Centrosomes, genomic instability, and cervical carcinogenesis

Critical Reviews in Eukaryotic Gene Expression

Volumn 13, Issue 1, 2003, Pages 9-23

  Duensing, Stefan ^a   Münger, Karl ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Centrosomes; Cervical cancer; E6 and E7 oncoproteins; Genomic instability; Human papillomaviruses; p53; pRB

Indexed keywords

ONCOPROTEIN; PROTEIN P53;

ANEUPLOIDY; CANCER RISK; CELL DIVISION; CENTROSOME; CHROMOSOME ABERRATION; CHROMOSOME SEGREGATION; GENE DUPLICATION; GENETIC SELECTION; HIGH RISK PATIENT; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; STEM CELL; TUMOR SUPPRESSOR GENE; UTERINE CERVIX CARCINOMA; VIRUS CELL INTERACTION;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; CELL TRANSFORMATION, VIRAL; CENTROSOME; CHROMOSOMAL INSTABILITY; FEMALE; HUMANS; MODELS, GENETIC; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; TUMOR SUPPRESSOR PROTEIN P53; UTERINE CERVICAL NEOPLASMS;

HUMAN PAPILLOMAVIRUS; PAPILLOMAVIRUS;

EID: 10744229405     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukaryotGeneExpr.v13.i1.20     Document Type: Review

References (106)

1. Amon A (1999): The spindle checkpoint. Curr Opin Genet Dev 9:69-75.
2. Baksch C, Wagenbach N, Nonn M, Leistritz S, Stanbridge E, Schneider A, Dürst M (2001): Microcell-mediated transfer of chromosome 4 into Hela cells suppresses telomerase activity. Genes Chromosomes Cancer 31:196-198.
3. Balczon R, Bao L, Zimmer WE, Brown K, Zinkowski RP, Brinkley BR (1995): Dissociation of centrosome replication events from cycles of DNA synthesis and mitotic division in hydroxyurea-arrested Chinese hamster ovary cells. J Cell Biol 130:105-115.
4. Bardelli A, Cahill DP, Lederer G, Speicher MR, Kinzler KW, Vogelstein B, Lengauer C (2001): Carcinogen-specific induction of genetic instability. Proc Natl Acad Sci U S A 98:5770-5775.
5. Bibbo M, Dytch HE, Alenghat E, Bartels PH, Wied GL (1989): DNA ploidy profiles as prognostic indicators in CIN lesions. Am J Clin Pathol 92:261-265.
6. Bornens M (2002): Centrosome composition and microtubule anchoring mechanisms. Curr Opin Cell Biol 14: 25-34.
7. Bouckson-Castaing V, Moudjou M, Ferguson DJ, Mucklow S, Belkaid Y, Milon G, Crocker PR (1996): Molecular characterization of ninein, a new coiled-coil protein of the centrosome. J Cell Sci 109:179-190.
8. Boveri T (1914): "Zur Frage der Entstehung maligner Tumoren" Jena: G. Fischer.
9. Boyer SN, Wazer DE, Band V (1996): E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res 56:4620-4624.
10. Brinkley BR (2001): Managing the centrosome numbers game: from chaos to stability in cancer cell division. Trends Cell Biol 11:18-21.
11. Bulten J, Poddighe PJ, Robben JCM, Gemmink JH, de Wilde PCM, Hanselaar AGJM (1998): Interphase cytogenetic analysis of cervical intraepithelial neoplasia. Am J Pathol 152:495-503.
12. Cahill DP, Kinzler KW, Vogelstein B, Lengauer C (1999): Genetic instability and Darwinian selection in tumours. Trends Cell Biol 9:M57-60.
13. Chen Z, Indjeian VB, McManus M, Wang L, Dynlacht BD (2002): CP110, a cell-cycle-dependent cdk substrate, regulates centrosome duplication in human cells. Dev Cell 3:339-350.
14. Coursen JD, Bennett WP, Gollahon L, Shay JW, Harris CC (1997): Genomic instability and telomerase activity in human bronchial epithelial cells during immortalization by human papillomavirus-16 E6 and E7 genes. Exp Cell Res 235:245-253.
15. Crum CP, Ikenberg H, Richart RM, Gissmann L (1984): Human papillomavirus type 16 and early cervical neoplasia. N Engl J Med 310:880-883.
16. Doxsey SJ (2001): Centrosomes as command centres for cellular control. Nat Cell Biol 3:E105-108.
17. Doxsey SJ, Stein P, Evans L, Calarco P, Kirschner M (1994): Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76:639-650.
18. Duensing S, Duensing A, Crum CP, Munger K (2001a): Human papillomavirus type 16 E7 oncoprotein-induced abnormal centrosome synthesis is an early event in the evolving malignant phenotype. Cancer Res 61: 2356-2360.
19. Duensing S, Duensing A, Flores ER, Do A, Lambert PF, Munger K (2001b): Centrosome abnormalities and genomic instability by episomal expression of human papillomavirus type 16 in raft cultures of human keratinocytes. J Virol 75:7712-7716.
20. Duensing S, Lee LY, Duensing A, Basile J, Piboonniyom S, Gonzalez S, Crum CP, Munger K (2000): 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 Nad Acad Sci U S A 97: 10002-10007.
21. Duensing S, Munger K (2001): Centrosome abnormalities, genomic instability and carcinogenic progression. Biochim Biophys Acta 2:M81-88.
22. Duensing S, Münger K (2002a): Human papillomaviruses and centrosome duplication errors: modeling the origins of genomic instability. Oncogene 21:6241-6248.
23. Duensing S, Münger K (2002b): The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res 62:7075-7082.
24. Durst M, Croce CM, Gissmann L, Schwarz E, Huebner K (1987): Papillomavirus sequences integrate near cellular oncogenes in some cervical carcinoma. Proc Natl Acad Sci U S A 84:1070-1074.
25. Fisk HA, Winey M (2001): The mouse Mps1p-like kinase regulates centrosome duplication. Cell 106:95-104.
26. Freed E, Lacey KR, Huie P, Lyapina SA, Deshaies RJ, Steams T, Jackson PK (1999): Components of an SCF ubiquitin ligase localize to the centrosome and regulate the centrosome duplication cycle. Genes Dev 13:2242-2257.
27. Fu YS, Reagan JW, Richart RM (1981): Definition of precursors. Gynecol Oncol 12:S220-S231.
28. Funk JO, Waga S, Harry JB, Espling E, Stillman B, Galloway DA (1997): Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV-16 E7 oncoprotein. Genes Dev 11:2090-2100.
29. Gonzalez SL, Stremlau M, He X, Basile J, Munger K (2001): Degradation of the retinoblastoma tumor suppressor by the human papillomavirus type 16 E7 oncoprotein is important for functional inactivation and is separable from proteasomal degradation of E7. J Virol 75:7583-7591.
30. Hartwell L (1992): Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 71:543-546.
31. Hashida T, Yasumoto S (1991): Induction of chromosome abnormalities in mouse and human epidermal keratinocytes by the human papillomavirus type 16 E7 oncogene. J Gen Virol 72:1569-1577.
32. Hawley-Nelson P, Vousden KH, Hubbert NL, Lowy DR, Schiller JT (1989): HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J 8:3905-3910.
33. Heselmeyer K, Macville M, Schrock E, Blegen H, Hellstrom AC, Shah K, Auer G, Ried T (1997): Advanced-stage cervical carcinomas are defined by a recurrent pattern of chromosomal aberrations revealing high genetic instability and a consistent gain of chromosome arm 3q. Genes Chromosomes Cancer 19:233-240.
34. Heselmeyer K, Schrock E, du Manoir S, Blegen H, Shah K, Steinbeck R, Auer G, Ried T (1996): Gain of chromosome 3q defines the transition from severe dysplasia to invasive carcinoma of the uterine cervix. Proc Natl Acad Sci U S A 93:479-484.
35. Hinchcliffe EH, Li C, Thompson EA, Maller JL, Sluder G (1999): Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283:851-854.
36. Hinchcliffe EH, Sluder G (2001): "It takes two to tango": understanding how centrosome duplication is regulated throughout the cell cycle. Genes Dev 15:1167-1181.
37. Howley PM, Lowy DR (2001): Papillomaviruses and their replication. In DM Knipe, PM Howley (eds): "Fields' Virology." Philadelphia: Lippincott Williams & Wilkins, 2197-2229.
38. Hurlin PJ, Kaur P, Smith PP, Perez-Reyes N, Blanton RA, McDougall JK (1991): Progression of human papillomavirus type 18-immortalized human keratinocytes to a malignant phenotype. Proc Natl Acad Sci U S A 88: 570-574.
39. Job D, Valiron O, Oakley B (2003): Microtubule nucleation. Curr Opin Cell Biol 15:111-117.
40. Johnson DG, Schwarz JK, Cress WD, Nevins JR (1993): Expression of transcription factor E2F1 induces quiescent cells to enter S phase. Nature 365:349-352.
41. Jones DL, Alani RM, Munger K (1997): The human papillomavirus E7 oncoprotein can uncouple cellular differentiation and proliferation in human keratinocytes by abrogating p21Cip1-mediated inhibition of cdk2. Genes Dev 11:2101-2111.
42. Kellogg DR, Moritz M, Alberts BM (1994): The centrosome and cellular organization. Annu Rev Biochem 63:639-674.
43. Kessis TD, Connolly DC, Hedrick L, Cho KR (1996): Expression of HPV16 E6 or E7 increases integration of foreign DNA. Oncogene 13:427-431.
44. Kessis TD, Slebos RJ, Nelson WG, Kastan MB, Plunkett BS, Han SM, Lorincz AT, Hedrick L, Cho KR (1993): Human papillomavirus 16 E6 expression disrupts the p53-mediated cellular response to DNA damage. Proc Natl Acad Sci U S A 90:3988-3992.
45. Klimov E, Vinokourova S, Moisjak E, Rakhmanaliev E, Kobseva V, Laimins L, Kisseljov F, Sulimova G (2003): Human papilloma viruses and cervical tumours: mapping of integration sites and analysis of adjacent cellular sequences. BMC Cancer 2:24-32.
46. Klingelhutz AJ, Foster SA, McDougall JK (1996): Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 380:79-82.
47. Koi M, Morita H, Yamada H, Satoh H, Barrett JC, Oshimura M (1989): Normal human chromosome 11 suppresses tumorigenicity of human cervical tumor cell line SiHa. Mol Carcinogen 2:12-21.
48. Lacey KR, Jackson PK, Stearns T (1999): Cyclin-dependent kinase control of centrosome duplication. Proc Natl Acad Sci U S A 96:2817-2822.
49. Lambert JD, Nagy LM (2002): Asymmetric inheritance of centrosomally localized mRNAs during embryonic cleavages. Nature 420:682-686.
50. Li Q, Dang CV (1999): c-Myc overexpression uncouples DNA replication from mitosis. Mol Cell Biol 19: 5339-5351.
51. Lingle WL, Barrett SL, Negron VC, D'Assoro AB, Boeneman K, Liu W, Whitehead CM, Reynolds C, Salisbury JL (2002): Centrosome amplification drives chromosomal instability in breast tumor development. Proc Natl Acad Sci U S A 99:1978-1983.
52. Lowy DR, Howley PM (2001): Papillomaviruses. In DM Knipe, P M Howley (eds): "Fields' Virology." Philadelphia: Lippincott Williams & Wilkens, 2231-2264.
53. Mailand N, Lukas C, Kaiser BK, Jackson PK, Bartek J, Lukas J (2002): Deregulated human Cdc14A phosphatase disrupts centrosome separation and chromosome segregation. Nat Cell Biol 4:318-322.
54. Martin LG, Demers GW, Galloway DA (1998): Disruption of the G1/S transition in human papillomavirus type 16 E7-expressing human cells is associated with altered regulation of cyclin E. J Virol 72:975-985.
55. Matsumoto Y, Hayashi K, Nishida E (1999): Cyclin-dependent kinase 2 (Cdk2) is required for centrosome duplication in mammalian cells. Curr Biol 9:429-432.
56. Matsumoto Y, Maller JL (2002): Calcium, calmodulin, and CaMKII requirement for initiation of centrosome duplication in Xenopus egg extracts. Science 295: 499-502.
57. McClintock B (1940): The stability of broken ends of chromosomes in Zea mays. Genetics 26:234-282.
58. Meraldi P, Honda R, Nigg EA (2002): Aurora-A overexpression reveals tetraploidization as a major route to centrosome amplification in p53-/- cells. EMBO J 21:483-492.
59. Meraldi P, Lukas J, Fry AM, Bartek J, Nigg EA (1999): Centrosome duplication in mammalian somatic cells requires E2F and Cdk2-cyclin A. Nat Cell Biol 1:88-93.
60. Meraldi P, Nigg EA (2002): The centrosome cycle. FEBS Lett 521:9-13.
61. Minella AC, Swanger J, Bryant E, Welcker M, Hwang H, Clurman BE (2002): p53 and p21 form an inducible barrier that protects cells against cyclin E-cdk2 deregulation. Curr Biol 12:1817-1827.
62. Mitelman F, Johansson B, Mertens F (2003): Mitelman Database of Chromosome Aberrations in Cancer. http://cgap.nci.nih.gov/Chromosomes/Mitelman
63. Muller H, Bracken AP, Vernell R, Moroni MC, Christians F, Grassili E, Prosperini E, Vigo E, Oliner JD, Helin K (2001): E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis. Genes Dev 15:267-285.
64. Munger K (2002): The role of human papillomaviruses in human cancers. Front Biosci 7:641-649.
65. Munger K, Basile JR, Duensing S, Eichten A, Gonzalez SL, Grace M, Zacny VL (2001): Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 20:7888-7898.
66. Munger K, Phelps WC, Bubb V, Howley PM, Schlegel R (1989): The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J Virol 63:4417-4421.
67. Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, Snijders PJF, Meijer CJLM (2003): Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 348:518-527.
68. Nevins JR, Vogt PK (1996): Cell transformation by viruses. In Fields BN, Knipe DM, Howley PM, et al. (eds): "Fields' Virology." Philadelphia: Lippincott-Raven, 301-343.
69. Nigg EA (2002): Centrosome aberrations: cause or consequence of cancer progression? Nat Rev Cancer 2:1-11.
70. O'Connell KF, Caron C, Kopish KR, Hurd DD, Kemphues KJ, Li Y, White JG (2001): The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo. Cell 105:547-558.
71. Okuda M, Horn HF, Tarapore P, Tokuyama Y, Smulian AG, Chan PK, Knudsen ES, Hofmann IA, Snyder JD, Bove KE, Fukasawa K (2000): Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication. Cell 103:127-140.
72. Piboonniyom S, Duensing S, Swilling NW, Hasskarl J, Hinds PW, Munger K (2003): Abrogation of the retinoblastoma tumor suppressor checkpoint during keratinocyte immortalization is not sufficient for induction of centrosome-mediated genomic instability. Cancer Res 63:476-483.
73. Pihan GA, Doxsey SJ (1999): The mitotic machinery as a source of genetic instability in cancer. Sem Cancer Biol 9:289-302.
74. Pihan GA, Purohit A, Wallace J, Knecht H, Woda B, Quesenberry P, Doxsey SJ (1998): Centrosome defects and genetic instability in malignant tumors. Cancer Res 58:3974-3985.
75. Plug-Demaggio AW, McDougall JK (2002): The human papillomavirus type 16 E6 oncogene induces premature mitotic chromosome segregation. Oncogene 21: 7507-7513.
76. Reid R, Crum CP, Herschman BR, Fu YS, Braun L, Shah KV, Agronow SJ, Stanhope CR (1984): Genital warts and cervical cancer. III. Subclinical papillomaviral infection and cervical neoplasia are linked by a spectrum of continuous morphologic and biologic change. Cancer 53:943-953.
77. Ren B, Cam H, Takahashi Y, Volkert T, Terragni J, Young RA, Dynlacht BD (2002): E2F integrates cell cycle progression with DNA repair, replication, and G2/M checkpoints. Genes Dev 16:245-256.
78. Rihet S, Lorenzato M, Clavel C (1996): Oncogenic human papillomaviruses and ploidy in cervical lesions. J Clin Pathol 49:892-896.
79. Rodriguez JA, Barros F, Carracedo A, Mugica-van Herckenrode CM (1998): Low incidence of microsatellite instability in patients with cervical carcinomas. Diagn Mol Pathol 7:276-282.
80. Salisbury JL (2003): Centrosomes: coiled-coils organize the cell center. Curr Biol 13:R88-R90.
81. Salisbury JL, Suino KM, Busby R, Springett M (2002): Centrin-2 is required for centriole duplication in mammalian cells. Curr Biol 12:1287-1292.
82. Salisbury JL, Whitehead CM, Lingle WL, Barrett SL (1999): Centrosomes and cancer. Biol Cell 91:451-460.
83. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM (1990): The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63:1129-1136.
84. Schulze A, Mannhardt B, Zerfass-Thome K, Zwerschke W, Jansen-Durr P (1998): Anchorage-independent transcription of the cyclin A gene induced by the E7 oncoprotein of human papillomavirus type 16. J Virol 72:2323-2334.
85. Shih IM, Zhou W, Goodman SN, Lengauer C, Kinzler KW, Vogelstein B (2001): Evidence that genetic instability occurs at an early stage of colorectal tumorigenesis. Cancer Res 61:818-822.
86. Sibon OC, Kelkar A, Lemstra W, Theurkauf WE (2000): DNA-replication/DNA-damage-dependent centrosome inactivation in Drosophila embryos. Nat Cell Biol 2:90-95.
87. Skyldberg B, Fujioka K, Hellstrom AC, Sylven L, Moberger B, Auer G (2001): Human papillomavirus infection, centrosome aberration, and genetic stability in cervical lesions. Mod Pathol 14:279-284.
88. Solinas-Toldo S, Durst M, Lichter P (1997): Specific chromosomal imbalances in human papillomavirus-transfected cells during progression toward immortality. Proc Natl Acad Sci U S A 94:3854-3859.
89. Southern SA, Evans MF, Herrington CS (1997): Basal cell tetrasomy in low-grade cervical squamous intraepithelial lesions infected with high-risk human papillomaviruses. Cancer Res 57:4210-4213.
90. Southern SA, Noya F, Meyers C, Broker TR, Chow LT, Herrington CS (2001): Tetrasomy is induced by human papillomavirus type 18 E7 gene expression in keratinocyte raft cultures. Cancer Res 61:4858-4863.
91. Stanbridge EJ (1988): Genetic analysis of human malignancies using somatic cell hybrids and monochromosome transfer. Cancer Surv 7:317-324.
92. Steinbeck RG (1997): Proliferation and DNA aneuploidy in mild dysplasia imply early steps of cervical carcinogenesis. Acta Oncol 36:3-12.
93. Thomas JT, Laimins LA (1998): Human papillomavirus oncoproteins E6 and E7 independently abrogate the mitotic spindle checkpoint. J Virol 72:1131-1137.
94. Thompson DA, Belinsky G, Chang TH,Jones DL, Schlegel R, Munger K (1997): The human papillomavirus-16 E6 oncoprotein decreases the vigilance of mitotic check-points. Oncogene 15:3025-3035.
95. Tindle RW (2002): Immune evasion in human papillomavirus-associated cervical cancer. Nat Rev Cancer 2:1-7.
96. Tlsty TD, Briot A, Gualberto A, Hall I, Hess S, Hixon M, Kuppuswamy D, Romanov S, Sage M, White A (1995): Genomic instability and cancer. Mutation Res 337:1-7.
97. Uejima H, Mitsuya K, Kugoh H, Horikawa I, Oshimura M (1995): Normal chromosome 2 induces cellular senescence in the cervical carcinoma cell line SiHa. Genes Chromosomes Cancer 14:120-127.
98. Urbani L, Stearns T (1999): The centrosome. Curr Biol 9:R315-317.
99. Vafa O, Wade M, Kern S, Beeche M, Pandita TK, Hampton GM, Wahl GM (2002): c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell 9:1031-1044.
100. White AE, Livanos EM, Tlsty TD (1994): Differential disruption of genomic integrity and cell cycle regulation in normal human fibroblasts by the HPV oncoproteins. Genes Dev 8:666-677.
101. WHO (1995): "Human papillomaviruses." IARC Monographs on the evaluation of carcinogenic risks to humans, Vol. 64. IARC Press, Lyon, France.
102. Xiong Y, Kuppuswamy D, Li Y, Livanos EM, Hixon M, White A, Beach D, Tlsty TD (1996): Alteration of cell cycle kinase complexes in human papillomavirus E6 and E7-expressing fibroblasts precedes neoplastic transformation. J Virol 70:999-1008.
103. Zerfass K, Schulze A, Spitkovsky D, Friedman V, Henglein B, Jansen-Durr P (1995): Sequential activation of cyclin E and cyclin A gene expression by human papillomavirus type 16 E7 through sequences necessary for transformation. J Virol 69:6389-6399.
104. Zerfass-Thome K, Zwerschke W, Mannhardt B, Tindle R, Botz JW, Jansen-Durr P (1996): Inactivation of the cdk inhibitor p27KIP1 by the human papillomavirus type 16 E7 oncoprotein. Oncogene 13:2323-2330.
105. zur Hausen H (1991): Viruses in human cancers. Science 254:1167-1173.
106. zur Hausen H (2002): Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342-350.