Differential gene hypermethylation in genital lichen sclerosus and cancer: A comparative study

Histopathology

Volumn 63, Issue 5, 2013, Pages 659-669

  Guerrero Setas, David ^a   Pérez Janices, Noemí ^a   Ojer, Amaya ^a   Blanco Fernandez, Laura ^a   Guarch Troyas, Carmen ^b   Guarch, Rosa ^c  

^a Atención Primaria Y Promoción de La Salud   (Spain)

^b Navarra Health Service   (Spain)

^c Universidad Pública de Navarra   (Spain)

Author keywords

Human papillomavirus; Hypermethylation; Lichen sclerosus; Penile cancer; Vulvar cancer

Indexed keywords

HEMOGLOBIN BETA CHAIN; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PROTEIN P16; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; THROMBOSPONDIN 1;

ADULT; ARTICLE; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; DNA METHYLATION; GENOTYPE; HUMAN; HUMAN TISSUE; LICHEN SCLEROSUS ET ATROPHICUS; MALE; PENIS CANCER; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; WART VIRUS;

HUMAN PAPILLOMAVIRUS;

HUMAN PAPILLOMAVIRUS; HYPERMETHYLATION; LICHEN SCLEROSUS; PENILE CANCER; VULVAR CANCER;

ADULT; AGED; CARCINOMA, SQUAMOUS CELL; DNA METHYLATION; FEMALE; HUMANS; LICHEN SCLEROSUS ET ATROPHICUS; MALE; MIDDLE AGED; PAPILLOMAVIRUS INFECTIONS; PENILE NEOPLASMS; VULVAR NEOPLASMS;

EID: 84885424054     PISSN: 03090167     EISSN: 13652559     Source Type: Journal    
DOI: 10.1111/his.12204     Document Type: Article

References (75)

1. Kulkarni S, Barbagli G, Kirpekar D, Mirri F, Lazzeri M. Lichen sclerosus of the male genitalia and urethra: surgical options and results in a multicenter international experience with 215 patients. Eur. Urol. 2009; 55; 945-956.
2. Bunker CB. Occlusion, urine and genital lichen sclerosus. Indian J. Dermatol. Venereol. Leprol. 2012; 78; 367-368.
3. Bunker CB, Patel N, Shim TN. Urinary voiding symptomatology (micro-incontinence) in male genital lichen sclerosus. Acta Derm. Venereol. 2013; 93; 246-248.
4. Edmonds E, Mavin S, Francis N, Ho-Yen D, Bunker C. Borrelia burgdorferi is not associated with genital lichen sclerosus in men. Br. J. Dermatol. 2009; 160; 459-460.
5. Riddell L, Edwards A, Sherrard J. Clinical features of lichen sclerosus in men attending a department of genitourinary medicine. Sex Transm. Infect. 2000; 76; 311-313.
6. Zapolski-Downar A, Nowak A, Bielecka-Grzela S. Lichen sclerosus et atrophicus in a married couple. Dermatol. Monatsschr. 1987; 173; 141-145.
7. Edmonds EV, Hunt S, Hawkins D, Dinneen M, Francis N, Bunker CB. Clinical parameters in male genital lichen sclerosus: a case series of 329 patients. J. Eur. Acad. Dermatol. Venereol. 2012; 26; 730-737.
8. Drut RM, Gomez MA, Drut R, Lojo MM. Human papillomavirus is present in some cases of childhood penile lichen sclerosus: an in situ hybridization and SP-PCR study. Pediatr. Dermatol. 1998; 15; 85-90.
9. Oertell J, Caballero C, Iglesias M et al. Differentiated precursor lesions and low-grade variants of squamous cell carcinomas are frequent findings in foreskins of patients from a region of high penile cancer incidence. Histopathology 2011; 58; 925-933.
10. Prowse DM, Ktori EN, Chandrasekaran D, Prapa A, Baithun S. Human papillomavirus-associated increase in p16INK4A expression in penile lichen sclerosus and squamous cell carcinoma. Br. J. Dermatol. 2008; 158; 261-265.
11. Nasca MR, Innocenzi D, Micali G. Association of penile lichen sclerosus and oncogenic human papillomavirus infection. Int. J. Dermatol. 2006; 45; 681-683.
12. von Krogh G, Dahlman-Ghozlan K, Syrjanen S. Potential human papillomavirus reactivation following topical corticosteroid therapy of genital lichen sclerosus and erosive lichen planus. J. Eur. Acad. Dermatol. Venereol. 2002; 16; 130-133.
13. Hussein MR, Haemel AK, Sudilovsky O, Wood GS. Genomic instability in radial growth phase melanoma cell lines after ultraviolet irradiation. J. Clin. Pathol. 2005; 58; 389-396.
14. Nasca MR, Innocenzi D, Micali G. Penile cancer among patients with genital lichen sclerosus. J. Am. Acad. Dermatol. 1999; 41; 911-914.
15. Nasca MR, Panetta C, Micali G, Innocenzi D. Microinvasive squamous cell carcinoma arising on lichen sclerosus of the penis. J. Eur. Acad. Dermatol. Venereol. 2003; 17; 337-339.
16. Quinn AG, Perkins W. Non-melanoma skin cancer and other epidermal skin tumours. In Burns T, Breathnach S, Cox N, Griffiths C eds. Rook's textbook of dermatology. 8th ed. Oxford, UK: Wiley-Blackwell, 2010.
17. Yoshinaga S, Hauptmann M, Sigurdson AJ et al. Nonmelanoma skin cancer in relation to ionizing radiation exposure among US radiologic technologists. Int. J. Cancer 2005; 115; 828-834.
18. Clouston D, Hall A, Lawrentschuk N. Penile lichen sclerosus (Balanitis xerotica obliterans). BJU Int. 2011; 108(Suppl. 2); 14-19.
19. Velazquez EF, Cubilla AL. Lichen sclerosus in 68 patients with squamous cell carcinoma of the penis: frequent atypias and correlation with special carcinoma variants suggests a precancerous role. Am. J. Surg. Pathol. 2003; 27; 1448-1453.
20. Renaud-Vilmer C, Cavelier-Balloy B, Verola O et al. Analysis of alterations adjacent to invasive squamous cell carcinoma of the penis and their relationship with associated carcinoma. J. Am. Acad. Dermatol. 2010; 62; 284-290.
21. Powell J, Strauss S, Gray J, Wojnarowska F. Genital carriage of human papilloma virus (HPV) DNA in prepubertal girls with and without vulval disease. Pediatr. Dermatol. 2003; 20; 191-194.
22. Barbagli G, Palminteri E, Mirri F, Guazzoni G, Turini D, Lazzeri M. Penile carcinoma in patients with genital lichen sclerosus: a multicenter survey. J. Urol. 2006; 175; 1359-1363.
23. Micali G, Nasca MR, Innocenzi D. Lichen sclerosus of the glans is significantly associated with penile carcinoma. Sex Transm. Infect. 2001; 77; 226.
24. Scurry J, Whitehead J, Healey M. Histology of lichen sclerosus varies according to site and proximity to carcinoma. Am. J. Dermatopathol. 2001; 23; 413-418.
25. Edmonds E, Barton G, Buisson S et al. Gene expression profiling in male genital lichen sclerosus. Int. J. Exp. Pathol. 2011; 92; 320-325.
26. Mannweiler S, Sygulla S, Beham-Schmid C, Razmara Y, Pummer K, Regauer S. Penile carcinogenesis in a low-incidence area: a clinicopathologic and molecular analysis of 115 invasive carcinomas with special emphasis on chronic inflammatory skin diseases. Am. J. Surg. Pathol. 2011; 35; 998-1006.
27. Pilatz A, Altinkilic B, Schormann E et al. Congenital phimosis in patients with and without lichen sclerosus: distinct expression patterns of tissue remodeling associated genes. J. Urol. 2013; 189; 268-274.
28. Regauer S, Beham-Schmid C. Detailed analysis of the T-cell lymphocytic infiltrate in penile lichen sclerosus: an immunohistochemical and molecular investigation. Histopathology 2006; 48; 730-735.
29. Esteller M. Epigenetics in cancer. N. Engl. J. Med. 2008; 358; 1148-1159.
30. Guerrero D, Guarch R, Ojer A et al. Hypermethylation of the thrombospondin-1 gene is associated with poor prognosis in penile squamous cell carcinoma. BJU Int. 2008; 102; 747-755.
31. Hellwinkel OJ, Kedia M, Isbarn H, Budaus L, Friedrich MG. Methylation of the TPEF- and PAX6-promoters is increased in early bladder cancer and in normal mucosa adjacent to pTa tumours. BJU Int. 2008; 101; 753-757.
32. Peters I, Rehmet K, Wilke N et al. RASSF1A promoter methylation and expression analysis in normal and neoplastic kidney indicates a role in early tumorigenesis. Mol. Cancer 2007; 6; 49-57.
33. Guerrero D, Guarch R, Ojer A et al. Differential hypermethylation of genes in vulvar cancer and lichen sclerosus coexisting or not with vulvar cancer. Int. J. Cancer 2011; 128; 2853-2864.
34. Soufir N, Queille S, Liboutet M et al. Inactivation of the CDKN2A and the p53 tumour suppressor genes in external genital carcinomas and their precursors. Br. J. Dermatol. 2007; 156; 448-453.
35. Hegi ME, Diserens AC, Gorlia T et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N. Engl. J. Med. 2005; 352; 997-1003.
36. Finegan MM, Han AC, Edelson MI, Rosenblum NG. p16 expression in squamous lesions of the female genital tract. J. Mol. Histol. 2004; 35; 111-114.
37. Jeong DH, Youm MY, Kim YN et al. Promoter methylation of p16, DAPK, CDH1, and TIMP-3 genes in cervical cancer: correlation with clinicopathologic characteristics. Int. J. Gynecol. Cancer 2006; 16; 1234-1240.
38. Donninger H, Vos MD, Clark GJ. The RASSF1A tumor suppressor. J. Cell Sci. 2007; 120(Pt 18); 3163-3172.
39. Cooper WN, Dickinson RE, Dallol A et al. Epigenetic regulation of the ras effector/tumour suppressor RASSF2 in breast and lung cancer. Oncogene 2008; 27; 1805-1811.
40. Guerrero-Setas D, Perez-Janices N, Blanco-Fernandez L et al. RASSF2 hypermethylation is present and related to shorter survival in squamous cervical cancer. Mod. Pathol. 2013; 26; 1111-1122.
41. Tabruyn SP, Griffioen AW. Molecular pathways of angiogenesis inhibition. Biochem. Biophys. Res. Commun. 2007; 355; 1-5.
42. Masuda M, Kikuchi S, Maruyama T et al. Tumor suppressor in lung cancer (TSLC)1 suppresses epithelial cell scattering and tubulogenesis. J. Biol. Chem. 2005; 280; 42164-42171.
43. Bertolo C, Guerrero D, Vicente F et al. Differences and molecular immunohistochemical parameters in the subtypes of infiltrating ductal breast cancer. Am. J. Clin. Pathol. 2008; 130; 414-424.
44. de Roda Husman AM, Snijders PJ, Stel HV, van deBrule AJ, Meijer CJ, Walboomers JM. Processing of long-stored archival cervical smears for human papillomavirus detection by the polymerase chain reaction. Br. J. Cancer 1995; 72; 412-417.
45. Van den Brule AJ, Pol R, Fransen-Daalmeijer N, Schouls LM, Meijer CJ, Snijders PJ. GP5 + /6 + PCR followed by reverse line blot analysis enables rapid and high-throughput identification of human papillomavirus genotypes. J. Clin. Microbiol. 2002; 40; 779-787.
46. Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl Acad. Sci. USA 1996; 93; 9821-9826.
47. Perceau G, Derancourt C, Clavel C et al. Lichen sclerosus is frequently present in penile squamous cell carcinomas but is not always associated with oncogenic human papillomavirus. Br. J. Dermatol. 2003; 148; 934-938.
48. Menzo S, Ciavattini A, Bagnarelli P, Marinelli K, Sisti S, Clementi M. Molecular epidemiology and pathogenic potential of underdiagnosed human papillomavirus types. BMC Microbiol. 2008; 8; 112-118.
49. Mattila R, Rautava J, Syrjanen S. Human papillomavirus in oral atrophic lichen planus lesions. Oral Oncol. 2012; 48; 980-984.
50. Schiffman M, Herrero R, Desalle R et al. The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 2005; 337; 76-84.
51. Campus GV, Alia F, Bosincu L. Squamous cell carcinoma and lichen sclerosus et atrophicus of the prepuce. Plast. Reconstr. Surg. 1992; 89; 962-964.
52. Botezatu A, Socolov D, Iancu IV et al. Methylenetetrahydrofolate reductase (MTHFR) polymorphisms and promoter methylation in cervical oncogenic lesions and cancer. J. Cell Mol. Med. 2013; 17; 543-549.
53. Nye MD, Hoyo C, Huang Z et al. Associations between methylation of paternally expressed gene 3 (PEG3), cervical intraepithelial neoplasia and invasive cervical cancer. PLoS ONE 2013; 8; e56325.
54. Gasco M, Sullivan A, Repellin C et al. Coincident inactivation of 14-3-3sigma and p16INK4a is an early event in vulval squamous neoplasia. Oncogene 2002; 21; 1876-1881.
55. Sutton BC, Allen RA, Moore WE, Dunn ST. Distribution of human papillomavirus genotypes in invasive squamous carcinoma of the vulva. Mod. Pathol. 2008; 21; 345-354.
56. Yanagawa N, Osakabe M, Hayashi M, Tamura G, Motoyama T. Frequent epigenetic silencing of the FHIT gene in penile squamous cell carcinomas. Virchows Arch. 2008; 452; 377-382.
57. Meffert JJ, Davis BM, Grimwood RE. Lichen sclerosus. J. Am. Acad. Dermatol. 1995; 32; 393-416.
58. Pietrzak P, Hadway P, Corbishley CM, Watkin NA. Is the association between balanitis xerotica obliterans and penile carcinoma underestimated? BJU Int. 2006; 98; 74-76.
59. Powell J, Robson A, Cranston D, Wojnarowska F, Turner R. High incidence of lichen sclerosus in patients with squamous cell carcinoma of the penis. Br. J. Dermatol. 2001; 145; 85-89.
60. Esteban S, Moya P, Fernandez-Suarez A, Vidaurreta M, Gonzalez-Peramato P, Sanchez-Carbayo M. Diagnostic and prognostic utility of methylation and protein expression patterns of myopodin in colon cancer. Tumour Biol. 2012; 33; 337-346.
61. Alvarez-Mugica M, Cebrian V, Fernandez-Gomez JM, Fresno F, Escaf S, Sanchez-Carbayo M. Myopodin methylation is associated with clinical outcome in patients with T1G3 bladder cancer. J. Urol. 2010; 184; 1507-1513.
62. Aitchison A, Warren A, Neal D, Rabbitts P. RASSF1A promoter methylation is frequently detected in both pre-malignant and non-malignant microdissected prostatic epithelial tissues. Prostate 2007; 67; 638-644.
63. Nakamura N, Carney JA, Jin L et al. RASSF1A and NORE1A methylation and BRAFV600E mutations in thyroid tumors. Lab. Invest. 2005; 85; 1065-1075.
64. Kang GH, Shim YH, Jung HY, Kim WH, Ro JY, Rhyu MG. CpG island methylation in premalignant stages of gastric carcinoma. Cancer Res. 2001; 61; 2847-2851.
65. Yang YX, Yang AH, Yang ZJ, Wang ZR, Xia XH. Involvement of tumor suppressor in lung cancer 1 gene expression in cervical carcinogenesis. Int. J. Gynecol. Cancer 2006; 16; 1868-1872.
66. Hui AB, Lo KW, Kwong J et al. Epigenetic inactivation of TSLC1 gene in nasopharyngeal carcinoma. Mol. Carcinog. 2003; 38; 170-178.
67. Kikuchi S, Yamada D, Fukami T et al. Promoter methylation of DAL-1/4.1B predicts poor prognosis in non-small cell lung cancer. Clin. Cancer Res. 2005; 11; 2954-2961.
68. Lerma E, Esteller M, Herman J, Prat J. Alterations of the p16/Rb/cyclin-D1 pathway in vulvar carcinoma, vulvar intraepithelial neoplasia, and lichen sclerosus. Hum. Pathol. 2002; 33; 1120-1125.
69. Ferreux E, Lont AP, Horenblas S et al. Evidence for at least three alternative mechanisms targeting the p16INK4A/cyclin D/Rb pathway in penile carcinoma, one of which is mediated by high-risk human papillomavirus. J. Pathol. 2003; 201; 109-118.
70. Furonaka O, Takeshima Y, Awaya H, Kushitani K, Kohno N, Inai K. Aberrant methylation and loss of expression of O-methylguanine-DNA methyltransferase in pulmonary squamous cell carcinoma and adenocarcinoma. Pathol. Int. 2005; 55; 303-309.
71. Lavon I, Zrihan D, Zelikovitch B et al. Longitudinal assessment of genetic and epigenetic markers in oligodendrogliomas. Clin. Cancer Res. 2007; 13; 1429-1437.
72. Sawhney M, Rohatgi N, Kaur J et al. MGMT expression in oral precancerous and cancerous lesions: correlation with progression, nodal metastasis and poor prognosis. Oral Oncol. 2007; 43; 515-522.
73. Hesson LB, Wilson R, Morton D et al. CpG island promoter hypermethylation of a novel Ras-effector gene RASSF2A is an early event in colon carcinogenesis and correlates inversely with K-ras mutations. Oncogene 2005; 24; 3987-3994.
74. Yesudian PD, Sugunendran H, Bates CM, O'Mahony C. Lichen sclerosus. Int. J. STD AIDS 2005; 16; 465-473.
75. Narayan G, Goparaju C, Arias-Pulido H et al. Promoter hypermethylation-mediated inactivation of multiple Slit-Robo pathway genes in cervical cancer progression. Mol. Cancer 2006; 5; 16-25.