Inactivating all three Rb family pocket proteins is insufficient to initiate cervical cancer

Cancer Research

Volumn 72, Issue 20, 2012, Pages 5418-5427

  Shin, Myeong Kyun ^a   Sage, Julien ^b   Lambert, Paul F ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; PROTEIN E7; PROTEIN P107; PROTEIN P130; RETINOBLASTOMA PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GRADING; CARCINOGENESIS; CONTROLLED STUDY; FEMALE; HUMAN PAPILLOMAVIRUS TYPE 16; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FAMILY; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA IN SITU;

ANIMALS; DNA REPLICATION; FEMALE; HUMANS; MICE; MICE, KNOCKOUT; RETINOBLASTOMA PROTEIN; UTERINE CERVICAL NEOPLASMS;

EID: 84867509019     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-2083     Document Type: Article

References (50)

1. American Cancer Society. Cancer facts & figures. Atlanta, GA: American Cancer Society. p. v.
2. Sankaranarayanan R, Ferlay J. Worldwide burden of gynaecological cancer: the size of the problem. Best Pract Res Clin Obstet Gynaecol 2006;20:207-25. (Pubitemid 43380597)
3. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-9. (Pubitemid 29406813)
4. Leechanachai P, Banks L, Moreau F, Matlashewski G. The E5 gene from human papillomavirus type 16 is an oncogene which enhances growth factor-mediated signal transduction to the nucleus. Oncogene 1992;7:19-25.
5. Hawley-Nelson P, Vousden KH, Hubbert NL, Lowy DR, Schiller JT. HPV-16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J 1989;8:3905-10. (Pubitemid 20016074)
6. zur Hausen H. Papillomavirus infections-a major cause of human cancers. Biochim Biophys Acta 1996;1288:F55-78.
7. Maufort JP, Shai A, Pitot HC, Lambert PF. A role for HPV-16 E5 in cervical carcinogenesis. Cancer Res 2010;70:2924-31.
8. Riley RR, Duensing S, Brake T, Munger K, Lambert PF, Arbeit JM. Dissection of human papillomavirus E6 and E7 function in transgenic mouse models of cervical carcinogenesis. Cancer Res 2003;63:4862-71. (Pubitemid 37022618)
9. Huh KW, DeMasi J, Ogawa H, Nakatani Y, Howley PM, Munger K. Association of the human papillomavirus type 16 E7 oncoprotein with the 600-kDa retinoblastoma protein-associated factor, p600. Proc Natl Acad Sci U S A 2005;102:11492-7. (Pubitemid 41153847)
10. McLaughlin-Drubin ME, Munger K. The human papillomavirus E7 oncoprotein. Virology 2009;384:335-44.
11. Munger K, Werness BA, Dyson N, Phelps WC, Harlow E, Howley PM. Complex formation of human papillomavirus E7 proteins with the retinoblastoma tumor suppressor gene product. EMBO J 1989;8:4099-105. (Pubitemid 20066852)
12. Burkhart DL, Sage J. Cellular mechanisms of tumour suppression by the retinoblastoma gene. Nat Rev Cancer 2008;8:671-82.
13. Boyer SN, Wazer DE, Band V. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res 1996;56:4620-4. (Pubitemid 26338060)
14. Balsitis SJ, Sage J, Duensing S, Munger K, Jacks T, Lambert PF. Recapitulation of the effects of the human papillomavirus type 16 E7 oncogene on mouse epithelium by somatic Rb deletion and detection of pRb-independent effects of E7 in vivo. Mol Cell Biol 2003;23:9094-103. (Pubitemid 37499799)
15. Collins AS, Nakahara T, Do A, Lambert PF. Interactions with pocket proteins contribute to the role of human papillomavirus type 16 E7 in the papillomavirus life cycle. J Virol 2005;79:14769-80. (Pubitemid 41636275)
16. Balsitis S, Dick F, Dyson N, Lambert PF. Critical roles for non-pRb targets of human papillomavirus type 16 E7 in cervical carcinogenesis. Cancer Res 2006;66:9393-400. (Pubitemid 44623635)
17. Pyeon D, Newton MA, Lambert PF, den Boon JA, Sengupta S, Marsit CJ, et al. Fundamental differences in cell cycle deregulation in human papillomavirus-positive and human papillomavirus-negative head/neck and cervical cancers. Cancer Res 2007;67:4605-19. (Pubitemid 46910165)
18. Munger K, Basile JR, Duensing S, Eichten A, Gonzalez SL, Grace M, et al. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 2001;20:7888-98. (Pubitemid 33135315)
19. Mayol X, Grana X, Baldi A, Sang N, Hu Q, Giordano A. Cloning of a new member of the retinoblastoma gene family (pRb2) which binds to the E1A transforming domain. Oncogene 1993;8:2561-6. (Pubitemid 23252387)
20. Hannon GJ, Demetrick D, Beach D. Isolation of the Rb-related p130 through its interaction with CDK2 and cyclins. Genes Dev 1993;7:2378-91. (Pubitemid 24003241)
21. Ewen ME, Ludlow JW, Marsilio E, DeCaprio JA, Millikan RC, Cheng SH, et al. An N-terminal transformation-governing sequence of SV40 large T antigen contributes to the binding of both p110Rb and a second cellular protein, p120. Cell 1989;58:257-67. (Pubitemid 19191408)
22. Dyson N, Buchkovich K, Whyte P, Harlow E. The cellular 107K protein that binds to adenovirus E1A also associates with the large T antigens of SV40 and JC virus. Cell 1989;58:249-55. (Pubitemid 19191407)
23. Classon M, Dyson N. p107 and p130: versatile proteins with interesting pockets. Exp Cell Res 2001;264:135-47. (Pubitemid 32989088)
24. Scambia G, Lovergine S, Masciullo V. RB family members as predictive and prognostic factors in human cancer. Oncogene 2006;25:5302-8. (Pubitemid 44299091)
25. Simpson DS, Mason-Richie NA, Gettler CA, Wikenheiser-Brokamp KA. Retinoblastoma family proteins have distinct functions in pulmonary epithelial cells in vivo critical for suppressing cell growth and tumorigenesis. Cancer Res 2009;69:8733-41.
26. Schaffer BE, Park KS, Yiu G, Conklin JF, Lin C, Burkhart DL, et al. Loss of p130 accelerates tumor development in a mouse model for human small-cell lung carcinoma. Cancer Res 2010;70:3877-83.
27. Robanus-Maandag E, Dekker M, van der Valk M, Carrozza ML, Jeanny JC, Dannenberg JH, et al. p107 is a suppressor of retinoblastoma development in pRb-deficient mice. Genes Dev 1998;12:1599-609. (Pubitemid 28299512)
28. Ho VM, Schaffer BE, Karnezis AN, Park KS, Sage J. The retinoblastoma gene Rb and its family member p130 suppress lung adenocarcinoma induced by oncogenic K-Ras. Oncogene 2009;28:1393-9.
29. Dannenberg JH, Schuijff L, Dekker M, van der Valk M, te Riele H. Tissue-specific tumor suppressor activity of retinoblastoma gene homologs p107 and p130. Genes Dev 2004;18:2952-62. (Pubitemid 39602313)
30. Shin MK, Pitot HC, Lambert PF. Pocket proteins suppress head and neck cancer. Cancer Res 2012;72:1280-9.
31. Viatour P, Somervaille TC, Venkatasubrahmanyam S, Kogan S, McLaughlin ME, Weissman IL, et al. Hematopoietic stem cell quiescence is maintained by compound contributions of the retinoblastoma gene family. Cell Stem Cell 2008;3:416-28.
32. Shin MK, Balsitis S, Brake T, Lambert PF. Human papillomavirus E7 oncoprotein overrides the tumor suppressor activity of p21Cip1 in cervical carcinogenesis. Cancer Res 2009;69:5656-63.
33. Brake T, Connor JP, Petereit DG, Lambert PF. Comparative analysis of cervical cancer in women and in a human papillomavirus-transgenic mouse model: identification of minichromosome maintenance protein 7 as an informative biomarker for human cervical cancer. Cancer Res 2003;63:8173-80. (Pubitemid 37549465)
34. Blow JJ, Hodgson B. Replication licensing-defining the proliferative state? Trends Cell Biol 2002;12:72-8.
35. Ishida S, Huang E, Zuzan H, Spang R, Leone G, West M, et al. Role for E2F in control of both DNA replication and mitotic functions as revealed from DNA microarray analysis. Mol Cell Biol 2001;21:4684-99. (Pubitemid 32588250)
36. Attwooll C, Lazzerini Denchi E, Helin K. The E2F family: specific functions and overlapping interests. EMBO J 2004;23:4709-16. (Pubitemid 40069701)
37. Vasioukhin V, Degenstein L, Wise B, Fuchs E. The magical touch: genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc Natl Acad Sci U S A 1999;96:8551-6. (Pubitemid 29354829)
38. Donovan SL, Schweers B, Martins R, Johnson D, Dyer MA. Compensation by tumor suppressor genes during retinal development in mice and humans. BMC Biol 2006;4:14.
39. He F, Mo L, Zheng XY, Hu C, Lepor H, Lee EY, et al. Deficiency of pRb family proteins and p53 in invasive urothelial tumorigenesis. Cancer Res 2009;69:9413-21.
40. Brehm A, Nielsen SJ, Miska EA, McCance DJ, Reid JL, Bannister AJ, et al. The E7 oncoprotein associates with Mi2 and histone deacetylase activity to promote cell growth. EMBO J 1999;18:2449-58. (Pubitemid 29213278)
41. McLaughlin-Drubin ME, Huh KW, Munger K. Human papillomavirus type 16 E7 oncoprotein associates with E2F6. J Virol 2008;82:8695-705.
42. Morey L, Helin K. Polycomb group protein-mediated repression of transcription. Trends Biochem Sci 2010;35:323-32.
43. McLaughlin-Drubin ME, Crum CP, Munger K. Human papillomavirus E7 oncoprotein induces KDM6A and KDM6B histone demethylase expression and causes epigenetic reprogramming. Proc Natl Acad Sci U S A 2011;108:2130-5.
44. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002;3:415-28. (Pubitemid 34587077)
45. Robertson KD. DNA methylation, methyltransferases, and cancer. Oncogene 2001;20:3139-55. (Pubitemid 32553570)
46. Burgers WA, Blanchon L, Pradhan S, de Launoit Y, Kouzarides T, Fuks F. Viral oncoproteins target the DNA methyltransferases. Oncogene 2007;26:1650-5. (Pubitemid 46398736)
47. Mitelman F, Johansson B, Mertens F. The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 2007;7:233-45. (Pubitemid 46480968)
48. Strati K, Lambert PF. Role of Rb-dependent and Rb-independent functions of papillomavirus E7 oncogene in head and neck cancer. Cancer Res 2007;67:11585-93.
49. Brake T, Lambert PF. Estrogen contributes to the onset, persistence, and malignant progression of cervical cancer in a human papillomavirus-transgenic mouse model. Proc Natl Acad Sci U S A 2005;102:2490-5. (Pubitemid 40279404)
50. Chung SH, Wiedmeyer K, Shai A, Korach KS, Lambert PF. Requirement for estrogen receptor alpha in a mouse model for human papillomavirus-associated cervical cancer. Cancer Res 2008;68:9928-34.