Cyclin B2 and p53 control proper timing of centrosome separation

Nature Cell Biology

Volumn 16, Issue 6, 2014, Pages 535-546

  Nam, Hyun Ja ^a   Van Deursen, Jan M ^a,b  

^a Mayo Clinic   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA A KINASE; CYCLIN B1; CYCLIN B2; POLO LIKE KINASE 1; PROTEIN P53; SEPARASE; AURKA PROTEIN, MOUSE; CCNB1 PROTEIN, MOUSE; CCNB2 PROTEIN, MOUSE; CELL CYCLE PROTEIN; ONCOPROTEIN; PHOTOPROTEIN; POLO-LIKE KINASE 1; PROTEIN SERINE THREONINE KINASE;

ANAPHASE; ANEUPLOIDY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL CYCLE G2 PHASE; CENTROSOME; CHROMOSOME SEGREGATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; LIVER ADENOMA; LUNG ADENOMA; LYMPHOMA; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; 129 MOUSE; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL TRANSFORMATION; CHROMOSOME ABERRATION; FEMALE; GENETIC TRANSFECTION; GENETICS; INTESTINE TUMOR; MALE; METABOLISM; PATHOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME; TUMOR SUPPRESSOR GENE;

MUS MUSCULUS;

ANEUPLOIDY; ANIMALS; AURORA KINASE A; CELL CYCLE PROTEINS; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CENTROSOME; CHROMOSOME ABERRATIONS; CHROMOSOME SEGREGATION; CYCLIN B1; CYCLIN B2; FEMALE; GENES, APC; INTESTINAL NEOPLASMS; LUMINESCENT PROTEINS; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; RNA INTERFERENCE; SEPARASE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84901766653     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2952     Document Type: Article

References (66)

1. Holland, A. J. & Cleveland, D. W. Losing balance: The origin and impact of aneuploidy in cancer. EMBO Rep. 13, 501-514 (2012).
2. Pfau, S. J. & Amon, A. Chromosomal instability and aneuploidy in cancer: From yeast to man. EMBO Rep. 13, 515-527 (2012).
3. Schvartzman, J. M., Sotillo, R. & Benezra, R. Mitotic chromosomal instability and cancer: Mouse modelling of the human disease. Nat. Rev. Cancer 10, 102-115 (2010).
4. Stirling, P. C. et al. The complete spectrum of yeast chromosome instability genes identifies candidate CIN cancer genes and functional roles for ASTRA complex components. PLoS Genet. 7, e1002057 (2011).
5. McGranahan, N., Burrell, R. A., Endesfelder, D., Novelli, M. R. & Swanton, C. Cancer chromosomal instability: Therapeutic and diagnostic challenges. EMBO Rep. 13, 528-538 (2012).
6. Ricke, R. M. & van Deursen, J. M. Aneuploidy in health, disease and aging. J. Cell Biol. 201, 11-21 (2013).
7. Glinsky, G. V., Berezovska, O. & Glinskii, A. B. Microarray analysis identifies a death-from-cancer signature predicting therapy failure in patients with multiple types of cancer. J. Clin. Invest. 115, 1503-1521 (2005). (Pubitemid 40814659)
8. Parris, T. Z. et al. Clinical implications of gene dosage and gene expression patterns in diploid breast carcinoma. Clin. Cancer Res. 16, 3860-3874 (2010).
9. Nakagawa, T. et al. A tissue biomarker panel predicting systemic progression after PSA recurrence post-definitive prostate cancer therapy. PLoS One 3, e2318 (2008).
10. Carter, S. L., Eklund, A. C., Kohane, I. S., Harris, L. N. & Szallasi, Z. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat. Genet. 38, 1043-1048 (2006). (Pubitemid 44325930)
11. Chapman, D. L. & Wolgemuth, D. J. Isolation of the murine cyclin B2 cDNA and characterization of the lineage and temporal specificity of expression of the B1 and B2 cyclins during oogenesis, spermatogenesis and early embryogenesis. Development 118, 229-240 (1993) (Pubitemid 23191625)
12. Draviam, V. M., Orrechia, S., Lowe, M., Pardi, R. & Pines, J. The localization of human cyclins B1 and B2 determines CDK1 substrate specificity and neither enzyme requires MEK to disassemble the Golgi apparatus. J. Cell Biol. 152, 945-958 (2001). (Pubitemid 34286071)
13. Pines, J. & Hunter, T. The differential localization of human cyclins A and B is due to a cytoplasmic retention signal in cyclin B. EMBO J. 13, 3772-3781 (1994). (Pubitemid 24275023)
14. Jackman, M., Firth, M. & Pines, J. Human cyclins B1 and B2 are localized to strikingly different structures: B1 to microtubules, B2 primarily to the Golgi apparatus. EMBO J. 14, 1646-1654 (1995).
15. Brandeis, M. et al. Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. Proc. Natl Acad. Sci. USA 95, 4344-4349 (1998).
16. Bailly, E., Pines, J., Hunter, T. & Bornens, M. Cytoplasmic accumulation of cyclin B1 in human cells: association with a detergent-resistant compartment and with the centrosome. J. Cell Sci. 101 (Pt 3), 529-545 (1992).
17. Pines, J. Cyclins: wheels within wheels. Cell Growth Differ. 2, 305-310 (1991).
18. Nigg, E. A. Cellular substrates of p34(cdc2) and its companion cyclin-dependent kinases. Trends Cell Biol. 3, 296-301 (1993). (Pubitemid 23242670)
19. Gavet, O. & Pines, J. Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Dev. Cell 18, 533-543 (2010).
20. Peters, J. M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 7, 644-656 (2006).
21. Spalluto, C., Wilson, D. I. & Hearn, T. Evidence for centriolar satellite localization of CDK1 and cyclin B2. Cell Cycle 12, 1802-1803 (2013).
22. Yoshitome, S., Furuno, N., Hashimoto, E. & Sagata, N. The C-terminal seven amino acids in the cytoplasmic retention signal region of cyclin B2 are required for normal bipolar spindle formation in Xenopus oocytes and embryos. Mol. Cancer Res. 1, 589-597 (2003). (Pubitemid 36706346)
23. Yoshitome, S., Furuno, N. & Sagata, N. Overexpression of the cytoplasmic retention signal region of cyclin B2, but not of cyclin B1, inhibits bipolar spindle formation in Xenopus oocytes. Biol. Cell. 90, 509-518 (1998).
24. Kotani, T., Yoshida, N., Mita, K. & Yamashita, M. Requirement of cyclin B2, but not cyclin B1, for bipolar spindle formation in frog (Rana japonica) oocytes. Mol. Reprod. Dev. 59, 199-208 (2001). (Pubitemid 32391246)
25. Beard, C., Hochedlinger, K., Plath, K., Wutz, A. & Jaenisch, R. Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells. Genesis 44, 23-28 (2006). (Pubitemid 43222207)
26. Hochedlinger, K., Yamada, Y., Beard, C. & Jaenisch, R. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 121, 465-477 (2005). (Pubitemid 40692305)
27. Kumada, K. et al. The selective continued linkage of centromeres from mitosis to interphase in the absence of mammalian separase. J. Cell Biol. 172, 835-846 (2006).
28. Wirth, K.G. et al. Separase: A universal trigger for sister chromatid disjunction but not chromosome cycle progression. J. Cell Biol. 172, 847-860 (2006).
29. Stemmann, O., Zou, H., Gerber, S. A., Gygi, S. P. & Kirschner, M. W. Dual inhibition of sister chromatid separation at metaphase. Cell 107, 715-726 (2001). (Pubitemid 34033665)
30. Kawabata, T. et al. Stalled fork rescue via dormant replication origins in unchallenged S phase promotes proper chromosome segregation and tumor suppression. Mol. Cell 41, 543-553 (2011).
31. Dawlaty, M. M. et al. Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIα. Cell 133, 103-115 (2008). (Pubitemid 351442988)
32. Jeganathan, K., Malureanu, L., Baker, D. J., Abraham, S. C. & van Deursen, J. M. Bub1 mediates cell death in response to chromosome missegregation and acts to suppress spontaneous tumorigenesis. J. Cell Biol. 179, 255-267 (2007). (Pubitemid 350004890)
33. Ganem, N. J., Godinho, S. A. & Pellman, D. A mechanism linking extra centrosomes to chromosomal instability. Nature 460, 278-282 (2009).
34. Silkworth, W. T., Nardi, I. K., Scholl, L. M. & Cimini, D. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLoS One 4, e6564 (2009).
35. Zhang, Y. et al. USP44 regulates centrosome positioning to prevent aneuploidy and suppress tumorigenesis. J. Clin. Invest. 122, 4362-4374 (2012).
36. Kabeche, L. & Compton, D. A. Checkpoint-independent stabilization of kinetochore-microtubule attachments by Mad2 in human cells. Curr. Biol. 22, 638-644 (2012).
37. Silkworth, W. T. & Cimini, D. Transient defects of mitotic spindle geometry and chromosome segregation errors. Cell Div. 7, 19-26 (2012).
38. Bruinsma, W., Raaijmakers, J. A. & Medema, R. H. Switching Polo-like kinase-1 on and off in time and space. Trends Biochem. Sci. 37, 534-542 (2012).
39. Wang, H. et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918 (2013).
40. Smith, E. et al. Differential control of Eg5-dependent centrosome separation by Plk1 and Cdk1. Embo J. 30, 2233-2245 (2011).
41. Chen, Y., Yeh, P. C., Huang, J. C., Yeh, C. C. & Juang, Y. L. The spindle checkpoint protein MAD1 regulates the expression of E-cadherin and prevents cell migration. Oncol. Rep. 27, 487-491 (2012).
42. Macurek, L. et al. Polo-like kinase-1 is activated by aurora A to promote checkpoint recovery. Nature 455, 119-123 (2008).
43. Seki, A., Coppinger, J. A., Jang, C. Y., Yates, J. R. & Fang, G. Bora and the kinase Aurora a cooperatively activate the kinase Plk1 and control mitotic entry. Science 320, 1655-1658 (2008). (Pubitemid 351931258)
44. Carmena, M. et al. The chromosomal passenger complex activates Polo kinase at centromeres. PLoS Biol. 10, e1001250 (2012).
45. Kiyomitsu, T. & Cheeseman, I. M. Chromosome-and spindle-pole-derived signals generate an intrinsic code for spindle position and orientation. Nat. Cell Biol. 14, 311-317 (2012).
46. Suijkerbuijk, S. J., Vleugel, M., Teixeira, A. & Kops, G. J. Integration of kinase and phosphatase activities by BUBR1 ensures formation of stable kinetochore-microtubule attachments. Dev. Cell 23, 745-755 (2012).
47. Hahn, W. C. et al. Enumeration of the simian virus 40 early region elements necessary for human cell transformation. Mol. Cell Biol. 22, 2111-2123 (2002). (Pubitemid 34224619)
48. Wu, C. C. et al. p53 negatively regulates Aurora A via both transcriptional and posttranslational regulation. Cell Cycle 11, 3433-3442 (2012).
49. Soria, J. C. et al. Overexpression of cyclin B1 in early-stage non-small cell lung cancer and its clinical implication. Cancer Res. 60, 4000-4004 (2000).
50. Yoshida, T., Tanaka, S., Mogi, A., Shitara, Y. & Kuwano, H. The clinical significance of Cyclin B1 and Wee1 expression in non-small-cell lung cancer. Ann. Oncol.: Official J. Eur. Soc. Med. Oncol./ESMO 15, 252-256 (2004). (Pubitemid 38262624)
51. Cooper, W. A. et al. Expression and prognostic significance of cyclin B1 and cyclin A in non-small cell lung cancer. Histopathology 55, 28-36 (2009).
52. Park, S. H. et al. NF-Y-dependent cyclin B2 expression in colorectal adenocarcinoma. Clin. Cancer Res. 13, 858-867 (2007).
53. Wang, A., Yoshimi, N., Ino, N., Tanaka, T. & Mori, H. Overexpression of cyclin B1 in human colorectal cancers. J. Cancer Res. Clin. Oncol. 123, 124-127 (1997). (Pubitemid 27062538)
54. Sarafan-Vasseur, N. et al. Overexpression of B-type cyclins alters chromosomal segregation. Oncogene 21, 2051-2057 (2002). (Pubitemid 34270893)
55. Dove, W. F. et al. The intestinal epithelium and its neoplasms: genetic, cellular and tissue interactions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 915-923 (1998). (Pubitemid 28314374)
56. Moser, M. J. et al. Genetic instability and hematologic disease risk in Werner syndrome patients and heterozygotes. Cancer Res. 60, 2492-2496 (2000). (Pubitemid 30262443)
57. Babu, J. R. et al. Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J. Cell Biol. 160, 341-353 (2003). (Pubitemid 36182725)
58. Van Ree, J. H., Jeganathan, K. B., Malureanu, L. & van Deursen, J. M. Overexpression of the E2 ubiquitin-conjugating enzyme UbcH10 causes chromosome missegregation and tumor formation. J. Cell Biol. 188, 83-100 (2010).
59. Kasper, L. H. et al. CREB binding protein interacts with nucleoporin-specific FG repeats that activate transcription and mediate NUP98-HOXA9 oncogenicity. Mol. Cell Biol. 19, 764-776 (1999). (Pubitemid 29018477)
60. Hart, P. E., Glantz, J. N., Orth, J. D., Poynter, G. M. & Salisbury, J. L. Testis-specific murine centrin, Cetn1: genomic characterization and evidence for retroposition of a gene encoding a centrosome protein. Genomics 60, 111-120 (1999). (Pubitemid 29463669)
61. Baker D. J., Jin, F., Jeganathan, K. B. & van Deursen, J. M. Whole chromosome instability caused by Bub1 insufficiency drives tumorigenesis through tumor suppressor gene loss of heterozygosity. Cancer Cell 16, 475-486 (2009).
62. Jeganathan, K., Malureanu, L., Baker, D. J., Abraham, S. C. & van Deursen, J. M. Bub1 mediates cell death in response to chromosome missegregation and acts to suppress spontaneous tumorigenesis. J. Cell Biol. 179, 255-267 (2007). (Pubitemid 350004890)
63. Malureanu, L. et al. Cdc20 hypomorphic mice fail to counteract de novo synthesis of cyclin B1 in mitosis. J. Cell Biol. 191, 313-329 (2010).
64. Sakaue-Sawano, A. et al. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132, 487-498 (2008). (Pubitemid 351191996)
65. Bakhoum, S. F., Thompson, S. L., Manning, A. L. & Compton, D. A. Genome stability is ensured by temporal control of kinetochore-microtubule dynamics. Nat. Cell Biol. 11, 27-35 (2009).
66. McKenzie, L. et al. p53-dependent repression of polo-like kinase-1 (PLK1). Cell Cycle 9, 4200-4212 (2010).