Cellularization in Drosophila melanogaster is disrupted by the inhibition of Rho activity and the activation of Cdc42 function

Developmental Biology

Volumn 204, Issue 1, 1998, Pages 151-164

  Crawford, Janice M ^a   Harden, Nicholas ^b   Leung, Thomas ^b   Lim, Louis ^b,c   Kiehart, Daniel P ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; DNA; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE TRIPHOSPHATE; RHO FACTOR;

ANIMAL CELL; ARTICLE; CYTOSKELETON; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; ENZYME INHIBITION; MICROTUBULE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL;

ANIMALIA; CLOSTRIDIUM BOTULINUM; DROSOPHILA MELANOGASTER; MELANOGASTER;

EID: 0032373709     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1998.9061     Document Type: Article

References (78)

1. Adams, A. E., Cooper, J. A., and Drubin, D. G. (1993). Unexpected combinations of null mutations in genes encoding the actin cytoskeleton are lethal in yeast. Mol. Biol. Cell 4, 459-468.
2. Aktories, K., Braun, U., Rösener, S., Just, I., and Hall, A. (1989). The Rho gene product expressed in E. coli is a substrate of botulinum ADP-ribosyltransferase C3. Biochem. Biophys. Res. Commun. 158, 209-213.
3. Amano, M., Ito, K., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271, 20246-20249.
4. Bagrodia, S., Derijard, B., Davis, R., and Cerione, R. (1995). Cdc42 and PAK-mediated signaling leads to Jun kinase and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 270, 27995-27998.
5. Braun, U., Habermann, B., Just, I., Aktories, K., and Vanderkerckhove, J. (1989). Purification of the 22 kDa protein substrate of botulinum ADP-ribosyltransferase C3 from porcine brain cytosol and its characterization as a GTP-binding protein highly homologous to the Rho gene product. FEBS Lett. 243, 70-76.
6. Chrzanowska-Wodnicka, M., and Burridge, K. (1996). Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133, 1403-1415.
7. Coso, O., Chiariello, M., Yu, J., Teramoto, H., Crespo, P., Xu, N., Miki, T., and Gutkind, J. (1995). The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146.
8. DeLozanne, A., and Spudich, J. (1987). Disruption of the Dictyostelium discoideum myosin heavy chain gene by homologous recombination. Science 263, 1086-1091.
9. Drechsel, D., Hyman, A., Hall, A., and Glotzer, M. (1997). A requirement for Rho and Cdc42 during cytokinesis in Xenopus embryos. Curr. Biol. 7, 12-23.
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. Edwards, K. A., and Kiehart, D. P. (1996). Drosophila nonmuscle myosin II has multiple essential roles in imaginal disc and egg chamber morphogenesis. Development 122, 1499-1511.
13. H prevent its activation by GTP. Mol. Cell. Biol. 11, 4822-4829.
14. Fehon, R. G., Oren, T., Lajeunesse, D. R., Melby, T. E., and McCartney, B. M. (1997). Isolation of mutation 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.
15. Feig, L. A., and Cooper, G. M. (1988). Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol. Cell. Biol. 8, 3235-3243.
16. Foe, V. E., and Alberts, B. M. (1983). Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J. Cell Sci. 61, 31-70.
17. Foe, V. E., Odell, G. M., and Edgar, B. A. (1993). Mitosis and morphogenesis in the Drosophila embryo: Point and counterpoint. In "The Development of Drosophila melanogaster" (M. Bate and A. Martinez Arias, Eds.). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
18. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
19. 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.
20. 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 m elanogaster: Overexpressing Rho 1 in retinal cells causes a late developmental defect. EMBO J. 14, 292-302.
21. Kamisoyama, H., Araki, Y., and Ikebe, M. (1994). Mutagenesis of the phosphorylation site (serine 19) of smooth muscle myosin regulatory light chain and its effects on the properties of myosin. Biochemistry 33, 840-847.
22. Karess, R. E., Chang, X., Edwards, K., Kulkarni, S., Aguilera, I., and Kiehart, D. P. (1991). The regulatory light chain of nonmuscle myosin is encoded by spaghetti-squash, a gene required for cytokinesis in Drosophila. Cell 65, 1177-1189.
23. Kaufmann, N., Wills, Z. P., and Van Vactor, D. (1998). Rac1 controls motor axon guidance. Development 125, 453-461.
24. Kiehart, D. P. (1981). Studies on the in vivo sensitivity of spindle microtubules to calcium ions and evidence for a vesicular calcium-sequestering system. J. Cell Biol. 88, 604-617.
25. Kiehart, D. P. (1982). Microinjection of echinoderm eggs: Apparatus and procedures. Methods Cell Biol. 25, 13-31.
26. Kiehart, D. P., and Feghali, R. (1986). Cytoplasmic myosin from Drosophila melanogaster. J. Cell Biol. 103, 1517-1525.
27. Kiehart, D. P., Ketchum, A., Young, P., Lutz, D., Alfenito, M. R., Chang, X. J., Awobuluyi, M., Pesacreta, T. C., Inoue, S., and Stewart, C. T. (1990). Contractile proteins in Drosophila development. Ann. N.Y. Acad. Sci. 582, 233-251.
28. Kiehart, D. P., Montague, R. A., Rickoll, W. L., Foard, D., and Thomas, G. H. (1994). High-resolution microscopic methods for the analysis of cellular movements in Drosophila embryos. In "Methods in Cell Biology" (L. S. B. Goldstein and E. A. Fyrberg, Eds.), Vol. 44, pp. 507-532. Academic Press, San Diego.
29. Kimura, K., Ito, M., Amano, M., Chihara, K., Fukata, Y., Nakafuku, M., Yamamori, B., Feng, J., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996). Regulation of myosin phosphatase by the Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
30. 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.
31. Kozma, R., Sarner, S., Ahmed, S., and Lim, L. (1997). Rho family GTPases and neuronal growth cone remodelling: Relationships between increased complexity induced by Cdc42Hs, Rac1, and acetylcholine and collapse induced by RhoA and lysophosphatidic acid. Mol. Cell. Biol. 17, 1201-1211.
32. Kreisberg, J. I., Ghosh-Choudhury, N., Radnik, R. A., and Schwartz, M. A. (1997). Role of Rho and myosin phosphorylation in actin stress fiber assembly in mesangial cells. Am. J. Physiol. 273, F283-F288.
33. Larochelle, D. A., Vithalani, K., and De Lozanne, A. (1996). A novel member of the Rho subfamily of small GTP-binding proteins is specifically required for cytokinesis. J. Cell Biol. 133, 1321-1329.
34. Lee, G. M. (1989). Measurement of volume injected into individual cells by quantitative fluorescence microscopy. J. Cell Sci. 94, 443-447.
35. 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.
36. Leung, T., Chen, X. Q., Manser, E., and Lim, L. (1996). The p160 RhoA-binding kinase ROK alpha is a member of a kinase family and is involved in the reorganization of the cytoskeleton. Mol. Cell. Biol. 16, 5313-5327.
37. Leung, T., Chen, X.-Q., Tan, I., Manser, E., and Lim, L. (1998). Myotonic dystrophy kinase-related Cdc42-binding kinase acts as a Cdc42 effector in promoting cytoskeletal reorganization. Mol. Cell. Biol. 18, 130-140.
38. 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.
39. ras/Ras1, an essential component of torso signaling in Drosophila. Genes Dev. 7, 621-632.
40. Lundell, M., and Hirsh, J. (1994). A new visible light DNA fluorochrome for confocal microscopy. Biotechniques 16, 434-440.
41. 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.
42. Luo, L., Lee, T., Tsai, L., Tang, G., Jan, L. Y., and Jan, Y. N. (1997). Genghis Khan (Gek) as a putative effector for Drosophila Cdc42 and regulator of actin polymerization. Proc. Natl. Acad. Sci. USA 94, 12963-12968.
43. Mabuchi, I., and Okuno, M. (1977). The effect of myosin antibody on the division of starfish blastomeres. J. Cell Biol. 74, 251-263.
44. Mabuchi, I., Hamaguchi, Y., Fujimoto, H., Morii, N., Mishima, M., and Naurumiya, S. (1993). A Rho-like protein is involved in the organization of the contractile ring in dividing sand dollar eggs. Zygote 1, 325-331.
45. Machesky, L. M., and Hall, A. (1997). Role of actin polymerization and adhesion to extracellular matrix in Rac- and Rho-induced cytoskeletal reorganization. J. Cell Biol. 138, 913-926.
46. Manser, E., Leung, T., Salihuddin, H., Zhao, Z., and Lim, L. (1994). A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367, 40-46.
47. Manser, E., Leung, T., and Lim, L. (1995). Purification and assay of kinases that interact with Rac/Cdc42. Methods Enzymol. 356, 215-227.
48. Manser, E., Huang, H., Loo, T., Chen, X., Dong, J., 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.
49. Matsui, T., Amano, M., Yamamoto, T., Chihara, K., Nakafuku, M., Ito, M., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996). Rho-associated kinase, a novel serine/threonine kinase, as a putative target for the small GTP-binding protein Rho. EMBO J. 15, 2208-2216.
50. Menard, L., Tomhave, E., Casey, P. J., Uhing, R. J., Snyderman, R., and Didsbury, J. R. (1992). Rac1, a low-molecular-mass GTP-binding-protein with high intrinsic GTPase activity and distinct biochemical properties. Eur. J. Biochem. 206, 537-546.
51. Miller, K. G., and Kiehart, D. P (1995) Fly division. J. Cell Biol. 131, 1-5.
52. Minden, A., Lin, L., Claret, F., Abo, A., and Karin, M. (1995). Selective activation of the JNK signalling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81, 1147-1157.
53. 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.
54. Narumiya, S., Sekine, A., and Fujiwara, M. (1988). Substrate for botulinum ADP-ribosyltransferase, Gb, has an amino acid sequence homologous to a putative Rho gene product. J. Biol. Chem. 263, 17255-17257.
55. Nemoto, Y., Namba, T., Kozaki, S., and Narumiya, S. (1991). Clostridium botulinum C3 ADP-ribosyltransferase gene. J. Biol. Chem. 266, 19312-19319.
56. 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.
57. Olson, M., 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.
58. Perrimon, N., Lanjuin, A., Arnold, C., and Noll, E. (1996). Zygotic lethal mutations with maternal effect phenotypes in Drosophila melanogaster. II. Loci on the second and third chromosomes identified by P-element-induced mutations. Genetics 144, 1681-1692.
59. Ridley, A. J., and Hall, A. (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.
60. 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.
61. 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.
62. Sasamura, T., Kobayashi, T., Kojima, S., Qadota, H., Ohya, Y., Masai, I., and Hotta, Y. (1997). Molecular cloning and characterization of Drosophila genes encoding small GTPases of the rab and rho families. Mol. Gen. Genet. 254, 486-494.
63. Schejter, E. D., and Wieschaus, E. (1993). Functional elements of the cytoskeleton in the early Drosophila embryo. Annu. Rev. Cell Biol. 9, 67-99.
64. Sekine, A., Fujiwara, M., and Narumiya, S. (1989). Asparagine residue in the Rho gene product is the modification site for botulinum ADP-ribosyltransferase. J. Biol. Chem. 264, 8602-8605.
65. Sells, M., Knaus, U., Bagrodia, S., Ambrose, D., Bokoch, G., and Chernoff, J. (1997). Human p21-activated kinase (PakI) regulates actin organization in mammalian cells. Curr. Biol. 7, 202-210.
66. Smith, D. E., Gruenbaum, Y., Berrios, M., and Fisher, P. A. (1987). Biosynthesis and interconversion of Drosophila nuclear lamin isoforms during normal growth and in response to heat shock. J. Cell Biol. 105, 771-790.
67. Strutt, D. I., Weber, U., and Mlodzik, M. (1997). The role of RhoA in tissue polarity and Frizzled signalling. Nature 387, 292-295.
68. Sullivan, W., and Theurkauf, W. E. (1995). The cytoskeleton and morphogenesis of the early Drosophila embryo. Curr. Opin. Cell Biol. 7, 18-22.
69. Tan, J., Ravid, S., and Spudich, J. (1992). Control of nonmuscle myosins by phosphorylation. Annu. Rev. Biochem. 61, 721-759.
70. Thomas, G. H., and Kiehart, D. P. (1994). Beta heavy-spectrin has a restricted tissue and subcellular distribution during Drosophila embryogenesis. Development 120, 2039-2050.
71. Tong, L. A., de Vos, A. M., Milburn, M. V., Jancarik, J., Noguchi, S., Nishimura, S., Miura, K., Ohtsuka, E., and Kim, S. H. (1989). Structural differences between a ras oncogene protein and the normal protein. Nature 337, 90-93.
72. Tuazon, P., Stull, J., and Traugh, J. (1982). Phosphorylation of myosin light chain by a protease-activated kinase from rabbit skeletal muscle. Biochem. Biophys. Res. Commun. 108, 910-917.
73. Tuazon, P., and Traugh, J. (1984). Activation of actin-activated ATPase in smooth muscle by phosphorylation of myosin light chain with protease-activated kinase I. J. Biol. Chem. 259, 541-546.
74. Van Aelst, L., and D'Susza-Schorey, C. (1997). Rho GTPases and signalling networks. Genes Dev. 11, 2295-2322.
75. Wheatley, S., Kulkarni, S., and Karess, R. (1995). Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos. Development 121, 1937-1945.
76. Wieschaus, E., and Nüsslein-Volhard, C. (1986). Looking at embryos. In "Drosophila, a Practical Approach" (D. B. Roberts, Ed.). IRL Press, Washington, DC.
77. Young, P., Pesacreta, T., and Kiehart, D. (1991). Dynamic changes in the distribution of cytoplasmic myosin during Drosophila embryogenesis. Development 111, 1-14.
78. Zhao, Z., Leung, T., Manser, E., and Lim, L. (1995). Pheromone signalling in Saccharomyces cerevisiae requires the small GTP-binding protein Cdc42p and its activator CDC24. Mol. Cell. Biol. 15, 5246-5257.