Participation of small GTPases in dorsal closure of the Drosophila embryo: Distinct roles for Rho subfamily proteins in epithelial morphogenesis

Journal of Cell Science

Volumn 112, Issue 3, 1999, Pages 273-284

  Harden, Nicholas ^a,c   Ricos, Michael ^a   Ong, Yong Mei ^a   Chia, William ^a   Lim, Louis ^a,b  

^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; Drosophila; Morphogenesis; Rac; Ras; Rho; Small GTPase

Indexed keywords

ACTIN; GUANOSINE TRIPHOSPHATASE; MYOSIN ADENOSINE TRIPHOSPHATASE; PROTEIN SERINE THREONINE KINASE; RHO FACTOR; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; CELL SHAPE; CYTOSKELETON; DOWN REGULATION; DROSOPHILA; EMBRYO; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL;

HEXAPODA; MAMMALIA;

EID: 0033000016     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Allen, W. E., Jones, G. E., Pollard, J. W. and Ridley, A. J. (1997). Rho. Rac and Cdc42 regulate actin organization and cell adhesion in macrophages. J. Cell Sci. 110, 707-720.
2. Ashburner, M. (1989). Drosophila: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
3. Barrett, K., Leptin, M. and Settleman, J. (1997). The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 91, 905-915.
4. 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.
5. Brown, N. H. (1993). Integrins hold Drosophila together. BioEssays 15, 383-390.
6. Campos-Ortega, J. A. and Hartenstein, V. (1985). The Embryonic Development of Drosophila melanogaster. Berlin: Springer-Verlag.
7. Crawford, J. M., Harden, N., Leung, T., Lim, L. and Kiehart, D. P. (1998). Cellularization in Drosophila melanogaster is disrupted by the inhibition of Rho activity and the activation of Cdc42 function. Dev. Biol. 204, 151-164.
8. Dharmawardhane, S., Sanders, L. C., Martin, S. S., Daniels, R. H. and Bokoch, G. M. (1997). Localization of p21-activated kinase 1 (PAKI) to pinocytic vesicles and cortical actin structures in stimulated cells. J. Cell Biol. 138, 1265-1278.
9. Dickson, B. and Hafen, E. (1994). Genetics of signal transduction in invertebrates. Curr. Opin. Genet. Dev. 4, 64-70.
10. Eaton, S., Auvinen, P., Luo, L., Jan, Y. N. and Simons, K. (1995). CDC42 and Rac1 control different actin-dependent processes in the Drosophila wing disc epithelium. J. Cell Biol. 131, 151-164.
11. Eaton, S., Wepf, R. and Simons, K. (1996). Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J. Cell Biol. 135, 1277-1289.
12. Glise, B., Bourbon, H. and Noselli, S. (1995). hemipterous encodes a novel Drosophila MAP kinase kinase, required for epithelial cell sheet movement. Cell 83, 451-461.
13. Glise, B. and Noselli, S. (1997). Coupling of Jun amino-terminal kinase and Decapentaplegic signaling pathways in Drosophila morphogenesis. Genes Dev. 11, 1738-1747.
14. 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.
15. Harden, N., Lee, J., Loh, H.-Y., Ong, Y.-M., Tan, I., Leung, T., Manser, E. and Lim, L. (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.
16. Hariharan, I. K., Hu, K.-Q., Asha, H., Quintanilla, A., Ezzell, R. M. and Settleman, J. (1995). Characterization of rho GTPase family homologues in Drosophila melanogaster: overexpressing Rhol in retinal cells causes a late developmental defect. EMBO J. 14, 292-302.
17. Hinz, U., Giebel, B. and Campos-Ortega, J. A. (1994). The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76, 77-87.
18. 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 trunsduction pathway in regulating epithelial cell sheet movement. Genes Dev. 11, 1728-1737.
19. Kaufmann, N., Wills, Z. P. and Van Vactor, D. (1998). Drosophila Rac1 controls motor axon guidance. Development 125, 453-461.
20. Kiehart, D. P. and Feghali, R. (1986). Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol. 103, 1517-1525.
21. Knust, E. (1997). Drosophila morphogenesis: movements behind the edge. Curr. Biol. 7, R558-R561.
22. Kockel, L., Zeitlinger, J., Staszewski, L. M., 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.
23. 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.
24. Kozma, R., Sarner, S., Ahmed, S. and Lim, L. (1997). Rho family GTPases and neuronal growth cone remodelling: relationship between increased complexity induced by Cdc42Hs, Rac 1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17, 1201-1211.
25. Lee, T., Feig, L. and Montell, D. J. (1996). Two distinct roles for Ras in a developmentally regulated cell migration. Development 122, 409-418.
26. Leung, T., Manser, E., Tan, L. and Lim, L. (1995). A novel serine/threonine kinase binding the Ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J. Biol. Chem. 270, 29051-29054.
27. Leung, T., Chen, X.-Q., Manser, E. and Lim, L. (1996). The p160 RhoA-binding kinase ROKα is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16, 5313-5327.
28. 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 signalling pathways. Eur. J. Biochem. 242, 171-185.
29. ras/Ras1, an essential component of torso signaling in Drosophila. Genes Dev. 7, 621-632.
30. 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.
31. Luo, L., Hensch, T. K., Ackerman, L., Barbel, S., Jan, L. Y. and Jan, Y. N. (1996). Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines. Nature 379, 837-840.
32. 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.
33. Martin-Blanco, E. (1997). Regulation of cell differentiation by the Drosophila Jun kinase cascade. Curr. Opin. Genet. Dev. 7, 666-671.
34. Murphy, A. M. and Montell, D. J. (1996). Cell type-specific roles for Cdc42, Rac. and RhoL in Drosophila oogenesis. J. Cell Biol. 133, 617-630.
35. Nakano, Y., Guerrero, I., Hidalgo, A., Taylor, A., Whittle, J. R. S. and Ingham, P. W. (1989). A protein with several possible membrane-spanning domains encoded by the Drosophila segment polarity gene patched. Nature 341, 508-513.
36. Narumiya, S., Ishizaki, T. and Watanabe, N. (1997). Rho effectors and reorganization of actin cytoskeleton. FEBS Lett. 410, 68-72.
37. Nobes, C. D. and Hall, A. (1995). Rho. Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
38. Noselli, S. (1998). JNK signaling and morphogenesis in Drosophila. Trends Genet. 14, 33-38.
39. O'Connor, M. and Chia, W. (1993). P element-mediated germ-line transformation of Drosophila. In Methods in Molecular Biology, vol. 18: Transgenesis Techniques: Principles and Protocols (ed. D. Murphy and D. A. Carter), pp. 75-85. Totowa, NJ: Humana Press Inc.
40. Qiu, R.-G., Abo, A., McCormick, F. and Symons, M. (1997). Cdc42 regulates anchorage-independent growth and is necessary for Ras transformation. Mol. Cell. Biol. 17, 3449-3458.
41. 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.
42. Riesgo-Escovar, J. R. and Hafen, E. (1997). 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.
43. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor. NY: Cold Spring Harbor Laboratory Press.
44. Sluss, H. K., Han, Z., Barrett, T., Davis, R. J. and Ip, Y. T. (1996) A JNK signal transduction pathway that mediates morphogenesis and an immune response in Drosophila. Genes Dev. 10, 2745-2758.
45. Strutt, D. I., Weber, U. and Mlodzik, M. (1997). The role of RhoA in tissue polarity and Frizzled signalling. Nature 387, 292-295.
46. Symons, M. (1996). Rho family GTPases: the cytoskeleton and beyond. Trends Biochem. Sci. 21, 178-181.
47. Tang, Y., Chen, Z., Ambrose, D., Liu, J., Gibbs, J. R., Chernoff, J. and Field, J. (1997). Kinase-deticient Pakl mutants inhibit Ras transformation of Rat-1 fibroblasts. Mol. Cell. Biol. 17, 4454-4464.
48. Tang, Y., Marwaha, S., Rutkowski, J. L., Tennekoon, G. I., Phillips, P. C. and Field, J. (1998). A role for Pak protein kinases in Schwann cell transformation. Proc. Nat. Acad. Sci. USA 95, 5139-5144.
49. Van Aelst, L. and D'Souza-Schorey, C. (1997). Rho GTPases and signaling networks. Genes Dev. 11, 2295-2322.
50. Wodarz, A., Hinz, U., Engelbert, M. and Knust, E. (1995). Expression of Crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82, 67-76.
51. 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.