Distinct susceptibility of induction of methylation of p16ink4a and p19arf CpG islands by X-radiation and chemical carcinogen in mice

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 768, Issue , 2014, Pages 42-50

  Yang, Chen ^a,b   Gu, Liankun ^a   Deng, Dajun ^a  

^a PEKING UNIVERSITY CANCER HOSPITAL AND INSTITUTE   (China)

^b Department of Medicine of King Medical Diagnostics Center ^*  (China)

Author keywords

DNA methylation; H. felis; Ink4a Arf; N nitrosomethylurea; Susceptibility; X radiation

Indexed keywords

BISULFITE; CARCINOGEN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; GENOMIC DNA; METHYLNITROSOUREA; P19ARF PROTEIN; PROTEIN P16; PROTEIN P19; UNCLASSIFIED DRUG; ALKYLATING AGENT; CDKN2A PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; CPG ISLAND; DENATURING HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; DNA EXTRACTION; GASTROINTESTINAL TRACT; HELICOBACTER FELIS; HELICOBACTER INFECTION; IMMUNOHISTOCHEMISTRY; INTESTINE; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METHYLATION; SMALL INTESTINE TUMOR; X IRRADIATION; X RAY; ANIMAL; ANTIBODY SPECIFICITY; BIOSYNTHESIS; DNA METHYLATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PROMOTER REGION; RADIATION RESPONSE;

HELICOBACTER FELIS; MUS;

ALKYLATING AGENTS; ANIMALS; CARCINOGENS; CPG ISLANDS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DNA METHYLATION; GENE EXPRESSION REGULATION; HELICOBACTER FELIS; HELICOBACTER INFECTIONS; METHYLNITROSOUREA; MICE; ORGAN SPECIFICITY; PROMOTER REGIONS, GENETIC; X-RAYS;

EID: 84901634779     PISSN: 13835718     EISSN: 18793592     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2014.04.012     Document Type: Article

References (37)

1. Beroukhim R., Mermel C.H., Porter D., Wei G., Raychaudhuri S., Donovan J., Barretina J., Boehm J.S., Dobson J., Urashima M., Mc Henry K.T., Pinchback R.M., Ligon A.H., Cho Y.J., Haery L., Greulich H., Reich M., Winckler W., Lawrence M.S., Weir B.A., Tanaka K.E., Chiang D.Y., Bass A.J., Loo A., Hoffman C., Prensner J., Liefeld T., Gao Q., Yecies D., Signoretti S., Maher E., Kaye F.J., Sasaki H., Tepper J.E., Fletcher J.A., Tabernero J., Baselga J., Tsao M.S., Demichelis F., Rubin M.A., Janne P.A., Daly M.J., Nucera C., Levine R.L., Ebert B.L., Gabriel S., Rustgi A.K., Antonescu C.R., Ladanyi M., Letai A., Garraway L.A., Loda M., Beer D.G., True L.D., Okamoto A., Pomeroy S.L., Singer S., Golub T.R., Lander E.S., Getz G., Sellers W.R., Meyerson M. The landscape of somatic copy-number alteration across human cancers. Nature 2010, 463:899-905.
2. Sherr C.J., Roberts J.M. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 1999, 13:1501-1512.
3. arf, interacts with MDM2 and neutralizes MDM2's inhibition of p53. Cell 1998, 92:713-723.
4. ink4a and p14ARF in melanoma. J. Natl. Cancer Inst. 2008, 100:757-759.
5. arf. Cell 1997, 91:649-659.
6. ink4a confers susceptibility to metastatic melanoma in mice. Nature 2001, 413:83-86.
7. arf predisposes mice to tumorigenesis. Nature 2001, 413:86-91.
8. Merlo A., Herman J.G., Mao L., Lee D.J., Gabrielson E., Burger P.C., Baylin S.B., Sidransky D. 5' CpG island methylation is associated with transcriptional silencing of the tumour suppressor p16/CDKN2/MTS1 in human cancers. Nat. Med. 1995, 1:686-692.
9. Herman J.G., Merlo A., Mao L., Lapidus R.G., Issa J.P., Davidson N.E., Sidransky D., Baylin S.B. Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. Cancer Res. 1995, 55:4525-4530.
10. Gonzalez-Zulueta M., Bender C.M., Yang A.S., Nguyen T., Beart R.W., Van Tornout J.M., Jones P.A. Methylation of the 5' CpG island of the p16/CDKN2 tumor suppressor gene in normal and transformed human tissues correlates with gene silencing. Cancer Res. 1995, 55:4531-4535.
11. Belinsky S.A., Nikula K.J., Palmisano W.A., Michels R., Saccomanno G., Gabrielson E., Baylin S.B., Herman J.G. Aberrant methylation of p16(INK4a) is an early event in lung cancer and a potential biomarker for early diagnosis. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:11891-11896.
12. Sun Y., Deng D., You W.C., Bai H., Zhang L., Zhou J., Shen L., Ma J.L., Xie Y.Q., Li J.Y. Methylation of p16 CpG islands associated with malignant transformation of gastric dysplasia in a population-based study. Clin. Cancer Res. 2004, 10:5087-5093.
13. Cao J., Zhou J., Gao Y., Gu L., Meng H., Liu H., Deng D. Methylation of p16 CpG island associated with malignant progression of oral epithelial dysplasia: a prospective cohort study. Clin. Cancer Res. 2009, 15:5178-5183.
14. ink4a genes in colon cancer. Lab. Invest. 2001, 81:217-229.
15. Lee S., Hwang K.S., Lee H.J., Kim J.S., Kang G.H. Aberrant CpG island hypermethylation of multiple genes in colorectal neoplasia. Lab. Invest. 2004, 84:884-893.
16. Bai H., Gu L., Zhou J., Deng D. p16 hypermethylation during gastric carcinogenesis of Wistar rats by N-methyl-N'-nitro-N-nitrosoguanidine. Mutat. Res. 2003, 535:73-78.
17. Melendez B., Malumbres M., Perez de Castro I., Santos J., Pellicer A., Fernandez-Piqueras J. Characterization of the murine p19(ARF) promoter CpG island and its methylation pattern in primary lymphomas. Carcinogenesis 2000, 21:817-821.
18. Ilnytskyy Y., Kovalchuk O. Non-targeted radiation effects - an epigenetic connection. Mutat. Res. 2011, 714:113-125.
19. Yang C., Gu L., Deng D. Bone marrow-derived cells may not be the original cells for carcinogen-induced mouse gastrointestinal carcinomas. PLoS ONE 2013, 8:e79615.
20. Houghton J., Stoicov C., Nomura S., Rogers A.B., Carlson J., Li H., Cai X., Fox J.G., Goldenring J.R., Wang T.C. Gastric cancer originating from bone marrow-derived cells. Science 2004, 306:1568-1571.
21. Eads C.A., Laird P.W. Combined bisulfite restriction analysis (COBRA). Methods Mol. Biol. 2002, 200:71-85.
22. Deng D., Deng G., Smith M.F., Zhou J., Xin H., Powell S.M., Lu Y. Simultaneous detection of CpG methylation and single nucleotide polymorphism by denaturing high performance liquid chromatography. Nucleic Acids Res. 2002, 30:E13.
23. Tu S., Bhagat G., Cui G., Takaishi S., Kurt-Jones E.A., Rickman B., Betz K.S., Penz-Oesterreicher M., Bjorkdahl O., Fox J.G., Wang T.C. Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice. Cancer Cell 2008, 14:408-419.
24. Kovalchuk O., Burke P., Besplug J., Slovack M., Filkowski J., Pogribny I. Methylation changes in muscle and liver tissues of male and female mice exposed to acute and chronic low-dose X-ray-irradiation. Mutat. Res. 2004, 548:75-84.
25. Antwih D.A., Gabbara K.M., Lancaster W.D., Ruden D.M., Zielske S.P. Radiation-induced epigenetic DNA methylation modification of radiation-response pathways. Epigenetics 2013, 8:839-848.
26. Krakowczyk L., Blamek S., Strzelczyk J.K., Plachetka A., Maciejewski A., Poltorak S., Wiczkowski A. Effects of X-ray irradiation on methylation levels of p16, MGMT and APC genes in sporadic colorectal carcinoma and corresponding normal colonic mucosa. Med. Sci. Monit. 2010, 16:CR469-CR474.
27. IARC WHO N-nitroso-n-methylurea. IARC Monogr. Eval. Carcinog. Risks Hum. 1978, 17:227-255.
28. Deng D., Xin H. Formation of N-(nitrosomethyl)urea in stomachs of experimental pigs and human volunteers given fish sauce in vivo. J. Agric. Food Chem. 2000, 48:2495-2498.
29. Deng D. Progress of gastric cancer etiology: N-nitrosamides in the 1990s. World J. Gastroenterol. 2000, 6:318-613.
30. Nam K.T., Hahm K.B., Oh S.Y., Yeo M., Han S.U., Ahn B., Kang Y.B., Jang D.D., Yang K.H., Kim D.Y. The selective cyclooxygenase-2 inhibitor nimesulide prevents Helicobacter pylori-associated gastric cancer development in a mouse model. Clin. Cancer Res. 2004, 10:8105-8113.
31. Ionizing radiation, part 1: X- and gamma-radiation, and neutrons. Overall introduction. IARC Monogr. Eval. Carcinog. Risks Hum. 2000, 75(Pt 1):35-115.
32. Avital I., Moreira A.L., Klimstra D.S., Leversha M., Papadopoulos E.B., Brennan M., Downey R.J. Donor-derived human bone marrow cells contribute to solid organ cancers developing after bone marrow transplantation. Stem Cells 2007, 25:2903-2909.
33. Esteller M., Corn P.G., Baylin S.B., Herman J.G. A gene hypermethylation profile of human cancer. Cancer Res. 2001, 61:3225-3229.
34. Lu Z.M., Zhou J., Wang X., Guan Z., Bai H., Liu Z.J., Su N., Pan K., Ji J., Deng D. Nucleosomes correlate with in vivo progression pattern of de novo methylation of p16 CpG islands in human gastric carcinogenesis. PLoS ONE 2012, 7:e35928.
35. Dong C.X., Deng D.J., Pan K.F., Zhang L., Zhang Y., Zhou J., You W.C. Promoter methylation of p16 associated with Helicobacter pylori infection in precancerous gastric lesions: a population-based study. Int. J. Cancer 2009, 124:434-439.
36. Maekita T., Nakazawa K., Mihara M., Nakajima T., Yanaoka K., Iguchi M., Arii K., Kaneda A., Tsukamoto T., Tatematsu M., Tamura G., Saito D., Sugimura T., Ichinose M., Ushijima T. High levels of aberrant DNA methylation in Helicobacter pylori-infected gastric mucosae and its possible association with gastric cancer risk. Clin. Cancer Res. 2006, 12:989-995.
37. Niwa T., Tsukamoto T., Toyoda T., Mori A., Tanaka H., Maekita T., Ichinose M., Tatematsu M., Ushijima T. Inflammatory processes triggered by Helicobacter pylori infection cause aberrant DNA methylation in gastric epithelial cells. Cancer Res. 2010, 70:1430-1440.