Human papillomavirus type 16 E5 oncoprotein as a new target for cervical cancer treatment

Biochemical Pharmacology

Volumn 80, Issue 12, 2010, Pages 1930-1935

  Kim, Mi Kyung ^a   Kim, Hee Seung ^a   Kim, Su Hyeong ^a   Oh, Jung Min ^a   Han, Jae Yong ^b   Lim, Jeong Mook ^b   Juhnn, Yong Sung ^a   Song, Yong Sang ^a,b  

^a Seoul National University College of Medicine   (South Korea)

^b Seoul National University   (South Korea)

Author keywords

Cervical cancer; COX 2; E5; EGFR; Human papillomavirus

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; ONCOPROTEIN; ONCOPROTEIN E5; TUMOR VACCINE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANGIOGENESIS; APOPTOSIS; CANCER THERAPY; CARCINOGENESIS; CELL PROLIFERATION; DRUG MECHANISM; GENE TARGETING; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; INFLAMMATORY CELL; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; REVIEW; UTERINE CERVIX CANCER;

ANIMALS; APOPTOSIS; CANCER VACCINES; CELL PROLIFERATION; FEMALE; GENE THERAPY; HUMANS; MOLECULAR TARGETED THERAPY; NEOVASCULARIZATION, PATHOLOGIC; ONCOGENE PROTEINS, VIRAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; UTERINE CERVICAL NEOPLASMS;

EID: 78049451565     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bcp.2010.07.013     Document Type: Review

References (87)

1. Parkin D.M., Bray F., Ferlay J., Pisani P. Global cancer statistics, 2002. CA: A Cancer Journal for Clinicians 2005, 55:74-108.
2. Moore D.H., Blessing J.A., McQuellon R.P., Thaler H.T., Cella D., Benda J., et al. Phase III study of cisplatin with or without paclitaxel in stage IVB, recurrent, or persistent squamous cell carcinoma of the cervix: a gynecologic oncology group study. Journal of Clinical Oncology 2004, 22:3113-3119.
3. Monk B.J., Sill M.W., McMeekin D.S., Cohn D.E., Ramondetta L.M., Boardman C.H., et al. Phase III trial of four cisplatin-containing doublet combinations in stage IVB, recurrent, or persistent cervical carcinoma: a gynecologic oncology group study. Journal of Clinical Oncology 2009, 27:4649-4655.
4. zur Hausen H., de Villiers E.M. Human papillomaviruses. Annual Review of Microbiology 1994, 48:427-447.
5. Clifford G.M., Smith J.S., Plummer M., Munoz N., Franceschi S. Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis. British Journal of Cancer 2003, 88:63-73.
6. Smith J.S., Lindsay L., Hoots B., Keys J., Franceschi S., Winer R., et al. Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. International Journal of Cancer 2007, 121:621-632.
7. Paavonen J., Jenkins D., Bosch F.X., Naud P., Salmeron J., Wheeler C.M., et al. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial. Lancet 2007, 369:2161-2170.
8. Quadrivalent vaccine against human papillomavirus to prevent high-grade cervical lesions. The New England Journal of Medicine 2007, 356:1915-1927. The Future II Study Group.
9. zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nature Reviews 2002, 2:342-350.
10. Werness B.A., Levine A.J., Howley P.M. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science (New York, NY) 1990, 248:76-79.
11. Dyson N., Howley P.M., Munger K., Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science (New York, NY) 1989, 243:934-937.
12. Conrad M., Bubb V.J., Schlegel R. The human papillomavirus type 6 and 16 E5 proteins are membrane-associated proteins which associate with the 16-kilodalton pore-forming protein. Journal of Virology 1993, 67:6170-6178.
13. 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.
14. Straight S.W., Hinkle P.M., Jewers R.J., McCance D.J. The E5 oncoprotein of human papillomavirus type 16 transforms fibroblasts and effects the downregulation of the epidermal growth factor receptor in keratinocytes. Journal of Virology 1993, 67:4521-4532.
15. Chen S.L., Huang C.H., Tsai T.C., Lu K.Y., Tsao Y.P. The regulation mechanism of c-jun and junB by human papillomavirus type 16 E5 oncoprotein. Archives of Virology 1996, 141:791-800.
16. Valle G.F., Banks L. The human papillomavirus (HPV)-6 and HPV-16 E5 proteins co-operate with HPV-16 E7 in the transformation of primary rodent cells. The Journal of General Virology 1995, 76(Pt 5):1239-1245.
17. Genther Williams S.M., Disbrow G.L., Schlegel R., Lee D., Threadgill D.W., Lambert P.F. Requirement of epidermal growth factor receptor for hyperplasia induced by E5, a high-risk human papillomavirus oncogene. Cancer Research 2005, 65:6534-6542.
18. Maufort J.P., Williams S.M., Pitot H.C., Lambert P.F. Human papillomavirus 16 E5 oncogene contributes to two stages of skin carcinogenesis. Cancer Research 2007, 67:6106-6112.
19. Maufort J.P., Shai A., Pitot H.C., Lambert P.F. A role for HPV16 E5 in cervical carcinogenesis. Cancer Research 2010, 70:2924-2931.
20. Oelze I., Kartenbeck J., Crusius K., Alonso A. Human papillomavirus type 16 E5 protein affects cell-cell communication in an epithelial cell line. Journal of Virology 1995, 69:4489-4494.
21. Tomakidi P., Cheng H., Kohl A., Komposch G., Alonso A. Connexin 43 expression is downregulated in raft cultures of human keratinocytes expressing the human papillomavirus type 16 E5 protein. Cell and Tissue Research 2000, 301:323-327.
22. DiMaio D., Mattoon D. Mechanisms of cell transformation by papillomavirus E5 proteins. Oncogene 2001, 20:7866-7873.
23. Schwarz E., Freese U.K., Gissmann L., Mayer W., Roggenbuck B., Stremlau A., et al. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 1985, 314:111-114.
24. Chang J.L., Tsao Y.P., Liu D.W., Huang S.J., Lee W.H., Chen S.L. The expression of HPV-16 E5 protein in squamous neoplastic changes in the uterine cervix. Journal of Biomedical Science 2001, 8:206-213.
25. Dannenberg A.J., Lippman S.M., Mann J.R., Subbaramaiah K., DuBois R.N. Cyclooxygenase-2 and epidermal growth factor receptor: pharmacologic targets for chemoprevention. Journal of Clinical Oncology 2005, 23:254-266.
26. Straight S.W., Herman B., McCance D.J. The E5 oncoprotein of human papillomavirus type 16 inhibits the acidification of endosomes in human keratinocytes. Journal of Virology 1995, 69:3185-3192.
27. Pim D., Collins M., Banks L. Human papillomavirus type 16 E5 gene stimulates the transforming activity of the epidermal growth factor receptor. Oncogene 1992, 7:27-32.
28. Crusius K., Auvinen E., Steuer B., Gaissert H., Alonso A. The human papillomavirus type 16 E5-protein modulates ligand-dependent activation of the EGF receptor family in the human epithelial cell line HaCaT. Experimental Cell Research 1998, 241:76-83.
29. Tomakidi P., Cheng H., Kohl A., Komposch G., Alonso A. Modulation of the epidermal growth factor receptor by the human papillomavirus type 16 E5 protein in raft cultures of human keratinocytes. European Journal of Cell Biology 2000, 79:407-412.
30. Crusius K., Rodriguez I., Alonso A. The human papillomavirus type 16 E5 protein modulates ERK1/2 and p38 MAP kinase activation by an EGFR-independent process in stressed human keratinocytes. Virus Genes 2000, 20:65-69.
31. Crusius K., Auvinen E., Alonso A. Enhancement of EGF- and PMA-mediated MAP kinase activation in cells expressing the human papillomavirus type 16 E5 protein. Oncogene 1997, 15:1437-1444.
32. Gu Z., Matlashewski G. Effect of human papillomavirus type 16 oncogenes on MAP kinase activity. Journal of Virology 1995, 69:8051-8056.
33. Bouvard V., Matlashewski G., Gu Z.M., Storey A., Banks L. The human papillomavirus type 16 E5 gene cooperates with the E7 gene to stimulate proliferation of primary cells and increases viral gene expression. Virology 1994, 203:73-80.
34. Chen S.L., Lin Y.K., Li L.Y., Tsao Y.P., Lo H.Y., Wang W.B., et al. E5 proteins of human papillomavirus types 11 and 16 transactivate the c-fos promoter through the NF1 binding element. Journal of Virology 1996, 70:8558-8563.
35. Hwang E.S., Nottoli T., Dimaio D. The HPV16 E5 protein: expression, detection, and stable complex formation with transmembrane proteins in COS cells. Virology 1995, 211:227-233.
36. Chen S.L., Lin S.T., Tsai T.C., Hsiao W.C., Tsao Y.P. ErbB4 (JM-b/CYT-1)-induced expression and phosphorylation of c-Jun is abrogated by human papillomavirus type 16 E5 protein. Oncogene 2007, 26:42-53.
37. Venuti A., Salani D., Poggiali F., Manni V., Bagnato A. The E5 oncoprotein of human papillomavirus type 16 enhances endothelin-1-induced keratinocyte growth. Virology 1998, 248:1-5.
38. Tsao Y.P., Li L.Y., Tsai T.C., Chen S.L. Human papillomavirus type 11 and 16 E5 represses p21(WafI/SdiI/CipI) gene expression in fibroblasts and keratinocytes. Journal of Virology 1996, 70:7535-7539.
39. Pedroza-Saavedra A., Lam E.W., Esquivel-Guadarrama F., Gutierrez-Xicotencatl L. The human papillomavirus type 16 E5 oncoprotein synergizes with EGF-receptor signaling to enhance cell cycle progression and the down-regulation of p27(Kip1). Virology 2010, 400:44-52.
40. Eberhart C.E., Coffey R.J., Radhika A., Giardiello F.M., Ferrenbach S., DuBois R.N. Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterology 1994, 107:1183-1188.
41. Ristimaki A., Honkanen N., Jankala H., Sipponen P., Harkonen M. Expression of cyclooxygenase-2 in human gastric carcinoma. Cancer Research 1997, 57:1276-1280.
42. Kondo M., Yamamoto H., Nagano H., Okami J., Ito Y., Shimizu J., et al. Increased expression of COX-2 in nontumor liver tissue is associated with shorter disease-free survival in patients with hepatocellular carcinoma. Clinical Cancer Research 1999, 5:4005-4012.
43. Kulkarni S., Rader J.S., Zhang F., Liapis H., Koki A.T., Masferrer J.L., et al. Cyclooxygenase-2 is overexpressed in human cervical cancer. Clinical Cancer Research 2001, 7:429-434.
44. Kim J.Y., Lim S.J., Park K., Lee C.M., Kim J. Cyclooxygenase-2 and c-erbB-2 expression in uterine cervical neoplasm assessed using tissue microarrays. Gynecologic Oncology 2005, 97:337-341.
45. Kim K., Jeon Y.T., Park I.A., Kim J.W., Park N.H., Kang S.B., et al. Cyclooxygenase-2 expression in cervical intraepithelial neoplasia. Annals of the New York Academy of Sciences 2009, 1171:111-115.
46. Farley J.H., Truong V., Goo E., Uyehara C., Belnap C., Larsen W.I. A randomized double-blind placebo-controlled phase II trial of the cyclooxygenase-2 inhibitor Celecoxib in the treatment of cervical dysplasia. Gynecologic Oncology 2006, 103:425-430.
47. Hefler L.A., Grimm C., Speiser P., Sliutz G., Reinthaller A. The cyclooxygenase-2 inhibitor rofecoxib (Vioxx) in the treatment of cervical dysplasia grade II-III A phase II trial. European Journal of Obstetrics, Gynecology, and Reproductive Biology 2006, 125:251-254.
48. Ferrandina G., Lauriola L., Distefano M.G., Zannoni G.F., Gessi M., Legge F., et al. Increased cyclooxygenase-2 expression is associated with chemotherapy resistance and poor survival in cervical cancer patients. Journal of Clinical Oncology 2002, 20:973-981.
49. Gaffney D.K., Holden J., Davis M., Zempolich K., Murphy K.J., Dodson M. Elevated cyclooxygenase-2 expression correlates with diminished survival in carcinoma of the cervix treated with radiotherapy. International Journal of Radiation Oncology, Biology, Physics 2001, 49:1213-1217.
50. Kim M.H., Seo S.S., Song Y.S., Kang D.H., Park I.A., Kang S.B., et al. Expression of cyclooxygenase-1 and -2 associated with expression of VEGF in primary cervical cancer and at metastatic lymph nodes. Gynecologic Oncology 2003, 90:83-90.
51. Kang S., Kim M.H., Park I.A., Kim J.W., Park N.H., Kang D., et al. Elevation of cyclooxygenase-2 is related to lymph node metastasis in adenocarcinoma of uterine cervix. Cancer Letters 2006, 237:305-311.
52. Subbaramaiah K., Dannenberg A.J. Cyclooxygenase-2 transcription is regulated by human papillomavirus 16 E6 and E7 oncoproteins: evidence of a corepressor/coactivator exchange. Cancer Research 2007, 67:3976-3985.
53. Kim S.H., Oh J.M., No J.H., Bang Y.J., Juhnn Y.S., Song Y.S. Involvement of NF-kappaB and AP-1 in COX-2 upregulation by human papillomavirus 16 E5 oncoprotein. Carcinogenesis 2009, 30:753-757.
54. Greenhough A., Smartt H.J., Moore A.E., Roberts H.R., Williams A.C., Paraskeva C., et al. The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment. Carcinogenesis 2009, 30:377-386.
55. Oh J.M., Kim S.H., Lee Y.I., Seo M., Kim S.Y., Song Y.S., et al. Human papillomavirus E5 protein induces expression of the EP4 subtype of prostaglandin E2 receptor in cyclic AMP response element-dependent pathways in cervical cancer cells. Carcinogenesis 2009, 30:141-149.
56. Sales K.J., Katz A.A., Davis M., Hinz S., Soeters R.P., Hofmeyr M.D., et al. Cyclooxygenase-2 expression and prostaglandin E(2) synthesis are up-regulated in carcinomas of the cervix: a possible autocrine/paracrine regulation of neoplastic cell function via EP2/EP4 receptors. The Journal of Clinical Endocrinology and Metabolism 2001, 86:2243-2249.
57. Chell S.D., Witherden I.R., Dobson R.R., Moorghen M., Herman A.A., Qualtrough D., et al. Increased EP4 receptor expression in colorectal cancer progression promotes cell growth and anchorage independence. Cancer Research 2006, 66:3106-3113.
58. Mutoh M., Watanabe K., Kitamura T., Shoji Y., Takahashi M., Kawamori T., et al. Involvement of prostaglandin E receptor subtype EP(4) in colon carcinogenesis. Cancer Research 2002, 62:28-32.
59. Ma X., Kundu N., Rifat S., Walser T., Fulton A.M. Prostaglandin E receptor EP4 antagonism inhibits breast cancer metastasis. Cancer Research 2006, 66:2923-2927.
60. Hanahan D., Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996, 86:353-364.
61. Folkman J., Hanahan D. Switch to the angiogenic phenotype during tumorigenesis. Princess Takamatsu Symposia 1991, 22:339-347.
62. Kerbel R.S. Tumor angiogenesis. The New England Journal of Medicine 2008, 358:2039-2049.
63. Spannuth W.A., Sood A.K., Coleman R.L. Angiogenesis as a strategic target for ovarian cancer therapy. Nature Clinical Practice 2008, 5:194-204.
64. Paley P.J., Staskus K.A., Gebhard K., Mohanraj D., Twiggs L.B., Carson L.F., et al. Vascular endothelial growth factor expression in early stage ovarian carcinoma. Cancer 1997, 80:98-106.
65. Ishigami S.I., Arii S., Furutani M., Niwano M., Harada T., Mizumoto M., et al. Predictive value of vascular endothelial growth factor (VEGF) in metastasis and prognosis of human colorectal cancer. British Journal of Cancer 1998, 78:1379-1384.
66. Ohta Y., Tomita Y., Oda M., Watanabe S., Murakami S., Watanabe Y. Tumor angiogenesis and recurrence in stage I non-small cell lung cancer. The Annals of Thoracic Surgery 1999, 68:1034-1038.
67. Cheng W.F., Chen C.A., Lee C.N., Wei L.H., Hsieh F.J., Hsieh C.Y. Vascular endothelial growth factor and prognosis of cervical carcinoma. Obstetrics and Gynecology 2000, 96:721-726.
68. Toussaint-Smith E., Donner D.B., Roman A. Expression of human papillomavirus type 16 E6 and E7 oncoproteins in primary foreskin keratinocytes is sufficient to alter the expression of angiogenic factors. Oncogene 2004, 23:2988-2995.
69. Tang X., Zhang Q., Nishitani J., Brown J., Shi S., Le A.D. Overexpression of human papillomavirus type 16 oncoproteins enhances hypoxia-inducible factor 1 alpha protein accumulation and vascular endothelial growth factor expression in human cervical carcinoma cells. Clinical Cancer Research 2007, 13:2568-2576.
70. Kim S.H., Juhnn Y.S., Kang S., Park S.W., Sung M.W., Bang Y.J., et al. Human papillomavirus 16 E5 up-regulates the expression of vascular endothelial growth factor through the activation of epidermal growth factor receptor MEK/ERK1,2 and PI3K/Akt. Cellular and Molecular Life Science 2006, 63:930-938.
71. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
72. Arechaga-Ocampo E., Pereira-Suarez A.L., del Moral-Hernandez O., Cedillo-Barron L., Rodriguez-Sastre M.A., Castillo-Alvarez A., et al. HPV+ cervical carcinomas and cell lines display altered expression of caspases. Gynecologic Oncology 2008, 108:10-18.
73. Das H., Koizumi T., Sugimoto T., Chakraborty S., Ichimura T., Hasegawa K., et al. Quantitation of Fas and Fas ligand gene expression in human ovarian, cervical and endometrial carcinomas using real-time quantitative RT-PCR. British Journal of Cancer 2000, 82:1682-1688.
74. 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, 63:1129-1136.
75. Thomas M., Banks L. Inhibition of Bak-induced apoptosis by HPV-18 E6. Oncogene 1998, 17:2943-2954.
76. Filippova M., Parkhurst L., Duerksen-Hughes P.J. The human papillomavirus 16 E6 protein binds to Fas-associated death domain and protects cells from Fas-triggered apoptosis. The Journal of Biological Chemistry 2004, 279:25729-25744.
77. Gross-Mesilaty S., Reinstein E., Bercovich B., Tobias K.E., Schwartz A.L., Kahana C., et al. Basal and human papillomavirus E6 oncoprotein-induced degradation of Myc proteins by the ubiquitin pathway. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:8058-8063.
78. Kabsch K., Alonso A. The human papillomavirus type 16 E5 protein impairs TRAIL- and FasL-mediated apoptosis in HaCaT cells by different mechanisms. Journal of Virology 2002, 76:12162-12172.
79. Zhang B., Spandau D.F., Roman A. E5 protein of human papillomavirus type 16 protects human foreskin keratinocytes from UV B-irradiation-induced apoptosis. Journal of Virology 2002, 76:220-231.
80. Oh J.M., Kim S.H., Cho E.A., Song Y.S., Kim W.H., Juhnn Y.S. Human papillomavirus type 16 E5 protein inhibits hydrogen-peroxide-induced apoptosis by stimulating ubiquitin-proteasome-mediated degradation of Bax in human cervical cancer cells. Carcinogenesis 2010, 31:402-410.
81. Kabsch K., Alonso A. The human papillomavirus type 16 (HPV-16) E5 protein sensitizes human keratinocytes to apoptosis induced by osmotic stress. Oncogene 2002, 21:947-953.
82. Liu D.W., Tsao Y.P., Hsieh C.H., Hsieh J.T., Kung J.T., Chiang C.L., et al. Induction of CD8 T cells by vaccination with recombinant adenovirus expressing human papillomavirus type 16 E5 gene reduces tumor growth. Journal of Virology 2000, 74:9083-9089.
83. Chen Y.F., Lin C.W., Tsao Y.P., Chen S.L. Cytotoxic-T-lymphocyte human papillomavirus type 16 E5 peptide with CpG-oligodeoxynucleotide can eliminate tumor growth in C57BL/6 mice. Journal of Virology 2004, 78:1333-1343.
84. Wang W., Sima N., Kong D., Luo A., Gao Q., Liao S., et al. Selective targeting of HPV-16 E6/E7 in cervical cancer cells with a potent oncolytic adenovirus and its enhanced effect with radiotherapy in vitro and vivo. Cancer Letters 2010, 291:67-75.
85. Wang X.G., Revskaya E., Bryan R.A., Strickler H.D., Burk R.D., Casadevall A., et al. Treating cancer as an infectious disease-viral antigens as novel targets for treatment and potential prevention of tumors of viral etiology. PloS One 2007, 2:e1114.
86. Sima N., Wang W., Kong D., Deng D., Xu Q., Zhou J., et al. RNA interference against HPV16 E7 oncogene leads to viral E6 and E7 suppression in cervical cancer cells and apoptosis via upregulation of Rb and p53. Apoptosis 2008, 13:273-281.
87. Jonson A.L., Rogers L.M., Ramakrishnan S., Downs L.S. Gene silencing with siRNA targeting E6/E7 as a therapeutic intervention in a mouse model of cervical cancer. Gynecologic Oncology 2008, 111:356-364.