Cdc37 is essential for chromosome segregation and cytokinesis in higher eukaryotes

EMBO Journal

Volumn 21, Issue 20, 2002, Pages 5364-5374

  Lange, Bodo M H ^a   Rebollo, Elena ^a   Herold, Andrea ^b   González, Cayetano ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b Gene Expression Program   (Germany)

Author keywords

Aurora B; Cdc37; Cell cycle; Cytokinesis; Mitosis

Indexed keywords

AURORA B KINASE; CELL CYCLE PROTEIN 37; HEAT SHOCK PROTEIN 90; PHOSPHOTRANSFERASE; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMOSOME SEGREGATION; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINESIS; DROSOPHILA; ENZYME INACTIVATION; HUMAN; HUMAN CELL; MEIOSIS; MITOSIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STABILITY;

ANIMALS; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIVISION; CHROMOSOME SEGREGATION; DROSOPHILA; DROSOPHILA PROTEINS; GENES, INSECT; HSP90 HEAT-SHOCK PROTEINS; MALE; MEIOSIS; MITOTIC SPINDLE APPARATUS; MOLECULAR CHAPERONES; MUTATION; PROTEIN-SERINE-THREONINE KINASES; RNA INTERFERENCE; SPERMATOCYTES;

ANIMALIA; ARACHNIDA; EUKARYOTA; HEXAPODA;

EID: 0037107454     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdf531     Document Type: Article

References (54)

1. Adams, R.R., Maiato, H., Earnshaw, W.C. and Carmena, M. (2001) 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.
2. 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.
3. Brown, N.H., and Kafatos, F.C. (1988) Functional cDNA libraries from Drosophila embryos. J. Mol. Biol., 203, 425-437.
4. Clemens, J.C., Worby, C.A., Simonson-Leff, N., Muda, M., Maehama, T., Hemmings, B.A. and Dixon, J.E. (2000) Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl. Acad. Sci. USA., 97, 6499-6503.
5. Cutforth, T. and Rubin, G.M. (1994) Mutations in Hsp83 and cdc37 impair signaling by the sevenless receptor tyrosine kinase in Drosophila. Cell, 77, 1027-1036.
6. Dai, K., Kobayashi, R. and Beach, D. (1996) Physical interaction of mammalian Cdc37 with CDK4. J. Biol. Chem., 271, 22030-22034.
7. Dej, K.J. and Orr-Weaver, T.L. (2000) Separation anxiety at the centromere. Trends Cell Biol., 10, 392-399.
8. Dey, B., Lightbody, J.J. and Boschelli, F. (1996) Cdc37 is required for p60v-src activity in yeast. Mol. Biol. Cell, 7, 1405-1417.
9. de Cárcer, G., do Carmo Avides, M., Lallena, M.J., Glover, D.M. and Gonzalez, C. (2001) Requirement of Hsp90 for centrosomal function reflects its regulation of Polo kinase stability. EMBO J., 20, 2878-2884.
10. Fuller, M.T. (1993) Spermatogenesis. In Bate, M. and Arias, A.M. (eds), The Development of Drosophila Melanogaster. Vol. I. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. pp. 71-147.
11. 1 and mitotic cyclins. Proc. Natl. Acad. Sci. USA, 92, 4651-4655.
12. Giansanti, M.G., Bonaccorsi, S., Williams, B., Williams, E.V., Santolamazza, C., Goldberg, M.L. and Gatti, M. (1998) Cooperative interactions between the central spindle and the contractile ring during Drosophila cytokinesis. Genes Dev., 12, 396-410.
13. 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.
14. Glotzer, M. (2001) Animal cell cytokinesis. Annu. Rev. Cell Dev. Biol., 17, 351-386.
15. Glover, C.V., III (1998) On the physiological role of casein kinase II in Saccharomyces cerevisiae. Prog. Nucleic Acid Res. Mol. Biol., 59, 95-133.
16. Goldstein, L.S. (1980) Mechanisms of chromosome orientation revealed by two meiotic mutants in Drosophila melanogaster. Chromosoma, 78, 79-111.
17. Gonzalez, C. and Glover, D.M. (1993) Techniques for studying mitosis in Drosophila. In Fantes, P. and Brook, R. (eds), The Cell Cycle: Practical Approach. IRL Press at Oxford University Press, pp. 143-175.
18. Gonzalez, C., Casal, J. and Ripoll, P. (1989) Relationship between chromosome content and nuclear diameter in early spermatids of Drosophila melanogaster. Genet. Res., 54, 205-212.
19. Grammatikakis, N., Lin, J.H., Grammatikakis, A., Tsichlis, P.N. and Cochran, B.H. (1999) p50(cdc37) acting in concert with Hsp90 is required for Raf-1 function. Mol. Cell. Biol., 19, 1661-1672.
20. 2/M in Saccharomyces cerevisiae. J. Biol. Chem., 270, 25905-25914.
21. Herrmann, S., Amorim, I., Sunkel, C.E. (1998) The POLO kinase is required at multiple stages during spermatogenesis in Drosophila melanogaster. Chromosoma, 107, 440-451.
22. Huang, L., Grammatikakis, N. and Toole, B.P. (1998) Organization of the chick Cdc37 gene. J. Biol. Chem., 273, 3598-3603.
23. Hunter, T. and Poon, R.Y.C. (1997) Cdc37: A protein kinase chaperon. Trends Cell Biol., 7, 157-161.
24. Kaitna, S., Mendoza, M., Jantsch-Plunger, V. and Glotzer, M. (2000) Nucleotide Incenp and an Aurora-like kinase form a complex essential for chromosome segregation and efficient completion of cytokinesis. Curr. Biol., 10, 1172-1181.
25. Kaitna, S., Pasierbek, P., Jantsch, M., Loidl, J. and Glotzer, M. (2002) The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous chromosomes during meiosis. Curr. Biol., 12, 798-812.
26. Kallio, M.J., McCleland, M.L., Stukenberg, P.T. and Gorbsky, G.J. (2002) Inhibition of aurora B kinase blocks chromosome segregation, overrides the spindle checkpoint, and perturbs microtubule dynamics in mitosis. Curr. Biol., 12, 900-905.
27. Karaiskou, A., Perez, L.H., Ferby, I., Ozon, R., Jessus, C. and Nebreda, A.R. (2001) Differential regulation of Cdc2 and Cdk2 by RINGO and cyclins. J. Biol. Chem., 276, 36028-36034.
28. Kimura, Y., Rutherford, S.L., Miyata, Y., Yahara, I., Freeman, B.C., Yue, L., Morimoto, R.I. and Lindquist, S. (1997) Cdc37 is a molecular chaperone with specific functions in signal transduction. Genes Dev., 11, 1775-1785.
29. Lange, B.M.H. and Gull, K. (1995) A molecular marker for centriole maturation in the mammalian cell cycle. J. Cell Biol., 130, 919-927.
30. Moritz, M., Braunfeld, M.B., Fung, J.C., Sedat, J.W., Alberts, B.M. and Agard, D.A. (1995) Three-dimensional structural characterization of centrosomes from early Drosophila embryos. J. Cell Biol., 130, 1149-1159.
31. Nigg, E. (2001) Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell. Biol., 2, 21-32.
32. Pearl, L.H. and Prodromou, C. (2000) Structure and in vivo function of Hsp90. Curr. Opin. Struct. Biol. 10, 46-51.
33. Perdew, G., Wiegand, H., Vanden Heuvel, J., Mitchell, C. and Singh, S. (1997) A 50 kiloDalton protein associated with Raf and pp60v-src protein kinase is a mammalian homolog of the cell cycle control protein Cdc37. Biochemistry, 36, 3600-3607.
34. Pines, J. (1999) Four-dimensional control of the cell cycle. Nat. Cell Biol., 1, E73-E79.
35. Ploubidou, A., Moreau, V., Ashman, K., Reckmann, I., Gonzalez, C. and Way, M. (2000) Vaccinia virus infection disrupts microtubule organization and centrosome function. EMBO J., 19, 3932-3944.
36. Pratt, W.B. and Toft, D.O. (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev., 18, 306-360.
37. Rebollo, E. and González, C. (2000) Visualizing the spindle checkpoint in Drosophila spermatocytes. EMBO Rep., 1, 65-70.
38. Reed, S.I. (1980) The selection of S. cerevisiae mutants defective in the start event of cell division. Genetics, 95, 561-577.
39. Robinson, J.P., Darzynkiewicz, Z., Dean, P., Orfao, A., Rabinovitch, P., Stewart, C., Tanke, H. and Wheeless, L. (eds) (1999) Current Protocols in Flow Cytometry, Vol. I. Wiley, New York, NY.
40. Rogers, E., Bishop, J.D., Waddle, J.A., Schumacher, J.M. and Lin, R. (2002) The aurora kinase AIR-2 functions in the release of chromosome cohesion in Caenorhabditis elegans meiosis. J. Cell Biol., 157, 219-229.
41. Roos, U.P. (1976) Light and electron microscopy of rat kangaroo cells in mitosis. III. Patterns of chromosome behavior during prometaphase. Chromosoma, 54, 363-385.
42. Schutz, A.R., Giddings, T.H., Jr, Steiner, E. and Winey, M. (1997) The yeast Cdc37 gene interacts with MPS1 and is required for proper execution of spindle pole body duplication. J. Cell Biol., 136, 969-982.
43. Silverstein, A.M., Grammatikakis, N., Cochran, B.H., Chinkers, M. and Pratt, W.B. (1998) p50(cdc37) binds directly to the catalytic domain of Raf as well as to a site on hsp90 that is topologically adjacent to the tetratricopeptide repeat binding site. J. Biol. Chem., 273, 20090-20095.
44. Simizu, S. and Osada, H. (2000) Mutations in the Plk gene lead to instability of Plk protein in human tumour cell lines. Nat. Cell Biol., 2, 852-854.
45. Stepanova, L., Leng, X., Parker, S.B. and Harper, J.W. (1996) Mammalian p50Cdc37 is a protein kinase-targeting subunit of Hsp90 that binds and stabilizes Cdk4. Genes Dev., 10, 1491-502.
46. Stepanova, L., Leng, X. and Harper, J.W. (1997) Analysis of mammalian Cdc37, a protein kinase targeting subunit of heat shock protein 90. Methods Enzymol., 283, 220-229.
47. Stepanova, L., Finegold, M., DeMayo, F., Schmidt, E.V. and Harper, J.W. (2000a) The oncoprotein kinase chaperone Cdc37 functions as an oncogene in mice and collaborates with both c-myc and cyclin DI in transformation of multiple tissues. Mol. Cell. Biol., 20, 4462-4473.
48. Stepanova, L., Yang, G., DeMayo, F., Wheeler, T.M., Finegold, M., Thompson, T.C. and Harper, J.W. (2000b) Induction of human Cdc37 in prostate cancer correlates with the ability of targeted Cdc37 expression to promote prostatic hyperplasia. Oncogene, 19, 2186-2193.
49. Sunkel, C.E. and Glover, D.M. (1988) polo, a mitotic mutant of Drosophila displaying abnormal spindle poles. J. Cell Sci., 89, 25-38.
50. Tanaka, T.U., Rachidi, N., Janke, C., Pereira, G., Galova, M., Schiebel, E., Stark, M.J. and Nasmyth, K. (2002) Evidence that the Ip11-Sli15 (Aurora kinase-INCENP) complex promotes chromosome bi-orientation by altering kinetochore-spindle pole connections. Cell, 108, 317-429.
51. Tatsuka, M., Katayama, H., Ota, T., Tanaka, T., Odashima, S., Suzuki, F. and Terada, Y. (1998) Multinuclearity and increased ploidy caused by overexpression of the Aurora- and Ip11-like midbody-associated protein mitotic kinase in human cancer cells. Cancer Res., 58, 4811-4816.
52. 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.
53. van der Straten, A., Rommel, C., Dickson, B. and Hafen, E. (1997) The heat shock protein 83 (Hsp83) is required for Raf-mediated signalling in Drosophila. EMBO J., 16, 1961-1969.
54. Zhou, H., Kuang, J., Zhong, L., Kuo, W.L., Gray, J.W., Sahin, A., Brinkley, B.R. and Sen, S. (1998) Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation. Nat. Genet., 20, 189-193.