The Asian-American E6 variant protein of human papillomavirus 16 alone is sufficient to promote immortalization, transformation, and migration of primary human foreskin keratinocytes

Journal of Virology

Volumn 86, Issue 22, 2012, Pages 12384-12396

  Niccoli, Sarah ^a,b   Abraham, Suraj ^a   Richard, Christina ^b   Zehbe, Ingeborg ^a  

^a Thunder Bay Regional Research Institute   (Canada)

^b LAKEHEAD UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN; PROTEIN E6; PROTEIN E7; PROTEIN P53; VIRUS PROTEIN;

ARTICLE; CANCER RISK; CARCINOGENESIS; CELL IMMORTALIZATION; CELL MIGRATION; CELL TRANSFORMATION; CONTROLLED STUDY; G1 PHASE CELL CYCLE CHECKPOINT; GENE DUPLICATION; GENE FUNCTION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; KERATINOCYTE; METASTASIS POTENTIAL; NONHUMAN; ONCOGENE E6; ONCOGENE E7; PREPUCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; UTERINE CERVIX CANCER; VIRUS CULTURE; VIRUS ONCOGENE;

ASIAN AMERICANS; CELL CYCLE; CELL MOVEMENT; CELL SURVIVAL; FEMALE; FORESKIN; GENETIC VARIATION; HUMANS; KERATINOCYTES; MALE; ONCOGENE PROTEINS, VIRAL; REPRESSOR PROTEINS; TELOMERASE; TUMOR SUPPRESSOR PROTEIN P53; UTERINE CERVICAL NEOPLASMS;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS - 16; HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 84869146680     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01512-12     Document Type: Article

References (76)

1. Adams JC, Watt FM. 1989. Fibronectin inhibits the terminal differentiation of human keratinocytes. Nature 340:307-309.
2. Baudoin C, Fantin L, Meneguzzi G. 2005. Proteolytic processing of the laminin α3 G domain mediates assembly of hemidesmosomes but has no role on keratinocyte migration. J. Investig. Dermatol. 125:883-888.
3. Berumen J, et al. 2001. Asian American variant of human papillomavirus 16 and risk for cervical cancer: a case-control study. J. Natl. Cancer Inst.93:1325-1330.
4. Bond JA, et al. 1999. Control of replicative life span in human cells:barriers to clonal expansion intermediate between M1 senescence and M2 crisis. Mol. Cell. Biol. 19:3103-3114.
5. Boulenouar S, et al. 2010. Effects of HPV-16 E5, E6 and E7 proteins on survival, adhesion, migration and invasion of trophoblastic cells. Carcinogenesis 31:473-480.
6. Burk RD, et al. 2003. Distribution of human papillomavirus types 16 and 18 variants in squamous cell carcinomas and adenocarcinomas of the cervix. Cancer Res. 63:7215-7220.
7. Charette ST, McCance DJ. 2007. The E7 protein from human papillomavirus type 16 enhances keratinocyte migration in an Akt-dependent manner. Oncogene 26:7386-7390.
8. Colgin LM, Reddel RR. 1999. Telomere maintenance mechanisms and cellular immortalization. Curr. Opin. Genetic. Dev. 9:97-103.
9. Counter CM, et al. 1992. Telomere shortening associated with chromosome instability is arrested in immortal cells with express telomere activity. EMBO J. 11:1921-1929.
10. DeCarlo CA, et al. 2008. Gene expression analysis of interferon κ in laser capture microdissected cervical epithelium. Anal. Biochem. 381:59-66.
11. DeFilippis RA, Goodwin EC, Wu L, DiMaio D. 2003. Endogenous human papillomavirus E6 and E7 proteins differentially regulate proliferation,senescence, and apoptosis in HeLa cervical carcinoma cells. J. Virol.77:1551-1563.
12. Fidler IJ, Radinsky R. 1990. Genetic control of cancer metastasis. J. Natl. Cancer Inst. 82:166-168.
13. Fodde R, Brabletz T. 2007. Wnt/β-catenin signalling in cancer stemness and malignant behavior. Curr. Opin. Cell Biol. 19:150-158.
14. Foster SA, Demers GW, Etscheid BG, Galloway DA. 1994. The ability of human papillomavirus E6 proteins to target p53 for degradation in vivo correlates with their ability to abrogate actinomycin D-induced growth arrest. J. Virol. 68:5698-5705.
15. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C. 2006. Clonogenic assay of cells in vitro. Nat. Protoc. 1:2315-2319.
16. Frisch SM, Francis H. 1994. Disruption of epithelial cell-matrix interactions induces apoptosis. J. Cell Biol. 124:620-626.
17. Fuchs E, Segre JA. 2000. Stem cells: a new lease on life. Cell 100:143-155.
18. Greider CW, Blackburn EH. 1985. Identification of a specific telomere terminal transferase activity in tetrahymena extracts. Cell 43:405-413.
19. Hahn WC, Meyerson M. 2001. Telomerase activation, cellular immortalization and cancer. Ann. Med. 33:123-129.
20. Halbert CL, Demers GW, Galloway DA. 1991. The E7 gene of human papillomavirus type 16 is sufficient for immortalization for human epithelial cells. J. Virol. 65:473-478.
21. 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.
22. Hellner K, Mar J, Fang F, Quackenbush J, Munger K. 2009. HPV16 E7 oncogene expression in normal human epithelial cells causes molecular changes indicative of an epithelial to mesenchymal transition. Virology 391:57-63.
23. Herman L, Hubert P, Caberg Evrard J-HB, Kedzia W, Boniver J, Delvenne P. 2007. MIP3 alpha stimulates the migration of Langerhans cells in models of human papillomavirus (HPV)-associated (pre)neoplastic epithelium. Cancer Immunol. Immunother. 56:1087-1096.
24. Hickman ES, Bates S, Vousden KH. 1997. Perturbation of the p53 response by human papillomavirus type 16 E7. J. Virol. 71:3710-3718.
25. Hines MD, Jin HC, Wheelock MJ, Jensen PJ. 1999. Inhibition of cadherin function differentially affects markers of terminal differentiation in cultured human keratinocytes. J. Cell Sci. 112:4569-4579.
26. Jensen PJ, Telegan B, Lavker RM, Wheelock MJ. 1997. E-cadherin and P-cadherin have partially redundant roles in human epidermal stratification. Cell Tissue Res. 288:307-316.
27. Jones DL, Thompson DA, Suh-Bürgmann E, Grace M, Münger K. 1999. Expression of the HPV E7 oncoprotein mimics but does not evoke a p53-dependent cellular DNA damage response pathway. Virology 258:406-414.
28. Kastan MB, Onyekwere O, Sidransky Vogelstein DB, Craig RW. 1991.Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51:6304-6311.
29. Kaur P, McDougall JK, Cone R. 1989. Immortalization of primary human epithelial cells by cloned cervical carcinoma DNA containing human papillomavirus type 16 E6/E7 open reading frames. J. Gen. Virol.70:1261-1266.
30. Klingelhutz AJ, Barber S, Smith PP, Dyer K, McDougall JK. 1994. Restoration of telomeres in human papillomavirus-immortalized human anogenital epithelial cells. Mol. Cell. Biol. 14:961-969.
31. Klingelhutz AJ, Foster SA, McDougall JK. 1996. Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 380:79-82.
32. Kong CS, et al. 2009. The relationship between human papillomavirus status and other molecular prognostic markers in head and neck squamous cell carcinomas. Int. J. Radiat. Oncol. Biol. Phys. 74:553-561.
33. Kuhn NZ, Tuan RS. 2010. Regulation of stemness and stem cell niche of mesenchymal stem cells: implications in tumorigenesis and metastasis. J.Cell. Physiol. 222:268-277.
34. Lesnikova I, Lidang M, Hamilton-Dutoit S, Koch J. 2010. Rapid, sensitive, type specific PCR detection of the E7 region of human papillomavirus type 16 and 18 from paraffin embedded sections of cervical carcinoma.Infect. Agents Cancer 5:2-6.
35. Liu L, et al. 2008. Hypoxia induced HIF-1 accumulation and VEGF expression in gastric epithelial mucosa cells: involvement of ERK1/2 and PI3K/Akt. Mol. Biol. 42:403-412.
36. Liu X, et al. 2009. HPV E6 protein interacts physically and functionally with the cellular telomerase complex. Proc. Natl. Acad. Sci. U. S. A. 106:18780-18785.
37. Liu X, Disbrow GL, Yuan H, Tomaic V, Schlegel R. 2007. Myc and human papillomavirus type 16 E7 genes cooperate to immortalize human keratinocytes. J. Virol. 81:12689-12695.
38. Loncaster JA, et al. 2001. Carbonic anhydrase (CA IX) expression, a potential new intrinsic marker of hypoxia: correlations with tumor oxygen measurements and prognosis in locally advanced carcinoma of the cervix. Cancer Res. 61:6394-6399.
39. Matthews K, et al. 2003. Depletion of Langerhans cells in human papillomavirus type 16-infected skin is associated with the E6-mediated down regulation of E-cadherin. J. Virol. 77:8378-8385.
40. McMurray HR, McCance DJ. 2004. Degradation of p53, not telomerase activation, by E6 is required for bypass of crisis and immortalization by human papillomavirus type 16 E6/E7. J. Virol. 78:5698-5706.
41. McMurray HR, McCance DJ. 2003. Human papillomavirus type 16 E6 activates TERT gene transcription through induction of c-Myc and release of USF-mediated repression. J. Virol. 77:9852-9861.
42. Morgenstern JP, Land H. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
43. Munger K, Phelps WC, Bubb V, Howley PM, Schlegel R. 1989. The E6 and E7 genes of human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J. Virol. 63:4417-4421.
44. Oh ST, Kyo S, Laimins LA. 2001. Telomerase activation by human papillomavirus type 16 E6 protein: induction of human telomerase reverse transcriptase expression through Myc and GC-rich Sp1 binding sites. J. Virol. 75:5559-5566.
45. Pastoreková S, Závada J. 2004. Carbonic anhydrase IX (CA IX) as a potential target for cancer therapy. J. Cancer Ther. 2:245-262.
46. Pilcher BK, et al. 1997. The activity of collagenase-1 is required for keratinocyte migration on a type 1 collagen matrix. J. Cell Biol. 137:1445-1457.
47. Plug-DeMaggio AW, et al. 2004. Telomere erosion and chromosomal instability in cells expressing theHPVoncogene 16E6. Oncogene 23:3561-3571.
48. Raffaella R, et al. 2004. The interferon-inducible IFI16 gene inhibits tube morphogenesis and proliferation of primary, but not HPV 16 E6/E7-immortalized human endothelial cells. Exp. Cell Res. 293:331-345.
49. Rangarajan A, et al. 2001. Activated Notch1 signaling cooperates with papillomavirus oncogenes in transformation and generates resistance to apoptosis on matrix withdrawal through PKB/Akt. Virology 286:23-30.
50. INK4A-and p53-dependent keratinocyte senescence mechanism that limits replicative potential independent of telomere status. Mol. Cell. Biol. 22:5157-5172.
51. Richard C, et al. 2010. The immortalizing and transforming ability of two common human papillomavirus 16 E6 variants with different prevalences in cervical cancer. Oncogene 29:3435-3445.
52. Sedman SA, et al. 1991. The full-length E6 protein of human papillomavirus type 16 has transforming and trans-activating activities and cooperates with E7 to immortalize keratinocytes in culture. J. Virol. 65:4860-4866.
53. Semenza GL. 2010. HIF-1: upstream and downstream of cancer metabolism.Curr. Opin. Genet. Dev. 20:51-56.
54. Shay JW, Wright WE. 2005. Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis 26:867-874.
55. Shay JW, Wright WE, Brasiskyte D, Van der Haegen BA. 1993. E6 of human papillomavirus type 16 can overcome the M1 stage of immortalization in human mammary epithelial cells but not in human fibroblasts. Oncogene 8:1407-1413.
56. Shay JW, Wright WE, Werbin H. 1991. Defining the molecular mechanisms of human cell immortalization. Biochim. Biophys. Acta 1072:1-7.
57. Stewart D, et al. 2006. The inter-relationship of hypoxia and phospho-Akt in the pathobiology of malignant pleural mesothelioma. J. Clin. Oncol.24:17057.
58. Stöppler H, et al. 1998. The E7 protein of human papillomavirus type 16 sensitizes primary human keratinocytes to apoptosis. Oncogene 17:1207-1214.
59. Tunggal JA, et al. 2005. E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J. 24:1146-1156.
60. Üren A, Fallen et al. 2005. Activation of the canonical Wnt pathway during genital keratinocyte transformation: a model for cervical cancer progression. Cancer Res. 65:6199-6206.
61. VanDenBrule FA, Clausse N, Delvenne P, Franzen-Detrooz E, Cas-tronovo. 2000. Combined interferon-γ and tumor necrosis factor-α treatment differentially affects adhesion and migration of keratinocyte-derived cells to laminin-1. Cell Adhesion Comm. 7:321-329.
62. Veldman T, Horikawa I, Barrett JC, Schlegel R. 2001. Transcriptional activation of the telomerase hTERT gene by human papillomavirus type 16 E6 oncoprotein. J. Virol. 75:4467-4472.
63. Villa LL, et al. 2000. Molecular variants of human papillomavirus types 16 and 18 preferentially associated with cervical neoplasia. J. Gen. Virol. 81:2959-2968.
64. Weijzen S, Zlobin A, Braid M, Miele L, Kast WM. 2003. HPV16 E6 and E7 oncoproteins regulate Notch-1 expression and cooperate to induce transformation. J. Cell. Physiol. 194:356-362.
65. Weinberg RA. 2007. The biology of cancer. Garland Science, New York, NY.
66. Willey JC, et al. 1991. Immortalization of normal human bronchial epithelial cells by human papillomaviruses 16 or 18. Cancer Res. 51:5370-5377.
67. Wright WE, Pereira-Smith OM, Shay JW. 1989. Reversible cellular senescence: implications for immortalization of normal human diploid fibroblasts. Mol. Cell. Biol. 9:3088-3092.
68. Wright WE, Shay JW. 1992. The two-stage mechanism controlling cellular senescence and immortalization. Exp. Gerontol. 27:383-389.
69. Wu K-J, Grandori C, Amacker M, Simon-Vermot N, Polack A, Lingner J, Dalla-Favera R. 1999. Direct activation of TERT transcription by c-MYC. Nat. Genet. 21:220-224.
70. Xi LF, et al. 1997. Genomic variation of human papillomavirus type 16 and risk for high grade cervical intraepithelial neoplasia. J. Natl. Cancer Inst. 89:796-802.
71. Xi LF, et al. 2007. Risk for high-grade cervical intraepithelial neoplasia associated with variants of human papillomavirus types 16 and 18. Cancer Epidemiol. Biomarkers Prev. 16:4-10.
72. Yamada T, et al. 1997. Human papillomavirus type 16 sequence variation in cervical cancers: a worldwide perspective. J. Virol. 71:2463-2472.
73. Yasumoto S, et al. 1996. Telomerase activity in normal human epithelial cells. Oncogene 13:433-439.
74. Zehbe I, et al. 2009. Human papillomavirus 16 E6 variants differ in their dysregulation of human keratinocyte differentiation and apoptosis. Virology 383:69-77.
75. Zehbe I, Wilander E, Delius H, Tommasino M. 1998. Human papillomavirus 16 E6 variants are more prevalent in invasive cervical carcinoma than the prototype. Cancer Res. 58:829-833.
76. zur Hausen H, De Villiers E-M. 1994. Human papilloma viruses. Annu. Rev. Microbiol. 48:427-447.