Functional significance of the specific sites phosphorylated in desmin at cleavage furrow: Aurora-B may phosphorylate and regulate type III intermediate filaments during cytokinesis coordinatedly with Rho-kinase

Molecular Biology of the Cell

Volumn 14, Issue 4, 2003, Pages 1489-1500

  Kawajiri, Aie ^a,b   Yasui, Yoshihiro ^a   Goto, Hidemasa ^a   Tatsuka, Masaaki ^c   Takahashi, Masahide ^b   Nagata, Koh ichi ^a   Inagaki, Masaki ^a  

^a AICHI CANCER CENTER HOSPITAL   (Japan)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; ANTIBODY; AURORA B KINASE; DESMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLYCINE; PROTEIN KINASE; RHO KINASE; SERINE; THREONINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CELL DIVISION; CELL LINE; CONTROLLED STUDY; CYTOKINESIS; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; IN VITRO STUDY; INTERMEDIATE FILAMENT; MOLECULAR RECOGNITION; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL DIVISION; CELL LINE; COS CELLS; DESMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; INTERMEDIATE FILAMENTS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; SERINE;

ANIMALIA;

EID: 0038371015     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E02-09-0612     Document Type: Article

References (46)

1. Adams, R.R., Carmena, M., and Earnshaw, W.C. (2001a). Chromosomal passengers and the (aurora) ABCs of mitosis. Trends Cell Biol. 11, 49-54.
2. Adams, R.R., Maiato, H., Earnshaw, W.C., and Carmena, M. (2001b). Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation. J. Cell Biol. 153, 865-880.
3. Bischoff, J.R. et al. (1998). A homologue of Drosophila aurora kinase is oncogenic and amplified in human colorectal cancers. EMBO J. 17, 3052-3065.
4. Bischoff, J.R., and Plowman, G.D. (1999). The Aurora/Ipl1p kinase family: regulators of chromosome segregation and cytokinesis. Trends Cell Biol. 9, 454-459.
5. Bishop, J.D., and Schumacher, J.M. (2002). Phosphorylation of the carboxyl terminus of inner centromere protein (INCENP) by the Aurora B kinase stimulates Aurora B kinase activity. J. Biol. Chem. 277, 27577-27580.
6. Eriksson, J.E., Opal, P., and Goldman, R.D. (1992). Intermediate filament dynamics. Curr. Opin. Cell Biol. 4, 99-104.
7. Fuchs, E., and Weber, K. (1994). Intermediate filaments: structure, dynamics, function, and disease. Annu. Rev. Biochem. 63, 345-382.
8. Giet, R., and Glover, D.M. (2001). Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J. Cell Biol. 152, 669-682.
9. Giet, R., and Prigent, C. (1999). Aurora/Ipl1p-related kinases, a new oncogenic family of mitotic serine-threonine kinases. J. Cell Sci. 112, 3591-3601.
10. Giet, R., and Prigent, C. (2000). The Xenopus laevis aurora/Ip11prelated kinase pEg2 participates in the stability of the bipolar mitotic spindle. Exp. Cell Res. 258, 145-151.
11. Glover, D.M., Leibowitz, M.H., McLean, D.A., and Parry, H. (1995). Mutations in aurora prevent centrosome separation leading to the formation of monopolar spindles. Cell 81, 95-105.
12. Goto, H., Kosako, H., Tanabe, K., Yanagida, M., Sakurai, M., Amano, M., Kaibuchi, K., and Inagaki, M. (1998). Phosphorylation of vimentin by Rho-associated kinase at a unique amino-terminal site that is specifically phosphorylated during cytokinesis. J. Biol. Chem. 273, 11728-11736.
13. Goto, H., Yasui, Y., Nigg, E.A., and Inagaki, M. (2002). Aurora-B phosphorylates Histone H3 at serine28 with regard to the mitotic chromosome condensation. Genes Cells 7, 11-17.
14. Hsu, J.Y. et al. (2000). Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102, 279-291.
15. Hunt, T. (1991). Cyclins and their partners: from a simple idea to complicated reality. Semin. Cell Biol. 2, 213-222.
16. Inada, H., Goto, H., Tanabe, K., Nishi, Y., Kaibuchi, K., and Inagaki, M. (1998). Rho-associated kinase phosphorylates desmin, the myogenic intermediate filament protein, at unique amino-terminal sites. Biochem. Biophys. Res. Commun. 253, 21-25.
17. Inada, H., Togashi, H., Nakamura, Y., Kaibuchi, K., Nagata, K., and 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.
18. Inagaki, M., Gonda, Y., Matsuyama, M., Nishizawa, K., Nishi, Y., and Sato, C. (1988). Intermediate filament reconstitution in vitro. The role of phosphorylation on the assembly-disassembly of desmin. J. Biol. Chem. 263, 5970-5978.
19. Inagaki, M., Matsuoka, Y., Tsujimura, K., Ando, S., Tokui, T., Takahashi, T., and Inagaki, N. (1996). Dynamic property of intermediate filaments: regulation by phosphorylation. Bioessays 18, 481-487.
20. Kaibuchi, K., Kuroda, S., and Amano, M. (1999). Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68, 459-486.
21. Kaitna, S., Mendoza, M., Jantsch-Plunger, V., and Glotzer, M. (2000). Incenp and an aurora-like kinase form a complex essential for chromosome segregation and efficient completion of cytokinesis. Curr. Biol. 10, 1172-1181.
22. Klymkowsky, M.W. (1995). Intermediate filaments: new proteins, some answers, more questions. Curr. Opin. Cell Biol. 7, 46-54.
23. Kosako, H., Amano, M., Yanagida, M., Tanabe, K., Nishi, Y., Kaibuchi, K., and Inagaki, M. (1997). Phosphorylation of glial fibrillary acidic protein at the same sites by cleavage furrow kinase and Rho-associated kinase. J. Biol. Chem. 272, 10333-10336.
24. Kosako, H. et al. (1999). Specific accumulation of Rho-associated kinase at the cleavage furrow during cytokinesis: cleavage furrowspecific phosphorylation of intermediate filaments. Oncogene 18, 2783-2788.
25. Machesky, L.M., and Hall, A. (1996). Rho: a connection between membrane receptor signaling and the cytoskeleton. Trends Cell Biol. 6, 304-310.
26. Matsuoka, Y., Nishizawa, K., Yano, T., Shibata, M., Ando, S., Takahashi, T., and Inagaki, M. (1992). Two different protein kinases act on a different time schedule as glial filament kinases during mitosis. EMBO J. 11, 2895-2902.
27. Meyer, H.E., Hoffmann-Posorske, E., Korte, H., and Heilmeyer, L.M.G. (1986). Sequence analysis of phosphoserine-containing peptides. Modification for picomolar sensitivity. FEBS Lett. 204, 61-66.
28. Mishima, M., Kaitna, S., and Glotzer, M. (2002). Central spindle assembly, and cytokinesis require a kinesin-like protein/RhoGAP complex with microtubule bundling activity. Dev. Cell 2, 41-54.
29. Murata-Hori, M., M. Tatsuka, and Y.L. Wang. (2002) Probing the dynamics and functions of Aurora B kinase in living cells during mitosis and cytokinesis. Mol. Biol. Cell 13, 1099-1108.
30. Murnion, M.E., Adams, R.R., Callister, D.M., Allis, C.D., Earnshaw, W.C., and Swedlow, J.R. (2001). Chromatin-associated protein phosphatase 1 regulates aurora-B and histone H3 phosphorylation. J. Biol. Chem. 276, 26656-26665.
31. Nigg, E.A. (2001). Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell. Biol. 2, 21-32.
32. Nigg, E.A. (1993). Targets of cyclin-dependent protein kinases. Curr. Opin. Cell Biol. 5, 187-193.
33. Nishizawa, K., Yano, T., Shibata, M., Ando, S., Saga, S., Takahashi, T., and Inagaki, M. (1991). Specific localization of phosphointermediate filament protein in the constricted area of dividing cells. J. Biol. Chem. 266, 3074-3079.
34. Norbury, C., and Nurse, P. (1992). Animal cell cycles and their control. Annu. Rev. Biochem. 61, 441-470.
35. Reeves, S.A., Helman, L.J., Allison, A., and Israel, M.A. (1989). Molecular cloning and primary structure of human glial fibrillary acidic protein. Proc. Natl. Acad. Sci. USA 86, 5178-5182.
36. Roghi, C. et al. (1998). The Xenopus protein kinase pEg2 associates with the centrosome in a cell cycle-dependent manner, binds to the spindle microtubules and is involved in bipolar mitotic spindle assembly. J. Cell Sci. 111, 557-572.
37. Schumacher, J.M., Golden, A., and Donovan, P.J. (1998). AIR-2: an Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos. J. Cell Biol. 143, 1635-1646.
38. Sekimata, M., Tsujimura, K., Tanaka, J., Takeuchi, Y., Inagaki, N., and Inagaki, M. (1996). Detection of protein kinase activity specifically activated at metaphase-anaphase transition. J. Cell Biol. 132, 635-641.
39. Steinert, P.M., and Roop, D.R. (1988). Molecular and cellular biology of intermediate filaments. Annu. Rev. Biochem. 57, 593-625.
40. Severson, A.F., Hamill, D.R., Carter, J.C., Schumacher, J., and Bowerman, B. (2000). The Aurora-related kinase AIR-2 recruits ZEN-4/CeMKLP1 to the mitotic spindle at metaphase, and is required for cytokinesis. Curr. Biol. 10, 1162-1171.
41. Terada, Y., Tatsuka, M., Suzuki, F., Yasuda, Y., Fujita, S., and Otsu, M. (1998). AIM-1: a mammalian midbody-associated protein required for cytokinesis. EMBO J. 17, 667-676.
42. Wei, Y., Yu, L., Bowen, J., Gorovsky, M.A., and Allis, C.D. (1999). Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97, 99-109.
43. Yasui, Y., Amano, M., Nagata, K., Inagaki, N., Nakamura, H., Saya, H., Kaibuchi, K., and Inagaki, M. (1998). Roles of Rho-associated kinase in cytokinesis; mutations in Rho-associated kinase phosphorylation sites impair cytokinetic segregation of glial filaments. J. Cell Biol. 143, 1249-1258.
44. Yasui, Y., Goto, H., Matsui, S., Manser, E., Lim, L., Nagata, K., and Inagaki, M. (2001). Protein kinases required for segregation of vimentin filaments in mitotic process. Oncogene 20, 2868-2876.
45. Zeitlin, S.G., Barber, C.M., Allis, C.D., and Sullivan, K.F. (2001a). Differential regulation of CENP-A and histone H3 phosphorylation in G2/M. J. Cell Sci. 114, 653-661.
46. Zeitlin, S.G., Shelby, R.D., and Sullivan, K.F. (2001b). CENP-A is phosphorylated by Aurora B kinase and plays an unexpected role in completion of cytokinesis. J. Cell Biol. 155, 1147-1157.