HPV-related oropharyngeal cancers: From pathogenesis to new therapeutic approaches

Cancer Letters

Volumn 351, Issue 2, 2014, Pages 198-205

  Tornesello, Maria Lina ^a   Perri, Francesco ^a   Buonaguro, Luigi ^a   Ionna, Franco ^a   Buonaguro, Franco M ^a   Caponigro, Francesco ^a  

^a NATIONAL CANCER INSTITUTE   (Italy)

Author keywords

Carcinogenesis; Head and neck cancer; Human papillomavirus; Oropharyngeal cancer

Indexed keywords

CANCER VACCINE; CETUXIMAB; CISPLATIN; CYCLIN D1; DNA VACCINE; EPIDERMAL GROWTH FACTOR; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; PROTEIN P16; PROTEIN P53;

CANCER EPIDEMIOLOGY; CANCER IMMUNIZATION; CHEMORADIOTHERAPY; DISEASE ASSOCIATION; DRUG TARGETING; HEAD AND NECK CANCER; HUMAN; MOLECULAR PATHOLOGY; NONHUMAN; OROPHARYNX CANCER; PAPILLOMAVIRUS INFECTION; PRIORITY JOURNAL; SHORT SURVEY; TREATMENT PLANNING; TUMOR PROMOTION; VIRUS CARCINOGENESIS; ANIMAL; COMPLICATION; ISOLATION AND PURIFICATION; OROPHARYNGEAL NEOPLASMS; PAPILLOMA VIRUS; PAPILLOMAVIRUS INFECTIONS; PATHOLOGY; PROGNOSIS; VIROLOGY;

HUMAN PAPILLOMAVIRUS;

ANIMALS; HUMANS; OROPHARYNGEAL NEOPLASMS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PROGNOSIS;

EID: 84904733550     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.06.003     Document Type: Review

References (97)

1. J. Ferlay, I. Soerjomataram, M. Ervik, R. Dikshit, S. Eser, C. Mathers, M. Rebelo, D.M. Parkin, D. Forman, F. Bray. GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet], International Agency for Research on Cancer, Lyon, France.Ref Type: Electronic Citation. http://globocan.iarc.fr.2013.
2. Ryerson A.B., Peters E.S., Coughlin S.S., Chen V.W., Gillison M.L., Reichman M.E., Wu X., Chaturvedi A.K., Kawaoka K. Burden of potentially human papillomavirus-associated cancers of the oropharynx and oral cavity in the US, 1998-2003. Cancer 2008, 113:2901-2909.
3. Pfister D.G., Ang K.K., Brizel D.M., Burtness B.A., Cmelak A.J., Colevas A.D., Dunphy F., Eisele D.W., Gilbert J., Gillison M.L., Haddad R.I., Haughey B.H., Hicks W.L., Hitchcock Y.J., Kies M.S., Lydiatt W.M., Maghami E., Martins R., McCaffrey T., Mittal B.B., Pinto H.A., Ridge J.A., Samant S., Sanguineti G., Schuller D.E., Shah J.P., Spencer S., Trotti A., Weber R.S., Wolf G.T., Worden F. Head and neck cancers. J. Natl. Compr. Canc. Netw. 2011, 9:596-650.
4. IARC IARC Monographs on the Evaluation of Carcinogenic Risks to Humans 2010, Alcohol Consumption and Ethyl Carbamate, Lyon, France.
5. Hashibe M., Brennan P., Chuang S.C., Boccia S., Castellsague X., Chen C., Curado M.P., Dal M.L., Daudt A.W., Fabianova E., Fernandez L., Wunsch-Filho V., Franceschi S., Hayes R.B., Herrero R., Kelsey K., Koifman S., La V.C., Lazarus P., Levi F., Lence J.J., Mates D., Matos E., Menezes A., McClean M.D., Muscat J., Eluf-Neto J., Olshan A.F., Purdue M., Rudnai P., Schwartz S.M., Smith E., Sturgis E.M., Szeszenia-Dabrowska N., Talamini R., Wei Q., Winn D.M., Shangina O., Pilarska A., Zhang Z.F., Ferro G., Berthiller J., Boffetta P. Interaction between tobacco and alcohol use and the risk of head and neck cancer: pooled analysis in the international head and neck cancer epidemiology consortium. Cancer Epidemiol. Biomark. Prev. 2009, 18:541-550.
6. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans Smokeless tobacco and some tobacco-specific N-nitrosamines. IARC Monogr. Eval. Carcinog. Risks Hum. 2007, 89:1-592.
7. Park B.J., Chiosea S.I., Grandis J.R. Molecular changes in the multistage pathogenesis of head and neck cancer. Cancer Biomark. 2010, 9:325-339.
8. Leemans C.R., Braakhuis B.J., Brakenhoff R.H. The molecular biology of head and neck cancer. Nat. Rev. Cancer 2011, 11:9-22.
9. Kreimer A.R., Clifford G.M., Boyle P., Franceschi S. Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review. Cancer Epidemiol. Biomark. Prev 2005, 14:467-475.
10. Syrjanen K., Syrjanen S. Detection of human papillomavirus in sinonasal carcinoma: systematic review and meta-analysis. Hum. Pathol. 2013, 44:983-991.
11. Chaturvedi A.K., Anderson W.F., Lortet-Tieulent J., Curado M.P., Ferlay J., Franceschi S., Rosenberg P.S., Bray F., Gillison M.L. Worldwide trends in incidence rates for oral cavity and oropharyngeal cancers. J Clin. Oncol. 2013, 31:4550-4559.
12. 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, 121:1813-1820.
13. Fakhry C., Westra W.H., Li S., Cmelak A., Ridge J.A., Pinto H., Forastiere A., Gillison M.L. Improved survival of patients with human papillomavirus-positive head and neck squamous cell carcinoma in a prospective clinical trial. J. Natl. Cancer Inst. 2008, 100:261-269.
14. Johnson S., McDonald J.T., Corsten M., Rourke R. Socio-economic status and head and neck cancer incidence in Canada: a case-control study. Oral Oncol. 2010, 46:200-203.
15. Carvalho A.L., Nishimoto I.N., Califano J.A., Kowalski L.P. Trends in incidence and prognosis for head and neck cancer in the United States: a site-specific analysis of the SEER database. Int. J. Cancer 2005, 114:806-816.
16. Marur S., D'Souza G., Westra W.H., Forastiere A.A. HPV-associated head and neck cancer: a virus-related cancer epidemic. Lancet Oncol. 2010, 11:781-789.
17. Ramqvist T., Dalianis T. Oropharyngeal cancer epidemic and human papillomavirus. Emerg. Infect. Dis. 2010, 16:1671-1677.
18. Hong A.M., Grulich A.E., Jones D., Lee C.S., Garland S.M., Dobbins T.A., Clark J.R., Harnett G.B., Milross C.G., O'Brien C.J., Rose B.R. Squamous cell carcinoma of the oropharynx in Australian males induced by human papillomavirus vaccine targets. Vaccine 2010, 28:3269-3272.
19. Auluck A., Hislop G., Bajdik C., Poh C., Zhang L., Rosin M. Trends in oropharyngeal and oral cavity cancer incidence of human papillomavirus (HPV)-related and HPV-unrelated sites in a multicultural population: the British Columbia experience. Cancer 2010, 116:2635-2644.
20. Blomberg M., Nielsen A., Munk C., Kjaer S.K. Trends in head and neck cancer incidence in Denmark, 1978-2007: focus on human papillomavirus associated sites. Int. J. Cancer 2011, 129:733-741.
21. Braakhuis B.J., Visser O., Leemans C.R. Oral and oropharyngeal cancer in The Netherlands between 1989 and 2006: increasing incidence but not in young adults. Oral Oncol. 2009, 45:e85-e89.
22. Mork J., Moller B., Dahl T., Bray F. Time trends in pharyngeal cancer incidence in Norway 1981-2005: a subsite analysis based on a reabstraction and recoding of registered cases. Cancer Causes Control 2010, 21:1397-1405.
23. Hammarstedt L., Lindquist D., Dahlstrand H., Romanitan M., Dahlgren L.O., Joneberg J., Creson N., Lindholm J., Ye W., Dalianis T., Munck-Wikland E. Human papillomavirus as a risk factor for the increase in incidence of tonsillar cancer. Int. J. Cancer 2006, 119:2620-2623.
24. Chaturvedi A.K., Engels E.A., Anderson W.F., Gillison M.L. Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States. J. Clin. Oncol. 2008, 26:612-619.
25. Reddy V.M., Cundall-Curry D., Bridger M.W. Trends in the incidence rates of tonsil and base of tongue cancer in England, 1985-2006. Ann. R. Coll. Surg. Engl. 2010, 92:655-659.
26. Chaturvedi A.K., Engels E.A., Pfeiffer R.M., Hernandez B.Y., Xiao W., Kim E., Jiang B., Goodman M.T., Sibug-Saber M., Cozen W., Liu L., Lynch C.F., Wentzensen N., Jordan R.C., Altekruse S., Anderson W.F., Rosenberg P.S., Gillison M.L. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J. Clin. Oncol. 2011, 29:4294-4301.
27. Gillison M.L., D'Souza G., Westra W., Sugar E., Xiao W., Begum S., Viscidi R. Distinct risk factor profiles for human papillomavirus type 16-positive and human papillomavirus type 16-negative head and neck cancers. J. Natl. Cancer Inst. 2008, 100:407-420.
28. Braakhuis B.J., Snijders P.J., Keune W.J., Meijer C.J., Ruijter-Schippers H.J., Leemans C.R., Brakenhoff R.H. Genetic patterns in head and neck cancers that contain or lack transcriptionally active human papillomavirus. J. Natl. Cancer Inst. 2004, 96:998-1006.
29. Lindel K., Beer K.T., Laissue J., Greiner R.H., Aebersold D.M. Human papillomavirus positive squamous cell carcinoma of the oropharynx: a radiosensitive subgroup of head and neck carcinoma. Cancer 2001, 92:805-813.
30. Butz K., Geisen C., Ullmann A., Spitkovsky D., Hoppe-Seyler F. Cellular responses of HPV-positive cancer cells to genotoxic anti-cancer agents: repression of E6/E7-oncogene expression and induction of apoptosis. Int. J. Cancer 1996, 68:506-513.
31. Kostareli E., Holzinger D., Hess J. New concepts for translational head and neck oncology: lessons from HPV-related oropharyngeal squamous cell carcinomas. Front. Oncol. 2012, 2:36.
32. Ang K.K., Harris J., Wheeler R., Weber R., Rosenthal D.I., Nguyen-Tan P.F., Westra W.H., Chung C.H., Jordan R.C., Lu C., Kim H., Axelrod R., Silverman C.C., Redmond K.P., Gillison M.L. Human papillomavirus and survival of patients with oropharyngeal cancer. N. Engl. J. Med. 2010, 363:24-35.
33. IARC, IARC monographs on the evaluation of carcinogenic risks to humans. A Review of Human Carcinogens Part B: Biological Agents, Lyon, France, 2011.
34. Parkin D.M., Bray F. The burden of HPV-related cancers. Vaccine 2006, 24(Suppl. 3):S11-S25. (Chapter 2).
35. Dahlgren L., Dahlstrand H.M., Lindquist D., Hogmo A., Bjornestal L., Lindholm J., Lundberg B., Dalianis T., Munck-Wikland E. Human papillomavirus is more common in base of tongue than in mobile tongue cancer and is a favorable prognostic factor in base of tongue cancer patients. Int. J. Cancer 2004, 112:1015-1019.
36. St Guily J.L., Jacquard A.C., Pretet J.L., Haesebaert J., Beby-Defaux A., Clavel C., Agius G., Birembaut P., Okais C., Leocmach Y., Soubeyrand B., Pradat P., Riethmuller D., Mougin C., Denis F. Human papillomavirus genotype distribution in oropharynx and oral cavity cancer in France - the EDiTH VI study. J. Clin. Virol. 2011, 51:100-104.
37. Doorbar J. Molecular biology of human papillomavirus infection and cervical cancer. Clin. Sci. (Lond) 2006, 110:525-541.
38. Pyeon D., Pearce S.M., Lank S.M., Ahlquist P., Lambert P.F. Establishment of human papillomavirus infection requires cell cycle progression. PLoS Pathog. 2009, 5:e1000318.
39. Doorbar J. The papillomavirus life cycle. J. Clin. Virol. 2005, 32(Suppl 1):S7-S15.
40. Moody C.A., Laimins L.A. Human papillomavirus oncoproteins: pathways to transformation. Nat. Rev. Cancer 2010, 10:550-560.
41. Khleif S.N., DeGregori J., Yee C.L., Otterson G.A., Kaye F.J., Nevins J.R., Howley P.M. Inhibition of cyclin D-CDK4/CDK6 activity is associated with an E2F-mediated induction of cyclin kinase inhibitor activity. Proc. Natl. Acad. Sci. USA 1996, 93:4350-4354.
42. Nakao Y., Yang X., Yokoyama M., Ferenczy A., Tang S.C., Pater M.M., Pater A. Induction of p16 during immortalization by HPV 16 and 18 and not during malignant transformation. Br. J. Cancer 1997, 75:1410-1416.
43. von Knebel D.M. New molecular tools for efficient screening of cervical cancer. Dis. Markers 2001, 17:123-128.
44. von Knebel D.M. New markers for cervical dysplasia to visualise the genomic chaos created by aberrant oncogenic papillomavirus infections. Eur. J. Cancer 2002, 38:2229-2242.
45. Pannone G., Rodolico V., Santoro A., Lo M.L., Franco R., Botti G., Aquino G., Pedicillo M.C., Cagiano S., Campisi G., Rubini C., Papagerakis S., De R.G., Tornesello M.L., Buonaguro F.M., Staibano S., Bufo P. Evaluation of a combined triple method to detect causative HPV in oral and oropharyngeal squamous cell carcinomas: p16 Immunohistochemistry, consensus PCR HPV-DNA, and in situ hybridization. Infect. Agent. Cancer 2012, 7:4.
46. Scheffner M., Huibregtse J.M., Vierstra R.D., Howley P.M. The HPV-16E6 and E6AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993, 75:495-505.
47. Patel D., Huang S.M., Baglia L.A., McCance D.J. The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300. EMBO J. 1999, 18:5061-5072.
48. Zimmermann H., Degenkolbe R., Bernard H.U., O'Connor M.J. The human papillomavirus type 16 E6 oncoprotein can down-regulate p53 activity by targeting the transcriptional coactivator CBP/p300. J. Virol. 1999, 73:6209-6219.
49. Kumar A., Zhao Y., Meng G., Zeng M., Srinivasan S., Delmolino L.M., Gao Q., Dimri G., Weber G.F., Wazer D.E., Band H., Band V. Human papillomavirus oncoprotein E6 inactivates the transcriptional coactivator human ADA3. Mol. Cell Biol. 2002, 22:5801-5812.
50. Hoffmann M., Lohrey C., Hunziker A., Kahn T., Schwarz E. Human papillomavirus type 16 E6 and E7 genotypes in head-and-neck carcinomas. Oral Oncol. 2004, 40:520-524.
51. Hopman A.H., Smedts F., Dignef W., Ummelen M., Sonke G., Mravunac M., Vooijs G.P., Speel E.J., Ramaekers F.C. Transition of high-grade cervical intraepithelial neoplasia to micro-invasive carcinoma is characterized by integration of HPV 16/18 and numerical chromosome abnormalities. J. Pathol. 2004, 202:23-33.
52. Annunziata C., Buonaguro L., Buonaguro F.M., Tornesello M.L. Characterization of the human papillomavirus (HPV) integration sites into genital cancers. Pathol. Oncol. Res. 2012, 18:803-808.
53. Schmitz M., Driesch C., Jansen L., Runnebaum I.B., Durst M. Non-random integration of the HPV genome in cervical cancer. PLoS One 2012, 7:e39632.
54. Lace M.J., Anson J.R., Klussmann J.P., Wang D.H., Smith E.M., Haugen T.H., Turek L.P. Human papillomavirus type 16 (HPV-16) genomes integrated in head and neck cancers and in HPV-16-immortalized human keratinocyte clones express chimeric virus-cell mRNAs similar to those found in cervical cancers. J. Virol. 2011, 85:1645-1654.
55. Akagi K., Li J., Broutian T.R., Padilla-Nash H., Xiao W., Jiang B., Rocco J.W., Teknos T.N., Kumar B., Wangsa D., He D., Ried T., Symer D.E., Gillison M.L. Genome-wide analysis of HPV integration in human cancers reveals recurrent, focal genomic instability. Genome Res. 2013.
56. Rothenberg S.M., Ellisen L.W. The molecular pathogenesis of head and neck squamous cell carcinoma. J. Clin. Invest. 2012, 122:1951-1957.
57. Chung C.H., Ely K., McGavran L., Varella-Garcia M., Parker J., Parker N., Jarrett C., Carter J., Murphy B.A., Netterville J., Burkey B.B., Sinard R., Cmelak A., Levy S., Yarbrough W.G., Slebos R.J., Hirsch F.R. Increased epidermal growth factor receptor gene copy number is associated with poor prognosis in head and neck squamous cell carcinomas. J. Clin. Oncol. 2006, 24:4170-4176.
58. Temam S., Kawaguchi H., El-Naggar A.K., Jelinek J., Tang H., Liu D.D., Lang W., Issa J.P., Lee J.J., Mao L. Epidermal growth factor receptor copy number alterations correlate with poor clinical outcome in patients with head and neck squamous cancer. J. Clin. Oncol. 2007, 25:2164-2170.
59. Mrhalova M., Plzak J., Betka J., Kodet R. Epidermal growth factor receptor-its expression and copy numbers of EGFR gene in patients with head and neck squamous cell carcinomas. Neoplasma 2005, 52:338-343.
60. Young R.J., Rischin D., Fisher R., McArthur G.A., Fox S.B., Peters L.J., Corry J., Lim A., Waldeck K., Solomon B. Relationship between epidermal growth factor receptor status, p16(INK4A), and outcome in head and neck squamous cell carcinoma. Cancer Epidemiol. Biomark. Prev. 2011, 20:1230-1237.
61. Yu Z., Weinberger P.M., Haffty B.G., Sasaki C., Zerillo C., Joe J., Kowalski D., Dziura J., Camp R.L., Rimm D.L., Psyrri A. Cyclin d1 is a valuable prognostic marker in oropharyngeal squamous cell carcinoma. Clin Cancer Res. 2005, 11:1160-1166.
62. Liang C., Marsit C.J., McClean M.D., Nelson H.H., Christensen B.C., Haddad R.I., Clark J.R., Wein R.O., Grillone G.A., Houseman E.A., Halec G., Waterboer T., Pawlita M., Krane J.F., Kelsey K.T. Biomarkers of HPV in head and neck squamous cell carcinoma. Cancer Res. 2012, 72:5004-5013.
63. Lo E.J., Bell D., Woo J.S., Li G., Hanna E.Y., El-Naggar A.K., Sturgis E.M. Human papillomavirus and WHO type I nasopharyngeal carcinoma. Laryngoscope 2010, 120:1990-1997.
64. Rietbergen M.M., Brakenhoff R.H., Bloemena E., Witte B.I., Snijders P.J., Heideman D.A., Boon D., Koljenovic S., Baatenburg-De Jong R.J., Leemans C.R. Human papillomavirus detection and comorbidity: critical issues in selection of patients with oropharyngeal cancer for treatment de-escalation trials. Ann. Oncol. 2013, 24:2740-2745.
65. Carozzi F., Confortini M., Dalla P.P., Del M.A., Gillio-Tos A., De M.L., Giorgi-Rossi P., Pontenani G., Rosso S., Sani C., Sintoni C., Segnan N., Zorzi M., Cuzick J., Rizzolo R., Ronco G. Use of p16-INK4A overexpression to increase the specificity of human papillomavirus testing: a nested substudy of the NTCC randomised controlled trial. Lancet Oncol. 2008, 9:937-945.
66. Rietbergen M.M., Snijders P.J., Beekzada D., Braakhuis B.J., Brink A., Heideman D.A., Hesselink A.T., Witte B.I., Bloemena E., Baatenburg-De Jong R.J., Rene L.C., Brakenhoff R.H. Molecular characterization of p16-immunopositive but HPV DNA-negative oropharyngeal carcinomas. Int. J. Cancer 2013.
67. Yarbrough W.G. The ARF-p16 gene locus in carcinogenesis and therapy of head and neck squamous cell carcinoma. Laryngoscope 2002, 112:2114-2128.
68. Olivier M., Hollstein M., Hainaut P. TP53 mutations in human cancers: origins, consequences, and clinical use. Cold Spring Harb. Perspect. Biol. 2010, 2:a001008.
69. Brown C.J., Lain S., Verma C.S., Fersht A.R., Lane D.P. Awakening guardian angels: drugging the p53 pathway. Nat. Rev. Cancer 2009, 9:862-873.
70. Stransky N., Egloff A.M., Tward A.D., Kostic A.D., Cibulskis K., Sivachenko A., Kryukov G.V., Lawrence M.S., Sougnez C., McKenna A., Shefler E., Ramos A.H., Stojanov P., Carter S.L., Voet D., Cortes M.L., Auclair D., Berger M.F., Saksena G., Guiducci C., Onofrio R.C., Parkin M., Romkes M., Weissfeld J.L., Seethala R.R., Wang L., Rangel-Escareno C., Fernandez-Lopez J.C., Hidalgo-Miranda A., Melendez-Zajgla J., Winckler W., Ardlie K., Gabriel S.B., Meyerson M., Lander E.S., Getz G., Golub T.R., Garraway L.A., Grandis J.R. The mutational landscape of head and neck squamous cell carcinoma. Science 2011, 333:1157-1160.
71. Agrawal N., Frederick M.J., Pickering C.R., Bettegowda C., Chang K., Li R.J., Fakhry C., Xie T.X., Zhang J., Wang J., Zhang N., El-Naggar A.K., Jasser S.A., Weinstein J.N., Trevino L., Drummond J.A., Muzny D.M., Wu Y., Wood L.D., Hruban R.H., Westra W.H., Koch W.M., Califano J.A., Gibbs R.A., Sidransky D., Vogelstein B., Velculescu V.E., Papadopoulos N., Wheeler D.A., Kinzler K.W., Myers J.N. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 2011, 333:1154-1157.
72. D.N. Hayes, J. Grandis, A.K. El-Naggar, Comprehensive genomic characterization of squamous cell carcinoma of the head and neck in the Cancer Genome Atlas, in: AACR Annual Meeting, Abstract 1117, 2013.
73. Pickering C.R., Zhang J., Yoo S.Y., Bengtsson L., Moorthy S., Neskey D.M., Zhao M., Ortega Alves M.V., Chang K., Drummond J., Cortez E., Xie T.X., Zhang D., Chung W., Issa J.P., Zweidler-McKay P.A., Wu X., El-Naggar A.K., Weinstein J.N., Wang J., Muzny D.M., Gibbs R.A., Wheeler D.A., Myers J.N., Frederick M.J. Integrative genomic characterization of oral squamous cell carcinoma identifies frequent somatic drivers. Cancer Discov. 2013, 3:770-781.
74. Bossi P., Orlandi E., Miceli R., Perrone F., Guzzo M., Mariani L., Granata R., Locati L., Fallai C., Cortelazzi B., Pilotti S., Scaramellini G., Gloghini A., Licitra L. Treatment-related outcome of oropharyngeal cancer patients differentiated by HPV dictated risk profile: a tertiary cancer centre series analysis. Ann. Oncol. 2014.
75. Licitra L., Perrone F., Bossi P., Suardi S., Mariani L., Artusi R., Oggionni M., Rossini C., Cantu G., Squadrelli M., Quattrone P., Locati L.D., Bergamini C., Olmi P., Pierotti M.A., Pilotti S. High-risk human papillomavirus affects prognosis in patients with surgically treated oropharyngeal squamous cell carcinoma. J. Clin. Oncol. 2006, 24:5630-5636.
76. Torres-Roca J.F., Eschrich S., Zhao H., Bloom G., Sung J., McCarthy S., Cantor A.B., Scuto A., Li C., Zhang S., Jove R., Yeatman T. Prediction of radiation sensitivity using a gene expression classifier. Cancer Res. 2005, 65:7169-7176.
77. Lohavanichbutr P., Houck J., Fan W., Yueh B., Mendez E., Futran N., Doody D.R., Upton M.P., Farwell D.G., Schwartz S.M., Zhao L.P., Chen C. Genomewide gene expression profiles of HPV-positive and HPV-negative oropharyngeal cancer: potential implications for treatment choices. Arch. Otolaryngol. Head Neck Surg. 2009, 135:180-188.
78. Mehra R., Serebriiskii I.G., Dunbrack R.L., Robinson M.K., Burtness B., Golemis E.A. Protein-intrinsic and signaling network-based sources of resistance to. Drug Resist. Updat. 2011, 14:260-279.
79. Kalyankrishna S., Grandis J.R. Epidermal growth factor receptor biology in head and neck cancer. J Clin. Oncol. 2006, 24:2666-2672.
80. Mirghani H., Amen F., Moreau F., Guigay J., Hartl D.M., Lacau G.J. St, Oropharyngeal cancers: relationship between epidermal growth factor receptor alterations and human papillomavirus status. Eur. J. Cancer 2014, 50:1100-1111.
81. Burtness B., Goldwasser M.A., Flood W., Mattar B., Forastiere A.A. Phase III randomized trial of cisplatin plus placebo compared with cisplatin plus cetuximab in metastatic/recurrent head and neck cancer: an eastern cooperative oncology group study. J. Clin. Oncol. 2005, 23:8646-8654.
82. Vermorken J.B., Mesia R., Rivera F., Remenar E., Kawecki A., Rottey S., Erfan J., Zabolotnyy D., Kienzer H.R., Cupissol D., Peyrade F., Benasso M., Vynnychenko I., De R.D., Bokemeyer C., Schueler A., Amellal N., Hitt R. Platinum-based chemotherapy plus cetuximab in head and neck cancer. N. Engl. J. Med. 2008, 359:1116-1127.
83. Bonner J.A., Harari P.M., Giralt J., Azarnia N., Shin D.M., Cohen R.B., Jones C.U., Sur R., Raben D., Jassem J., Ove R., Kies M.S., Baselga J., Youssoufian H., Amellal N., Rowinsky E.K., Ang K.K. Radiotherapy plus cetuximab for squamous-cell carcinoma of the head and neck. N. Engl. J. Med. 2006, 354:567-578.
84. Roda J.M., Joshi T., Butchar J.P., McAlees J.W., Lehman A., Tridandapani S., Carson W.E. The activation of natural killer cell effector functions by cetuximab-coated, epidermal growth factor receptor positive tumor cells is enhanced by cytokines. Clin. Cancer Res. 2007, 13:6419-6428.
85. Bellone S., Frera G., Landolfi G., Romani C., Bandiera E., Tognon G., Roman J.J., Burnett A.F., Pecorelli S., Santin A.D. Overexpression of epidermal growth factor type-1 receptor (EGF-R1) in cervical cancer: implications for Cetuximab-mediated therapy in recurrent/metastatic disease. Gynecol. Oncol. 2007, 106:513-520.
86. Jung A.C., Guihard S., Krugell S., Ledrappier S., Brochot A., Dalstein V., Job S., de Reynies Aurélien, Noel G., Wasylyk B., Clavel C., Abecassis J. CD8-alpha T-cell infiltration in human papillomavirus-related oropharyngeal carcinoma correlates with improved patient prognosis. Int.J. Cancer 2013, 132:E26-E36.
87. Vermorken J.B., Psyrri A., Mesia R., Peyrade F., Beier F., de Blas B., Celik I., Licitra L. Impact of tumor HPV status on outcome in patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck receiving chemotherapy with or without cetuximab: retrospective analysis of the phase III EXTREME trial. Ann. Oncol. 2014, 25:801-807.
88. Vermorken J.B., Stohlmacher-Williams J., Davidenko I., Licitra L., Winquist E., Villanueva C., Foa P., Rottey S., Skladowski K., Tahara M., Pai V.R., Faivre S., Blajman C.R., Forastiere A.A., Stein B.N., Oliner K.S., Pan Z., Bach B.A. Cisplatin and fluorouracil with or without panitumumab in patients with recurrent or metastatic squamous-cell carcinoma of the head and neck (SPECTRUM): an open-label phase 3 randomised trial. Lancet Oncol. 2013, 14:697-710.
89. Mirghani H., Amen F., Blanchard P., Moreau F., Guigay J., Hartl D.M., St Lacau G.J. Treatment de-escalation in HPV-positive oropharyngeal carcinoma: ongoing trials, critical issues and perspectives. Int. J. Cancer 2014.
90. Morrow M.P., Yan J., Sardesai N.Y. Human papillomavirus therapeutic vaccines: targeting viral antigens as immunotherapy for precancerous disease and cancer. Expert. Rev. Vaccines 2013, 12:271-283.
91. van der Burg S.H., Arens R., Melief C.J. Immunotherapy for persistent viral infections and associated disease. Trends Immunol. 2011, 32:97-103.
92. Kenter G.G., Welters M.J., Valentijn A.R., Lowik M.J., Berends-van der Meer D.M., Vloon A.P., Essahsah F., Fathers L.M., Offringa R., Drijfhout J.W., Wafelman A.R., Oostendorp J., Fleuren G.J., van der Burg S.H., Melief C.J. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N. Engl. J Med 2009, 361:1838-1847.
93. Welters M.J., Kenter G.G., de Vos van Steenwijk P.J., Lowik M.J., Berends-van der Meer D.M., Essahsah F., Stynenbosch L.F., Vloon A.P., Ramwadhdoebe T.H., Piersma S.J., van der Hulst J.M., Valentijn A.R., Fathers L.M., Drijfhout J.W., Franken K.L., Oostendorp J., Fleuren G.J., Melief C.J., van der Burg S.H. Success or failure of vaccination for HPV16-positive vulvar lesions correlates with kinetics and phenotype of induced T-cell responses. Proc. Natl. Acad. Sci. USA 2010, 107:11895-11899.
94. Daayana S., Elkord E., Winters U., Pawlita M., Roden R., Stern P.L., Kitchener H.C. Phase II trial of imiquimod and HPV therapeutic vaccination in patients with vulval intraepithelial neoplasia. Br. J. Cancer 2010, 102:1129-1136.
95. Best S.R., Peng S., Juang C.M., Hung C.F., Hannaman D., Saunders J.R., Wu T.C., Pai S.I. Administration of HPV DNA vaccine via electroporation elicits the strongest CD8+ T cell immune responses compared to intramuscular injection and intradermal gene gun delivery. Vaccine 2009, 27:5450-5459.
96. Lyford-Pike S., Peng S., Young G.D., Taube J.M., Westra W.H., Akpeng B., Bruno T.C., Richmon J.D., Wang H., Bishop J.A., Chen L., Drake C.G., Topalian S.L., Pardoll D.M., Pai S.I. Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res. 2013, 73:1733-1741.
97. Pai S.I. Mission impossible: how HPV-associated head and neck cancers escape a primed immune response. Oral Oncol. 2013, 49:723-725.