Status of p16INK4a and E-cadherin gene promoter methylation in Moroccan patients with cervical carcinoma

Oncology Research

Volumn 18, Issue 4, 2009, Pages 185-192

  Attaleb, Mohammed ^a   Hamadani, Wail El ^a   Khyatti, Meriem ^b   Benbacer, Laila ^a   Benchekroun, Nadia ^c   Benider, Abdellatif ^c   Amrani, Mariam ^d   Mzibri, Mohammed El ^a  

^a CENTRE NATIONAL DE L ENERGIE DES SCIENCES TECHNIQUES NUCLEAIRES   (Morocco)

^b Institut Pasteur du Maroc   (Morocco)

^c IBN ROCHD UNIVERSITY HOSPITAL   (Morocco)

^d NATIONAL INSTITUTE OF ONCOLOGY   (Morocco)

Author keywords

Cervical cancer; E cadherin; Hypermethylation; p16INK4a

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; UVOMORULIN; CADHERIN; DNA; VIRUS DNA;

ARTICLE; CANCER CELL CULTURE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOROCCO; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; UTERINE CERVIX CARCINOMA; WART VIRUS; CANCER INVASION; GENE EXPRESSION REGULATION; GENETICS; MIDDLE AGED; PAPILLOMA VIRUS; PAPILLOMAVIRUS INFECTION; PATHOLOGY; SQUAMOUS CELL CARCINOMA; TUMOR CELL CULTURE; UTERINE CERVIX TUMOR; VIROLOGY;

CADHERINS; CARCINOMA, SQUAMOUS CELL; CPG ISLANDS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA METHYLATION; DNA, NEOPLASM; DNA, VIRAL; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MIDDLE AGED; NEOPLASM INVASIVENESS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; TUMOR CELLS, CULTURED; UTERINE CERVICAL NEOPLASMS;

EID: 77649198547     PISSN: 09650407     EISSN: None     Source Type: Journal    
DOI: 10.3727/096504009790217416     Document Type: Article

References (51)

1. Roberts, C. C.; Tadesse, A. S.; Sands, J.; Halvorsen, T.; Schofield, T. L.; Dalen, A.; Skjeldestad, F. E.; Jansen, K. U. Detection of HPV in Norwegian cervical biopsy specimens with type-specific PCR and reverse line blot assays. J. Clin. Virol. 36:277-282; 2006.
2. Amrani, M.; Lalaoui, K.; El Mzibri, M.; Lazo, P.; Belabbas, M. A. Molecular detection of human papillomavirus in 594 uterine cervix samples from Moroccan women (147 biopsies and 447 swabs). J. Clin. Virol. 27:286-295; 2003.
3. Schiffman, M. H.; Castle, P. Epidemiologic studies of a necessary causal risk factor: Human papillomavirus infection and cervical neoplasia. J. Natl. Cancer Inst. 95:2E; 2003.
4. Zur Hausen, H. Papillomaviruses causing cancer: Evasion from host-cell control in early events in carcinogenesis. J. Natl. Cancer Inst. 92:690-698; 2000.
5. Ferenczy, A.; Franco, E. Cervical-cancer screening beyond the year 2000. Lancet Oncol. 2:27-32; 2001.
6. Holowaty, P.; Miller, A. B.; Rohan, T.; To, T. Natural history of dysplasia of the uterine cervix. J. Natl. Cancer Inst. 91:252-258; 1999.
7. Syrjanen, K. J. Spontaneous evolution of intraepithelial lesions according to the grade and type of the implicated human papillomavirus (hpv). Eur. J. Obstet. Gynecol. Reprod. Biol. 65:45-53; 1996.
8. Jones, P. A.; Baylin, S. B. The fundamental role of epigenetic events in cancer. Nat. Rev. Genet. 3:415-428; 2002.
9. Feinberg, A. P.; Tycko, B. The history of cancer epigenetics. Nat. Rev. Cancer 4:143-153; 2004.
10. Bird, A. P. CpG-rich islands and the function of DNA methylation. Nature 321:209-213; 1986.
11. Larsen, F.; Gundersen, G.; Lopez, R.; Prydz, H. CpG islands as gene markers in the human genome. Genomics 13:1095-1107; 1992.
12. Knudson, A. G. Two genetic hits (more or less) to cancer. Nat. Rev. Cancer 1:157-162; 2001.
13. Cottrell, S. E.; Laird, P. W. Sensitive detection of DNA methylation. Ann. NY Acad. Sci. 983:120-130; 2003.
14. Laird, P. W. The power and the promise of DNA methylation markers. Nat. Rev. Cancer 3:253-266; 2003.
15. Gonzalgo, M. L.; Hayashida, T.; Bender, C. M.; Pao, M. M.; Tsai, Y. C.; Gonzales, F. A.; Nguyen, H. D.; Nguyen, T. T.; Jones, P. A. The role of DNA methylation in expression of the p19/p16 locus in human bladder cancer cell lines. Cancer Res. 58:1245-1252; 1998.
16. Liu, X.; Clements, A.; Zhao, K. Structure of the human papillomavirus E7 oncoprotein and its mechanism for inactivation of retinoblastoma tumor suppressor. J. Biol. Chem. 281:578-586; 2006.
17. Ivanova, T. A.; Golovina, D. A.; Zavalishina, L. E.; Volgareva, G. M.; Katargin, A. N.; Andreeva, Y. Y.; Frank, G. A.; Kisseljov, F. L.; Kisseljova, N. P. Up-regulation of expression and lack of 5′ CpG island hypermethylation of p16 INK4a in HPV-positive cervical carcinomas. BMC Cancer 7:47-56; 2007.
18. Nehls, K.; Vinokurova, S.; Schmidt, D.; Kommoss, F.; Reuschenbach, M.; Kisseljov, F.; Einenkel, J.; von Knebel Doeberitz, M.; Wentzensen, N. p16 methylation does not affect protein expression in cervical carcinogenesis. Eur. J. Cancer 44:2496-2505; 2008.
19. Wentzensen, N.; Bergeron, C.; Cas, F.; Vinokurova, S.; von Knebel Doeberitz, M. Triage of women with ASCUS and LSIL cytology: Use of qualitative assessment of p16INK4a positive cells to identify patients with high-grade cervical intraepithelial neoplasia. Cancer 111:58-66; 2007.
20. Derksen, P. W.; Liu, X.; Saridin, F.; van der Gulden, H.; Zevenhoven, J.; Evers, B.; van Beijnum, J. R.; Griffioen, A. W.; Vink, J.; Krimpenfort, P.; Peterse, J. L.; Cardiff, R. D.; Berns, A.; Jonkers, J. Somatic inactivation of Ecadherin and p53 in mice leads to metastatic lobular mam mary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10:437-449; 2006.
21. Gould Rothberg, B. E.; Bracken, M. B. E-cadherin immunohistochemical expression as a prognostic factor in infiltrating ductal carcinoma of the breast: A systematic review and meta-analysis. Breast Cancer Res. Treat. 100:139-148; 2006.
22. Hirohashi, S. Inactivation of the E-cadherin-mediated cell adhesion system in human cancers. Am. J. Pathol. 153: 333-339; 1998.
23. de Boer, C. J.; van Dorst, E.; van Krieken, H.; Jansen-van Rhijn, C. M.; Warnaar, S. O.; Fleuren, G. J.; Litvinov, S. V. Changing roles of cadherins and catenins duringprog ression of squamous intraepithelial lesions in the uterine cervix. Am. J. Pathol. 155:505-515; 1999.
24. Chen, C. L.; Liu, S. S.; Ipb, S. M.; Wongb, L. C.; Ng, T. Y.; Nganb, H. Y. S. E-cadherin expression is silenced by DNA methylation in cervical cancer cell lines and tumours. Eur. J. Cancer 39:517-523; 2003.
25. Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular cloning: A laboratory manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press; 1989.
26. Herman, J. G.; Graff, J. R.; Myohanen, S.; Nelkin, B. D.; Baylin, S. B. Methylationspecific, PCR: A novel PCR assay for methylation status of CpG islands. Proc. Natl. Acad. Sci. USA 93:9821-9826; 1996.
27. Esteller, M.; Corn, P. G.; Baylin, S. B.; Herman, J. G. A gene hypermethylation profile of human cancer. Cancer Res. 61:3225-3229; 2001.
28. Dong, S. M.; Kim, H. S.; Rha, S. H.; Sidransky, D. Promoter hypermethylation of multiple genes in carcinoma of the uterine cervix. Clin. Cancer Res. 7:1982-1986; 2001.
29. Kuzmin, I.; Liu, L.; Dammann, R.; Geil, L.; Stanbridge, E. J.; Wilczynski, S. P.; Lerman, M. I.; Pfeifer, G. P. Inactivation of RAS association domain family 1A gene in cervical carcinomas and the role of human papillomavirus infection. Cancer Res. 63:1888-1893; 2003.
30. Müller, H. M.; Widschwendter, A.; Fiegl, H.; Goebel, G.; Wiedemair, A.; Müller-Holzner, E.; Marth, C.; Widschwendter, M. A DNA methylation pattern similar to normal tissue is associated with better prognosis in human cervical cancer. Cancer Lett. 25:231-236; 2004.
31. Virmani, A.; Muller, C.; Rayhi, A.; Zoechbauer-Mueller, S.; Mathis, M.; Gazdar, A. Aberrant methylation during cervical carcinogenesis. Clin. Cancer Res. 7:584-589; 2001.
32. Widschwendter, A.; Gattringer, C.; Ivarsson, L.; Fiegl, H.; Schneitter, A.; Ramoni, A.; Müller, H. M.; Wiedemair, A.; Jerabek, S.; Müller-Holzner, E.; Goebel, G.; Marth, C.; Widschwendter, M. Analysis of aberrant DNA methylation and human papillomavirus DNA in cervicovaginal specimens to detect invasive cervical cancer and its precursors. Clin. Cancer Res. 10:3396-3400; 2004.
33. Widschwendter, A.; Ivarsson, L.; Blassnig, A.; Müller, H. M.; Fiegl, H.; Wiedemair, A.; Müller-Holzner, E.; Goebel, G.; Marth, C.; Widschwendter, M. CDH1 and CDH13 methylation in serum is an independent prognostic marker in cervical cancer patients. Int. J. Cancer 109:163-166; 2004.
34. Widschwendter, A.; Müller, H. M.; Fiegl, H.; Ivarsson, L.; Wiedemair, A.; Müller-Holzner, E.; Goebel, G.; Marth, C.; Widschwendter, M. DNA methylation in serum and tumors of cervical cancer patients. Clin. Cancer Res. 10:565-571; 2004.
35. Yang, H. J.; Liu, V.; Wang, Y.; Tsang, P.; Ngan, H. Differential DNA methylation profiles in gynecological cancers and correlation with clinico-patholgical data. BMC Cancer 6:212-221; 2006.
36. Serrano, M.; Lin, A. W.; McCurrach, M. E.; Beach, D.; Lowe, S. W. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593-602; 1997.
37. Ziober, B. L.; Silverman, S. S.; Kramer, R. H. Adhesive mechanisms regulating invasion and metastasis in oral cancer. Crit. Rev. Oral. Biol. Med. 12:499-510; 2001.
38. Karayiannakis, A. J.; Syrigos, K. N.; Chatzigianni, E.; Papanikolaou, S.; Alexiou, D.; Kalahanis, N.; Rosenberg, T.; Bastounis, E. Aberrant E-cadherin expression associated with loss of differentiation and advanced stage in human pancreatic cancer. Anticancer Res. 18:4177-4180; 1998.
39. Sulzer, M. A.; Leers, M. P.; van Noord, J. A.; Bollen, E. C.; Theunissen, P. H. Reduced E-cadherin expression is associated with increased lymph node metastasis and unfavorable prognosis in non-small cell lung cancer. Am. J. Resp. Crit. Care Med. 157:1319-1323; 1998.
40. Zheng, Z.; Pan, J.; Chu, B.; Wong, Y. C.; Cheung, A. L.; Tsao, S. W. Downregulation and abnormal expression of E-cadherin and b-catenin in nasopharyngeal carcinoma: Close association with advanced disease stage and lymph node metastasis. Hum. Pathol. 30:458-466; 1999.
41. Narayan, G.; Arias-Pulido, H.; Koul, S.; Vargas, H.; Zhang, F. F.; Villella, J.; Schneider, A.; Terry, M. B.; Mansukhani, M.; Murty, V. V. Frequent promoter methylation of CDH1, DAPK, RARB, and HIC1 genes in carcinoma of cervix uteri: Its relationship to clinical outcome. Mol. Cancer 2:24-35; 2003.
42. Carico, E.; Atlante, M.; Bucci, B.; Nofroni, I.; Vecchione, A. E-cadherin and a-catenin expression during tumor progression of cervical carcinoma. Gynecol. Oncol. 80:156-161; 2001.
43. Graff, J. R.; Gabrielson, E.; Fujii, H. Methylation patterns of the Ecadherin 5′CpG island are unstable and reflect the dynamic, heterogeneous loss of E-cadherin expression during metastatic progression. J. Biol. Chem. 275:2727-2732; 2000.
44. Yang, H. J.; Liu, V. W. S.; Wang, Y.; Chan, K. Y. K.; Tsang, P. C. K.; Khoo, U. S.; Cheung, A. N. Y.; Ngan, H. Y. S. Detection of hypermethylated genes in tumor and plasma of cervical cancer patients. Gynecol. Oncol. 93:435-440; 2004.
45. Shivapurkar, N.; Sherman, M. E.; Stastny, V.; Echebiri, C.; Rader, J. S.; Nayar, R.; Bonfiglio, T. A.; Gazdar, A. F.; Wang, S. S. Evaluation of candidate methylation markers to detect cervical neoplasia. Gynecol. Oncol. 107:549-553; 2007.
46. Kang, S.; Kim, J.; Kim, H.; Shim, J.; Nam, E.; Kim, S.; Ahn, H.; Choi, Y.; Ding, B.; Song, K.; Cho, N. H. Methyl- ation of the p16 INK4a is a non-rare event in cervical intraepithelial neoplasia. Diagn. Mol. Pathol. 15:74-82; 2006.
47. Oki, Y.; Aoki, E.; Issa, J. P. Decitabine-bedside to bench. Crit. Rev. Oncol. Hematol. 67:140-152, 2007.
48. Ayadi, W.; Karray-Hakim, H.; Khabir, A.; Feki, L.; Charfi, S.; Boudawara, T.; Ghorbel, A.; Daoud, J.; Frikha, M.; Busson, P.; Hammami, A. Aberrant methylation of p16, DLEC1, BLU and E-cadherin gene promoters in nasopharyngeal carcinoma biopsies from Tunisian patients. Anticancer Res. 28:2161-2167; 2008.
49. Bornman, D. M.; Mathew, S.; Alsruhe, J.; Herman, J. G.; Gabrielson, E. Methylation of the E-cadherin gene in bladder neoplasia and in normal urothelial epithelium from elderly individuals. Am. J. Pathol. 159:831-835; 2001.
50. Nakajima, T.; Akiyama, Y.; Shiraishi, J.; Arai, T.; Yanagisawa, Y.; Ara, M.; Fukuda, Y.; Sawabe, M.; Saitoh, K.; Kamiyama, R.; Hirokawa, K.; Yuasa, Y. Age-related hypermethylation of the hMLH1 promoter in gastric cancers. Int. J. Cancer 94:208-211; 2001.
51. Waki, T.; Tamura, G.; Tsuchiya, T.; Sato, K.; Nishizuka, S.; Motoyama, T. Promoter methylation status of E-cadherin, hMLH1, and p16 genes in nonneoplastic gastric epithelia. Am. J. Pathol. 161:399-403; 2002.