HPV 16 E2 protein induces apoptosis in human and murine HPV 16 transformed epithelial cells and has antitumoral effects in vivo

Tumor Biology

Volumn 30, Issue 2, 2009, Pages 61-72

  Bermudez Morales V H ^a,d   Peralta Zaragoza, O ^a   Guzman Olea E ^b   Garcia Carranca A ^c   Bahena Roman M ^a   Alcocer Gonzalez J M ^e   Madrid Marina, V ^a  

^a INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^b Polytechnic University of Morelos State   (Mexico)

^c INSTITUTO NACIONAL DE CANCEROLOGÍA   (Mexico)

^d UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^e UNIVERSIDAD AUTÓNOMA DE NUEVO LEÓN   (Mexico)

Author keywords

Apoptosis; Cell death; Epithelial cells; HPV 16 E2

Indexed keywords

ADENOVIRUS VECTOR; CASPASE 3; CASPASE 8; GLYCOPROTEIN E2; DNA BINDING PROTEIN; E2 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 16; ONCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CELL GROWTH; CONTROLLED STUDY; DNA FRAGMENTATION; E6 ONCOGENE; E7 ONCOGENE; ENZYME ACTIVATION; EPITHELIUM CELL; EXPERIMENTAL MOUSE; FEMALE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IN VIVO STUDY; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS CELL TRANSFORMATION; VIRUS RECOMBINANT; ADENOVIRUS; ANIMAL; BAGG ALBINO MOUSE; CELL LINE; GENE THERAPY; GENE VECTOR; GENETICS; METABOLISM; NEOPLASM; PHYSIOLOGY; TUMOR CELL LINE; VIROLOGY;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELL TRANSFORMATION, VIRAL; DNA FRAGMENTATION; DNA-BINDING PROTEINS; EPITHELIAL CELLS; FEMALE; GENE THERAPY; GENETIC VECTORS; HUMAN PAPILLOMAVIRUS 16; HUMANS; MICE; MICE, INBRED BALB C; NEOPLASMS; ONCOGENE PROTEINS, VIRAL;

EID: 65449121124     PISSN: 10104283     EISSN: None     Source Type: Journal    
DOI: 10.1159/000214438     Document Type: Article

References (48)

1. Liaw KL, Hildesheim A, Burk RD, Gravitt P, Wacholder S, Manos MM, Scott DR, Sherman ME, Kurman RJ, Glass AG, Anderson SM, Schiffman M: A prospective study of human papillomavirus (HPV) type 16 DNA detection by polymerase chain reaction and its association with acquisition and persistence of other HPV types. J Infect Dis 2001; 183: 8-15.
2. Stanley MA, Pett MR, Coleman N: HPV: from infection to cancer. Biochem Soc Trans 2007; 35: 1456-1460.
3. Zur Hausen H: Human papillomaviruses in the pathogenesis of anogenital cancer. Virology 1991; 184:9-13.
4. Mantovani F, Banks L: The human papillo-mavirus E6 protein and its contribution to malignant progression. Oncogene 2001; 20: 7874 -7887.
5. Munger K, Basile JR, Duensing S, Eichten A, Gonzalez SL, Grace M, Zacny VL: Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Onco-gene 2001; 20:7888-7898.
6. Smith-McCune K, Kalman D, Robbins C, Shivakumar S, Yuschenkoff L, Bishop JM: Intranuclear localization of human papillo-mavirus 16 E7 during transformation and preferential binding of E7 to the RB family member p130. Proc Natl Acad Sci USA 1999; 96: 6999-7004.
7. Lee Jo, Russo AA, Pavletich NP: Structure of the retinoblastoma tumour-suppressor pocket domain bound to a peptide from HPV E7. Nature 1998; 391:859-865.
8. Lai MC, Teh BH, Tarn WY: A human papil-lomavirus E2 transcriptional activator. The interactions with cellular splicing factors and potential function in pre-mRNA processing. J Biol Chem 1999; 274:11832-11841.
9. Desaintes C, Demeret C: Control of papillo-mavirus DNA replication and transcription. Sem Ca ncer Biol 1996; 7: 339 -347.
10. Soeda E, Ferran MC, Baker CC, McBride AA: Repression of HPV16 early region transcription by the E2 protein. Virology 2006; 351: 29-41.
11. Baker CC, Phelps WC, Lindgren V, Braun MJ, Gonda MA, Howley PM: Structural and transcriptional analysis of human papillo-mavirus type 16 sequences in cervical carcinoma cell lines. J Virol 1987; 61: 962-971.
12. Schwarz E, Freese UK, Gissmann L, Mayer W, Roggenbuck B, Stremlau A, zur Hausen H: Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 1985; 314:111-114.
13. Stoler MH, Rhodes CR, Whitbeck A, Wolin-sky SM, Chow LT, Broker TR: Human papil-lomavirus type 16 and 18 gene expression in cervical neoplasias. Hum Pathol 1992; 23: 117-12 8 .
14. Francis DA, Schmid SI, Howley PM: Repression of the integrated papillomavirus E6/E7 promoters is required for growth suppression of cervical cancer cells. J Virol 2000; 74: 2679-2686.
15. Thierry F: Transcriptional regulation of the papillomavirus oncogenes by cellular and viral transcription factors in cervical carcinoma. Virology 2009; 384:375-379.
16. Bernard BA, Bailly C, Lenoir MC, Darmon M, Thierry F, Yaniv M: The human papillo-mavirus type 18 (HPV18) E2 gene product is a repressor of the HPV18 regulatory region in human keratinocytes. J Virol 1989; 63: 4317-4324.
17. Park JS, Hwang ES, Park SN, Ahn HK, Um SJ, Kim CJ, Kim SJ, Namkoong SE: Physical status and expression of HPV genes in cervical cancers. Gynecol Oncol 1997; 65:121- 129.
18. Schneider-Maunoury S, Croissant O, Orth G: Integration of human papillomavirus type 16 DNA sequences: a possible early event in the progression of genital tumors. J Virol 1987; 61: 395-3298.
19. Romanczuk H, Howley PM: Disruption of either the E1 or the E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc Natl Acad Sci USA 1992; 89:3159-3163.
20. Tonon SA, Picconi MA, Bos PD, Zinovich JB, Galuppo J, Alonio LV, Teyssie AR: Physical status of the E2 human papillomavirus 16 viral gene in cervical preneoplastic and neo-plastic lesions. J Clin Virol 2001; 21: 129- 134.
21. Thierry F, Ya niv M: The BPV-1 E2 trans -acting protein can be either an activator or re-pressor of the HPV-18 regulatory region. EMBO J 1987; 6:3391-3397.
22. Hwang ES, Naegerm LK, DiMario D: Activation of the endogenous p53 growth in-hibitory pathway in HeLa cervical carcinoma cells by expression of the bovine papillomavirus E2 gene. Oncogene 1996; 12: 795-803.
23. Hwang E, Riese DR, Settleman J, Nilson L, Honig J, Flynn S, DiMario D: Inhibition of cervical carcinoma cell line proliferation by introduction of a bovine papillomavirus regulatory gene. J Virol 1993; 67:3720-3729.
24. Desaintes C, Demeret C, Goyat S, Yaniv M, Thierry F: Expression of the papillomavirus E2 protein in HeLa cells leads to apoptosis. EMBO J 1997; 16:504-514.
25. Dowhanick JJ, McBride AA, Howley PM: Suppression of cellular proliferation by the papillomavirus E2 protein. J Virol 1995; 69: 7791-7799.
26. Demeret C, Garcia-Carranca A, Thierry F: Transcription-independent triggering of the extrinsic pathway of apoptosis by human papillomavirus 18 E2 protein. Oncogene 2003; 22: 16 8 -17 5 .
27. Blachon S, Demeret C: The regulatory E2 proteins of human genital papillomaviruses are pro-apoptotic. Biochimie 2003; 85:813- 819.
28. Blachon S, Bellanger S, Demeret C, Tierry F: Nucleo-cytoplasmic shuttling of high risk human papillomavirus E2 proteins induces apoptosis. J Biol Chem 2005; 280: 36088- 36098.
29. Webster K, Parish J, Pandya M, Stern PL, Clarke AR, Gaston K: The human papillo-mavirus (HP) 16 E2 protein induces apopto-sis in the absence of other HPV proteins and via a p53-dependent pathway. J Biol Chem 2000; 275: 87-94.
30. Frattini MG, Hurst SD, Lim HB, Swamina-than S, Laimins LA: Abrogation of a mitotic checkpoint by E2 proteins from oncogenic human papillomaviruses correlates with in-creased turnover of the p53 tumor suppressor protein. EMBO J 1997; 16:318-331.
31. Goodwin EC, DiMaio D: Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc Natl Acad Sci USA 2000; 9723: 12513-12518.
32. Parish JL, Kowalczyk A, Chen HT, Roeder GE , Sessions R, Buck le M, Gaston K: E2 proteins from high- and low-risk human papil-lomavirus types differ in their ability to bind p53 and induce apoptotic cell death. J Virol 2006; 80:4580-4590.
33. Green KL, Brown C, Roeder GE, Southgate TD, Gaston K: A cancer cell-specific inducer of apoptosis. Hum Gene Ther 2007; 18:547- 561.
34. Rosales C, Graham V V, Rosas GA, Merchant H, Rosales R: A recombinant vaccinia virus containing the papilloma E2 protein promotes tumor regression by stimulating mac-rophage antibody-dependent cytotoxicity. Cancer Immunol Immunother 2000; 49: 347-360.
35. Valdez Graham V, Sutter G, José MV, Gar-cía-Carranca A, Erfle V, Moreno Mendoza N, Merchant H, Rosales R: Human tumor growth is inhibited by a vaccinia virus carrying the E2 gene of bovine papillomavirus. Cancer 2000; 88: 16 5 0 -16 6 2 .
36. Hallez S, Detremmerie O, Giannouli C, Thielemans K, Gajewski TF, Burny A, Leo O: Interleukin-12-secreting human papilloma-virus type 16-transformed cells provide a potent cancer vaccine that generates E7-direct-ed immunity. Int J Cancer 1999; 81: 428-437.
37. Veress G, Szarka K, Dong XP, Gergely L, Pfister H: Functional significance of sequence variation in the E2 gene and long control region of human papillomavirus type 16. J General Virol 1999; 80:1035-1043.
38. Chomczynski P, Mackey K, Drews R, Wilfin-ger W: DNAzol: a reagent for the rapid isolation of genomic DNA. Biotechniques 1997; 22: 550 -553.
39. Chua KY, Ramos JD, Cheong N: Production of monoclonal antibody by DNA immunization with electroporation. Methods Mol Biol 2008; 423: 509-520.
40. Kasinrerk W, Moonsom S, Chawansuntati K: Production of antibodies by single DNA immunization: comparison of various immunization routes. Hybrid Hybridomics 2002; 21:287-293.
41. He T-C, Kinzler K, Vogelstein B: A practical guide for using the AdEasy system. www. coloncancer.org/adeasy/protocol2.htm (accessed February 25, 2009).
42. Nishimura A, Ono T, Ishimoto A, Dow-hanick JJ, Frizzell MA, Howley PM, Sakai H: Mechanisms of human papillomavirus E2-mediated repression of viral oncogene expression and cervical cancer cell growth inhibition. J Virol 2000; 74:3752-3760.
43. DeFilippis RA, Goodwin EC, Wu L, DiMaio D: Endogenous human papillomavirus E6 and E7 proteins differentially regulate proliferation, senescence, and apoptosis in HeLa cer vical carcinoma cells. J Virol 2003; 77: 1551-1563.
44. Berumen J, Casas L, Segura E, Amezcua J, Garcia-Carranca A: Genome amplification of human papillomavirus type 16 and 18 in cervical carcinomas is related to the retention of E1/E2 genes. Int J Cancer 1994; 56:640-645.
45. Münger K, Howley PM: Human papilloma-virus immortalization and transformation functions. Virus Res 2002; 89:213-228.
46. Dostatni N, Lambert PF, Sousa R, Ham J, Howley PM, Yaniv M: The functional BPV-1 E2 trans-activating protein can act as a re-pressor by preventing formation of initiation complex. Genes Dev 1991; 5:1657-1671.
47. Demeret C, Desaintes C, Yaniv M, Thierry F: Different mechanisms contribute to the E2-mediated transcriptional repression of human papillomavirus type 18 viral oncogenes. J Virol 1997; 71: 9343-9349.
48. Desaintes C, Goyat S, Garbay S, Yaniv M, Thierry F: Papillomavirus E2 induces p53-independent apoptosis in HeLa cells. Oncogene 1999; 18:4538-4545.