Human papillomavirus type 16 E6 and E 7 proteins alter NF-kB in cultured cervical epithelial cells and inhibition of NF-kB promotes cell growth and immortalization

Virology

Volumn 425, Issue 1, 2012, Pages 53-60

  Vandermark, Erik R ^a   Deluca, Krysta A ^a   Gardner, Courtney R ^a   Marker, Daniel F ^a   Schreiner, Cynthia N ^a   Strickland, David A ^a   Wilton, Katelynn M ^a   Mondal, Sumona ^a   Woodworth, Craig D ^a  

^a CLARKSON UNIVERSITY   (United States)

Author keywords

Cervical cancer; Defensins; Foreskin; Immortalization; NF kB; Oral epithelium; Papillomavirus; Transformation zone

Indexed keywords

I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN E6; PROTEIN E7; REPRESSOR PROTEIN; SYNAPTOTAGMIN I; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL GROWTH; CELL IMMORTALIZATION; CELL PROLIFERATION; CELL TRANSFORMATION; CELL TYPE; COLONY FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; UTERINE CERVIX CANCER; UTERINE CERVIX EPITHELIUM;

CELL TRANSFORMATION, VIRAL; CELLS, CULTURED; CERVIX UTERI; EPITHELIAL CELLS; FEMALE; FORESKIN; GENE EXPRESSION REGULATION; HUMAN PAPILLOMAVIRUS 16; HUMANS; MALE; NF-KAPPA B; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS E7 PROTEINS; REPRESSOR PROTEINS;

HUMAN PAPILLOMAVIRUS TYPE 16; PAPILLOMAVIRIDAE;

EID: 84856562062     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.12.023     Document Type: Article

References (55)

1. Baud V., Karin M. Is NF-kappaB a good target for cancer therapy? Hopes and pitfalls. Nat. Rev. Drug Discov. 2009, 8(1):33-40.
2. Branca M., Giorgi C., Ciotti M., Santini D., Di Bonito L., Costa S., Benedetto A., Bonifacio D., Di Bonito P., Paba P., Accardi L., Mariani L., Ruutu M., Syrjanen S., Favalli C., Syrjanen K. Upregulation of nuclear factor-kappaB (NF-kappaB) is related to the grade of cervical intraepithelial neoplasia, but is not an independent predictor of high-risk human papillomavirus or disease outcome in cervical cancer. Diagn. Cytopathol. 2006, 34(8):555-563.
3. Burghardt E., Ostor A.G. Site and origin of squamous cervical cancer: a histomorphologic study. Obstet. Gynecol. 1983, 62(1):117-127.
4. Chang Y.E., Laimins L.A. Microarray analysis identifies interferon-inducible genes and Stat-1 as major transcriptional targets of human papillomavirus type 31. J. Virol. 2000, 74(9):4174-4182.
5. Cook J.L., Walker T.A., Worthen G.S., Radke J.R. Role of the E1A Rb-binding domain in repression of the NF-kappa B-dependent defense against tumor necrosis factor-alpha. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(15):9966-9971.
6. Dajee M., Lazarov M., Zhang J.Y., Cai T., Green C.L., Russell A.J., Marinkovich M.P., Tao S., Lin Q., Kubo Y., Khavari P.A. NF-kappaB blockade and oncogenic Ras trigger invasive human epidermal neoplasia. Nature 2003, 421(6923):639-643.
7. Diamond G., Beckloff N., Ryan L.K. Host defense peptides in the oral cavity and the lung: similarities and differences. J. Dent. Res. 2008, 87(10):915-927.
8. Edmonds C., Vousden K.H. A point mutational analysis of human papillomavirus type 16 E7 protein. J. Virol. 1989, 63(6):2650-2656.
9. Erez N., Truitt M., Olson P., Arron S.T., Hanahan D. Cancer-associated fibroblasts are activated in incipient neoplasia to orchestrate tumor-promoting inflammation in an NF-kappaB-dependent manner. Cancer Cell 2010, 17(2):135-147.
10. Fontaine V., van der Meijden E., de Graaf J., ter Schegget J., Struyk L. A functional NF-kappaB binding site in the human papillomavirus type 16 long control region. Virology 2000, 272(1):40-49.
11. Georgopoulos N.T., Proffitt J.L., Blair G.E. Transcriptional regulation of the major histocompatibility complex (MHC) class I heavy chain, TAP1 and LMP2 genes by the human papillomavirus (HPV) type 6b, 16 and 18 E7 oncoproteins. Oncogene 2000, 19(42):4930-4935.
12. Greten F.R., Eckmann L., Greten T.F., Park J.M., Li Z.W., Egan L.J., Kagnoff M.F., Karin M. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004, 118(3):285-296.
13. Halbert C.L., Demers G.W., Galloway D.A. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 1991, 65(1):473-478.
14. Hasan U.A., Bates E., Takeshita F., Biliato A., Accardi R., Bouvard V., Mansour M., Vincent I., Gissmann L., Iftner T., Sideri M., Stubenrauch F., Tommasino M. TLR9 expression and function is abolished by the cervical cancer-associated human papillomavirus type 16. J. Immunol. 2007, 178(5):3186-3197.
15. Havard L., Delvenne P., Frare P., Boniver J., Giannini S.L. Differential production of cytokines and activation of NF-kappaB in HPV-transformed keratinocytes. Virology 2002, 298(2):271-285.
16. Havard L., Rahmouni S., Boniver J., Delvenne P. High levels of p105 (NFKB1) and p100 (NFKB2) proteins in HPV16-transformed keratinocytes: role of E6 and E7 oncoproteins. Virology 2005, 331(2):357-366.
17. Hayden M.S., West A.P., Ghosh S. NF-kappaB and the immune response. Oncogene 2006, 25(51):6758-6780.
18. Hinata K., Gervin A.M., Jennifer Zhang Y., Khavari P.A. Divergent gene regulation and growth effects by NF-kappa B in epithelial and mesenchymal cells of human skin. Oncogene 2003, 22(13):1955-1964.
19. Hiscott J., Nguyen T.L., Arguello M., Nakhaei P., Paz S. Manipulation of the nuclear factor-kappaB pathway and the innate immune response by viruses. Oncogene 2006, 25(51):6844-6867.
20. Huang S.M., McCance D.J. Down regulation of the interleukin-8 promoter by human papillomavirus type 16 E6 and E7 through effects on CREB binding protein/p300 and P/CAF. J. Virol. 2002, 76(17):8710-8721.
21. Hussain I., Fathallah I., Accardi R., Yue J., Saidj D., Shukla R., Hasan U., Gheit T., Niu Y., Tommasino M., Sylla B.S. NF-{kappa}B protects HPV38E6/E7-immortalized human keratinocyte against TNF-{alpha} and UV-mediated apoptosis. J. Virol. 2011, 85(17):9013-9022.
22. James M.A., Lee J.H., Klingelhutz A.J. Human papillomavirus type 16 E6 activates NF-kappaB, induces cIAP-2 expression, and protects against apoptosis in a PDZ binding motif-dependent manner. J. Virol. 2006, 80(11):5301-5307.
23. Jones D.L., Thompson D.A., Munger K. Destabilization of the RB tumor suppressor protein and stabilization of p53 contribute to HPV type 16 E7-induced apoptosis. Virology 1997, 239(1):97-107.
24. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006, 441(7092):431-436.
25. Karin M. NF-kappaB as a critical link between inflammation and cancer. Cold Spring Harb. Perspect. Biol. 2009, 1(5):a000141.
26. Khan M.A., Canhoto A.J., Housley P.R., Creek K.E., Pirisi L. Glucocorticoids stimulate growth of human papillomavirus type 16 (HPV16)-immortalized human keratinocytes and support HPV16-mediated immortalization without affecting the levels of HPV16 E6/E7 mRNA. Exp. Cell Res. 1997, 236(1):304-310.
27. Klingelhutz A.J., Foster S.A., McDougall J.K. Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 1996, 380(6569):79-82.
28. Li Q., Withoff S., Verma I.M. Inflammation-associated cancer: NF-kappaB is the lynchpin. Trends Immunol. 2005, 26(6):318-325.
29. Maeda S., Kamata H., Luo J.L., Leffert H., Karin M. IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 2005, 121(7):977-990.
30. Munger K., Phelps W.C., Bubb V., Howley P.M., Schlegel R. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J. Virol. 1989, 63(10):4417-4421.
31. Nair A., Venkatraman M., Maliekal T.T., Nair B., Karunagaran D. NF-kappaB is constitutively activated in high-grade squamous intraepithelial lesions and squamous cell carcinomas of the human uterine cervix. Oncogene 2003, 22(1):50-58.
32. Nees M., Geoghegan J.M., Hyman T., Frank S., Miller L., Woodworth C.D. Papillomavirus type 16 oncogenes downregulate expression of interferon-responsive genes and upregulate proliferation-associated and NF-kappaB-responsive genes in cervical keratinocytes. J. Virol. 2001, 75(9):4283-4296.
33. Perea S.E., Massimi P., Banks L. Human papillomavirus type 16 E7 impairs the activation of the interferon regulatory factor-1. Int. J. Mol. Med. 2000, 5(6):661-666.
34. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29(9):e45.
35. Pikarsky E., Porat R.M., Stein I., Abramovitch R., Amit S., Kasem S., Gutkovich-Pyest E., Urieli-Shoval S., Galun E., Ben-Neriah Y. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004, 431(7007):461-466.
36. Prusty B.K., Husain S.A., Das B.C. Constitutive activation of nuclear factor -kB: preferntial homodimerization of p50 subunits in cervical carcinoma. Front. Biosci. 2005, 10:1510-1519.
37. Ronco L.V., Karpova A.Y., Vidal M., Howley P.M. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev. 1998, 12(13):2061-2072.
38. Rovillain E., Mansfield L., Caetano C., Alvarez-Fernandez M., Caballero O.L., Medema R.H., Hummerich H., Jat P.S. Activation of nuclear factor-kappa B signalling promotes cellular senescence. Oncogene 2011, 30(20):2356-2366.
39. Scheffner M., Werness B.A., Huibregtse J.M., Levine A.J., Howley P.M. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990, 63(6):1129-1136.
40. Seitz C.S., Lin Q., Deng H., Khavari P.A. Alterations in NF-kappaB function in transgenic epithelial tissue demonstrate a growth inhibitory role for NF-kappaB. Proc. Natl. Acad. Sci. U. S. A. 1998, 95(5):2307-2312.
41. Spitkovsky D., Hehner S.P., Hofmann T.G., Moller A., Schmitz M.L. The human papillomavirus oncoprotein E7 attenuates NF-kappa B activation by targeting the Ikappa B kinase complex. J. Biol. Chem. 2002, 277(28):25576-25582.
42. Takebayashi T., Higashi H., Sudo H., Ozawa H., Suzuki E., Shirado O., Katoh H., Hatakeyama M. NF-kappa B-dependent induction of cyclin D1 by retinoblastoma protein (pRB) family proteins and tumor-derived pRB mutants. J. Biol. Chem. 2003, 278(17):14897-14905.
43. Van Antwerp D.J., Martin S.J., Kafri T., Green D.R., Verma I.M. Suppression of TNF-alpha-induced apoptosis by NF-kappaB. Science 1996, 274(5288):787-789.
44. van Hogerlinden M., Rozell B.L., Ahrlund-Richter L., Toftgard R. Squamous cell carcinomas and increased apoptosis in skin with inhibited Rel/nuclear factor-kappaB signaling. Cancer Res. 1999, 59(14):3299-3303.
45. Venkatraman M., Anto R.J., Nair A., Varghese M., Karunagaran D. Biological and chemical inhibitors of NF-kappaB sensitize SiHa cells to cisplatin-induced apoptosis. Mol. Carcinog. 2005, 44(1):51-59.
46. von Knebel Doeberitz M., Rittmuller C., zur Hausen H., Durst M. Inhibition of tumorigenicity of cervical cancer cells in nude mice by HPV E6-E7 anti-sense RNA. Int. J. Cancer 1992, 51(5):831-834.
47. Webster G.A., Perkins N.D. Transcriptional cross talk between NF-kappaB and p53. Mol. Cell. Biol. 1999, 19(5):3485-3495.
48. Woodworth C.D., Simpson S. Comparative lymphokine secretion by cultured normal human cervical keratinocytes, papillomavirus-immortalized, and carcinoma cell lines. Am. J. Pathol. 1993, 142(5):1544-1555.
49. Woodworth C., Secott T., Isom H.C. Transformation of rat hepatocytes by transfection with simian virus 40 DNA to yield proliferating differentiated cells. Cancer Res. 1986, 46(8):4018-4026.
50. Woodworth C.D., Bowden P.E., Doniger J., Pirisi L., Barnes W., Lancaster W.D., DiPaolo J.A. Characterization of normal human exocervical epithelial cells immortalized in vitro by papillomavirus types 16 and 18 DNA. Cancer Res. 1988, 48(16):4620-4628.
51. Woodworth C.D., Waggoner S., Barnes W., Stoler M.H., DiPaolo J.A. Human cervical and foreskin epithelial cells immortalized by human papillomavirus DNAs exhibit dysplastic differentiation in vivo. Cancer Res. 1990, 50(12):3709-3715.
52. Woodworth C.D., Cheng S., Simpson S., Hamacher L., Chow L.T., Broker T.R., DiPaolo J.A. Recombinant retroviruses encoding human papillomavirus type 18 E6 and E7 genes stimulate proliferation and delay differentiation of human keratinocytes early after infection. Oncogene 1992, 7(4):619-626.
53. Woodworth C.D., McMullin E., Iglesias M., Plowman G.D. Interleukin 1 alpha and tumor necrosis factor alpha stimulate autocrine amphiregulin expression and proliferation of human papillomavirus-immortalized and carcinoma-derived cervical epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 1995, 92(7):2840-2844.
54. Xu M., Katzenellenbogen R.A., Grandori C., Galloway D.A. NFX1 plays a role in human papillomavirus type 16 E6 activation of NFkappaB activity. J. Virol. 2010, 84(21):11461-11469.
55. Zhang J.Y., Green C.L., Tao S., Khavari P.A. NF-kappaB RelA opposes epidermal proliferation driven by TNFR1 and JNK. Genes Dev. 2004, 18(1):17-22.