Cancer Letters
Volume 230, Issue 1 , Pages 6-19 , 8 December 2005

Centrosome amplification, chromosome instability and cancer development

Received 7 December 2004 ,Accepted 15 December 2004.

References 

  1. Foulds L. The experimental study of tumor progression: a review. Cancer Res. 1954;14:327–339
  2. Nowell P. The clonal evolution of tumor cell populations. Science. 1976;194:23–28
  3. Loeb LA. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res. 1991;51:3075–3079
  4. Doxsey S. The centrosome—a tiny organelle with big potential. Nat. Genet. 1998;20:104–106
  5. D'Assoro AB, Lingle WL, Salisbury JL. Centrosome amplification and the development of cancer. Oncogene. 2002;21:6146–6153
  6. Paintrand M, Moudjou M, Delacroix H, Bornens M. Centrosome organization and centriole architecture: their sensitivity to divalent cations. J. Struct. Biol. 1992;108:107–128
  7. Bornens M. Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 2002;14:25–34
  8. Mazia D. The chromosome cycle and the centrosome cycle in the mitotic cycle. Int. Rev. Cytol. 1987;100:49–92
  9. Dulic V, Lees E, Reed SI. Association of human cyclin E with a periodic G1–S phase protein kinase. Science. 1992;257:1958–1961
  10. Koff A, Giordano A, Desai D, Yamashita K, Harper JW, Elledge S, et al. Formation and activation of a cyclin E–cdk2 complex during the G1 phase of the human cell cycle. Science. 1992;257:1689–1694
  11. Harper JW. Cyclin dependent kinase inhibitors. Cancer Surv. 1997;29:91–107
  12. Mussman JG, Horn HF, Carroll PE, Okuda M, Donehower LA, Fukasawa K. Synergistic induction of centrosome hyperamplification by loss of p53 and cyclin E overexpression. Oncogene. 2000;19:1635–1946
  13. Minella AC, Swanger J, Bryant E, Welcker M, Hwang H, Clurman BE. p53 and p21 form an inducible barrier that protects cells against cyclin E–cdk2 deregulation. Curr. Biol. 2002;12:1817–1827
  14. Nevins JR. E2F: a link between the Rb tumor suppressor protein and viral oncoproteins. Science. 1992;258:424–429
  15. Hinchcliffe EH, Li C, Thompson EA, Maller JL, Sluder G. Requirement of Cdk2–cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science. 1999;283:851–854
  16. Lacey KR, Jackson PK, Stearns T. Cyclin-dependent kinase control of centrosome duplication. Proc. Natl Acad. Sci. USA. 1999;96:2817–2822
  17. Matsumoto Y, Hayashi K, Nishida E. Cyclin-dependent kinase 2 (Cdk2) is required for centrosome duplication in mammalian cells. Curr. Biol. 1999;9:429–432
  18. Tarapore P, Okuda M, Fukasawa K. A mammalian in vitro centriole duplication system: evidence for involvement of CDK2/cyclin E and nucleophosmin/B23 in centrosome duplication. Cell Cycle. 2002;1:75–81
  19. Okuda M, Horn HF, Tarapore P, Tokuyama Y, Smulian AG, Chan P-K, et al. Nucleophosmin/B23 is a target of CDK2–cyclin E in centrosome duplication. Cell. 2000;103:127–140
  20. Fisk HA, Winey M. The mouse Mps1p-like kinase regulates centrosome duplication. Cell. 2001;106:95–104
  21. Chen Z, Indjeian VB, McManus M, Wang L, Dynlacht BD. CP110, a cell cycle-dependent CDK substrate, regulates centrosome duplication in human cells. Dev. Cell. 2002;3:339–350
  22. Uetake Y, Sluder G. Cell cycle progression after cleavage failure: mammalian somatic cells do not possess a ‘tetraploidy checkpoint’. J. Cell Biol. 2004;165:609–615
  23. Forgues M, Difilippantonio MJ, Linke SP, Ried T, Nagashima K, Feden J, et al. Involvement of Crm1 in hepatitis B virus X protein-induced aberrant centriole replication and abnormal mitotic spindles. Mol. Cell. Biol. 2003;23:5282–5292
  24. Hut HM, Lemstra W, Blaauw EH, Van Cappellen GW, Kampinga HH, Sibon OC. Centrosomes split in the presence of impaired DNA integrity during mitosis. Mol. Biol. Cell. 2003;14:1993–2004
  25. Khodjakov A, Rieder CL, Sluder G, Cassels G, Sibon O, Wang CL. De novo formation of centrosomes in vertebrate cells arrested during S phase. J. Cell Biol. 2002;158:1171–1181
  26. Gard DL. Organization, nucleation, and acetylation of microtubules in Xenopus laevis oocytes: a study by confocal immunofluorescence microscopy. Dev. Biol. 1991;143:346–362
  27. Pihan GA, Purohit A, Wallace J, Knecht H, Woda B, Quesenberry P, et al. Centrosome defects and genetic instability in malignant tumors. Cancer Res. 1998;58:3974–3985
  28. Carroll PE, Okuda M, Horn HF, Biddinger P, Stambrook PJ, Gleich LL, et al. Centrosome hyperamplification in human cancer: chromosome instability induced by p53 mutation and/or Mdm2 overexpression. Oncogene. 1999;18:1935–1944
  29. Lingle WL, Salisbury JL. Altered centrosome structure is associated with abnormal mitoses in human breast tumors. Am. J. Pathol. 1999;155:1941–1951
  30. Lingle WL, Barrett SL, Negron VC, D'Assoro AB, Boeneman K, Liu W, et al. Centrosome amplification drives chromosomal instability in breast tumor development. Proc. Natl Acad. Sci. USA. 2002;99:1978–1983
  31. Kawamura K, Moriyama M, Shiba N, Ozaki M, Tanaka T, Nojima T, et al. Centrosome hyperamplification and chromosomal instability in bladder cancer. Eur. Urol. 2003;43:505–515
  32. Jiang F, Caraway NP, Sabichi AL, Zhang HZ, Ruitrok A, Grossman HB, et al. Centrosomal abnormality is common in and a potential biomarker for bladder cancer. Int. J. Cancer. 2003;106:661–665
  33. Kawamura K, Izumi H, Ma Z, Ikeda R, Moriyama M, Tanaka T, et al. Induction of centrosome amplification and chromosome instability in human bladder cancer cells by p53 mutation and cyclin E overexpression. Cancer Res. 2004;64:4800–4809
  34. Weber RG, Bridger JM, Benner A, Weisenberger D, Ehemann V, Reifenberger G, et al. Centrosome amplification as a possible mechanism for numerical chromosome aberrations in cerebral primitive neuroectodermal tumors with TP53 mutations. Cytogenet. Cell Genet. 1998;83:266–269
  35. Al-Romaih K, Bayani J, Vorobyova J, Karaskova J, Park PC, Zielenska M, et al. Chromosomal instability in osteosarcoma and its association with centrosome abnormalities. Cancer Genet. Cytogenet. 2003;144:91–99
  36. Gisselsson D, Palsson E, Yu C, Mertens F, Mandahl N. Mitotic instability associated with late genomic changes in bone and soft tissue tumours. Cancer Lett. 2004;206:69–76
  37. Nakajima T, Moriguchi M, Mitsumoto Y, Sekoguchi S, Nishikawa T, Takashima H, et al. Centrosome aberration accompanied with p53 mutation can induce genetic instability in hepatocellular carcinoma. Mod. Pathol. 2004;17:722–727
  38. Pihan GA, Purohit A, Wallace J, Malhotra R, Liotta L, Doxsey SJ. Centrosome defects can account for cellular and genetic changes that characterize prostate cancer progression. Cancer Res. 2001;61:2212–2219
  39. Sato N, Mizumoto K, Nakamura M, Nakamura K, Kusumoto M, Niiyama H, et al. Centrosome abnormalities in pancreatic ductal carcinoma. Clin. Cancer Res. 1999;5:963–970
  40. L.C. Hsu, M. Kapali, J.A. Deloia, H.H. Gallion, Centrosome abnormalities in ovarian cancer, Int. J. Cancer 113 (2005) 746–751.
  41. Mayer F, Stoop H, Sen S, Bokemeyer C, Oosterhuis JW, Looijenga LH. Aneuploidy of human testicular germ cell tumors is associated with amplification of centrosomes. Oncogene. 2003;22:3859–3866
  42. Skyldberg B, Fujioka K, Hellstrom AC, Sylven L, Moberger B, Auer G. Human papillomavirus infection, centrosome aberration, and genetic stability in cervical lesions. Mod. Pathol. 2001;14:279–284
  43. Kuo KK, Sato N, Mizumoto K, Maehara N, Yonemasu H, Ker CG, et al. Centrosome abnormalities in human carcinomas of the gallbladder and intrahepatic and extrahepatic bile ducts. Hepatology. 2000;31:59–64
  44. Roshani L, Fujioka K, Auer G, Kjellman M, Lagercrantz S, Larsson C. Aberrations of centrosomes in adrenocortical tumors. Int. J. Oncol. 2002;20:1161–1165
  45. Gustafson LM, Gleich LL, Fukasawa K, Chadwell J, Miller MA, Stambrook PJ, et al. Centrosome hyperamplification in head and neck squamous cell carcinoma: a potential phenotypic marker of tumor aggressiveness. Laryngoscope. 2000;110:1798–1801
  46. Neben K, Tews B, Wrobel G, Hahn M, Kokocinski F, Giesecke C, et al. Gene expression patterns in acute myeloid leukemia correlate with centrosome aberrations and numerical chromosome changes. Oncogene. 2004;23:2379–2384
  47. Neben K, Giesecke C, Schweizer S, Ho AD, Kramer A. Centrosome aberrations in acute myeloid leukemia are correlated with cytogenetic risk profile. Blood. 2003;23:2379–2384(Epub 2002 Jun 28)
  48. Kramer A, Schweizer S, Neben K, Giesecke C, Kalla J, Katzenberger T, et al. Centrosome aberrations as a possible mechanism for chromosomal instability in non-Hodgkin's lymphoma. Leukemia. 2003;17:2207–2213
  49. Fukasawa K, Choi T, Kuriyama R, Rulong S, Vande Woude GF. Abnormal amplification of centrosomes and genetic instability in the absence of p53. Science. 1996;271:1744–1747
  50. Fukasawa K, Wiener F, Vande Woude GF, Mai S. Genome destabilization by the loss of p53 and c-Myc overexpression. Oncogene. 1997;15:1295–1302
  51. Balczon R, Bao L, Zimmer WE, Brown K, Zinkowski RP, Brinkley BR. Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells. J. Cell Biol. 1995;130:105–115
  52. Tarapore P, Horn HF, Tokuyama Y, Fukasawa K. Direct regulation of the centrosome duplication cycle by the p53–p21Waf1/Cip1 pathway. Oncogene. 2001;20:3173–3184
  53. Nayak BK, Das GM. Stabilization of p53 and transactivation of its target genes in response to replication blockade. Oncogene. 2002;21:7226–7229
  54. C. Wong, T. Stearns, Centrosome number is controlled by a centrosome-intrinsic block to re-duplication, Nat. Cell Biol. 5 (2003) 539–544.
  55. Wang XJ, Greenhalgh DA, Jiang A, He D, Zhong L, Brinkley BR, et al. Analysis of centrosome abnormalities and angiogenesis in epidermal-targeted p53 172H mutant and p53-knockout mice after chemical carcinogenesis: evidence for a gain of function. Mol. Carcinog. 1998;23:185–192
  56. Duensing S, Lee LY, Duensing A, Basile J, Piboonniyom S, Gonzalez S, et al. The human papillomavirus type 16 E6 and E7 oncoproteins cooperate to induce mitotic defects and genomic instability by uncoupling centrosome duplication from the cell division cycle. Proc. Natl Acad. Sci. USA. 2000;97:10002–10007
  57. Bunz F, Fauth C, Speicher MR, Dutriaux A, Sedivy JM, Kinzler KW, et al. Targeted inactivation of p53 in human cells does not result in aneuploidy. Cancer Res. 2002;62:1129–1133
  58. Botz J, Zerfass-Thome K, Spitkovsky D, Delius H, Vogt B, Eilers M, et al. Cell cycle regulation of the murine cyclin E gene depends on an E2F binding site in the promoter. Mol. Cell. Biol. 1996;16:3401–3409
  59. Ekholm SV, Zickert P, Reed SI, Zetterberg A. Accumulation of cyclin E is not a prerequisite for passage through the restriction point. Mol. Cell. Biol. 2001;21:3256–3265
  60. Keyomarsi K, Herliczek TW. The role of cyclin E in cell proliferation, development and cancer. Prog. Cell Cycle Res. 1997;3:171–191
  61. Karakaidos P, Taraviras S, Vassiliou LV, Zacharatos P, Kastrinakis NG, Kougiou D, et al. Overexpression of the replication licensing regulators hCdt1 and hCdc6 characterizes a subset of non-small-cell lung carcinomas: synergistic effect with mutant p53 on tumor growth and chromosomal instability—evidence of E2F-1 transcriptional control over hCdt1. Am. J. Pathol. 2004;165:1165–1351
  62. Furihata M, Ohtsuki Y, Sonobe H, Shuin T, Yamamoto A, Terao N, et al. Prognostic significance of cyclin E and p53 protein overexpression in carcinoma of the renal pelvis and ureter. Br. J. Cancer. 1998;77:783–788
  63. Sakaguchi T, Watanabe A, Sawada H, Yamada Y, Yamashita J, Matsuda M, et al. Prognostic value of cyclin E and p53 expression in gastric carcinoma. Cancer. 1998;82:1238–1243
  64. Miki Y, Swensen J, Shattuck-Eidens D, Futreal PA, Harshman K, Tavtigian S, et al. A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science. 1994;266:66–71
  65. Xu X, Weaver Z, Linke SP, Li C, Gotay J, Wang XW, et al. Centrosome amplification and a defective G2–M cell cycle checkpoint induce genetic instability in BRCA1 exon 11 isoform-deficient cells. Mol. Cell. 1999;3:389–395
  66. Wooster R, Bignell G, Lancaster J, Swift S, Seal S, Mangion J, et al. Identification of the breast cancer susceptibility gene BRCA2. Nature. 1995;378:789–792
  67. Tutt A, Gabriel A, Bertwistle D, Connor F, Paterson H, Peacock J, et al. Absence of Brca2 causes genomic instability by chromosome breakage and loss associated with centrosome amplification. Curr. Biol. 1999;9:1107–1110
  68. Moynahan ME, Chiu JW, Koller BH, Jasin M. Brca1 controls homology-directed DNA repair. Mol. Cell. 1999;4:511–518
  69. Deng CX, Wang RH. Roles of BRCA1 in DNA damage repair: a link between development and cancer. Hum. Mol. Genet. 2003;12:113–123
  70. MacLachlan TK, Takimoto R, El-Deiry WS. BRCA1 directs a selective p53-dependent transcriptional response towards growth arrest and DNA repair targets. Mol. Cell. Biol. 2002;22:4280–4292
  71. Welcsh PL, Lee MK, Gonzalez-Hernandez RM, Black DJ, Mahadevappa M, Swisher EM, et al. BRCA1 transcriptionally regulates genes involved in breast tumorigenesis. Proc. Natl Acad. Sci. USA. 2002;99:7560–7565
  72. Bochar DA, Wang L, Beniya H, Kinev A, Xue Y, Lane WS, et al. BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell. 2000;21:257–265
  73. Baer R, Ludwig T. The BRCA1/BARD1 heterodimer, a tumor suppressor complex with ubiquitin E3 ligase activity. Curr. Opin. Genet. Dev. 2002;12:86–91
  74. Kerr P, Ashworth A. New complexities for BRCA1 and BRCA2. Curr. Biol. 2001;11:668–676
  75. Moynahan MH. The cancer connection: BRCA1 and BRCA2 tumor suppression in mice and humans. Oncogene. 2002;21:8994–9007
  76. Mizuta R, LaSalle JM, Cheng HL, Shinohara A, Ogawa H, Copeland N, et al. RAB22 and RAB163/mouse BRCA2: proteins that specifically interact with the RAD51 protein. Proc. Natl Acad. Sci. USA. 1997;94:6927–6932
  77. Scully R, Chen J, Plug A, Xiao Y, Weaver D, Feunteun J, et al. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell. 1997;88:265–275
  78. Sharan SK, Morimatsu M, Albrecht U, Lim DS, Regel E, Dinh C, et al. Embryonic lethality and radiation hypersensitivity mediated by Rad51 in mice lacking Brca2. Nature. 1997;386:804–810
  79. Wong AK, Pero R, Ormonde PA, Tavtigian SV, Bartel PL. RAD51 interacts with the evolutionarily conserved BRC motifs in the human breast cancer susceptibility gene brca2. J. Biol. Chem. 1997;272:31941–31944
  80. Baumann P, Benson FE, West SC. Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell. 1996;87:757–766
  81. Bertrand P, Lambert S, Joubert C, Lopez BS. Overexpression of mammalian Rad51 does not stimulate tumorigenesis while a dominant-negative Rad51 affects centrosome fragmentation, ploidy and stimulates tumorigenesis, in p53-defective CHO cells. Oncogene. 2003;22:7587–7592
  82. Dodson H, Bourke E, Jeffers LJ, Vagnarelli P, Sonoda E, Takeda S, et al. Centrosome amplification induced by DNA damage occurs during a prolonged G2 phase and involves ATM. Eur. Mol. Biol. Org. J. 2004;23:3864–3873
  83. Deans B, Griffin CS, O'Regan P, Jasin M, Thacker J. Homologous recombination deficiency leads to profound genetic instability in cells derived from Xrcc2-knockout mice. Cancer Res. 2003;63:8181–8187
  84. Sato N, Mizumoto K, Nakamura M, Tanaka M. adiation-induced centrosome overduplication and multiple mitotic spindles in human tumor cells. Exp. Cell Res. 2000;255:321–326
  85. Heim S, Mandahl N, Mitelman F. Genetic convergence and divergence in tumor progression. Cancer Res. 1988;48:5911–5916
  86. Chiba S, Okuda M, Mussman JG, Fukasawa K. Genomic convergence and suppression of centrosome hyperamplification in primary p53−/− cells in prolonged culture. Exp. Cell Res. 2000;258:310–321
  87. Ring D, Hubble R, Kirschner M. Mitosis in a cell with multiple centrioles. J. Cell Biol. 1982;94:549–556
  88. Bennet RA, Izumi H, Fukasawa K. Induction of centrosome amplification and chromosome instability in p53-null cells by transient exposure to sub-toxic levels of S-phase targeting anti-cancer drugs. Oncogene. 2004;23:6823–6829

PII: S0304-3835(04)00988-7

doi: 10.1016/j.canlet.2004.12.028

Cancer Letters
Volume 230, Issue 1 , Pages 6-19 , 8 December 2005

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