Dynamic changes in DNA methylation during multistep rat lung carcinogenesis induced by 3-methylcholanthrene and diethylnitrosamine

Toxicology Letters

Volumn 189, Issue 1, 2009, Pages 5-13

  Liu, Wen bin ^a   Liu, Jin yi ^a   Ao, Lin ^a   Zhou, Zi yuan ^a   Zhou, Yan hong ^a   Cui, Zhi hong ^a   Yang, Huan ^a   Cao, Jia ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Carcinogenesis; DNA methylation; Genotoxic carcinogen; Lung cancer; p16 (CDKN2A)

Indexed keywords

3 METHYLCHOLANTHRENE; 5 AZA 2' DEOXYCYTIDINE; 5 METHYLCYTOSINE; DIETHYLNITROSAMINE; DNA FRAGMENT; PROTEIN P15; PROTEIN P16;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; FEMALE; GENOTOXICITY; HISTOPATHOLOGY; LUNG CARCINOGENESIS; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRECANCER; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RAT;

ANIMALS; AZACITIDINE; CELL LINE; COCARCINOGENESIS; CYCLIN-DEPENDENT KINASE INHIBITOR P15; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DIETHYLNITROSAMINE; DNA METHYLATION; FEMALE; IMMUNOHISTOCHEMISTRY; LUNG; LUNG NEOPLASMS; MALE; METHYLCHOLANTHRENE; MICRODISSECTION; RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ANIMALIA; RATTUS; RODENTIA;

EID: 67349121731     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2009.04.022     Document Type: Article

References (48)

1. Bachman A.N., Curtin G.M., Doolittle D.J., and Goodman J.I. Altered methylation in gene-specific and GC-rich regions of DNA is progressive and nonrandom during promotion of skin tumorigenesis. Toxicol. Sci. 91 (2006) 406-418
2. Bagnyukova T.V., Tryndyak V.P., Montgomery B., Churchwell M.I., Karpf A.R., James S.R., Muskhelishvili L., Beland F.A., and Pogribny I.P. Genetic and epigenetic changes in rat preneoplastic liver tissue induced by 2-acetylaminofluorene. Carcinogenesis 29 (2008) 638-646
3. Bai H., Gu L., Zhou J., and Deng D. p16 hypermethylation during gastric carcinogenesis of Wistar rats by N-methyl-N'-nitro-N-nitrosoguanidine. Mutat. Res. 535 (2003) 73-78
4. Belinsky S.A., Nikula K.J., and Palmisano W.A. 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. 95 (1998) 11891-11896
5. Belinsky S.A., Snow S.S., Nikula K.J., Finch G.L., Tellez C.S., and Palmisano W.A. Aberrant CpG island methylation of the p16 (INK4a) and estrogen receptor genes in rat lung tumors induced by particulate carcinogens. Carcinogenesis 23 (2002) 335-339
6. Blanco D., Vicent S., Fraga M.F., Fernandez-Garcia I., Freire J., Lujambio A., Esteller M., Ortiz-de-Solorzano C., Pio R., Lecanda F., and Montuenqa L.M. Molecular analysis of a multistep lung cancer model induced by chronic inflammation reveals epigenetic regulation of p16 and activation of the DNA damage response pathway. Neoplasia 9 (2007) 840-852
7. Chen H.L., Diao L.M., Chen D.G., Li H.G., Chen F.C., and Liu M.Q. Dynamic expression on G1/S phase regulation gene during in rat lung carcinogenesis. Chin. J. Tuberc. Respir. Dis. 25 (2002) 376-377
8. Damiani L.A., Yingling C.M., Leng S., Romo P.E., Nakamura J., and Belinsky S.A. Carcinogen-induced gene promoter hypermethylation is mediated by DNMT1 and causal for transformation of immortalized bronchial epithelial cells. Cancer Res. 68 (2008) 9005-9014
9. Ding L., Getz G., Wheeler D.A., Mardis E.R., McLellan M.D., Cibulskis K., Sougnez C., Greulich H., Muzny D.M., Morgan M.B., Fulton L., Fulton R.S., Zhang Q., Wendl M.C., Lawrence M.S., Larson D.E., Chen K., Dooling D.J., Sabo A., Hawes A.C., Shen H., Jhangiani S.N., Lewis L.R., Hall O., Zhu Y., Mathew T., Ren Y., Yao J., Scherer S.E., Clerc K., Metcalf G.A., Ng B., Milosavljevic A., Gonzalez-Garay M.L., Osborne J.R., Meyer R., Shi X., Tang Y., Koboldt D.C., Lin L., Abbott R., Miner T.L., Pohl C., Fewell G., Haipek C., Schmidt H., Dunford-Shore B.H., Kraja A., Crosby S.D., Sawyer C.S., Vickery T., Sander S., Robinson J., Winckler W., Baldwin J., Chirieac L.R., Dutt A., Fennell T., Hanna M., Johnson B.E., Onofrio R.C., Thomas R.K., Tonon G., Weir B.A., Zhao X., Ziaugra L., Zody M.C., Giordano T., Orringer M.B., Roth J.A., Spitz M.R., Wistuba I.I., Ozenberger B., Good P.J., Chang A.C., Beer D.G., Watson M.A., Ladanyi M., Broderick S., Yoshizawa A., Travis W.D., Pao W., Province M.A., Weinstock G.M., Varmus H.E., Gabriel S.B., Lander E.S., Gibbs R.A., Meyerson M., and Wilson R.K. Somatic mutations affect key pathways in lung adenocarcinoma. Nature 455 (2008) 1069-1075
10. Dixon D., Herbert R.A., Kissling G.E., Brix A.E., Miller R.A., and Maronpot R.R. Summary of chemically induced pulmonary lesions in the National Toxicology Program (NTP) toxicology and carcinogenesis studies. Toxicol. Pathol. 36 (2008) 428-439
11. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet. 8 (2007) 286-298
12. Esteller M., and Almouzni G. How epigenetics integrates nuclear functions Workshop on epigenetics and chromatin: transcriptional regulation and beyond. EMBO Rep. 6 (2005) 624-628
13. Fuke C., Shimabukuro M., Petronis A., Sugimoto J., Oda T., Miura K., Miyazaki T., Ogura C., Okazaki Y., and Jinno Y. Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Ann. Hum. Genet. 68 (2004) 196-204
14. Gaudet F., Hodgson J.G., Eden A., Jackson-Grusby L., Dausman J., Gray J.W., Leonhardt H., and Jaenisch R. Induction of tumors in mice by genomic hypomethylation. Science 300 (2003) 489-492
15. Gonzalgo M.L., Liang G., Spruck C.H., Zingg J.M., Rideout W.M., and Jones P.A. Identification and characterization of differentially methylated regions of genomic DNA by methylation-sensitive arbitrarily primed PCR. Cancer Res. 57 (1997) 594-599
16. Hanahan D., and Weinberg R.A. The hallmarks of cancer. Cell 100 (2000) 57-70
17. Herman J.G., Graff J.R., Myöhänen S., Nelkin B.D., and Baylin S.B. Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 9821-9826
18. Hunter T., and Pines J. Cyclins and cancer II: cyclin D and CDK inhibitors come of age. Cell 79 (1994) 573-582
19. Ji W., Yang L., Yu L., Yuan J., Hu D., Zhang W., Yang J., Pang Y., Li W., Lu J., Fu J., Chen J., Lin Z., Chen W., and Zhuang Z. Epigenetic silencing of O6-methylguanine DNA methyltransferase gene in NiS-transformed cells. Carcinogenesis 29 (2008) 1267-1275
20. Kato A., Shimizu K., Shimoichi Y., Fujii H., Honoki K., and Tsujiuchi T. Aberrant DNA methylation of E-cadherin and p16 genes in rat lung adenocarcinomas induced by N-nitrosobis(2-hydroxypropyl)amine. Mol. Carcinog. 45 (2006) 106-111
21. Kondo K., Takahashi Y., Hirose Y., Nagao T., Tsuyuquchi M., Hashimoto M., Ochiai A., Monden Y., and Tanqoku A. The reduced expression and aberrant methylation of p16 (INK4a) in chromate workers with lung cancer. Lung Cancer 53 (2006) 295-302
22. Lee S.H., Lee S.J., Kim J.H., and Park B.J. Chemical carcinogen, N-methyl-N'-nitro-N-nitrosoguanidine, is a specific activator of oncogenic Ras. Cell Cycle 6 (2007) 1257-1264
23. Lehmann U., and Kreipe H. Real-time PCR analysis of DNA and RNA extracted from formalin-fixed and paraffin-embedded biopsies. Methods 25 (2001) 409-418
24. Li H.G., Liu M.Q., Diao L.M., Yu L.Y., Chen H.L., Chen F.C., and Liu X. Microdissection and PCR-SSCP detected mutation and expression of p53 and K-ras gene in carcinogenesis and development of induced rat lung carcinoma. Chin. J. Pathol. 31 (2002) 331-336
25. Liu W.B., Liu J.Y., and Cao J. Comparison of establishing rat model of lung squamous cell carcinoma by different anesthesia. Chin. J. Compara. Med. 18 (2008) 54-57
26. Lukas J., Aagaard L., Strauss M., and Bartek J. Oncogenic aberrations of p16INK4/CDKN2 and cyclin D1 cooperate to deregulate G1 control. Cancer Res. 55 (1995) 4818-4823
27. Moore L.E., Pfeiffer R.M., Poscablo C., Real F.X., Kogevinas M., Silverman D., García-Closas R., Chanock S., Tardón A., Serra C., Carrato A., Dosemeci M., García-Closas M., Esteller M., Fraga M., Rothman N., and Malats N. Genomic DNA hypomethylation as biomarker for bladder cancer susceptibility in the Spanish Bladder Cancer Study: a case-control study. Lancet Oncol. 9 (2008) 359-366
28. O'Donnell E.P., Zerbe L.K., Dwyer-Nield L.D., Kisley L.R., and Malkinson A.M. Quantitative analysis of early chemically-induced pulmonary lesions in mice of varying susceptibilities to lung tumorigenesis. Cancer Lett. 241 (2006) 197-202
29. Ohnishi T., Fukamachi K., Ohshima Y., Jiegou X., Ueda S., Iigo M., Takasuka N., Naito A., Fujita K., Matsuoka Y., Izumi K., and Tsuda H. Possible application of human c-Ha-ras proto-oncogene transgenic rats in a medium-term bioassay model for carcinogens. Toxicol. Pathol. 35 (2007) 436-443
30. Patel A.C., Anna C.H., Foley J.F., Stockton P.S., Tyson F.L., Barrett J.C., and Devereux T.R. Hypermethylation of the p16 (Ink4a) promoter in B6C3F1 mouse primary lung adenocarcinomas and mouse lung cell lines. Carcinogenesis 21 (2000) 1691-1700
31. Phillips J.M., Yamamoto Y., Negishi M., Maronpot R.R., and Goodman J.I. Orphan nuclear receptor constitutive active/androstane receptor-mediated alterations in DNA methylation during phenobarbital promotion of liver tumorigenesis. Toxicol. Sci. 96 (2007) 72-82
32. Piyathilake C.J., Frost A.R., Bell W.C., Oelschlager D., Weiss H., Johanning G.L., Heimburger D.C., and Grizzle W.E. Altered global methylation of DNA: an epigenetic difference in susceptibility for lung cancer is associated with its progression. Hum. Pathol. 32 (2001) 856-862
33. Piyathilake C.J., Henao O., Frost A.R., Macaluso M., Bell W.C., Johanning G.L., Heimburger D.C., Niveleau A., and Grizzle W.E. Race- and age-dependent alterations in global methylation of DNA in squamous cell carcinoma of the lung (United States). Cancer Causes Control 14 (2003) 37-42
34. Sakai H., Tsukamoto T., Yamamoto M., Kobayashi K., Yuasa H., Imai T., Yanai T., Masegi T., and Tatematsu M. Distinction of carcinogens from mutagens by induction of liver cell foci in a model for detection of initiation activity. Cancer Lett. 188 (2002) 33-38
35. Sherr C.J., and Roberts J.M. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev. 9 (1995) 1149-1163
36. Shimizu K., Itsuzaki Y., Onishi M., Fujii H., Honoki K., and Tsujiuchi T. Reduced expression of the Tslc1 gene and its aberrant DNA methylation in rat lung tumors. Biochem. Biophys. Res. Commun. 347 (2006) 358-362
37. Swafford D.S., Middleton S.K., Palmisano W.A., Nikula K.J., Tesfaiqzi J., Baylin S.B., Herman J.G., and Belinsky S.A. Frequent aberrant methylation of p16INK4a in primary rat lung tumors. Mol. Cell Biol. 17 (1997) 1366-1374
38. Tian H.S., Liu M.Q., Gao W.Q., Zuo R.D., Xiong Y.Y., and Chen Z.F. Induction of lung carcinoma by intralobar bronchial instillation of iodized oil in rats. Chin. Med. J. 97 (1984) 36-40
39. Tryndyak V.P., Kovalchuk O., Muskhelishvili L., Montgomery B., Rodriguez-Juarez R., Melnyk S., Ross S.A., Beland F.A., and Pogribny I.P. Epigenetic reprogramming of liver cells in tamoxifen-induced rat hepatocarcinogenesis. Mol. Carcinog. 46 (2007) 187-197
40. Tsujiuchi T., Masaoka T., Sugata E., Onishi M., Fujii H., Shimizu K., and Honoki K. Hypermethylation of the Dal-1 gene in lung adenocarcinomas induced by N-nitrosobis (2-hydroxypropyl) amine in rats. Mol. Carcinog. 46 (2007) 819-823
41. Umemura T., Kodama Y., Nishikawa A., Hioki K., Nomura T., Kanki K., Kuroiwa Y., Ishii Y., Kurokawa Y., and Hirose M. Nine-week detection of six genotoxic lung carcinogens using the rasH2/BHT mouse model. Cancer Lett. 231 (2006) 314-318
42. Wang J., Chen H.L., Zhu R.Q., Diao L.M., Jiang M., Yang F., and Liu M.Q. Expression of apoptosis and proliferation related genes in carcinogenesis of lung squamous carcinoma in rats. Chin. J. Cancer 22 (2003) 471-476
43. Wang Y.C., Lin R.K., Tan Y.H., Chen J.T., and Chen C.Y. Wild-type p53 overexpression and its correlation with MDM2 and p14ARF alterations: an alternative pathway to non-small-cell lung cancer. J. Clin. Oncol. 23 (2005) 154-164
44. Watson R.E., Curtin G.M., Doolittle D.J., and Goodman J.I. Progressive alterations in global and GC-rich DNA methylation during tumorigenesis. Toxicol. Sci. 75 (2003) 289-299
45. Wild C.P. Environmental exposure measurement in cancer epidemiology. Mutagenesis 24 (2009) 117-125
46. Ye B., Zhang Y.X., Yang F., Chen H.L., Xia D., Liu M.Q., and Lai B.T. Induction of lung lesions in Wistar rats by 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and its inhibition by aspirin and phenethyl isothiocyanate. BMC Cancer 7 (2007) 90
47. Zafirellis K., Agrogiannis G., Zachaki A., Gravani K., Karameris A., and Kombouras C. Prognostic significance of VEGF expression evaluated by quantitative immunohistochemical analysis in colorectal cancer. J. Surg. Res. 147 (2008) 99-107
48. Zhong C.X., and Mass M.J. Both hypomethylation and hypermethylation of DNA associated with arsenite exposure in cultures of human cells identified by methylation-sensitive arbitrarily-primed PCR. Toxicol. Lett. 122 (2001) 223-234