Inhalation of cigarette smoke induces regions of altered DNA methylation (RAMs) in SENCAR mouse lung

Toxicology

Volumn 260, Issue 1-3, 2009, Pages 7-15

  Phillips, Jennifer M ^a   Goodman, Jay I ^b  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Biomarker; Cigarette smoke; DNA methylation; Lung; SENCAR mouse

Indexed keywords

BIOLOGICAL MARKER; CIGARETTE SMOKE; DIMETHYLBENZ[A]ANTHRACENE;

AIR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY ELECTROPHORESIS; CELL POPULATION; CHEMICAL CARCINOGENESIS; CIGARETTE SMOKING; CONTROLLED STUDY; DIGESTION; DNA METHYLATION; ENVIRONMENTAL EXPOSURE; EPIGENETICS; FEMALE; HISTOPATHOLOGY; LUNG CARCINOGENESIS; MOUSE; NONHUMAN; PARTICULATE MATTER; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RISK ASSESSMENT; SENSITIVE TO CARCINOGENESIS MOUSE;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; CARCINOGENS; DNA; DNA METHYLATION; DNA RESTRICTION ENZYMES; ELECTROPHORESIS, CAPILLARY; FEMALE; HISTOCYTOCHEMISTRY; LUNG NEOPLASMS; MICE; MICE, INBRED SENCAR; POLYMERASE CHAIN REACTION; RISK ASSESSMENT; SMOKING;

MUS;

EID: 67349118349     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2009.03.001     Document Type: Article

References (41)

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. Bachman A.N., Kamendulis L.M., and Goodman J.I. Diethanolamine and phenobarbital produce an altered pattern of methylation in GC-rich regions of DNA in B6C3F1 mouse hepatocytes similar to that resulting from choline deficiency. Toxicol. Sci. 90 (2006) 317-320
3. Bachman A.N., Phillips J.M., and Goodman J.I. Phenobarbital induces progressive patterns of GC-rich and gene-specific altered DNA methylation in the liver of tumor-prone B6C3F1 mice. Toxicol. Sci. 91 (2006) 393-405
4. Balansky R., Ganchev G., Iltcheva M., Steele V.E., D'Agostini F., and De Flora S. Potent carcinogenicity of cigarette smoke in mice exposed early in life. Carcinogenesis 28 (2007) 2236-2243
5. Belinsky S.A., Liechty K.C., Gentry F.D., Wolf H.J., Rogers J., Vu K., Haney J., Kennedy T.C., Hirsch F.R., Miller Y., Franklin W.A., Herman J.G., Baylin S.B., Bunn P.A., and Byers T. Promoter hypermethylation of multiple genes in sputum precedes lung cancer incidence in a high-risk cohort. Cancer Res. 66 (2006) 3338-3344
6. 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
7. Bhutani M., Pathak A.K., Fan Y.-H., Liu D.D., Lee J.J., Tang H., Kurie J.M., Morice R.C., Kim E.S., Hong W.K., and Mao L. Oral epithelium as a surrogate tissue for assessing smoking-induced molecular alterations in the lungs. Cancer Prev. Res. 1 (2008) 39-44
8. Bracke K.R., D'hulst A.I., Maes T., Moerloose K.B., Demedts I.K., Lebecque S., Joos G.F., and Brusselle G.G. Cigarette smoke-induced pulmonary inflammation and emphysema are attenuated in CCR6-deficient mice. J. Immunol. 177 (2006) 4350-4359
9. Brock M.V., Hooker C.M., Ota-Machida E., Han Y., Guo M., Ames S., Glöckner S., Piantadosi S., Gabrielson E., Pridham G., Pelosky K., Belinsky S.A., Yang S.C., Baylin S.B., and Herman J.G. DNA methylation markers and early recurrence in stage I lung cancer. N. Engl. J. Med. 358 (2008) 1118-1128
10. Churg A., Dai J., Tai H., Xie C., and Wright J.L. Tumor necrosis factor-α is central to acute cigarette smoke-induced inflammation and connective tissue breakdown. Am. J. Respir. Crit. Care Med. 166 (2002) 849-854
11. Cosio M.G., and Guerassimov A. Chronic obstructive pulmonary disease. Inflammation of small airways and lung parenchyma. Am. J. Respir. Crit. Care Med. 160 5 Pt 2 (1999) S21-S25
12. Coussens L.M., and Werb Z. Inflammation and cancer. Nature 420 (2002) 860-867
13. Curtin G.M., Higuchi M.A., Ayres P.H., Swauger J.E., and Mosberg A.T. Lung tumorigenicity in A/J and rasH2 transgenic mice following mainstream tobacco smoke inhalation. Toxicol. Sci. 81 (2004) 26-34
14. De Flora S., Balansky R.M., D'Agostini F., Izzotti A., Camoirano A., Bennicelli C., Zhang Z., Wang Y., Lubet R.A., and You M. Molecular alterations and lung tumors in p53 mutant mice exposed to cigarette smoke. Cancer Res. 63 (2003) 793-800
15. de Visser K.E., Korets L.V., and Coussens L.M. De novo carcinogenesis promoted by chronic inflammation is B lymphocyte development. Cancer Cell 7 (2005) 411-423
16. DeMarini D.M. Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat. Res. 567 (2004) 447-474
17. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet. 8 (2007) 286-298
18. Feinberg A.P., Gehrke C.W., Kuo K.C., and Ehrlich M. Reduced genomic 5-methylcytosine content in human colonic neoplasia. Cancer Res. 48 (1988) 1159-1161
19. Feinberg A.P., and Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 301 (1983) 89-92
20. Gonzalgo M.L., Liang G., Spruck III C.H., Zingg J.M., Rideout III 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
21. Goodman J.I., and Watson R.E. Altered DNA methylation: a secondary mechanism involved in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 42 (2002) 501-525
22. Hecht S.S. Tobacco smoke carcinogens and lung cancer. J. Natl. Cancer Inst. 91 (1999) 1194-1210
23. Hussain S.P., and Harris C.C. Inflammation and cancer: an ancient link with novel potentials. Int. J. Cancer 121 (2007) 2373-2380
24. Hutt J.A., Vuillemenot B.R., Barr E.B., Grimes M.J., Hahn F.F., Hobbs C.H., March T.H., Gigliotti A.P., Seilkop S.K., Finch G.L., Mauderly J.L., and Belinsky S.A. Life-span inhalation exposure to mainstream cigarette smoke induces lung cancer in B6C3F1 mice through genetic and epigenetic pathways. Carcinogenesis 26 (2005) 1999-2009
25. Issa J.-P.J., Ahuja N., Toyota M., Bronner M.P., and Brentnall T.A. Accelerated age-related CpG island methylation in ulcerative colitis. Cancer Res. 61 (2001) 3573-3577
26. INK4a and histology-specific methylation of CpG islands by exposure to tobacco smoke in non-small cell lung cancer. Cancer Res. 61 (2001) 3419-3424
27. Liu H., Zhou Y., Boggs S.E., Belinsky S.A., and Liu J. Cigarette smoke induces demethylation of prometastatic oncogene synuclein-γ in lung cancer cells by downregulation of DNMT3B. Oncogene 26 (2007) 5900-5910
28. 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., and 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. 12 (2006) 989-995
29. Pulling L.C., Vuillemenot B.R., Hutt J.A., Devereux T.R., and Belinsky S.A. Aberrant promoter hypermethylation of the death-associated protein kinase gene is early and frequent in murine lung tumors induced by cigarette smoke and tobacco carcinogens. Cancer Res. 64 (2004) 3844-3848
30. Rauch T.A., Zhong X., Wu X., Wang M., Kernstine K.H., Wang Z., Riggs A.D., and Pfeifer G.P. High-resolution mapping of DNA hypermethylation and hypomethylation in lung cancer. Proc. Natl. Acad. Sci. U.S.A. 105 (2008) 252-257
31. Russo A.L., Thiagalingam A., Pan H., Califano J., Cheng K.H., Ponte J.F., Chinnappan D., Nemani P., Sidransky D., and Thiagalingam S. Differential DNA hypermethylation of critical genes mediates the stage-specific tobacco smoke-induced neoplastic progression of lung cancer. Clin. Cancer Res. 11 (2005) 2466-2470
32. Schulmann K., Sterian A., Berki A., Yin J., Sato F., Xu Y., Olaru A., Wang S., Mori Y., Deacu E., Hamilton J., Kan T., Krasna M.J., Beer D.G., Pepe M.S., Abraham J.M., Feng Z., Schmiegel W., Greenwald B.D., and Meltzer S.J. Inactivation of p16, RUNX3, and HPP1 occurs early in Barrett's-associated neoplastic progression and predicts progression risk. Oncogene 24 (2005) 4138-4148
33. Shiraishi M., Lerman L.S., and Sekiya T. Preferential isolation of DNA fragments associated with CpG islands. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 4229-4233
34. Toyooka S., Suzuki M., Tsuda T., Toyooka K.O., Maruyama R., Tsukuda K., Fukuyama Y., Iizasa T., Fujisawa T., Shimizu N., Minna J.D., and Gazdar A.F. Dose effect of smoking on aberrant methylation in non-small cell lung cancers. Int. J. Cancer 110 (2004) 462-464
35. Tsou J.A., Hagen J.A., Carpenter C.L., and Laird-Offringa I.A. DNA methylation analysis: a powerful new tool for lung cancer diagnosis. Oncogene 21 (2002) 5450-5461
36. Vuillemenot B.R., Pulling L.C., Palmisano W.A., Hutt J.A., and Belinsky S.A. Carcinogen exposure differentially modulates RAR-β promoter hypermethylation, an early and frequent event in mouse lung carcinogenesis. Carcinogenesis 25 (2004) 623-629
37. Ward J.M., Rehm S., Devor D., Hennings H., and Wenk M.L. Differential carcinogenic effects of intraperitoneal initiation with 7,12-dimethylbenz(a)anthracene or urethane and topical promotion with 12-O-tetradecanoylphorbol-13-acetate in skin and internal tissues of female SENCAR and BALB/c mice. Environ. Health Perspect. 68 (1986) 61-68
38. 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
39. Watson R.E., and Goodman J.I. Epigenetics and DNA methylation come of age in toxicology. Toxicol. Sci. 67 (2002) 11-16
40. Weisburger J.H., and Williams G.M. Carcinogen testing: current problems and new approaches. Science 214 (1981) 401-407
41. Witschi H., Espiritu I., Peake J.L., Wu K., Maronpot R.R., and Pinkerton K.E. The carcinogenicity of environmental tobacco smoke. Carcinogenesis 18 (1997) 575-586