Identification of oropharyngeal squamous cell carcinomas with active HPV16 involvement by immunohistochemical analysis of the retinoblastoma protein pathway

International Journal of Cancer

Volumn 133, Issue 6, 2013, Pages 1389-1399

  Holzinger, Dana ^a,b   Flechtenmacher, Christa ^a   Henfling, Nataly ^a   Kaden, Ines ^a   Grabe, Niels ^a,c   Lahrmann, Bernd ^a,c   Schmitt, Markus ^b   Hess, Jochen ^a,d   Pawlita, Michael ^b   Bosch, Franz X ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^d GERMAN CANCER RESEARCH CENTER   (Germany)

Author keywords

active HPV infection; Cyclin D1; head and neck squamous cell carcinoma; human papilloma virus; immunohistochemistry; oropharynx; p16INK4a; p53; pRb; tissue microarray

Indexed keywords

CYCLIN D1; FORMALDEHYDE; PROTEIN P16; PROTEIN P53; RETINOBLASTOMA PROTEIN; TUMOR MARKER; VIRUS DNA; VIRUS RNA;

ARTICLE; BIOPSY; CANCER CLASSIFICATION; CANCER PROGNOSIS; CRYOPRESERVATION; DISEASE ASSOCIATION; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; OROPHARYNX CANCER; OVERALL SURVIVAL; PREDICTIVE VALUE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIVITY AND SPECIFICITY; SNAP FROZEN BIOPSY; SQUAMOUS CELL CARCINOMA; TISSUE MICROARRAY;

ACTIVE HPV INFECTION; CYCLIN D1; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN PAPILLOMA VIRUS; IMMUNOHISTOCHEMISTRY; OROPHARYNX; P16INK4A; P53; PRB; TISSUE MICROARRAY;

CARCINOMA, SQUAMOUS CELL; CYCLIN D1; HUMAN PAPILLOMAVIRUS 16; HUMANS; IMMUNOHISTOCHEMISTRY; NEOPLASM PROTEINS; OROPHARYNGEAL NEOPLASMS; RETINOBLASTOMA PROTEIN; RETROSPECTIVE STUDIES; RNA, VIRAL; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84879936681     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28142     Document Type: Article

References (55)

1. Andl T, Kahn T, Pfuhl A, et al. Etiological involvement of oncogenic human papillomavirus in tonsillar squamous cell carcinomas lacking retinoblastoma cell cycle control. Cancer Res 1998; 58: 5-13.
2. Gillison ML, Koch WM, Capone RB, et al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst 2000; 92: 709-20.
3. Paz IB, Cook N, Odom-Maryon T, et al. 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: 595-604.
4. Snijders PJ, Cromme FV, van den Brule AJ, et al. Prevalence and expression of human papillomavirus in tonsillar carcinomas, indicating a possible viral etiology. Int J Cancer 1992; 51: 845-50.
5. Auluck A, Hislop G, Bajdik C, et al. 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: 2635-44.
6. Blomberg M, Nielsen A, Munk C, et al. Trends in head and neck cancer incidence in Denmark, 1978-2007: focus on human papillomavirus associated sites. Int J Cancer 2011; 129: 733-41.
7. Braakhuis BJ, Visser O, Leemans CR,. Oral and oropharyngeal cancer in The Netherlands between 1989 and 2006: Increasing incidence, but not in young adults. Oral Oncol 2009; 45: e85-9.
8. Chaturvedi AK, Engels EA, Anderson WF, et al. Incidence trends for human papillomavirus-related and -unrelated oral squamous cell carcinomas in the United States. J Clin Oncol 2008; 26: 612-9.
9. Conway DI, Stockton DL, Warnakulasuriya KA, et al. Incidence of oral and oropharyngeal cancer in United Kingdom (1990-1999)-recent trends and regional variation. Oral Oncol 2006; 42: 586-92.
10. Hammarstedt L, Lindquist D, Dahlstrand H, et al. Human papillomavirus as a risk factor for the increase in incidence of tonsillar cancer. Int J Cancer 2006; 119: 2620-3.
11. Hocking JS, Stein A, Conway EL, et al. Head and neck cancer in Australia between 1982 and 2005 show increasing incidence of potentially HPV-associated oropharyngeal cancers. Br J Cancer 2011; 104: 886-91.
12. Holzinger D, Schmitt M, Dyckhoff G, et al. Viral RNA patterns and high viral load reliably define oropharynx carcinomas with active HPV16 Involvement. Cancer Res 2012; 72: 4993-5003.
13. Jung AC, Briolat J, Millon R, et al. Biological and clinical relevance of transcriptionally active human papillomavirus (HPV) infection in oropharynx squamous cell carcinoma. Int J Cancer 2010; 126: 1882-94.
14. Klussmann JP, Weissenborn SJ, Wieland U, et al. Prevalence, distribution, and viral load of human papillomavirus 16 DNA in tonsillar carcinomas. Cancer 2001; 92: 2875-84.
15. van Houten VM, Snijders PJ, van den Brekel MW, et al. Biological evidence that human papillomaviruses are etiologically involved in a subgroup of head and neck squamous cell carcinomas. Int J Cancer 2001; 93: 232-5.
16. Wiest T, Schwarz E, Enders C, et al. Involvement of intact HPV16 E6/E7 gene expression in head and neck cancers with unaltered p53 status and perturbed pRb cell cycle control. Oncogene 2002; 21: 1510-7.
17. Ang KK, Harris J, Wheeler R, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010; 363: 24-35.
18. Fakhry C, Westra WH, 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: 261-9.
19. Lindel K, Beer KT, Laissue J, et al. Human papillomavirus positive squamous cell carcinoma of the oropharynx: a radiosensitive subgroup of head and neck carcinoma. Cancer 2001; 92: 805-13.
20. Ritchie JM, Smith EM, Summersgill KF, et al. Human papillomavirus infection as a prognostic factor in carcinomas of the oral cavity and oropharynx. Int J Cancer 2003; 104: 336-44.
21. Shi W, Kato H, Perez-Ordonez B, et al. Comparative prognostic value of HPV16 E6 mRNA compared with in situ hybridization for human oropharyngeal squamous carcinoma. J Clin Oncol 2009; 27: 6213-21.
22. Weinberger PM, Yu Z, Haffty BG, et al. Molecular classification identifies a subset of human papillomavirus-associated oropharyngeal cancers with favorable prognosis. J Clin Oncol 2006; 24: 736-47.
23. Hafkamp HC, Manni JJ, Haesevoets A, et al. Marked differences in survival rate between smokers and nonsmokers with HPV 16-associated tonsillar carcinomas. Int J Cancer 2008; 122: 2656-64.
24. Smith EM, Wang D, Kim Y, et al. P16INK4a expression, human papillomavirus, and survival in head and neck cancer. Oral Oncol 2008; 44: 133-42.
25. Halec G, Schmitt M, Dondog B, et al. Biological activity of probable/possible high-risk human papillomavirus types in cervical cancer. Int J Cancer 2012.
26. Klaes R, Friedrich T, Spitkovsky D, et al. Overexpression of p16(INK4A) as a specific marker for dysplastic and neoplastic epithelial cells of the cervix uteri. Int J Cancer 2001; 92: 276-84.
27. von Knebel Doeberitz M,. New molecular tools for efficient screening of cervical cancer. Disease Markers 2001; 17: 123-8.
28. Hafkamp HC, Speel EJ, Haesevoets A, et al. A subset of head and neck squamous cell carcinomas exhibits integration of HPV 16/18 DNA and overexpression of p16INK4A and p53 in the absence of mutations in p53 exons 5-8. Int J Cancer 2003; 107: 394-400.
29. Hoffmann M, Ihloff AS, Gorogh T, et al. p16(INK4a) overexpression predicts translational active human papillomavirus infection in tonsillar cancer. Int J Cancer 2010; 127: 1595-602.
30. Klussmann JP, Gultekin E, Weissenborn SJ, et al. Expression of p16 protein identifies a distinct entity of tonsillar carcinomas associated with human papillomavirus. Am J Pathol 2003; 162: 747-53.
31. Kumar B, Cordell KG, Lee JS, 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: 3128-37.
32. Li W, Thompson CH, O'Brien CJ, et al. Human papillomavirus positivity predicts favourable outcome for squamous carcinoma of the tonsil. Int J Cancer 2003; 106: 553-8.
33. Reimers N, Kasper HU, Weissenborn SJ, et al. Combined analysis of HPV-DNA, p16 and EGFR expression to predict prognosis in oropharyngeal cancer. Int J Cancer 2007; 120: 1731-8.
34. Rischin D, Young RJ, Fisher R, et al. Prognostic significance of p16INK4A and human papillomavirus in patients with oropharyngeal cancer treated on TROG 02.02 phase III trial. J Clin Oncol 2010; 28: 4142-8.
35. Rotnaglova E, Tachezy R, Salakova M, et al. HPV involvement in tonsillar cancer: prognostic significance and clinically relevant markers. Int J Cancer 2011; 129: 101-10.
36. Weinberger PM, Yu Z, Haffty BG, et al. Prognostic significance of p16 protein levels in oropharyngeal squamous cell cancer. Clin Cancer Res 2004; 10: 5684-91.
37. Smeets SJ, Hesselink AT, Speel EJ, et al. A novel algorithm for reliable detection of human papillomavirus in paraffin embedded head and neck cancer specimen. Int J Cancer 2007; 121: 2465-72.
38. Weinberger PM, Merkley MA, Khichi SS, et al. Human papillomavirus-active head and neck cancer and ethnic health disparities. Laryngoscope 2010; 120: 1531-7.
39. Boyer SN, Wazer DE, Band V,. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res 1996; 56: 4620-4.
40. Bates S, Parry D, Bonetta L, et al. Absence of cyclin D/cdk complexes in cells lacking functional retinoblastoma protein. Oncogene 1994; 9: 1633-40.
41. Scheffner M, Werness BA, Huibregtse JM, et al. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990; 63: 1129-36.
42. Schmitt M, Bravo IG, Snijders PJ, et al. Bead-based multiplex genotyping of human papillomaviruses. J Clin Microbiol 2006; 44: 504-12.
43. Schmitt M, Dondog B, Waterboer T, et al. Homogeneous amplification of genital human alpha papillomaviruses by PCR using novel broad-spectrum GP5+ and GP6+ primers. J Clin Microbiol 2008; 46: 1050-9.
44. Schmitt M, Depuydt C, Benoy I, et al. Viral load of high-risk human papillomaviruses as reliable clinical predictor for the presence of cervical lesions. Cancer Epidemiol Biomarkers Prev 2013.
45. Schmitt M, Depuydt C, Benoy I, et al. Prevalence and viral load of 51 genital human papillomavirus types and three subtypes. Int J Cancer 2012.
46. Schmitt M, Dalstein V, Waterboer T, et al. Diagnosing cervical cancer and high-grade precursors by HPV16 transcription patterns. Cancer Res 2010; 70: 249-56.
47. Karsai S, Abel U, Roesch-Ely M, et al. Comparison of p16(INK4a) expression with p53 alterations in head and neck cancer by tissue microarray analysis. J Pathol 2007; 211: 314-22.
48. Nasser W, Flechtenmacher C, Holzinger D, et al. Aberrant expression of p53, p16(INK4a) and Ki-67 as basic biomarker for malignant progression of oral leukoplakias. J Oral Pathol Med 2011; 40: 629-35.
49. Young R, Rischin D, Fisher R, et al. Relationship between epidermal growth factor receptor status, p16INK4A and outcome in head and neck squamous cell carcinoma. Cancer Epidemiol Biomarkers Prev 2011; 20: 1230-7.
50. (TFI) WTFI. WHO Report on the Global Tobacco Epidemic; Appendix VII-Table Age-standardized prevalence estimates for smoking, 2006 2009.
51. Ernster JA, Sciotto CG, O'Brien MM, et al. Rising incidence of oropharyngeal cancer and the role of oncogenic human papilloma virus. Laryngoscope 2007; 117: 2115-28.
52. Sturgis EM, Cinciripini PM,. Trends in head and neck cancer incidence in relation to smoking prevalence: an emerging epidemic of human papillomavirus-associated cancers? Cancer 2007; 110: 1429-35.
53. Dai M, Clifford GM, le Calvez F, et al. Human papillomavirus type 16 and TP53 mutation in oral cancer: matched analysis of the IARC multicenter study. Cancer Res 2004; 64: 468-71.
54. Bosch FX, Ritter D, Enders C, et al. Head and neck tumor sites differ in prevalence and spectrum of p53 alterations but these have limited prognostic value. Int J Cancer 2004; 111: 530-8.
55. Hong AM, Dobbins TA, Lee CS, et al. Use of cyclin D1 in conjunction with human papillomavirus status to predict outcome in oropharyngeal cancer. Int J Cancer 2011; 128: 1532-45.