Differences in methylation profiles between HPV-positive and HPV-negative oropharynx squamous cell carcinoma: A systematic review

Epigenetics

Volumn 9, Issue 2, 2014, Pages

  van Kempen, Pauline M W ^a   Noorlag, Rob ^a   Braunius, Weibel W ^a   Stegeman, Inge ^a   Willems, Stefan M ^a,b   Grolman, Wilko ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Epigenetic; Head and neck cancer; HPV; Methylation; Oropharynx; Systematic review

Indexed keywords

ALCOHOL CONSUMPTION; DNA METHYLATION; EPIGENETICS; GENOMIC INSTABILITY; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; OROPHARYNX; OROPHARYNX CARCINOMA; OVERALL SURVIVAL; PAPILLOMAVIRUS INFECTION; POLYMERASE CHAIN REACTION; PROGNOSIS; PROMOTER REGION; PYROSEQUENCING; REVIEW; SQUAMOUS CELL CARCINOMA; TUMOR SUPPRESSOR GENE; EPIGENETIC; GENETIC EPIGENESIS; GENETICS; HEAD AND NECK CANCER; HUMAN PAPILLOMAVIRUS TYPE 16; METABOLISM; METHYLATION; OROPHARYNX TUMOR; PHYSIOLOGY; SYSTEMATIC REVIEW; VIROLOGY; WART VIRUS;

EPIGENETIC; HEAD AND NECK CANCER; HPV; METHYLATION; OROPHARYNX; SYSTEMATIC REVIEW;

CARCINOMA, SQUAMOUS CELL; DNA METHYLATION; EPIGENESIS, GENETIC; HUMAN PAPILLOMAVIRUS 16; HUMANS; OROPHARYNGEAL NEOPLASMS; PROMOTER REGIONS, GENETIC;

EID: 84892619242     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.26881     Document Type: Review

References (68)

1. Tsai HC, Baylin SB. Cancer epigenetics: linking basic biology to clinical medicine. Cell Res 2011; 21:502-17; PMID:21321605; http://dx.doi.org/10.1038/ cr.2011.24
2. Berdasco M, Esteller M. Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev Cell 2010; 19:698-711; PMID:21074720; http:// dx.doi.org/10.1016/j.devcel.2010.10.005
3. Ng HH, Bird A. DNA methylation and chromatin modification. Curr Opin Genet Dev 1999; 9:158-63; PMID:10322130; http://dx.doi.org/10.1016/ S0959-437X(99)80024-0
4. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002; 3:415-28; PMID:12042769
5. Robertson KD. DNA methylation and human disease. Nat Rev Genet 2005; 6:597-610; PMID:16136652; http://dx.doi.org/10.1038/nrg1655
6. Eden S, Cedar H. Role of DNA methylation in the regulation of transcription. Curr Opin Genet Dev 1994; 4:255-9; PMID:8032203; http://dx.doi. org/10.1016/S0959-437X(05)80052-8
7. Weisenberger DJ, Campan M, Long TI, Kim M, Woods C, Fiala E, Ehrlich M, Laird PW. Analysis of repetitive element DNA methylation by MethyLight. Nucleic Acids Res 2005; 33:6823-36; PMID:16326863; http://dx.doi.org/10.1093/nar/ gki987
8. Stebbing J, Bower M, Syed N, Smith P, Yu V, Crook T. Epigenetics: an emerging technology in the diagnosis and treatment of cancer. Pharmacogenomics 2006; 7:747-57; PMID:16886899; http://dx.doi. org/10.2217/14622416.7.5.747
9. Baylin SB, Herman JG. DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet 2000; 16:168-74; PMID:10729832; http:// dx.doi.org/10.1016/S0168-9525(99)01971-X
10. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003; 349:2042-54; PMID:14627790; http:// dx.doi.org/10.1056/NEJMra023075
11. Ehrlich M. DNA hypomethylation, cancer, the immunodeficiency, centromeric region instability, facial anomalies syndrome and chromosomal rearrangements. J Nutr 2002; 132(Suppl):2424S-9S; PMID:12163705
12. Leemans CR, Braakhuis BJ, Brakenhoff RH. The molecular biology of head and neck cancer. Nat Rev Cancer 2011; 11:9-22; PMID:21160525; http:// dx.doi.org/10.1038/nrc2982
13. Smith EM, Rubenstein LM, Haugen TH, Hamsikova E, Turek LP. Tobacco and alcohol use increases the risk of both HPV-associated and HPV-independent head and neck cancers. Cancer Causes Control 2010; 21:1369-78; PMID:20401530; http://dx.doi. org/10.1007/s10552-010-9564-z
14. Curado MP, Hashibe M. Recent changes in the epidemiology of head and neck cancer. Curr Opin Oncol 2009; 21:194-200; PMID:19363341; http://dx.doi. org/10.1097/CCO.0b013e32832a68ca
15. Marur S, D'Souza G, Westra WH, Forastiere AA. HPV-associated head and neck cancer: a virusrelated cancer epidemic. Lancet Oncol 2010; 11:781-9; PMID:20451455; http://dx.doi.org/10.1016/ S1470-2045(10)70017-6
16. Gillison ML. Human papillomavirus-associated head and neck cancer is a distinct epidemiologic, clinical, and molecular entity. Semin Oncol 2004; 31:744-54; PMID:15599852; http://dx.doi.org/10.1053/j. seminoncol.2004.09.011
17. Fakhry C, Westra WH, Li S, Cmelak A, Ridge JA, Pinto H, Forastiere A, Gillison ML. 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; PMID:18270337; http://dx.doi.org/10.1093/jnci/ djn011
18. Stransky N, Egloff AM, Tward AD, Kostic AD, Cibulskis K, Sivachenko A, Kryukov GV, Lawrence MS, Sougnez C, McKenna A, et al. The mutational landscape of head and neck squamous cell carcinoma. Science 2011; 333:1157-60; PMID:21798893; http:// dx.doi.org/10.1126/science.1208130
19. Chung CH, Gillison ML. Human papillomavirus in head and neck cancer: its role in pathogenesis and clinical implications. Clin Cancer Res 2009; 15:6758-62; PMID:19861444; http://dx.doi. org/10.1158/1078-0432.CCR-09-0784
20. Lechner M, Frampton GM, Fenton T, Feber A, Palmer G, Jay A, Pillay N, Forster M, Cronin MT, Lipson D, et al. Targeted next-generation sequencing of head and neck squamous cell carcinoma identifies novel genetic alterations in HPV+ and HPV-tumors. Genome Med 2013; 5:49; PMID:23718828; http:// dx.doi.org/10.1186/gm453
21. Kimple RJ, Smith MA, Blitzer GC, Torres AD, Martin JA, Yang RZ, Peet CR, Lorenz LD, Nickel KP, Klingelhutz AJ, et al. Enhanced radiation sensitivity in HPV-positive head and neck cancer. Cancer Res 2013; 73:4791-800; PMID:23749640; http:// dx.doi.org/10.1158/0008-5472.CAN-13-0587
22. Lohavanichbutr P, Houck J, Fan W, Yueh B, Mendez E, Futran N, Doody DR, Upton MP, Farwell DG, Schwartz SM, et al. Genomewide gene expression profiles of HPV-positive and HPV-negative oropharyngeal cancer: potential implications for treatment choices. Arch Otolaryngol Head Neck Surg 2009; 135:180-8; PMID:19221247; http://dx.doi. org/10.1001/archoto.2008.540
23. Martinez I, Wang J, Hobson KF, Ferris RL, Khan SA. Identification of differentially expressed genes in HPV-positive and HPV-negative oropharyngeal squamous cell carcinomas. Eur J Cancer 2007; 43:415-32; PMID:17079134; http://dx.doi.org/10.1016/j. ejca.2006.09.001
24. Schlecht NF, Burk RD, Adrien L, Dunne A, Kawachi N, Sarta C, Chen Q, Brandwein-Gensler M, Prystowsky MB, Childs G, et al. Gene expression profiles in HPV-infected head and neck cancer. J Pathol 2007; 213:283-93; PMID:17893858; http://dx.doi. org/10.1002/path.2227
25. Slebos RJ, Yi Y, Ely K, Carter J, Evjen A, Zhang X, Shyr Y, Murphy BM, Cmelak AJ, Burkey BB, et al. Gene expression differences associated with human papillomavirus status in head and neck squamous cell carcinoma. Clin Cancer Res 2006; 12:701-9; PMID:16467079; http://dx.doi.org/10.1158/1078-0432.CCR-05-2017
26. Leonard SM, Wei W, Collins SI, Pereira M, Diyaf A, Constandinou-Williams C, Young LS, Roberts S, Woodman CB. Oncogenic human papillomavirus imposes an instructive pattern of DNA methylation changes which parallel the natural history of cervical HPV infection in young women. Carcinogenesis 2012; 33:1286-93; PMID:22552403; http://dx.doi. org/10.1093/carcin/bgs157
27. Burgers WA, Blanchon L, Pradhan S, de Launoit Y, Kouzarides T, Fuks F. Viral oncoproteins target the DNA methyltransferases. Oncogene 2007; 26:1650-5; PMID:16983344; http://dx.doi.org/10.1038/ sj.onc.1209950
28. Bennett KL, Lee W, Lamarre E, Zhang X, Seth R, Scharpf J, Hunt J, Eng C. HPV status-independent association of alcohol and tobacco exposure or prior radiation therapy with promoter methylation of FUSSEL18, EBF3, IRX1, and SEPT9, but not SLC5A8, in head and neck squamous cell carcinomas. Genes Chromosomes Cancer 2010; 49:319-26; PMID:20029986
29. Colacino JA, Dolinoy DC, Duffy SA, Sartor MA, Chepeha DB, Bradford CR, McHugh JB, Patel DA, Virani S, Walline HM, et al. Comprehensive analysis of DNA methylation in head and neck squamous cell carcinoma indicates differences by survival and clinicopathologic characteristics. PLoS One 2013; 8:e54742; PMID:23358896; http://dx.doi. org/10.1371/journal.pone.0054742
30. Dong SM, Sun DI, Benoit NE, Kuzmin I, Lerman MI, Sidransky D. Epigenetic inactivation of RASSF1A in head and neck cancer. Clin Cancer Res 2003; 9:3635-40; PMID:14506151
31. de Freitas Cordeiro-Silva M, Stur E, Agostini LP, de Podestá JR, de Oliveira JC, Soares MS, Mendonça EF, Gouvea SA, Von Zeidler SV, Louro ID. Promoter hypermethylation in primary squamous cell carcinoma of the oral cavity and oropharynx: a study of a Brazilian cohort. Mol Biol Rep 2012; 39:10111-9; PMID:22936053; http://dx.doi.org/10.1007/ s11033-012-1885-4
32. Furniss CS, Marsit CJ, Houseman EA, Eddy K, Kelsey KT. Line region hypomethylation is associated with lifestyle and differs by human papillomavirus status in head and neck squamous cell carcinomas. Cancer Epidemiol Biomarkers Prev 2008; 17:966-71; PMID:18398038; http://dx.doi.org/10.1158/1055-9965.EPI-07-2775
33. Gubanova E, Brown B, Ivanov SV, Helleday T, Mills GB, Yarbrough WG, Issaeva N. Downregulation of SMG-1 in HPV-positive head and neck squamous cell carcinoma due to promoter hypermethylation correlates with improved survival. Clin Cancer Res 2012; 18:1257-67; PMID:22247495; http://dx.doi. org/10.1158/1078-0432.CCR-11-2058
34. Lechner M, Fenton T, West J, Wilson G, Feber A, Henderson S, Thirlwell C, Dibra HK, Jay A, Butcher L, et al. Identification and functional validation of HPV-mediated hypermethylation in head and neck squamous cell carcinoma. Genome Med 2013; 5:15; PMID:23419152; http://dx.doi.org/10.1186/gm419
35. Marsit CJ, McClean MD, Furniss CS, Kelsey KT. Epigenetic inactivation of the SFRP genes is associated with drinking, smoking and HPV in head and neck squamous cell carcinoma. Int J Cancer 2006; 119:1761-6; PMID:16708382; http://dx.doi. org/10.1002/ijc.22051
36. Marsit CJ, Posner MR, McClean MD, Kelsey KT. Hypermethylation of E-cadherin is an independent predictor of improved survival in head and neck squamous cell carcinoma. Cancer 2008; 113:1566-71; PMID:18711702; http://dx.doi.org/10.1002/ cncr.23770
37. O'Regan EM, Toner ME, Finn SP, Fan CY, Ring M, Hagmar B, Timon C, Smyth P, Cahill S, Flavin R, et al. p16(INK4A) genetic and epigenetic profiles differ in relation to age and site in head and neck squamous cell carcinomas. Hum Pathol 2008; 39:452-8; PMID:18261630; http://dx.doi.org/10.1016/j. humpath.2007.08.004
38. Poage GM, Houseman EA, Christensen BC, Butler RA, Avissar-Whiting M, McClean MD, Waterboer T, Pawlita M, Marsit CJ, Kelsey KT. Global hypomethylation identifies Loci targeted for hypermethylation in head and neck cancer. Clin Cancer Res 2011; 17:3579-89; PMID:21505061; http://dx.doi. org/10.1158/1078-0432.CCR-11-0044
39. Richards KL, Zhang B, Baggerly KA, Colella S, Lang JC, Schuller DE, Krahe R. Genome-wide hypomethylation in head and neck cancer is more pronounced in HPV-negative tumors and is associated with genomic instability. PLoS One 2009; 4:e4941; PMID:19293934; http://dx.doi.org/10.1371/journal. pone.0004941
40. Sartor MA, Dolinoy DC, Jones TR, Colacino JA, Prince ME, Carey TE, Rozek LS. Genome-wide methylation and expression differences in HPV(+) and HPV(-) squamous cell carcinoma cell lines are consistent with divergent mechanisms of carcinogenesis. Epigenetics 2011; 6:777-87; PMID:21613826; http://dx.doi.org/10.4161/epi.6.6.16216
41. Taioli E, Ragin C, Wang XH, Chen J, Langevin SM, Brown AR, Gollin SM, Garte S, Sobol RW. Recurrence in oral and pharyngeal cancer is associated with quantitative MGMT promoter methylation. BMC Cancer 2009; 9:354; PMID:19807915; http://dx.doi.org/10.1186/1471-2407-9-354
42. Weiss D, Basel T, Sachse F, Braeuninger A, Rudack C. Promoter methylation of cyclin A1 is associated with human papillomavirus 16 induced head and neck squamous cell carcinoma independently of p53 mutation. Mol Carcinog 2011; 50:680-8; PMID:21563216; http://dx.doi.org/10.1002/ mc.20798
43. Weiss D, Stockmann C, Schrödter K, Rudack C. Protein expression and promoter methylation of the candidate biomarker TCF21 in head and neck squamous cell carcinoma. Cell Oncol (Dordr) 2013; 36:213-24; PMID:23529585; http://dx.doi. org/10.1007/s13402-013-0129-5
44. Kostareli E, Holzinger D, Bogatyrova O, Hielscher T, Wichmann G, Keck M, Lahrmann B, Grabe N, Flechtenmacher C, Schmidt CR, et al. HPV-related methylation signature predicts survival in oropharyngeal squamous cell carcinomas. J Clin Invest 2013; 123:2488-501; PMID:23635773; http://dx.doi. org/10.1172/JCI67010
45. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j. cell.2011.02.013
46. Laird PW. The power and the promise of DNA methylation markers. Nat Rev Cancer 2003; 3:253-66; PMID:12671664; http://dx.doi.org/10.1038/ nrc1045
47. Verma M, Srivastava S. Epigenetics in cancer: implications for early detection and prevention. Lancet Oncol 2002; 3:755-63; PMID:12473517; http:// dx.doi.org/10.1016/S1470-2045(02)00932-4
48. Demokan S, Dalay N. Role of DNA methylation in head and neck cancer. Clin Epigenetics 2011; 2:123-50; PMID:22704334; http://dx.doi.org/10.1007/ s13148-011-0045-3
49. König F, Krekeler G, Hönig JF, Cordon-Cardo C, Fischer G, Korabiowska M. Relation between human papillomavirus positivity and p16 expression in head and neck carcinomas--a tissue microarray study. Anticancer Res 2007; 27(1A):283-8; PMID:17352245
50. Au Yeung CL, Tsang WP, Tsang TY, Co NN, Yau PL, Kwok TT. HPV-16 E6 upregulation of DNMT1 through repression of tumor suppressor p53. Oncol Rep 2010; 24:1599-604; PMID:21042757
51. Dyson N, Howley PM, Münger K, Harlow E. The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 1989; 243:934-7; PMID:2537532; http://dx.doi. org/10.1126/science.2537532
52. Näsman A, Attner P, Hammarstedt L, Du J, Eriksson M, Giraud G, Ahrlund-Richter S, Marklund L, Romanitan M, Lindquist D, et al. Incidence of human papillomavirus (HPV) positive tonsillar carcinoma in Stockholm, Sweden: an epidemic of viralinduced carcinoma? Int J Cancer 2009; 125:362-6; PMID:19330833; http://dx.doi.org/10.1002/ ijc.24339
53. Deng Z, Hasegawa M, Matayoshi S, Kiyuna A, Yamashita Y, Maeda H, Suzuki M. Prevalence and clinical features of human papillomavirus in head and neck squamous cell carcinoma in Okinawa, southern Japan. Eur Arch Otorhinolaryngol 2011; 268:1625-31; PMID:21328000; http://dx.doi.org/10.1007/ s00405-011-1515-0
54. Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Sibug-Saber M, Cozen W, et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 2011; 29:4294-301; PMID:21969503; http://dx.doi.org/10.1200/ JCO.2011.36.4596
55. Braakhuis BJ, Snijders PJ, Keune WJ, Meijer CJ, Ruijter-Schippers HJ, Leemans CR, Brakenhoff RH. Genetic patterns in head and neck cancers that contain or lack transcriptionally active human papillomavirus. J Natl Cancer Inst 2004; 96:998-1006; PMID:15240783; http://dx.doi.org/10.1093/jnci/ djh183
56. Smeets SJ, Braakhuis BJ, Abbas S, Snijders PJ, Ylstra B, van de Wiel MA, Meijer GA, Leemans CR, Brakenhoff RH. Genome-wide DNA copy number alterations in head and neck squamous cell carcinomas with or without oncogene-expressing human papillomavirus. Oncogene 2006; 25:2558-64; PMID:16314836; http://dx.doi.org/10.1038/ sj.onc.1209275
57. Smeets SJ, Hesselink AT, Speel EJ, Haesevoets A, Snijders PJ, Pawlita M, Meijer CJ, Braakhuis BJ, Leemans CR, Brakenhoff RH. A novel algorithm for reliable detection of human papillomavirus in paraffin embedded head and neck cancer specimen. Int J Cancer 2007; 121:2465-72; PMID:17680565; http://dx.doi.org/10.1002/ijc.22980
58. Specht K, Richter T, Müller U, Walch A, Werner M, Höfler H. Quantitative gene expression analysis in microdissected archival formalin-fixed and paraffinembedded tumor tissue. Am J Pathol 2001; 158:419-29; PMID:11159180; http://dx.doi.org/10.1016/ S0002-9440(10)63985-5
59. Lu J, Richardson JA, Olson EN. Capsulin: a novel bHLH transcription factor expressed in epicardial progenitors and mesenchyme of visceral organs. Mech Dev 1998; 73:23-32; PMID:9545521; http://dx.doi. org/10.1016/S0925-4773(98)00030-6
60. Weiss D, Koopmann M, Basel T, Rudack C. Cyclin A1 shows age-related expression in benign tonsils, HPV16-dependent overexpression in HNSCC and predicts lower recurrence rate in HNSCC independently of HPV16. BMC Cancer 2012; 12:259; PMID:22712549; http://dx.doi. org/10.1186/1471-2407-12-259
61. Gudas LJ. Emerging roles for retinoids in regeneration and differentiation in normal and disease states. Biochim Biophys Acta 2012; 1821:213-21; PMID:21855651; http://dx.doi.org/10.1016/j. bbalip.2011.08.002
62. Srivenugopal KS, Ali-Osman F. The DNA repair protein, O(6)-methylguanine-DNA methyltransferase is a proteolytic target for the E6 human papillomavirus oncoprotein. Oncogene 2002; 21:5940-5; PMID:12185595; http://dx.doi.org/10.1038/ sj.onc.1205762
63. Salazar CR, Smith RV, Garg MK, Haigentz M Jr., Schiff BA, Kawachi N, Anayannis N, Belbin TJ, Prystowsky MB, Burk RD, et al. Human Papillomavirus-Associated Head and Neck Squamous Cell Carcinoma Survival: A Comparison by Tumor Site and Initial Treatment. Head Neck Pathol 2013; Forthcoming; PMID:24002971; http://dx.doi. org/10.1007/s12105-013-0486-4
64. Rodriguez J, Frigola J, Vendrell E, Risques RA, Fraga MF, Morales C, Moreno V, Esteller M, Capellà G, Ribas M, et al. Chromosomal instability correlates with genome-wide DNA demethylation in human primary colorectal cancers. Cancer Res 2006; 66:8462-9468; PMID:16951157; http://dx.doi. org/10.1158/0008-5472.CAN-06-0293
65. Wilson AS, Power BE, Molloy PL. DNA hypomethylation and human diseases. Biochim Biophys Acta 2007; 1775:138-62; PMID:17045745
66. Wild L, Flanagan JM. Genome-wide hypomethylation in cancer may be a passive consequence of transformation. Biochim Biophys Acta 2010; 1806:50-7; PMID:20398739
67. Saito Y, Kanai Y, Sakamoto M, Saito H, Ishii H, Hirohashi S. Overexpression of a splice variant of DNA methyltransferase 3b, DNMT3b4, associated with DNA hypomethylation on pericentromeric satellite regions during human hepatocarcinogenesis. Proc Natl Acad Sci U S A 2002; 99:10060-5; PMID:12110732; http://dx.doi.org/10.1073/ pnas.152121799
68. Hennessey PT, Ochs MF, Mydlarz WW, Hsueh W, Cope L, Yu W, Califano JA. Promoter methylation in head and neck squamous cell carcinoma cell lines is significantly different than methylation in primary tumors and xenografts. PLoS One 2011; 6:e20584; PMID:21637785; http://dx.doi.org/10.1371/journal. pone.0020584