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Protein kinases required for segregation of vimentin filaments in mitotic process

Oncogene volume 20, pages 2868–2876 (2001)Cite this article

Abstract

Vimentin, one of type III intermediate filament (IF) proteins, is expressed not only in mesenchymal cells but also in most types of tumor cells. In the present study, we introduced several types of vimentin mutated at putative phosphorylation sites in its amino-terminal head domain into type III IF-negative T24 cells. Site-specific mutation induced the formation of an unusually long bridge-like IF structure between the unseparated daughter cells, although these mutants formed the filament network similar to wild type in interphase cells. Together with sites phosphorylated by Rho-kinase and protein kinase C (PKC), vimentin-Ser72, which can not be phosphorylated by any known vimentin kinase, was one of the mutation sites essential for this phenotype. We further demonstrated that vimentin-Ser72 was phosphorylated specifically at the cleavage furrow during cytokinesis. These observations suggest the existence of a novel protein kinase responsible for vimentin filament separation through the cleavage furrow-specific vimentin phosphorylation. We propose that Rho-kinase, PKC, and an unidentified vimentin-Ser72 kinase may play important roles in vimentin filament separation during cytokinesis.

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Abbreviations

IF:

intermediate filament

GFAP:

glial fibrillary acidic protein

PKC:

protein kinase C

CaM kinase II:

Ca2+-calmodulin-dependent protein kinase II.

References

  • Bischoff JR, Plowman GD . 1999 Trends Cell Biol. 9: 454–459

  • Celis JE, Lasen PM, Fey SJ, Celis A . 1983 J. Cell Biol. 97: 1429–1434

  • Chou YH, Bischoff JR, Beach D, Goldman RD . 1990 Cell 62: 1063–1071

  • Chung CY, Firtel RA . 1999 J. Cell Biol. 147: 559–575

  • Eriksson JE, Opal P, Goldman RD . 1992 Curr. Opin. Cell Biol. 4: 99–104

  • Evans RM, Flik LM . 1982 Cell 29: 43–52

  • Evans RM . 1984 J. Biol. Chem. 259: 5372–5375

  • Foisner R . 1997 BioEssays 19: 297–305

  • Franke WW, Schmid E, Grund C . 1982 Cell 30: 103–113

  • Fuchs E, Weber K . 1994 Annu. Rev. Biochem. 63: 345–382

  • Goss VL, Hocevar BA, Thompson LJ, Stratton CA . 1994 J. Biol. Chem. 269: 19074–19080

  • Goto H, Kosako H, Tanabe K, Yanagida M, Sakurai M, Amano M, Kaibuchi K, Inagaki M . 1998 J. Biol. Chem. 273: 11728–11736

  • Goto H, Kosako H, Inagaki M . 2000 Microscopy Res. Technique 49: 173–182

  • Hall A . 1998 Science 279: 509–514

  • Holly SP, Blumer KJ . 1999 J. Cell Biol. 147: 845–856

  • Inada H, Togashi H, Nakamura Y, Kaibuchi K, Nagata K, Inagaki M . 1999 J. Biol. Chem. 274: 34932–34939

  • Inagaki M, Nishi Y, Nishizawa K, Matsuyama M, Sato C . 1987 Nature 328: 649–652

  • Inagaki M, Matsuoka Y, Tsujimura K, Ando S, Tokui T, Takahashi T, Inagaki N . 1996 BioEssays 18: 481–487

  • Inagaki M, Inagaki N, Takahashi T, Takai Y . 1997a J. Biochem. 121: 407–414

  • Inagaki N, Ito M, Nakano T, Inagaki M . 1994 Trends Biochem. Sci. 19: 448–452

  • Inagaki N, Goto H, Ogawara M, Nishi Y, Ando S, Inagaki M . 1997b J. Biol. Chem. 272: 25195–25199

  • Kosako H, Amano M, Yanagida M, Tanabe K, Nishi Y, Kaibuchi K, Inagaki M . 1997 J. Biol. Chem. 272: 10333–10336

  • Kosako H, Goto H, Yanagida M, Matsuzawa K, Fujita M, Tomono Y, Okigaki T, Odai H, Kaibuchi K, Inagaki M . 1999 Oncogene 18: 2783–2788

  • Ku NO, Liao J, Chou CF, Omary MB . 1998 Cancer Metastasis Rev. 15: 429–444

  • Lane HA, Nigg EA . 1997 Trends Cell Biol. 7: 63–68

  • Livneh E, Fishman DD . 1997 Eur. J. Biochem. 248: 1–9

  • Madaule P, Eda M, Watanabe N, Fujisawa K, Matsuoka T, Bito H, Ishizaki T, Narumiya S . 1998 Nature 394: 491–494

  • Matsuoka Y, Nishizawa K, Yano T, Shibata M, Ando S, Takahashi T, Inagaki M . 1992 EMBO J. 11: 2895–2902

  • Nigg EA . 1998 Curr. Opin. Cell Biol. 10: 776–783

  • Nishizuka Y . 1992 Science 258: 607–614

  • Nishizawa K, Yano T, Shibata M, Ando S, Saga S, Takahashi T, Inagaki M . 1991 J. Biol. Chem. 266: 3074–3079

  • Ogawara M, Inagaki N, Tsujimura K, Takai Y, Sekimata M, Ha MH, Imajoh-Ohmi S, Hirai S, Ohno S, Sugiura H, Yamauchi T, Inagaki M . 1995 J. Cell Biol. 131: 1055–1066

  • Passalacqua M, Patrone M, Sparatore B, Pedrazzi M, Melloni E,, Pontremoli S . 1999 FEBS Lett. 453: 249–253

  • Prokopenko SN, Saint R, Bellen HJ . 2000 J. Cell Biol. 148: 843–848

  • Schumacher JM, Golden A, Donovan PJ . 1998 J. Cell Biol. 143: 1635–1646

  • Sekimata M, Tsujimura K, Tanaka J, Takeuchi Y, Inagaki N, Inagaki M . 1996 J. Cell Biol. 132: 635–641

  • Steinert PM, Roop DR . 1988 Ann. Rev. Biochem. 57: 593–625

  • Takai Y, Sasaki T, Tanaka K, Nakanishi H . 1995 Trends Biochem. Sci. 20: 227–231

  • Takai Y, Ogawara M, Tomono Y, Moritoh C, Imajoh-Ohmi S, Tsutsumi O, Taketani Y, Inagaki M . 1996 J. Cell Biol. 133: 141–149

  • Terada Y, Tatsuka M, Suzuki F, Yasuda Y, Fujita S, Otsu M . 1998 EMBO J. 17: 667–676

  • Thompson LJ, Fields AP . 1996 J. Biol. Chem. 271: 15045–15053

  • Tsujimura K, Ogawara M, Takeuchi Y, Imajoh-Ohmi S, Ha MH, Inagaki M . 1994 J. Biol. Chem. 269: 31097–31106

  • Yasui Y, Amano M, Nagata K, Inagaki N, Nakamura H, Saya H, Kaibuchi K, Inagaki M . 1998 J. Cell Biol. 143: 1249–1258

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Acknowledgements

We thank M Ohara for critique of the manuscript. This research was supported in part by Grants-in-Aid for Scientific Research and Cancer Research from the Ministry of Education, Science, Sports, and Culture of Japan, Japan Society of the Promotion of Science Research for the Future; by a grant-in-aid for the Second Term Comprehensive 10-Year Strategy for Cancer Control from the Ministry of Health and Welfare, Japan; a grant from Bristol-Myers-Squibb; and the Princess Takamatsu Cancer Research Foundation.

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Author notes

  1. Hidemasa Goto

    Present address: Domestic Research Fellow, Japan Science and Technology Corporation, Kawaguchi, 332-0012, Saitama, Japan

  2. Yoshihiro Yasui and Hidemasa Goto: Y Yasui and H Goto contributed equally to this paper

Authors and Affiliations

  1. Division of Biochemistry, Aichi Cancer Center Research Institute, Chikusa-ku, 464-8681, Nagoya, Japan

    Yoshihiro Yasui, Hidemasa Goto, Seiya Matsui, Koh-ichi Nagata & Masaki Inagaki

  2. Glaxo-IMCB Group, Institute of Molecular & Cell Biology, Singapore, 117609, Singapore

    Edward Manser & Louis Lim

  3. Department of Biological Chemistry, Faculty of Pharmaceutical Sciences, Nagoya City University, Nagoya, 4678-603, Japan

    Seiya Matsui

  4. Institute of Neurology, University College London, London, WC1N 1PJ, UK

    Louis Lim

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Yasui, Y., Goto, H., Matsui, S. et al. Protein kinases required for segregation of vimentin filaments in mitotic process. Oncogene 20, 2868–2876 (2001). https://doi.org/10.1038/sj.onc.1204407

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