Roles of Rho-associated Kinase in Cytokinesis; Mutations in Rho-associated Kinase Phosphorylation Sites Impair Cytokinetic Segregation of Glial Filaments

doi:10.1083/jcb.143.5.1249

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J. Cell Biol., Volume 143, Number 5, November 30, 1998 1249-1258

Roles of Rho-associated Kinase in Cytokinesis; Mutations in Rho-associated Kinase Phosphorylation Sites Impair Cytokinetic Segregation of Glial Filaments

Yoshihiro Yasui,^* Mutsuki Amano, Koh-ichi Nagata,^* Naoyuki Inagaki,^* Hideo Nakamura,^§ Hideyuki Saya,^§ Kozo Kaibuchi, and Masaki Inagaki^*

^* Laboratory of Biochemistry, Aichi Cancer Center Research Institute, Chikusa-ku, Nagoya 464-0021, Japan; Division of Signal Transduction, Nara Institute of Science and Technology, Ikoma 630-0101, Japan; ^§ Department of Tumor Genetics and Biology, Kumamoto University School of Medicine, 2-2-1, Honjo, Kumamoto 860-0811, Japan

Rho-associated kinase (Rho-kinase), which is activated by the small GTPase Rho, regulates formation of stress fibers and focaladhesions, myosin fiber organization, and neurite retraction throughthe phosphorylation of cytoskeletal proteins, including myosinlight chain, the ERM family proteins (ezrin, radixin, and moesin)and adducin. Rho-kinase was found to phosphorylate a type IIIintermediate filament (IF) protein, glial fibrillary acidic protein(GFAP), exclusively at the cleavage furrow during cytokinesis.In the present study, we examined the roles of Rho-kinase in cytokinesis,in particular organization of glial filaments during cytokinesis.Expression of the dominant-negative form of Rho-kinase inhibitedthe cytokinesis of Xenopus embryo and mammalian cells, the resultbeing production of multinuclei. We then constructed a seriesof mutant GFAPs, where Rho-kinase phosphorylation sites were variouslymutated, and expressed them in type III IF-negative cells. Themutations induced impaired segregation of glial filament (GFAPfilament) into postmitotic daughter cells. As a result, an unusuallylong bridge-like cytoplasmic structure formed between the unseparateddaughter cells. Alteration of other sites, including the cdc2kinase phosphorylation site, led to no remarkable defect in glialfilament separation. These results suggest that Rho-kinase isessential not only for actomyosin regulation but also for segregationof glial filaments into daughter cells which in turn ensures correctcytokinetic processes.

Key words: intermediate filament; glial fibrillary acidic protein (GFAP); Rho; Rho-associated kinase; cytokinesis

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Tharaux, P.-L., Bukoski, R. C., Rocha, P. N., Crowley, S. D., Ruiz, P., Nataraj, C., Howell, D. N., Kaibuchi, K., Spurney, R. F., Coffman, T. M. (2003). Rho Kinase Promotes Alloimmune Responses by Regulating the Proliferation and Structure of T Cells. J. Immunol. 171: 96-105 [Abstract] [Full Text]
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Guertin, D. A., Trautmann, S., McCollum, D. (2002). Cytokinesis in Eukaryotes. Microbiol. Mol. Biol. Rev. 66: 155-178 [Abstract] [Full Text]
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Ishizaki, T., Uehata, M., Tamechika, I., Keel, J., Nonomura, K., Maekawa, M., Narumiya, S. (2000). Pharmacological Properties of Y-27632, a Specific Inhibitor of Rho-Associated Kinases. Mol. Pharmacol. 57: 976-983 [Abstract] [Full Text]
Prokopenko, S. N., Saint, R., Bellen, H. J. (2000). Untying the Gordian Knot of Cytokinesis: Role of Small G Proteins and Their Regulators. J. Cell Biol. 148: 843-848 [Abstract] [Full Text]
Inada, H., Togashi, H., Nakamura, Y., Kaibuchi, K., Nagata, K.-i., Inagaki, M. (1999). Balance between Activities of Rho Kinase and Type 1 Protein Phosphatase Modulates Turnover of Phosphorylation and Dynamics of Desmin/Vimentin Filaments. J. Biol. Chem. 274: 34932-34939 [Abstract] [Full Text]
Kawano, Y., Fukata, Y., Oshiro, N., Amano, M., Nakamura, T., Ito, M., Matsumura, F., Inagaki, M., Kaibuchi, K. (1999). Phosphorylation of Myosin-binding Subunit (MBS) of Myosin Phosphatase by Rho-Kinase In Vivo. J. Cell Biol. 147: 1023-1038 [Abstract] [Full Text]
Amano, M., Chihara, K., Nakamura, N., Kaneko, T., Matsuura, Y., Kaibuchi, K. (1999). The COOH Terminus of Rho-kinase Negatively Regulates Rho-kinase Activity. J. Biol. Chem. 274: 32418-32424 [Abstract] [Full Text]
Goto, H., Tomono, Y., Ajiro, K., Kosako, H., Fujita, M., Sakurai, M., Okawa, K., Iwamatsu, A., Okigaki, T., Takahashi, T., Inagaki, M. (1999). Identification of a Novel Phosphorylation Site on Histone H3 Coupled with Mitotic Chromosome Condensation. J. Biol. Chem. 274: 25543-25549 [Abstract] [Full Text]
Prokopenko, S. N., Brumby, A., O'Keefe, L., Prior, L., He, Y., Saint, R., Bellen, H. J. (1999). A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila. Genes Dev. 13: 2301-2314 [Abstract] [Full Text]
Ohan, N, Agazie, Y, Cummings, C, Booth, R, Bayaa, M, Liu, X. (1999). RHO-associated protein kinase alpha potentiates insulin-induced MAP kinase activation in Xenopus oocytes. J. Cell Sci. 112: 2177-2184 [Abstract]
Arimura, N., Inagaki, N., Chihara, K., Menager, C., Nakamura, N., Amano, M., Iwamatsu, A., Goshima, Y., Kaibuchi, K. (2000). Phosphorylation of Collapsin Response Mediator Protein-2 by Rho-kinase. EVIDENCE FOR TWO SEPARATE SIGNALING PATHWAYS FOR GROWTH CONE COLLAPSE. J. Biol. Chem. 275: 23973-23980 [Abstract] [Full Text]
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Togashi, H., Nagata, K.-i., Takagishi, M., Saitoh, N., Inagaki, M. (2000). Functions of a Rho-specific Guanine Nucleotide Exchange Factor in Neurite Retraction. POSSIBLE ROLE OF A PROLINE-RICH MOTIF OF KIAA0380 IN LOCALIZATION. J. Biol. Chem. 275: 29570-29578 [Abstract] [Full Text]
Sumi, T., Matsumoto, K., Nakamura, T. (2001). Specific Activation of LIM kinase 2 via Phosphorylation of Threonine 505 by ROCK, a Rho-dependent Protein Kinase. J. Biol. Chem. 276: 670-676 [Abstract] [Full Text]
Sahlgren, C. M., Mikhailov, A., Hellman, J., Chou, Y.-H., Lendahl, U., Goldman, R. D., Eriksson, J. E. (2001). Mitotic Reorganization of the Intermediate Filament Protein Nestin Involves Phosphorylation by cdc2 Kinase. J. Biol. Chem. 276: 16456-16463 [Abstract] [Full Text]
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