Drosophila Rho-kinase (DRok) is required for tissue morphogenesis in diverse compartments of the egg chamber during oogenesis

Developmental Biology

Volumn 297, Issue 2, 2006, Pages 417-432

  Verdier, Valerie ^a   Johndrow, James E ^b   Betson, Martha ^d   Chen, Guang Chao ^a   Hughes, David A ^c   Parkhurst, Susan M ^b   Settleman, Jeffrey ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d NONE

Author keywords

Actin; Cytoskeleton; Drosophila; Moesin; Oogenesis; Rho kinase

Indexed keywords

ACTIN; MOESIN; RHO KINASE;

ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; DROSOPHILA; EMBRYO POLARITY; ENZYME ACTIVATION; FEMALE; MORPHOGENESIS; NONHUMAN; OOCYTE; OOCYTE CORTEX; OOCYTE DEVELOPMENT; ORTHOLOGY; PHOSPHORYLATION; PRIORITY JOURNAL;

EID: 33748441543     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.05.016     Document Type: Article

References (69)

1. Amano M., Ito M., Kimura K., Fukata Y., Chihara K., Nakano T., Matsuura Y., and Kaibuchi K. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271 (1996) 20246-20249
2. Amano M., Chihara K., Nakamura N., Fukata Y., Yano T., Shibata M., Ikebe M., and Kaibuchi K. Myosin II activation promotes neurite retraction during the action of Rho and Rho-kinase. Genes Cells 3 (1998) 177-188
3. Bretscher A. Regulation of cortical structure by the Ezrin-Radixin-Moesin protein family. Curr. Opin. Cell Biol. 11 (1999) 109-116
4. Burridge K., and Wennerberg K. Rho and Rac take center stage. Cell 116 (2004) 167-179
5. Cant K., Knowles B.A., Mooseker M.S., and Cooley L. Drosophila singed, a fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J. Cell Biol. 125 (1994) 369-380
6. Cha B.J., Koppetsch B.S., and Theurkauf W.E. In vivo analysis of Drosophila bicoid mRNA localization reveals a novel microtubule-dependent axis specification pathway. Cell 106 (2001) 35-46
7. Chou T.B., and Perrimon N. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144 (1996) 1673-1679
8. Edwards D.C., Sanders L.C., Bokoch G.M., and Gill G.N. Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics. Nat. Cell Biol. 1 (1999) 253-259
9. Fukata Y., Oshiro N., and Kaibuchi K. Activation of moesin and adducin by Rho-kinase downstream of Rho. Biophys. Chem. 82 (1999) 139-147
10. Fukata Y., Oshiro N., Kinoshita N., Kawano Y., Matsuoka Y., Bennett V., Matsuura Y., and Kaibuchi K. Phosphorylation of adducin by Rho-kinase plays a crucial role in cell motility. J. Cell Biol. 145 (1999) 347-361
11. Ghiglione C., Bach E.A., Paraiso Y., Carraway III K.L., Noselli S., and Perrimon N. Mechanism of activation of the Drosophila EGF Receptor by the TGFalpha ligand Gurken during oogenesis. Development 129 (2002) 175-186
12. Goode S., Melnick M., Chou T.B., and Perrimon N. The neurogenic genes egghead and brainiac define a novel signaling pathway essential for epithelial morphogenesis during Drosophila oogenesis. Development 122 (1996) 3863-3879
13. Gutzeit H.O. The role of microfilaments in cytoplasmic streaming in Drosophila follicles. J. Cell Sci. 80 (1986) 159-169
14. Hall A. Rho GTPases and the actin cytoskeleton. Science 279 (1998) 509-514
15. Hill C.S., Wynne J., and Treisman R. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81 (1995) 1159-1170
16. Hirose M., Ishizaki T., Watanabe N., Uehata M., Kranenburg O., Moolenaar W.H., Matsumura F., Maekawa M., Bito H., and Narumiya S. Molecular dissection of the Rho-associated protein kinase (p160ROCK)-regulated neurite remodeling in neuroblastoma N1E-115 cells. J. Cell Biol. 141 (1998) 1625-1636
17. Ivetic A., and Ridley A.J. Ezrin/radixin/moesin proteins and Rho GTPase signalling in leucocytes. Immunology 112 (2004) 165-176
18. Jankovics F., Sinka R., Lukacsovich T., and Erdelyi M. MOESIN crosslinks actin and cell membrane in Drosophila oocytes and is required for OSKAR anchoring. Curr. Biol. 12 (2002) 2060-2065
19. Jeon S., Kim S., Park J.B., Suh P.G., Kim Y.S., Bae C.D., and Park J. RhoA and Rho kinase-dependent phosphorylation of moesin at Thr-558 in hippocampal neuronal cells by glutamate. J. Biol. Chem. 277 (2002) 16576-16584
20. Jiang W., Sordella R., Chen G.C., Hakre S., Roy A.L., and Settleman J. An FF domain-dependent protein interaction mediates a signaling pathway for growth factor-induced gene expression. Mol. Cell 17 (2005) 23-35
21. Jordan P., and Karess R. Myosin light chain-activating phosphorylation sites are required for oogenesis in Drosophila. J. Cell Biol. 139 (1997) 1805-1819
22. Kawano Y., Fukata Y., Oshiro N., Amano M., Nakamura T., Ito M., Matsumura F., Inagaki M., and Kaibuchi K. Phosphorylation of myosin-binding subunit (MBS) of myosin phosphatase by Rho-kinase in vivo. J. Cell Biol. 147 (1999) 1023-1038
23. Kim G.H., and Han J.K. JNK and ROKalpha function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements. Dev. Dyn. 232 (2005) 958-968
24. Kim-Ha J., Smith J.L., and Macdonald P.M. oskar mRNA is localized to the posterior pole of the Drosophila oocyte. Cell 66 (1991) 23-35
25. 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. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273 (1996) 245-248
26. Lai S.L., Chang C.N., Wang P.J., and Lee S.J. Rho mediates cytokinesis and epiboly via ROCK in zebrafish. Mol. Reprod. Dev. 71 (2005) 186-196
27. Maekawa M., Ishizaki T., Boku S., Watanabe N., Fujita A., Iwamatsu A., Obinata T., Ohashi K., Mizuno K., and Narumiya S. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science 285 (1999) 895-898
28. Magie C.R., Meyer M.R., Gorsuch M.S., and Parkhurst S.M. Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 126 (1999) 5353-5364
29. Mahajan-Miklos S., and Cooley L. The villin-like protein encoded by the Drosophila quail gene is required for actin bundle assembly during oogenesis. Cell 78 (1994) 291-301
30. Mangeat P., Roy C., and Martin M. ERM proteins in cell adhesion and membrane dynamics. Trends Cell Biol. 9 (1999) 187-192
31. Manseau L., Calley J., and Phan H. Profilin is required for posterior patterning of the Drosophila oocyte. Development 122 (1996) 2109-2116
32. Matsui T., Maeda M., Doi Y., Yonemura S., Amano M., Kaibuchi K., and Tsukita S. Rho-kinase phosphorylates COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140 (1998) 647-657
33. Matsui T., Yonemura S., and Tsukita S. Activation of ERM proteins in vivo by Rho involves phosphatidyl-inositol 4-phosphate 5-kinase and not ROCK kinases. Curr. Biol. 9 (1999) 1259-1262
34. Mizuno T., Amano M., Kaibuchi K., and Nishida Y. Identification and characterization of Drosophila homolog of Rho-kinase. Gene 238 (1999) 437-444
35. Muris D.F., Verschoor T., Divecha N., and Michalides R.J. Constitutive active GTPases Rac and Cdc42 are associated with endoreplication in PAE cells. Eur. J. Cancer 38 (2002) 1775-1782
36. Neuman-Silberberg F.S., and Schupbach T. The Drosophila dorsoventral patterning gene gurken produces a dorsally localized RNA and encodes a TGF alpha-like protein. Cell 75 (1993) 165-174
37. Neuman-Silberberg F.S., and Schupbach T. Dorsoventral axis formation in Drosophila depends on the correct dosage of the gene gurken. Development 120 (1994) 2457-2463
38. Neuman-Silberberg F.S., and Schupbach T. The Drosophila TGF-alpha-like protein Gurken: expression and cellular localization during Drosophila oogenesis. Mech. Dev. 59 (1996) 105-113
39. Ng J., and Luo L. Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44 (2004) 779-793
40. Nilson L.A., and Schupbach T. EGF receptor signaling in Drosophila oogenesis. Curr. Top. Dev. Biol. 44 (1999) 203-243
41. Nobes C.D., and Hall A. Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 23 (1995) 456-459
42. Nobes C.D., and Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81 (1995) 53-62
43. Nobes C.D., and Hall A. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144 (1999) 1235-1244
44. Ohashi K., Nagata K., Maekawa M., Ishizaki T., Narumiya S., and Mizuno K. Rho-associated kinase ROCK activates LIM-kinase 1 by phosphorylation at threonine 508 within the activation loop. J. Biol. Chem. 275 (2000) 3577-3582
45. O'Neill J.W., and Bier E. Double-label in situ hybridization using biotin and digoxigenin-tagged RNA probes. BioTechniques 17 870 (1994) 874-875
46. Oshiro N., Fukata Y., and Kaibuchi K. Phosphorylation of moesin by rho-associated kinase (Rho-kinase) plays a crucial role in the formation of microvilli-like structures. J. Biol. Chem. 273 (1998) 34663-34666
47. Piekny A.J., and Mains P.E. Rho-binding kinase (LET-502) and myosin phosphatase (MEL-11) regulate cytokinesis in the early Caenorhabditis elegans embryo. J. Cell Sci. 115 (2002) 2271-2282
48. Piekny A.J., Wissmann A., and Mains P.E. Embryonic morphogenesis in Caenorhabditis elegans integrates the activity of LET-502 Rho-binding kinase, MEL-11 myosin phosphatase, DAF-2 insulin receptor and FEM-2 PP2c phosphatase. Genetics 156 (2000) 1671-1689
49. Pietromonaco S.F., Simons P.C., Altman A., and Elias L. Protein kinase C-theta phosphorylation of moesin in the actin-binding sequence. J. Biol. Chem. 273 (1998) 7594-7603
50. Polesello C., Delon I., Valenti P., Ferrer P., and Payre F. Dmoesin controls actin-based cell shape and polarity during Drosophila melanogaster oogenesis. Nat. Cell Biol. 4 (2002) 782-789
51. Qualmann B., and Mellor H. Regulation of endocytic traffic by Rho GTPases. Biochem. J. 371 (2003) 233-241
52. Raftopoulou M., and Hall A. Cell migration: Rho GTPases lead the way. Dev. Biol. 265 (2004) 23-32
53. Ridley A.J. Rho: theme and variations. Curr. Biol. 6 (1996) 1256-1264
54. Riento K., and Ridley A.J. Rocks: multifunctional kinases in cell behaviour. Nat. Rev., Mol. Cell Biol. 4 (2003) 446-456
55. Sahai E., Alberts A.S., and Treisman R. RhoA effector mutants reveal distinct effector pathways for cytoskeletal reorganization, SRF activation and transformation. EMBO J. 17 (1998) 1350-1361
56. Spradling A.C. Germline cysts: communes that work. Cell 72 (1993) 649-651
57. Symons M., and Rusk N. Control of vesicular trafficking by Rho GTPases. Curr. Biol. 13 (2003) R409-R418
58. Symons M., and Settleman J. Rho family GTPases: more than simple switches. Trends Cell Biol. 10 (2000) 415-419
59. Theurkauf W.E., and Hazelrigg T.I. In vivo analyses of cytoplasmic transport and cytoskeletal organization during Drosophila oogenesis: characterization of a multi-step anterior localization pathway. Development 125 (1998) 3655-3666
60. Theurkauf W.E., Smiley S., Wong M.L., and Alberts B.M. Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development 115 (1992) 923-936
61. Uehata M., Ishizaki T., Satoh H., Ono T., Kawahara T., Morishita T., Tamakawa H., Yamagami K., Inui J., Maekawa M., and Narumiya S. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389 (1997) 990-994
62. Van Aelst L., and D'Souza-Schorey C. Rho GTPases and signaling networks. Genes Dev. 11 (1997) 2295-2322
63. van Eeden F., and St Johnston D. The polarisation of the anterior-posterior and dorsal-ventral axes during Drosophila oogenesis. Curr. Opin. Genet. Dev. 9 (1999) 396-404
64. Verheyen E.M., and Cooley L. Profilin mutations disrupt multiple actin-dependent processes during Drosophila development. Development 120 (1994) 717-728
65. Wei L., Roberts W., Wang L., Yamada M., Zhang S., Zhao Z., Rivkees S.A., Schwartz R.J., and Imanaka-Yoshida K. Rho kinases play an obligatory role in vertebrate embryonic organogenesis. Development 128 (2001) 2953-2962
66. Winter C.G., Wang B., Ballew A., Royou A., Karess R., Axelrod J.D., and Luo L. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105 (2001) 81-91
67. Wissmann A., Ingles J., McGhee J.D., and Mains P.E. Caenorhabditis elegans LET-502 is related to Rho-binding kinases and human myotonic dystrophy kinase and interacts genetically with a homolog of the regulatory subunit of smooth muscle myosin phosphatase to affect cell shape. Genes Dev. 11 (1997) 409-422
68. Xue F., and Cooley L. kelch encodes a component of intercellular bridges in Drosophila egg chambers. Cell 72 (1993) 681-693
69. Yue L., and Spradling A.C. hu-li tai shao, a gene required for ring canal formation during Drosophila oogenesis, encodes a homolog of adducin. Genes Dev. 6 (1992) 2443-2454