Human papillomavirus E7 induces rereplication in response to DNA damage

Journal of Virology

Volumn 87, Issue 2, 2013, Pages 1200-1210

  Fan, Xueli ^a   Liu, Yingwang ^a   Heilman, Susan A ^a   Chen, Jason J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLEOMYCIN; CISPLATIN; PROTEIN E7; PROTEIN TYROSINE PHOSPHATASE; REPLICATION LICENSING FACTOR CDT1; SMALL INTERFERING RNA;

ARTICLE; CANCER CELL; CDT1 GENE; CONTROLLED STUDY; DNA CONTENT; DNA DAMAGE; DNA REPLICATION; DNA REREPLICATION; DOWN REGULATION; ENDOREDUPLICATION; FEMALE; G2 PHASE CELL CYCLE CHECKPOINT; GENE; GENE EXPRESSION REGULATION; GENE SILENCING; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS 16 E7 GENE; KERATINOCYTE; MITOSIS; MOLECULAR DYNAMICS; NONHUMAN; ONCOGENE; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA INTERFERENCE; STEADY STATE; UPREGULATION; VIRUS CARCINOGENESIS; VIRUS GENOME;

CELL CYCLE PROTEINS; CELLS, CULTURED; DNA DAMAGE; DNA REPLICATION; FEMALE; GENE EXPRESSION; GENOMIC INSTABILITY; HUMAN PAPILLOMAVIRUS 16; HUMANS; PAPILLOMAVIRUS E7 PROTEINS; POLYPLOIDY; UP-REGULATION;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 84871942644     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02038-12     Document Type: Article

References (61)

1. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144:646-674.
2. Duelli DM, Padilla-Nash HM, Berman D, Murphy KM, Ried T, Lazeb-nik Y. 2007. A virus causes cancer by inducing massive chromosomal instability through cell fusion. Curr. Biol. 17:431-437.
3. Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D. 2005. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437:1043-1047.
4. Giannoudis A, Herrington CS. 2000. Differential expression of p53 and p21 in low grade cervical squamous intraepithelial lesions infected with low, intermediate, and high risk human papillomaviruses. Cancer 89: 1300-1307.
5. Olaharski AJ, Sotelo R, Solorza-Luna G, Gonsebatt ME, Guzman P, Mohar A, Eastmond DA. 2006. Tetraploidy and chromosomal instability are early events during cervical carcinogenesis. Carcinogenesis 27:337-343.
6. Porter AC. 2008. Preventing DNA over-replication: a Cdk perspective. Cell Div. 3:3.
7. Mariani BD, Schimke RT. 1984. Gene amplification in a single cell cycle in Chinese hamster ovary cells. J. Biol. Chem. 259:1901-1910.
8. Davidson IF, Li A, Blow JJ. 2006. Deregulated replication licensing causes DNA fragmentation consistent with head-to-tail fork collision. Mol. Cell 24:433-443.
9. Vaziri C, Saxena S, Jeon Y, Lee C, Murata K, Machida Y, Wagle N, Hwang DS, Dutta A. 2003. A p53-dependent checkpoint pathway prevents rereplication. Mol. Cell 11:997-1008.
10. Zhu W, Dutta A. 2006. An ATR-and BRCA1-mediated Fanconi anemia pathway is required for activating the G2/M checkpoint andDNAdamage repair upon rereplication. Mol. Cell. Biol. 26:4601-4611.
11. zur Hausen H. 2002. Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer 2:342-350.
12. Alvarez-Salas LM, Cullinan AE, Siwkowski A, Hampel A, DiPaolo JA. 1998. Inhibition of HPV-16 E6/E7 immortalization of normal keratinocytes by hairpin ribozymes. Proc. Natl. Acad. Sci. U. S. A. 95:1189-1194.
13. Chen JJ. 2010. Genomic instability induced by human papillomavirus oncogenes. N. Am. J. Med. Sci. 3(2):43-47.
14. Wentzensen N, Vinokurova S, von Knebel Doeberitz M. 2004. Systematic review of genomic integration sites of human papillomavirus genomes in epithelial dysplasia and invasive cancer of the female lower genital tract. Cancer Res. 64:3878-3884.
15. Hartwell LH, Kastan MB. 1994. Cell cycle control and cancer. Science 266:1821-1828.
16. Lanni JS, Jacks T. 1998. Characterization of the p53-dependent postmitotic checkpoint following spindle disruption. Mol. Cell. Biol. 18:1055-1064.
17. Sherr CJ, Roberts JM. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1501-1512.
18. Stewart ZA, Pietenpol JA. 2001. p53 signaling and cell cycle checkpoints. Chem. Res. Toxicol. 14:243-263.
19. Helt AM, Galloway DA. 2001. Destabilization of the retinoblastoma tumor suppressor by human papillomavirus type 16 E7 is not sufficient to overcome cell cycle arrest in human keratinocytes. J. Virol. 75:673-6747.
20. Damelin M, Bestor TH. 2007. The decatenation checkpoint. Br. J. Cancer 96:201-205.
21. Gewirtz DA. 1999. A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem. Pharmacol. 57:727-741.
22. Polager S, Ginsberg D. 2003. E2F mediates sustained G2 arrest and downregulation of Stathmin and AIM-1 expression in response to genotoxic stress. J. Biol. Chem. 278:1443-1449.
23. Thompson DA, Belinsky G, Chang TH, Jones DL, Schlegel R, Munger K. 1997. The human papillomavirus-16 E6 oncoprotein decreases the vigilance of mitotic checkpoints. Oncogene 15:3025-3035.
24. Spardy N, Covella K, Cha E, Hoskins EE, Wells SI, Duensing A, Duensing S. 2009. Human papillomavirus 16 E7 oncoprotein attenuates DNAdamage checkpoint control by increasing the proteolytic turnover of claspin. Cancer Res. 69:7022-7029.
25. Heilman SA, Nordberg JJ, Liu Y, Sluder G, Chen JJ. 2009. Abrogation of the postmitotic checkpoint contributes to polyploidization in human papillomavirus E7-expressing cells. J. Virol. 83:2756-2764.
26. Liu Y, Heilman SA, Illanes D, Sluder G, Chen JJ. 2007. p53-independent abrogation of a postmitotic checkpoint contributes to HPV E6-induced polyploidy. Cancer Res. 67:2603-2610.
27. Berger KL, Barriga F, Lace MJ, Turek LP, Zamba GJ, Domann FE, Lee JH, Klingelhutz AJ. 2006. Cervical keratinocytes containing stably replicating extrachromosomal HPV-16 are refractory to transformation by oncogenic H-Ras. Virology 356:68-78.
28. Ballabeni A, Melixetian M, Zamponi R, Masiero L, Marinoni F, Helin K. 2004. Human geminin promotes pre-RC formation and DNA replication by stabilizing CDT1 in mitosis. EMBO J. 23:3122-3132.
29. Nevis KR, Cordeiro-Stone M, Cook JG. 2009. Origin licensing and p53 status regulate Cdk2 activity during G(1). Cell Cycle 8:1952-1963.
30. Chen J, Stubbe J. 2005. Bleomycins: towards better therapeutics. Nat. Rev. 5:102-112.
31. Banerjee NS, Wang HK, Broker TR, Chow LT. 2011. Human papillomavirus (HPV) E7 induces prolonged G2 following S phase reentry in differentiated human keratinocytes. J. Biol. Chem. 286:15473-15482.
32. Duensing S, Munger K. 2002. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res. 62:7075-7082.
33. Rogoff HA, Pickering MT, Frame FM, Debatis ME, Sanchez Y, Jones S, Kowalik TF. 2004. Apoptosis associated with deregulated E2F activity is dependent on E2F1 and Atm/Nbs1/Chk2. Mol. Cell. Biol. 24:2968-2977.
34. Lindahl T. 1993. Instability and decay of the primary structure of DNA. Nature 362:709-715.
35. Goto H, Tomono Y, Ajiro K, Kosako H, Fujita M, Sakurai M, Okawa K, Iwamatsu A, Okigaki T, Takahashi T, Inagaki M. 1999. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation. J. Biol. Chem. 274:25543-25549.
36. Dunphy WG, Kumagai A. 1991. The cdc25 protein contains an intrinsic phosphatase activity. Cell 67:189-196.
37. Gautier J, Solomon MJ, Booher RN, Bazan JF, Kirschner MW. 1991. cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2. Cell 67:197-211.
38. Strausfeld U, Labbe JC, Fesquet D, Cavadore JC, Picard A, Sadhu K, Russell P, Doree M. 1991. Dephosphorylation and activation of a p34cdc2/cyclin B complex in vitro by human CDC25 protein. Nature 351:242-245.
39. Peng CY, Graves PR, Thoma RS, Wu Z, Shaw AS, Piwnica-Worms H. 1997. Mitotic and G2 checkpoint control: regulation of 14-3-3 protein binding by phosphorylation of Cdc25C on serine-216. Science 277:1501-1505.
40. Hutchins JR, Clarke PR. 2004. Many fingers on the mitotic trigger: posttranslational regulation of the Cdc25C phosphatase. Cell Cycle 3:41-45.
41. Machida YJ, Dutta A. 2007. The APC/C inhibitor, Emi1, is essential for prevention of rereplication. Genes Dev. 21:184-194.
42. Mihaylov IS, Kondo T, Jones L, Ryzhikov S, Tanaka J, Zheng J, Higa LA, Minamino N, Cooley L, Zhang H. 2002. Control of DNA replication and chromosome ploidy by geminin and cyclin A. Mol. Cell. Biol. 22: 1868-1880.
43. Nishitani H, Sugimoto N, Roukos V, Nakanishi Y, Saijo M, Obuse C, Tsurimoto T, Nakayama KI, Nakayama K, Fujita M, Lygerou Z, Nishimoto T. 2006. Two E3 ubiquitin ligases, SCF-Skp2 and DDB1-Cul4, target human Cdt1 for proteolysis. EMBO J. 25:1126-1136.
44. Yoshida K, Inoue I. 2004. Regulation of geminin and Cdt1 expression by E2F transcription factors. Oncogene 23:3802-3812.
45. Demers GW, Foster SA, Halbert CL, Galloway DA. 1994. Growth arrest by induction of p53 in DNA damaged keratinocytes is bypassed by human papillomavirus 16 E7. Proc. Natl. Acad. Sci. U. S. A. 91:4382-4386.
46. Hickman ES, Picksley SM, Vousden KH. 1994. Cells expressing HPV16 E7 continue cell cycle progression following DNA damage induced p53 activation. Oncogene 9:2177-2181.
47. Slebos RJC, Lee MH, Plunkett BS, Kessis TD, Williams BO, Jacks T, Hedrick L, Kastan MB, Cho KR. 1994. p53-dependent G1 arrest involves pRB-related proteins and is disrupted by the human papillomavirus 16 E7 oncoprotein. Proc. Natl. Acad. Sci. U. S. A. 91:5320-5324.
48. Davy CE, Jackson DJ, Raj K, Peh WL, Southern SA, Das P, Sorathia R, Laskey P, Middleton K, Nakahara T, Wang Q, Masterson PJ, Lambert PF, Cuthill S, Millar JB, Doorbar J. 2005. Human papillomavirus type 16 E1 E4-induced G2 arrest is associated with cytoplasmic retention of active Cdk1/cyclin B1 complexes. J. Virol. 79:3998-4011.
49. Davy C, Doorbar J. 2007. G2/M cell cycle arrest in the life cycle of viruses. Virology 368:219-226.
50. Li G, Park HU, Liang D, Zhao RY. 2010. Cell cycle G2/M arrest through an S phase-dependent mechanism by HIV-1 viral protein R. Retrovirology 7:59.
51. Higa LA, Banks D, Wu M, Kobayashi R, Sun H, Zhang H. 2006. L2DTL/CDT2 interacts with the CUL4/DDB1 complex and PCNA and regulates CDT1 proteolysis in response to DNA damage. Cell Cycle 5:1675-1680.
52. Jin J, Arias EE, Chen J, Harper JW, Walter JC. 2006. A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol. Cell 23:709-721.
53. Li X, Zhao Q, Liao R, Sun P, Wu X. 2003. The SCF(Skp2) ubiquitin ligase complex interacts with the human replication licensing factor Cdt1 and regulates Cdt1 degradation. J. Biol. Chem. 278:30854-30858.
54. Sugimoto N, Kitabayashi I, Osano S, Tatsumi Y, Yugawa T, Narisawa-Saito M, Matsukage A, Kiyono T, Fujita M. 2008. Identification of novel human Cdt1-binding proteins by a proteomics approach: proteolytic regulation by APC/CCdh1. Mol. Biol. Cell 19:1007-1021.
55. Patel D, McCance DJ. 2010. Compromised spindle assembly checkpoint due to altered expression of Ubch10 and Cdc20 in human papillomavirus type 16 E6-and E7-expressing keratinocytes. J. Virol. 84: 10956-10964.
56. Dowen SE, Scott A, Mukherjee G, Stanley MA. 2003. Overexpression of Skp2 in carcinoma of the cervix does not correlate inversely with p27 expression. Int. J. Cancer 105:326-330.
57. Oh KJ, Kalinina A, Wang J, Nakayama K, Nakayama KI, Bagchi S. 2004. The papillomavirus E7 oncoprotein is ubiquitinated by UbcH7 and Cullin 1-and Skp2-containing E3 ligase. J. Virol. 78:5338-5346.
58. Fujita M. 2006. Cdt1 revisited: complex and tight regulation during the cell cycle and consequences of deregulation in mammalian cells. Cell Div. 1:22.
59. Sugimoto N, Tatsumi Y, Tsurumi T, Matsukage A, Kiyono T, Nishitani H, Fujita M. 2004. Cdt1 phosphorylation by cyclin A-dependent kinases negatively regulates its function without affecting geminin binding. J. Biol. Chem. 279:19691-19697.
60. Fujita M, Yamada C, Tsurumi T, Hanaoka F, Matsuzawa K, Inagaki M. 1998. Cell cycle-and chromatin binding state-dependent phosphorylation of human MCM heterohexameric complexes. A role for cdc2 kinase. J. Biol. Chem. 273:17095-17101.
61. Itzhaki JE, Gilbert CS, Porter AC. 1997. Construction by gene targeting in human cells of a "conditional" CDC2 mutant that rereplicates its DNA. Nat. Genet. 15:258-265.