RhoA is required for cortical retraction and rigidity during mitotic cell rounding

Journal of Cell Biology

Volumn 160, Issue 2, 2003, Pages 255-265

  Maddox, Amy Shaub ^a   Burridge, Keith ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

Actin; Cortical rigidity; Mitosis; Mitotic cell rounding; RhoA

Indexed keywords

ACTIN; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SERINE; THREONINE;

ARTICLE; CELL ADHESION; CELL SHAPE; CYTOSKELETON; HUMAN; HUMAN CELL; INTERPHASE; MITOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANAPHASE; CELL ADHESION; CELL SIZE; CYTOSKELETON; ENZYME INHIBITORS; EUKARYOTIC CELLS; HELA CELLS; HUMANS; INTERPHASE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICROFILAMENTS; MITOSIS; PROTEIN-SERINE-THREONINE KINASES; RHOA GTP-BINDING PROTEIN;

EID: 0037455574     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200207130     Document Type: Article

References (64)

1. Amano, M., M. Ito, K. Kimura, Y. Fukata, K. Chihara, T. Nakano, Y. Matsuura, and K. Kaibuchi. 1996. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271:20246-20249.
2. Amano, T., N. Kaji, K. Ohashi, and K. Mizuno. 2002. Mitosis-specific activation of LIM motif-containing protein kinase and roles of cofilin phosphorylation and dephosphorylation in mitosis. J. Biol. Chem. 277:22093-22102.
3. Arthur, W.T., and K. Burridge. 2001. RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol. Biol. Cell. 12:2711-2720.
4. Arthur, W.T., L.A. Perch, and K. Burridge. 2000. Integrin engagement suppresses RhoA activity via a c-Src-dependent mechanism. Curr. Biol. 10:719-722.
5. Bishop, A.L., and A. Hall. 2000. Rho GTPases and their effector proteins. Biochem. J. 348(Pt. 2):241-255.
6. Brown, D.L., J.E. Little, N. Chaly, I. Schweitzer, and M. Paulin-Levasseur. 1985. Effects of taxol on microtubule organization in mouse splenic lymphocytes and on response to mitogenic stimulation. Eur. J. Cell Biol. 37:130-139.
7. Burton, K., and D.L. Taylor. 1997. Traction forces of cytokinesis measured with optically modified elastic substrata. Nature. 385:450-454.
8. Chackalaparampil, I., and D. Shalloway. 1988. Altered phosphorylation and activation of pp60c-src during fibroblast mitosis. Cell. 52:801-810.
9. Chardin, P., P. Boquet, P. Madaule, M.R. Popoff, E.J. Rubin, and D.M. Gill. 1989. The mammalian G protein rhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilaments in Vero cells. EMBO J. 8:1087-1092.
10. Chen, B.-H., J.T.C. Tzen, A.R. Bresnick, and H.-C. Chen. 2002. Roles of Rho-associated kinase and myosin light chain kinase in morphological and migratory defects of focal adhesion kinase-null cells. J. Biol. Chem. 277:33857-33863.
11. Chrzanowska-Wodnicka, M., and K. Burridge. 1996. Rho-stimulated contractility drives the formation of stress fibers and focal adhesions. J. Cell Biol. 133: 1403-1415.
12. Cortese, J.D., B. Schwab III, C. Frieden, and E.L. Elson. 1989. Actin polymerization induces a shape change in actin-containing vesicles. Proc. Natl. Acad. Sci. USA. 86:5773-5777.
13. Cramer, L.P., and T.J. Mitchison. 1997. Investigation of the mechanism of retraction of the cell margin and rearward flow of nodules during mitotic cell rounding. Mol. Biol. Cell. 8: 109-119.
14. Dumenil, G., P. Sansonetti, and G. Tran Van Nhieu. 2000. Src tyrosine kinase activity down-regulates Rho-dependent responses during Shigella entry into epithelial cells and stress fibre formation. J. Cell Sci. 113(Pt 1):71-80.
15. Enomoto, T. 1996. Microtubule disruption induces the formation of actin stress fibers and focal adhesions in cultured cells: possible involvement of the rho signal cascade. Cell Struct. Funct. 21:317-326.
16. Fincham, V.J., A. Chudleigh, and M.C. Frame. 1999. Regulation of p190 Rho-GAP by v-Src is linked to cytoskeletal disruption during transformation. J. Cell Sci. 112(Pt 6):947-956.
17. Fukata, Y., N. Oshiro, N. Kinoshita, Y. Kawano, Y. Matsuoka, V. Bennett, Y. Matsuura, and K. Kaibuchi. 1999. Phosphorylation of adducin by Rho-kinase plays a crucial role in cell motility. J. Cell Biol. 145:347-361.
18. Glotzer, M. 2001. Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol. 17:351-386.
19. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science. 279:509-514.
20. Hara, K., P. Tydeman, and M. Kirschner. 1980. A cytoplasmic clockwith the same period as the division cycle in Xenopus eggs. Proc. Natl. Acad. Sci. USA. 77: 462-466.
21. Harris, A.K. 1973. Location of cellular adhesions to solid substrata. Dev. Biol. 35: 97-114.
22. Hock, R.S., J.M. Sanger, and J.W. Sanger. 1989. Talin dynamics in living microinjected nonmuscle cells. Cell Motil. Cyroskeleton. 14:271-287.
23. Ishizaki, T., M. Maekawa, K. Fujisawa, K. Okawa, A. Iwamatsu, A. Fujita, N. Watanabe, Y. Saito, A. Kakizuka, N. Morii, and S. Narumiya. 1996. The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J. 15:1885-1893.
24. Jordan, M.A., R.J. Toso, D. Thrower, and L. Wilson. 1993. Mechanism of mitotic block and inhibition of cell proliferation by taxol at low concentrations. Proc. Natl. Acad. Sci. USA. 90:9552-9556.
25. Kimura, K., M. Ito, M. Amano, K. Chihara, Y. Fukata, M. Nakafuku, B. Yamamori, J. Feng, T. Nakano, K. Okawa, et al. 1996. Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science. 273:245-248.
26. Kimura, K., Y. Fukata, Y. Matsuoka, V. Bennett, Y. Matsuura, K. Okawa, A. Iwamatsu, and K. Kaibuchi. 1998. Regulation of the association of adducin with actin filaments by Rho-associated kinase (Rho-kinase) and myosin phosphatase. J. Biol. Chem. 273:5542-5548.
27. Kimura, K., T. Tsuji, Y. Takada, T. Miki, and S. Narumiya. 2000. Accumulation of GTP-bound RhoA during cytokinesis and a critical role of ECT2 in this accumulation. J. Biol. Chem. 275:17233-17236.
28. Kishi, K., T. Sasaki, S. Kuroda, T. Itoh, and Y. Takai. 1993. Regulation of cytoplasmic division of Xenopus embryo by rho p21 and its inhibitory GDP/ GTP exchange protein (rho GDI). J. Cell Biol. 120:1187-1195.
29. Kosako, H., T. Yoshida, F. Matsumura, T. Ishizaki, S. Narumiya, and M. Inagaki. 2000. Rho-kinase/ROCK is involved in cytokinesis through the phosphorylation of myosin light chain and not ezrin/radixin/moesin proteins at the cleavage furrow. Oncogene. 19:6059-6064.
30. Krendel, M., F.T. Zenke, and G.M. Bokoch. 2002. Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4:294-301.
31. Leung, T., E. Manser, L. Tan, and L. Lim. 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.
32. Liu, B.P., M. Chrzanowska-Wodnicka, and K. Burridge. 1998. Microtubule depolymerization induces stress fibers, focal adhesions, and DNA synthesis via the GTP-binding protein Rho. Cell Adhes. Commun. 5:249-255.
33. Maekawa, M., T. Ishizaki, S. Boku, N. Watanabe, A. Fujita, A. Iwamatsu, T. Obinata, K. Ohashi, K. Mizuno, and S. Narumiya. 1999. Signaling from Rho to the actin cytoskeleton through protein kinases ROCK and LIM-kinase. Science. 285:895-898.
34. Matsumura, F., G. Totsukawa, Y. Yamakita, and S. Yamashiro. 2001. Role of myosin light chain phosphorylation in the regulation of cytokinesis. Cell Srruct. Funct. 26:639-644.
35. Matzke, R., K. Jacobson, and M. Radmacher. 2001. Direct, high-resolution measurement of furrow stiffening during division of adherent cells. Nat. Cell Biol. 3:607-610.
36. Mitchison, J.M., and M.M. Swann. 1955. The mechanical properties of the cell surface. III. The sea urchin egg from fertilization to cleavage. J. Exp. Biol. 32: 734-750.
37. Nishikawa, M., J.R. Sellers, R.S. Adelstein, and H. Hidaka. 1984. Protein kinase C modulates in vitro phosphorylation of the smooth muscle heavy meromyosin by myosin light chain kinase. J. Biol. Chem. 259:8808-8814.
38. O'Connell, C.B., S.P. Wheatley, S. Ahmed, and Y.L. Wang. 1999. The small GTP-binding protein rho regulates cortical activities in cultured cells during division. J. Cell Biol. 144:305-313.
39. Paterson, H.F., A.J. Self, M.D. Garrett, I. Just, K. Aktories, and A. Hall. 1990. Microinjection of recombinant p21rho induces rapid changes in cell morphology. J. Cell Biol. 111:1001-1007.
40. Ren, X.D., W.B. Kiosses, and M.A. Schwartz. 1999. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18: 578-585.
41. 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.
42. Rieder, C.L., A. Schultz, R. Cole, and G. Sluder. 1994. Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J. Cell Biol 127:1301-1310.
43. Rubin, E.J., D.M. Gill, P. Boquet, and M.R. Popoff. 1988. Functional modification of a 21-kilodalton G protein when ADP-ribosylated by exoenzyme C3 of Clostridium botulinum. Mol. Cell. Biol. 8:418-426.
44. Sanger, J.M., A.M. Reingold, and J.W. Sanger. 1984. Cell surface changes during mitosis and cytokinesis of epithelial cells. Cell Tissue Res. 237:409-417.
45. Sanger, J.M., B. Mittal, M.B. Pochapin, and J.W. Sanger. 1987. Stress fiber and cleavage furrow formation in living cells microinjected with fluorescently labeled α-actinin. Cell Motil. Cytoskeleton. 7:209-220.
46. Sanger, J.M., B. Mittal, J.S. Dome, and J.W. Sanger. 1989. Analysis of cell division using fluorescently labeled actin and myosin in living PtK2 cells. Cell Motil. Cytoskeleton. 14:201-219.
47. Satterwhite, L.L., M.J. Lohka, K.L. Wilson, T.Y. Scherson, L.J. Cisek, J.L. Corden, and T.D. Pollard. 1992. Phosphorylation of myosin-II regulatory light chain by cyclin-p34cdc2: a mechanism for the timing of cytokinesis. J. Cell Biol. 118:595-605.
48. Shuster, C.B., and D.R. Burgess. 1999. Parameters that specify the timing of cytokinesis. J. Cell Biol. 146:981-992.
49. Sumi, T., K. Matsumoto, Y. Takai, and T. Nakamura. 1999. Cofilin phosphorylation and actin cytoskeletal dynamics regulated by rho- and Cdc42-activated LIM-kinase 2. J. Cell Biol. 147:1519-1532.
50. Trouliaris, S., U. Smola, J.H. Chang, S.J. Parsons, H. Niemann, and T. Tamura. 1995. Tyrosine 807 of the v-Fms oncogene product controls cell morphology and association with p120RasGAP. J. Virol. 69:6010-6020.
51. Uehata, M., T. Ishizaki, H. Satoh, T. Ono, T. Kawahara, T. Morishita, H. Tamakawa, K. Yamagami, J. Inui, M. Maekawa, and S. Narumiya. 1997. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature. 389:990-994.
52. Van Aelst, L., and C. D'Souza-Schorey. 1997. Rho GTPases and signaling networks. Genes Dev. 11:2295-2322.
53. Varlamova, O., A. Spektor, and A.R. Bresnick. 2001. Protein kinase C mediates phosphorylation of the regulatory light chain of myosin-II during mitosis. J. Muscle Res. Cell Motil. 22:243-250.
54. Vincent, S., and J. Settleman. 1999. Inhibition of RhoGAP activity is sufficient for the induction of Rho-mediated actin reorganization. Eur. J. Cell Biol. 78: 539-548.
55. Watanabe, N., P. Madaule, T. Reid, T. Ishizaki, G. Watanabe, A. Kakizuka, Y. Saito, K. Nakao, B.M. Jockusch, and S. Narumiya. 1997. p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16:3044-3056.
56. Watanabe, N., T. Kato, A. Fujita, T. Ishizaki, and S. Narumiya. 1999. Cooperation between mDial and ROCK in Rho-induced actin reorganization. Nat. Cell Biol. 1:136-143.
57. Wiegers, W., I. Just, H. Muller, A. Hellwig, P. Traub, and K. Aktories. 1991. Alteration of the cytoskeleton of mammalian cells cultured in vitro by Clostridium botulinum C2 toxin and C3 ADP-ribosyltransferase. Eur. J. Cell Biol. 54:237-245.
58. Worthylake, R.A., S. Lemoine, J.M. Watson, and K. Burridge. 2001. RhoA is required for monocyre tail retraction during transendothelial migration. J. Cell Biol. 154:147-160.
59. Yamaguchi, R., Y. Mazaki, K. Hirota, S. Hashimoto, and H. Sabe. 1997. Mitosis specific serine phosphorylation and downregulation of one of the focal adhesion protein, paxillin. Oncogene. 15:1753-1761.
60. Yamakita, Y., S. Yamashiro, and F. Matsumura. 1994. In vivo phosphorylation of regulatory light chain of myosin II during mitosis of cultured cells. J. Cell Biol. 124:129-137.
61. Yamakita, Y., G. Totsukawa, S. Yamashiro, D. Fry, X. Zhang, S.K. Hanks, and F. Matsumura. 1999. Dissociation of FAK/p130(CAS)/c-Src complex during mitosis: role of mitosis-specific serine phosphorylation of FAK. J. Cell Biol. 144:315-324.
62. Yamashiro, S., Y. Yamakita, H. Hosoya, and F. Matsumura. 1991. Phosphorylation of non-muscle caldesmon by p34cdc2 kinase during mitosis. Nature. 349:169-172.
63. Yoneda, M., and K. Dan. 1972. Tension at the surface of the dividing sea-urchin egg. J. Exp. Biol. 57:575-587.
64. Zhang, Q., M.K. Magnusson, and D.F. Mosher. 1997. Lysophosphatidic acid and microtubule-destabilizing agents stimulate fibronectin matrix assembly through Rho-depenclent actin stress fiber formation and cell contraction. Mol. Biol. Cell. 8:1415-1425.