Unravelling the biology of human papillomavirus (HPV) related tumours to enhance their radiosensitivity

Cancer Treatment Reviews

Volumn 36, Issue 8, 2010, Pages 629-636

  Vozenin, Marie Catherine ^a,b   Lord, Hannah Kate ^a   Hartl, Dana ^a   Deutsch, Eric ^a  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

HPV; New treatments; Oncoprotein; Radiosensitivity

Indexed keywords

CIDOFOVIR; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; EPIDERMAL GROWTH FACTOR RECEPTOR; GLUCOCORTICOID ANTAGONIST; MIFEPRISTONE; PROTEIN E6; PROTEIN E7; VASCULOTROPIN;

CANCER RADIOTHERAPY; CYTOMEGALOVIRUS INFECTION; DRUG MECHANISM; ENZYME INHIBITION; HEAD AND NECK CANCER; HUMAN; NONHUMAN; PROTEIN EXPRESSION; RADIOSENSITIVITY; REVIEW; SQUAMOUS CELL CARCINOMA; TREATMENT RESPONSE; TUMOR CELL; UTERINE CERVIX CANCER; UTERINE CERVIX CARCINOMA; WART VIRUS;

CARCINOMA, SQUAMOUS CELL; CELL TRANSFORMATION, NEOPLASTIC; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; MALE; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; PRECANCEROUS CONDITIONS; PROGNOSIS; RADIATION TOLERANCE; RADIATION-SENSITIZING AGENTS; TREATMENT OUTCOME; UTERINE CERVICAL NEOPLASMS;

EID: 78349308937     PISSN: 03057372     EISSN: 15321967     Source Type: Journal    
DOI: 10.1016/j.ctrv.2010.03.010     Document Type: Review

References (88)

1. Zur Hausen H. Papillomaviruses in the causation of human cancers - a brief historical account. Virology 2009, 392(1):1-100.
2. IARC IARC working group on the evaluation of carcinogenic risks to humans (1995) human papillomaviruses. IARC Monogr Eval Carcinogen Risks Hum 1995.
3. Matsukura T., Koi S., Sugase M. Both episomal and integrated forms of human papillomavirus type 16 are involved in invasive cervical cancers. Virology 1989, 172(1):63-72.
4. Fuchs P.G., Girardi F., Pfister H. Human papillomavirus 16 DNA in cervical cancers and in lymph nodes of cervical cancer patients: a diagnostic marker for early metastases?. Int J Cancer 1989, 43(1):41-44.
5. Lazo P.A. The molecular genetics of cervical carcinoma. Br J Cancer 1999, 80(12):2008-2018.
6. Frisch M., Glimelius B., van den Brule A.J., et al. Sexually transmitted infection as a cause of anal cancer. N Engl J Med 1997, 337(19):1350-1358.
7. Palefsky J.M., Holly E.A., Gonzales J., Berline J., Ahn D.K., Greenspan J.S. Detection of human papillomavirus DNA in anal intraepithelial neoplasia and anal cancer. Cancer Res 1991, 51(3):1014-1019.
8. Gillison M.L., Shah K.V. Human papillomavirus-associated head and neck squamous cell carcinoma: mounting evidence for an etiologic role for human papillomavirus in a subset of head and neck cancers. Curr Opin Oncol 2001, 13(3):183-188.
9. Paz I.B., Cook N., Odom-Maryon T., Xie Y., Wilczynski S.P. Human papillomavirus (HPV) in head and neck cancer. An association of HPV 16 with squamous cell carcinoma of Waldeyer's tonsillar ring. Cancer 1997, 79(3):595-604.
10. Park M.S., Chang Y.S., Shin J.H., et al. The prevalence of human papillomavirus infection in Korean non-small cell lung cancer patients. Yonsei Med J 2007, 48(1):69-77.
11. Lindel K., Forster A., Altermatt H.J., Greiner R., Gruber G. Breast cancer and human papillomavirus (HPV) infection: no evidence of a viral etiology in a group of Swiss women. Breast 2007, 16(2):172-177.
12. Schwartz S.R., Yueh B., McDougall J.K., Daling J.R., Schwartz S.M. Human papillomavirus infection and survival in oral squamous cell cancer: a population-based study. Otolaryngol Head Neck Surg 2001, 125(1):1-9.
13. Licitra L., Perrone F., Bossi P., et al. High-risk human papillomavirus affects prognosis in patients with surgically treated oropharyngeal squamous cell carcinoma. J Clin Oncol 2006, 24(36):5630-5636.
14. Van der Kogel A, Joiner M, editors. Basic clinical radiobiology. 4th ed.; 2009.
15. Yount G.L., Haas-Kogan D.A., Vidair C.A., Haas M., Dewey W.C., Israel M.A. Cell cycle synchrony unmasks the influence of p53 function on radiosensitivity of human glioblastoma cells. Cancer Res 1996, 56(3):500-506.
16. Wouters B.G., van den Beucken T., Magagnin M.G., Koritzinsky M., Fels D., Koumenis C. Control of the hypoxic response through regulation of mRNA translation. Semin Cell Dev Biol 2005, 16(4-5):487-501.
17. Lu Y., Wang H., Mills G.B. Targeting PI3K-AKT pathway for cancer therapy. Rev Clin Exp Hematol 2003, 7(2):205-228.
18. Gupta A.K., Cerniglia G.J., Mick R., et al. Radiation sensitization of human cancer cells in vivo by inhibiting the activity of PI3K using LY294002. Int J Radiat Oncol Biol Phys 2003, 56(3):846-853.
19. Vozenin MC, Bourhis J, Deutsch E. What have we learned from HPV positive tumors? Trying to connect data about biomarkers among HPV related squamous cell carcinomas. J Clin Oncol, in press.
20. Gillison M.L., Koch W.M., Capone R.B., et al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst 2000, 92(9):709-720.
21. D'Souza G., Kreimer A.R., Viscidi R., et al. Case-control study of human papillomavirus and oropharyngeal cancer. N Engl J Med 2007, 356(19):1944-1956.
22. Le Q.T., Giaccia A.J. Therapeutic exploitation of the physiological and molecular genetic alterations in head and neck cancer. Clin Cancer Res 2003, 9(12):4287-4295.
23. Fakhry C., Gillison M.L. Clinical implications of human papillomavirus in head and neck cancers. J Clin Oncol 2006, 24(17):2606-2611.
24. Weinberger P.M., Yu Z., Haffty B.G., et al. Prognostic significance of p16 protein levels in oropharyngeal squamous cell cancer. Clin Cancer Res 2004, 10(17):5684-5691.
25. Bova R.J., Quinn D.I., Nankervis J.S., et al. Cyclin D1 and p16INK4A expression predict reduced survival in carcinoma of the anterior tongue. Clin Cancer Res 1999, 5(10):2810-2819.
26. Fischer C.A., Zlobec I., Green E., et al. Is the improved prognosis of p16 positive oropharyngeal squamous cell carcinoma dependent of the treatment modality?. Int J Cancer 2009.
27. Ragin C.C., Taioli E. Survival of squamous cell carcinoma of the head and neck in relation to human papillomavirus infection: review and meta-analysis. Int J Cancer 2007, 121(8):1813-1820.
28. Perrone F., Suardi S., Pastore E., et al. Molecular and cytogenetic subgroups of oropharyngeal squamous cell carcinoma. Clin Cancer Res 2006, 12(22):6643-6651.
29. Sisk E.A., Soltys S.G., Zhu S., Fisher S.G., Carey T.E., Bradford C.R. Human papillomavirus and p53 mutational status as prognostic factors in head and neck carcinoma. Head Neck 2002, 24(9):841-849.
30. Worden F.P., Kumar B., Lee J.S., et al. Chemoselection as a strategy for organ preservation in advanced oropharynx cancer: response and survival positively associated with HPV16 copy number. J Clin Oncol 2008, 26(19):3138-3146.
31. Fakhry C., Westra W.H., Li S., et al. Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J Natl Cancer Inst 2008, 100(4):261-269.
32. Lassen P., Eriksen J.G., Hamilton-Dutoit S., Tramm T., Alsner J., Overgaard J. Effect of HPV-associated p16INK4A expression on response to radiotherapy and survival in squamous cell carcinoma of the head and neck. J Clin Oncol 2009, 27(12):1992-1998.
33. Lassen P., Eriksen J.G., Hamilton-Dutoit S., Tramm T., Alsner J., Overgaard J. HPV-associated p16-expression and response to hypoxic modification of radiotherapy in head and neck cancer. Radiother Oncol 2009.
34. Nakagawa S., Yoshikawa H., Onda T., Kawana T., Iwamoto A., Taketani Y. Type of human papillomavirus is related to clinical features of cervical carcinoma. Cancer 1996, 78(9):1935-1941.
35. Vu H.L., Sikora A.G., Fu S., Kao J. HPV-induced oropharyngeal cancer, immune response and response to therapy. Cancer Lett 2010, 288(2):149-155.
36. Liu S.S., Leung R.C., Chan K.Y., et al. P73 expression is associated with the cellular radiosensitivity in cervical cancer after radiotherapy. Clin Cancer Res 2004, 10(10):3309-3316.
37. Lai C.H., Chang C.J., Huang H.J., et al. Role of human papillomavirus genotype in prognosis of early-stage cervical cancer undergoing primary surgery. J Clin Oncol 2007, 25(24):3628-3634.
38. Kim J.Y., Park S., Nam B.H., et al. Low initial human papilloma viral load implicates worse prognosis in patients with uterine cervical cancer treated with radiotherapy. J Clin Oncol 2009, 27(30):5088-5093.
39. Durst M., Bosch F.X., Glitz D., Schneider A., Zur Hausen H. Inverse relationship between human papillomavirus (HPV) type 16 early gene expression and cell differentiation in nude mouse epithelial cysts and tumors induced by HPV-positive human cell lines. J Virol 1991, 65(2):796-804.
40. Shirasawa H., Tomita Y., Kubota K., et al. Detection of human papillomavirus type 16 DNA and evidence for integration into the cell DNA in cervical dysplasia. J Gen Virol 1986, 67(Pt 9):2011-2015.
41. Cullen A.P., Reid R., Campion M., Lorincz A.T. Analysis of the physical state of different human papillomavirus DNAs in intraepithelial and invasive cervical neoplasm. J Virol 1991, 65(2):606-612.
42. Kulmala S.M., Syrjanen S.M., Gyllensten U.B., et al. Early integration of high copy HPV16 detectable in women with normal and low grade cervical cytology and histology. J Clin Pathol 2006, 59(5):513-517.
43. Josefsson A.M., Magnusson P.K., Ylitalo N., et al. Viral load of human papilloma virus 16 as a determinant for development of cervical carcinoma in situ: a nested case-control study. Lancet 2000, 355(9222):2189-2193.
44. Contreras-Paredes A., De la Cruz-Hernandez E., Martinez-Ramirez I., Duenas-Gonzalez A., Lizano M. E6 variants of human papillomavirus 18 differentially modulate the protein kinase B/phosphatidylinositol 3-kinase (akt/PI3K) signaling pathway. Virology 2009, 383(1):78-85.
45. Weinstein I.B., Joe A. Oncogene addiction. Cancer Res 2008, 68(9):3077-3080. [discussion 80].
46. Duensing S., Munger K. Mechanisms of genomic instability in human cancer: insights from studies with human papillomavirus oncoproteins. Int J Cancer 2004, 109(2):157-162.
47. DeWeese T.L., Walsh J.C., Dillehay L.E., et al. Human papillomavirus E6 and E7 oncoproteins alter cell cycle progression but not radiosensitivity of carcinoma cells treated with low-dose-rate radiation. Int J Radiat Oncol Biol Phys 1997, 37(1):145-154.
48. Kamradt M.C., Mohideen N., Vaughan A.T. RU486 increases radiosensitivity and restores apoptosis through modulation of HPV E6/E7 in dexamethasone-treated cervical carcinoma cells. Gynecol Oncol 2000, 77(1):177-182.
49. Hampson L., El Hady E.S., Moore J.V., Kitchener H., Hampson I.N. The HPV16 E6 and E7 proteins and the radiation resistance of cervical carcinoma. FASEB J 2001, 15(8):1445-1447.
50. Zheng Y., Zhang J., Rao Z. Ribozyme targeting HPV16 E6E7 transcripts in cervical cancer cells suppresses cell growth and sensitizes cells to chemotherapy and radiotherapy. Cancer Biol Ther 2004, 3(11):1129-1134. [discussion 35-36].
51. Abdulkarim B., Sabri S., Deutsch E., et al. Antiviral agent Cidofovir restores p53 function and enhances the radiosensitivity in HPV-associated cancers. Oncogene 2002, 21(15):2334-2346.
52. Wang W., Sima N., Kong D., 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 Lett 2010, 291(1):67-75.
53. Prevo R., Deutsch E., Sampson O., et al. Class I PI3 kinase inhibition by the pyridinylfuranopyrimidine inhibitor PI-103 enhances tumor radiosensitivity. Cancer Res 2008, 68(14):5915-5923.
54. Yarbrough W.G., Whigham A., Brown B., Roach M., Slebos R. Phosphoinositide kinase-3 status associated with presence or absence of human papillomavirus in head and neck squamous cell carcinomas. Int J Radiat Oncol Biol Phys 2007, 69(2 Suppl):S98-S101.
55. Charette S.T., McCance D.J. The E7 protein from human papillomavirus type 16 enhances keratinocyte migration in an Akt-dependent manner. Oncogene 2007, 26(52):7386-7390.
56. Pim D., Massimi P., Dilworth S.M., Banks L. Activation of the protein kinase B pathway by the HPV-16 E7 oncoprotein occurs through a mechanism involving interaction with PP2A. Oncogene 2005, 24(53):7830-7838.
57. Spanos W.C., El-Deiry M., Lee J.H. Cidofovir incorporation into human keratinocytes with episomal HPV 16 results in nonselective cytotoxicity. Ann Otol Rhinol Laryngol 2005, 114(11):840-846.
58. Donne A.J., Hampson L., He X.T., Rothera M.P., Homer J.J., Hampson I.N. Cidofovir induces an increase in levels of low-risk and high-risk HPV E6. Head Neck 2009, 31(7):893-901.
59. Sirianni N., Wang J., Ferris R.L. Antiviral activity of Cidofovir on a naturally human papillomavirus-16 infected squamous cell carcinoma of the head and neck (SCCHN) cell line improves radiation sensitivity. Oral Oncol 2005, 41(4):423-428.
60. Donne A.J., Hampson L., He X.T., Rothera M.P., Homer J.J., Hampson I.N. Effects of Cidofovir on a novel cell-based test system for recurrent respiratory papillomatosis. Head Neck 2007, 29(8):741-750.
61. Andrei G., Snoeck R., Piette J., Delvenne P., De Clercq E. Inhibiting effects of Cidofovir (HPMPC) on the growth of the human cervical carcinoma (SiHa) xenografts in athymic nude mice. Oncol Res 1998, 10(10):533-539.
62. Gloss B., Bernard H.U., Seedorf K., Klock G. The upstream regulatory region of the human papilloma virus-16 contains an E2 protein-independent enhancer which is specific for cervical carcinoma cells and regulated by glucocorticoid hormones. EMBO J 1987, 6(12):3735-3743.
63. Kamradt M.C., Mohideen N., Krueger E., Walter S., Vaughan A.T. Inhibition of radiation-induced apoptosis by dexamethasone in cervical carcinoma cell lines depends upon increased HPV E6/E7. Br J Cancer 2000, 82(10):1709-1716.
64. Williams C.S., Tsujii M., Reese J., Dey S.K., DuBois R.N. Host cyclooxygenase-2 modulates carcinoma growth. J Clin Invest 2000, 105(11):1589-1594.
65. Gupta S., Srivastava M., Ahmad N., Bostwick D.G., Mukhtar H. Over-expression of cyclooxygenase-2 in human prostate adenocarcinoma. Prostate 2000, 42(1):73-78.
66. Ristimaki A., Honkanen N., Jankala H., Sipponen P., Harkonen M. Expression of cyclooxygenase-2 in human gastric carcinoma. Cancer Res 1997, 57(7):1276-1280.
67. 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(4):1183-1188.
68. Milas L., Kishi K., Hunter N., Mason K., Masferrer J.L., Tofilon P.J. Enhancement of tumor response to gamma-radiation by an inhibitor of cyclooxygenase-2 enzyme. J Natl Cancer Inst 1999, 91(17):1501-1504.
69. Kim H.J., Wu H.G., Park I.A., Ha S.W. High cyclooxygenase-2 expression is related with distant metastasis in cervical cancer treated with radiotherapy. Int J Radiat Oncol Biol Phys 2003, 55(1):16-20.
70. Gaffney D.K., Holden J., Zempolich K., Murphy K.J., Dicker A.P., Dodson M. Elevated COX-2 expression in cervical carcinoma: reduced cause-specific survival and pelvic control. Am J Clin Oncol 2001, 24(5):443-446.
71. RTOG. A phase I/II study of COX-2 inhibitor, Celebrex TM, (Celecoxib) and chemo-radiotherapy in patients with locally advanced cervical cancer. C-0128.
72. Kersemaekers A.M., Fleuren G.J., Kenter G.G., et al. Oncogene alterations in carcinomas of the uterine cervix: overexpression of the epidermal growth factor receptor is associated with poor prognosis. Clin Cancer Res 1999, 5(3):577-586.
73. Gaffney D.K., Haslam D., Tsodikov A., et al. Epidermal growth factor receptor (EGFR) and vascular endothelial growth factor (VEGF) negatively affect overall survival in carcinoma of the cervix treated with radiotherapy. Int J Radiat Oncol Biol Phys 2003, 56(4):922-928.
74. Bonner J.A., Harari P.M., Giralt J., et al. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N Engl J Med 2006, 354(6):567-578.
75. Almadori G., Cadoni G., Cattani P., et al. Human papillomavirus infection and epidermal growth factor receptor expression in primary laryngeal squamous cell carcinoma. Clin Cancer Res 2001, 7(12):3988-3993.
76. Kim S.H., Koo B.S., Kang S., et al. HPV integration begins in the tonsillar crypt and leads to the alteration of p16, EGFR and c-myc during tumor formation. Int J Cancer 2007, 120(7):1418-1425.
77. Na I.I., Kang H.J., Cho S.Y., et al. EGFR mutations and human papillomavirus in squamous cell carcinoma of tongue and tonsil. Eur J Cancer 2007, 43(3):520-526.
78. Kong C.S., Narasimhan B., Cao H., et al. The relationship between human papillomavirus status and other molecular prognostic markers in head and neck squamous cell carcinomas. Int J Radiat Oncol Biol Phys 2009, 74(2):553-561.
79. Lopez-Ocejo O., Viloria-Petit A., Bequet-Romero M., Mukhopadhyay D., Rak J., Kerbel R.S. Oncogenes and tumor angiogenesis: the HPV-16 E6 oncoprotein activates the vascular endothelial growth factor (VEGF) gene promoter in a p53 independent manner. Oncogene 2000, 19(40):4611-4620.
80. Bagnato A., Cirilli A., Salani D., et al. Growth inhibition of cervix carcinoma cells in vivo by endothelin A receptor blockade. Cancer Res 2002, 62(22):6381-6384.
81. 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. Clin Cancer Res 2007, 13(9):2568-2576.
82. Amine A., Vozenin-Brotons M.C., Abdulkarim B., Violot D., Aubel C., Bourhis J. Cidofovir administered with radiation displays an antiangiogenic effect mediated by E6 inhibition and subsequent TP53-dependent VEGF repression in HPV18+ cell lines. Radiat Res 2006, 166(4):600-610.
83. RTOG. A phase II study of bevacizumab in combination with definitive radiotherapy and cisplatin chemotherapy in untreated patients with locally advanced cervical cancer. 0417.
84. Kumar B., Cordell K.G., Lee J.S., et al. EGFR, p16, HPV Titer, Bcl-xL and p53, sex, and smoking as indicators of response to therapy and survival in oropharyngeal cancer. J Clin Oncol 2008, 26(19):3128-3137.
85. Jeon Y., Song Y., Kim S., et al. Influences of cyclooxygenase-1 and -2 expression on the radiosensitivities of human cervical cancer cell lines. Cancer Lett 2007, 18(256(1)):33-38.
86. Overgaard J., Hansen H.S., Andersen A.P., et al. Misonidazole combined with split-course radiotherapy in the treatment of invasive carcinoma of larynx and pharynx: report from the DAHANCA 2 study. Int J Radiat Oncol Biol Phys 1989, 16(4):1065-1068.
87. Dobrowsky W., Huigol N.G., Jayatilake R.S., et al. AK-2123 (Sanazol) as a radiation sensitizer in the treatment of stage III cervical cancer: results of an IAEA multicentre randomised trial. Radiother Oncol 2007, 82(1):24-29.
88. Bachtiary B., Schindl M., Potter R., et al. Overexpression of hypoxia-inducible factor 1alpha indicates diminished response to radiotherapy and unfavorable prognosis in patients receiving radical radiotherapy for cervical cancer. Clin Cancer Res 2003, 9(6):2234-2240.