal transduction pathway to the Decapentaplegic signal transduction pathway in regulating epithelial cell sheet movement. Genes Dev. 11, 1728-1737.
22. Hudson, J. B., Podos, S. D., Keith, K., Simpson, S. L. and Ferguson, E. L. (1998). The Drosophila Medea gene is required downstream of dpp and encodes a functional homologue of human Smad4. Development 125, 1407-1420.
23. Joneson, T., McDonough, M., Bar-Sagi, D. and Van Aelst, L. (1996). RAC regulation of actin polymerization and proliferation by a pathway distinct from Jun kinase. Science 274, 1374-1376.
24. Jurgens, C., Weischaus, E., Nusslein-Volhard, C. and Kluding, M. (1984). Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. II. Zygotic loci on the third chromosome. Wilhelm Roux's Arch. 193, 283-295.
25. Kiehart, D. P. and Feghali, R. (1986). Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol. 103, 1517-1525.
26. Kingsley, D. M. (1994). The TGF-β superfamily: New members, new receptors, and new genetic tests o function in different organisms. Genes Dev. 8, 133-146.
27. Knust, E. (1997). Drosophila morphogenesis: movements behind the edge. Curr. Biol. 7, R558-R561.
28. Kockel, L., Zeitlinger J., Staszewski L., Mlodzik, M. and Bohmann, D. (1997). Jun in Drosophila development: redundant and nonredundant functions and regulation by two MAPK signal transduction pathways. Genes Dev. 11, 1748-1758.
29. Kozma, R., Ahmed, S., Best, A. and Lim, L. (1995). The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 15, 1942-1952.
30. Kozma, R., Sarner, S., Ahmed, S. and Lim, L. (1997). Rho family GTPases and neuronal growth cone remodeling: relationship between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell Biol. 17, 1201-1211.
31. Lamarche, N., Tapon, N., Stowers, L., Burbelo, P. D., Aspenstrom, P., Bridges, T., Chant, J. and Hall, A. (1996). Rac and Cdc42 induce actin polymerisation and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell 87, 519-529.
32. Letsou, A., Arora, K., Wrana, J. L., Simin, K., Twombly, V., Jamal, J., Staehling-Hampton, K., Hoffmann, F. M., Gelbart, W. M., Massagué, J. and O'Connor, M. B. (1995). Drosophila Dpp signaling is mediated by the punt gene product: a dual ligand-binding type II receptor of the TGF beta receptor family. Cell 80, 899-908.
33. Lim, L., Manser, E., Leung, T. and Hall, C. (1996). Regulation of phosphorylation pathways by p21 GTPases: The p21 Ras-related Rho subfamily and its role in phosphorylation signaling pathways. Eur. J. Biochem. 242, 171-185.
34. Luo, L., Liao, Y. J., Jan, L. Y. and Jan, Y. N. (1994). Distinct morphogenetic functions of similar small GTPases: Drosophila Drac1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787-1802.
35. Manser, E., Leung, T. Salihuddin, H., Zhao, Z.-S. and Lim, L. (1994) A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367, 40-46.
36. Manser, E., Huang, H.-Y., Loo, T.-H., Chen, X.-Q., Dong, J.-M., Leung, T. and Lim, L. (1997). Expression of constitutively active α-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17, 1129-1143.
37. Martin-Blanco, E. (1997). Regulation of cell differentiation by the Drosophila Jun kinase cascade. Curr. Opin. Genet. Dev. 7, 666-671.
38. Martin-Blanco, E., Gampel, A, Ring, J., Virdee, K., Tolkovsky, A. M. and Martinez-Arias, A. (1998). puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 12, 557-570.
39. Massague, J. (1996). TGF-beta signaling: receptors, transducers and Mad proteins. Cell 78, 947-950.
40. Massague, J., Hata, A. and Liu, F. (1997). TGF-β signaling through the Smad pathway. Trends Cell Biol. 7, 187-192.
41. Minden, A., Lin, A., Claret, F.-X., Abo, A. and Karin, M. (1995). Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81, 1147-1157.
42. Moriguchi, T., Kuroyanagi, N., Yamaguchi, K., Goto, Y., Irie, K., Kano, T., Shirakabe, K., Muro, Y., Shibuya, H., Matsumoto, K., Nishida, E. and Hagiwara, M. (1996). A novel kinase cascade mediated by mitogen-activated protein kinase kinase 6 and MKK3 J. Biol. Chem. 271, 13675-13679.
43. Mucsi, I., Skorecki, K. L. and Goldberg, H. J. (1996). Extracellular signal-regulated kinase and the small GTP-binding protein. Rac, contribute to the effects of transforming growth factor-β1 on gene expression. J. Biol. Chem. 271, 16567-16572.
44. Nellen, D., Affolter, M. and Basler, K. (1994). Receptor serine/threonine kinases implicated in the control of Drosophila body pattern by decapentaplegic. Cell 78, 225-237.
45. Nobes, C. D. and Hall, A. (1995). Rho, Rac and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibres, lamellipodia and filopodia. Cell 81, 53-62.
46. Noselli, S. (1998). JNK signaling and morphogenesis in Drosophila. Trends Genet. 14, 33-38.
47. Nusslein-Volhard, C., Weischaus, E. and Kluding, M. (1984) Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. I. Zygotic loci on the second chromosome. Wilhelm Roux's Arch. 193, 267-282.
48. Olson, M. F., Ashworth, A. and Hall, A. (1995). An essential role for Rho, Rac and Cdc42 GTPases in cell cycle progression through G1. Science 269, 1270-1272.
49. Penton, A., Chen, Y., Staehling-Hampton, K., Wrana, J. L., Attisano, L., Szidonya, J., Cassill, J. A., Massagué, J. and Hoffmann, F. M. (1994). Identification of two bone morphogenetic protein type I receptors in Drosophila and evidence that Brk25D is a decapentaplegic receptor. Cell 78, 239-250.
50. Ramain, P., Heitzler, P., Haenlin, M. and Simpson, P. (1993). pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc finger protein with homology to the vertebrate transcription factor GATA-1. Development 119, 1277-1291.
51. Ridley, A. J. and Hall, A. (1992). The small GTP binding protein Rho regulates the assembly of focal adhesions and actin stress fibres in response to growth factors. Cell 70, 389-399.
52. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. and Hall, A. (1992). The small GTP-binding protein Rac regulates growth factor induced membrane ruffling. Cell 70, 401-410.
53. Riesgo-Escovar, J. R., Jenni, M., Fritz, A. and Hafen, E. (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.
54. Riesgo-Escovar, J. R. and Hafen, E. (1997a). Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure. Genes Dev. 11, 1717-1727.
55. Riesgo-Escovar, J. R. and Hafen, E. (1997b). Common and distinct roles of DFos and Djun during Drosophila development. Science 278, 669-672.
56. Ruberte, E., Marty, T., Nellen, D., Affolter, M. and Basler, K. (1995). An absolute requirement for both the type II and type I receptors, punt and thick veins, for Dpp signaling in vivo. Cell 80, 889-897.
57. Sluss, H. K., Han, Z., Barrett, T., Davis, J. R. and Ip, Y. T. (1996). A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev. 10, 2745-2758.
58. Sluss, H. K. and Davis, R. J. (1997). Embryonic morphogenesis signaling pathway mediated by JNK targets the transcription factor Jun and the TGF-β homologue decapentaplegic. J. Cell Biochem. 67, 1-12
59. Staehling-Hampton, K., Laughon, A. S. and Hoffmann, F. M. (1995). A Drosophila protein related to the human zinc finger transcription factor PRDII/MBPI/HIV-EP1 is required for dpp signaling. Development 121, 3393-3403.
60. Van Aelst, L. and D'Souza-Schorey, C. (1997). Rho GTPases and signaling networks. Genes Dev. 11, 2295-2322.
61. Wall, N. A. and Hogan, B. L. (1994). TGF-beta related genes in development. Curr. Opin. Genet. Dev. 4, 517-522.
62. Wang, W., Zhou, G., Hu, M. C-T., Yao, Z. and Tan, T-H. (1997). Activation of the Hematopoetic Progenitor Kinase-1 (HPK-1)-dependent, stress-activated c-Jun N-terminal kinase (JNK) pathway by transforming growth factor β (TGF-β)-activated kinase (TAK1), a kinase mediator of TGF β signal transduction. J. Biol. Chem. 272, 22771-22775.
63. Wilkinson, M. G. and Millar, J. B. A. (1998). SAPKs and transcription factors do the nucleocytoplasmic tango. Genes Dev. 12, 1391-1397.
64. Wrana, J. L. and Attisano, L. (1996). MAD-related proteins in TGF-β signaling. Trends Genet. 12, 493-496.
65. Yamaguchi, K., Shirakabe, K., Shibuya, H., Irie, K., Oishi, I., Ueno, N., Taniguchi, T., Nishida, E. and Matsumoto, K. (1995). Identification of a member of the MAPKKK family as a potential mediator of TGF-β signal transduction. Science 270, 2008-2011.
66. Young, P. E., Richman, A. M., Ketchum, A. S. and Kiehart, D. P. (1993). Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 7, 29-41.
67. Zeitlinger, J., Kockel, L., Peverali, F. A., Jackson, D. B., Mlodzik, M. and Bohmann, D. (1997). Defective dorsal closure and loss of epidermal decapentaplegic expression in Drosophila fos mutants. EMBO J. 16, 7393-7401.
68. Zhang, S., Han, J., Sells, M. A., Chernoff, J., Knaus, U. G., Ulevitch, R. J. and Bokoch, G. M. (1995). Rho family GTPases regulate p38 mitogen-activated protein kinase through the downstream mediator Pak1. J. Biol. Chem. 270, 23934-23936.