Stable loss of global DNA methylation in the radiation-target tissue - A possible mechanism contributing to radiation carcinogenesis?

Biochemical and Biophysical Research Communications

Volumn 337, Issue 2, 2005, Pages 526-533

  Koturbash, Igor ^a   Pogribny, Igor ^b   Kovalchuk, Olga ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

DNA damage; DNA methylation; Radiation carcinogenesis; Radiation target organs; Thymic lymphoma

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; DNA STRAND BREAKAGE; EPIGENETICS; FEMALE; GENE EXPRESSION; GENOMIC INSTABILITY; GENOTOXICITY; LYMPHOMA; MALE; MOUSE; MUSCLE TISSUE; NONHUMAN; PRIORITY JOURNAL; RADIATION CARCINOGENESIS; THYMUS; THYMUS LYMPHOMA; WHOLE BODY RADIATION;

ANIMALS; CARCINOGENS; DNA DAMAGE; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, RADIATION; GENE EXPRESSION; GENOMIC INSTABILITY; LYMPHOMA; MICE; RADIATION; THYMUS GLAND;

MURINAE; RODENTIA;

EID: 26444565751     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.09.084     Document Type: Article

References (60)

1. J.B. Little Radiation carcinogenesis Carcinogenesis 21 2000 397 404
2. J.B. Little Induction of genetic instability by ionizing radiation C. R. Acad. Sci. Paris 322 1999 127 134
3. H.C. March Leukemia in radiologists in a 20 year period Am. J. Med. Sci. 220 1950 282 286
4. J.H. Folley, W. Borges, and T. Yamawaki Incidence of leukemia in survivors of the atomic bomb in Hiroshima and Nagasaki, Japan Am. J. Med. 13 1952 311 321
5. K.B. Moysich, R.J. Menezes, and A.M. Michalek Chernobyl-related ionising radiation exposure and cancer risk: an epidemiological review Lancet Oncol. 3 2002 269 279
6. T.J. Lightfoot, and E. Roman Causes of childhood leukaemia and lymphoma Toxicol. Appl. Pharmacol. 199 2004 104 117
7. R. Boudreau, Y. St-Pierre, C. Beauchemin, and E.F. Potworowski TL antigen is not linked to radioinduced thymic lymphoma Cell. Immunol. 184 1998 161 167
8. M.M. Kossenko, M.O. Degteva, O.V. Vyushkova, D.L. Preston, K. Mabuchi, and V.P. Kozheurov Issues in the comparison of risk estimates for the population in the Techa River region and atomic bomb survivors Radiat. Res. 148 1997 154 163
9. G. Leone, L. Mele, A. Pulsoni, F. Equitani, and L. Pagano The incidence of secondary leukemias Haematologica 84 1999 937 945
10. M. Plumb Comments on the paper: microsatellite instability in acute myelocytic leukaemia developed from A-bomb survivors-a biological perspective Int. J. Radiat. Biol. 79 2003 367 370
11. American Cancer Society, Cancer facts and figures 2003, American Cancer Society, Atlanta, GA, 2003, pp. 1-52.
12. Y. Wakabayashi, J. Inoue, Y. Takahashi, A. Matsuki, H. Kosugi-Okano, T. Shinbo, Y. Mishima, O. Niwa, and R. Kominami Homozygous deletions and point mutations of the Rit1/Bcl11b gene in gamma-ray induced mouse thymic lymphomas Biochem. Biophys. Res. Commun. 301 2003 598 603
13. M. Utsuyama, and K. Hirokawa Radiation-induced-thymic lymphoma occurs in young, but not in old mice Exp. Mol. Pathol. 74 2003 319 325
14. M. Verlaet, C. Duyckaerts, S. Rahmouni, G. Denis, C. Humblet, R. Greimers, F.E. Sluse, J. Boniver, and M.P. Defresne Transient modifications of respiratory capacity in thymic cells during murine radioleukemogenesis Free Radic. Biol. Med. 33 2002 76 82
15. E. Boulton, H. Cleary, M. Plumb, and B. Myeloid T lymphoid and mixed lineage thymic lymphomas in the irradiated mouse Carcinogenesis 23 2002 1079 1085
16. H.S. Kaplan, and M.B. Brown Mortality of mice after total-body irradiation as influenced by alterations in total dose, fractionation, and periodicity of treatment J. Natl. Cancer Inst. 12 1952 765 775
17. H.S. Kaplan, and M.B. Brown Protection against radiation-induced lymphoma development by shielding and partial-body irradiation of mice Cancer Res. 12 1952 441 444
18. J.T. Babbitt, A.I. Kharazi, J.M. Taylor, C.B. Bonds, S.G. Mirell, E. Frumkin, D. Zhuang, and T.J. Hahn Hematopoietic neoplasia in C57BL/6 mice exposed to split-dose ionizing radiation and circularly polarized 60 Hz magnetic fields Carcinogenesis 21 2000 1379 1389
19. I. Pogribny, J. Raiche, M. Slovack, and O. Kovalchuk Dose-dependence, sex- and tissue-specificity and persistence of radiation-induced genomic DNA methylation changes Biochem. Biophys. Res. Commun. 320 2004 1253 1261
20. J. Raiche, R. Rodriguez-Juarez, I. Pogribny, and O. Kovalchuk Sex and tissue specific expression of maintenance and de novo DNA methyltransferases upon low dose X-irradiation in mice Biochem. Biophys. Res. Commun. 325 2004 39 47
21. I.P. Pogribny, S.J. James, S. Jernigan, and M. Pogribna Genomic hypomethylation is specific for preneoplastic liver in folate/methyl deficient rats and does not occur in non-target tissues Mutat Res. 548 2004 53 59
22. R. Rizwana, and P.J. Hahn CpG methylation reduces genomic instability J. Cell Sci. 112 1999 4513 4519
23. P.A. Jones, and D. Takai The role of DNA methylation in mammalian epigenetics Science 293 2001 1068 1070
24. M. Ehrlich DNA methylation in cancer: too much, but also too little Oncogene 21 2002 5400 5413
25. R. Jaenisch, and A. Bird Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals Nat. Genet. 33 2003 245 254
26. K.D. Robertson DNA methylation and chromatin-unraveling the tangled web Oncogene 21 2002 5361 5379
27. K.D. Robertson, and A.P. Wolffe DNA methylation in health and disease Nat. Rev. Genet. 1 2000 11 19
28. M.F. Fraga, E. Ballestar, A. Villar-Garea, M. Boix-Chornet, J. Espada, G. Schotta, T. Bonaldi, C. Haydon, S. Ropero, K. Petrie, N.G. Iyer, A. Perez-Rosado, E. Calvo, J.A. Lopez, A. Cano, M.J. Calasanz, D. Colomer, M.A. Piris, N. Ahn, A. Imhof, C. Caldas, T. Jenuwein, and M. Esteller Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer Nat. Genet. 37 2005 391 400
29. A.P. Feinberg, and B. Vogelstein Hypomethylation distinguishes genes of some human cancers from their normal counterparts Nature 301 1983 89 92
30. E. Flatau, E. Bogenmann, and P.A. Jones Variable 5-methylcytosine levels in human tumor cell lines and fresh pediatric tumor explants Cancer Res. 43 1983 4901 4905
31. M.A. Gama-Sosa, V.A. Slagel, R.W. Trewyn, R. Oxenhandler, K.C. Kuo, C.W. Gehrke, and M. Ehrlich The 5-methylcytosine content of DNA from human tumors Nucleic Acids Res. 11 1983 6883 6894
32. A.P. Feinberg The epigenetic of cancer etiology Semin. Cancer Biol. 14 2004 427 432
33. F. Gaudet, J.G. Hodgson, A. Eden, L. Jackson-Grusby, J. Dausman, J.W. Gray, H. Leonhardt, and R. Jaenisch Induction of tumors in mice by genomic hypomethylation Science 300 2003 489 492
34. G. Egger, G. Liang, A. Aparicio, and P.A. Jones Epigenetics in human disease and prospects for epigenetic therapy Nature 429 2004 457 463
35. P.A. Jones, and S.B. Baylin The fundamental role of epigenetic events in cancer Nat. Rev. Genet. 3 2002 415 428
36. M.F. Fraga, M. Herranz, J. Espada, E. Ballestar, M.F. Paz, S. Ropero, E. Erkek, O. Bozdogan, H. Peinado, A. Niveleau, J.H. Mao, A. Balmain, A. Cano, and M.A. Esteller Mouse skin multistage carcinogenesis model reflects the aberrant DNA methylation patterns of human tumors Cancer Res. 64 2004 5527 5534
37. I.P. Pogribny, S.A. Ross, C.A. Wise, M. Pogribna, E.A. Jones, V.P. Tryndyak, S.J. James, Y.P. Dragan, L.A. Poirier, Irreversible global DNA hypomethylation as a key step in hepatocarcinogenesis induced by dietary methyl deficiency. Mutat. Res. (2005) in press.
38. T.V. Karpinets, and B.D. Foy Tumorigenesis: the adaptation of mammalian cells to sustained stress environment by epigenetic alterations and succeeding matched mutations Carcinogenesis 26 2005 1323 1334
39. T. Minamoto, M. Mai, and Z. Ronai Environmental factors as regulators and effectors of multistep carcinogenesis Carcinogenesis 20 1999 519 527
40. J.F. Kalinich, G.N. Catravas, and S.L. Snyder The effect of γ irradiation on DNA methylation Radiat. Res. 117 1989 185 197
41. R. Tawa, Y. Kimura, J. Komura, Y. Miyamura, A. Kurishita, M.S. Sasaki, H. Sakurai, and T. Ono Effects of X-ray irradiation on genomic DNA methylation levels in mouse tissues J. Radiat. Res. 39 1998 271 278
42. O. Kovalchuk, C.A. Hendricks, S. Cassie, A.J. Engelward, and B.P. Engelward In vivo recombination after chronic damage exposure falls to below spontaneous levels in recombomice Mol. Cancer Res. 2 2004 567 573
43. E.D. Olfert, B.M. Cross, A.A. McWilliam, Guide to the care and use of experimental animals, Canadian Council on Animal Care, 1993.
44. I.P. Pogribny, P. Yi, and S.J. James A sensitive new method for rapid detection of abnormal methylation patterns in global DNA and within CpG islands Biochem. Biophys. Res. Commun. 262 1999 624 628
45. A.G. Basnakian, and S.J. James Quantification of 3′-OH DNA breaks by random oligonucleotide-primed synthesis (ROPS) assay DNA Cell Biol. 15 1996 255 262
46. O.A. Sedelnikova, I. Horikawa, D.B. Zimonjic, N.C. Popescu, W.M. Bonner, and J.C. Barrett Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks Nat. Cell Biol. 6 2004 168 170
47. R. Sokal, and F.J. Rohlf Biometry 1995 Freeman New York pp. 734-736
48. M.I. Panayiotidis, R.C. Rancourt, C.B. Allen, S.R. Riddle, B.K. Schneider, S. Ahmad, and C.W. White Hyperoxia-induced DNA damage causes decreased DNA methylation in human lung epithelial-like A549 cells Antioxid. Redox Signal. 6 2004 129 136
49. P.W. Turk, A. Laayoun, S.S. Smith, and S.A. Weitzman DNA adduct 8-hydroxyl-2′-deoxyguanosine (8-hydroxyguanine) affects function of human DNA methyltransferase Carcinogenesis 16 1995 1253 1255
50. A. Celeste, S. Difilippantonio, M.J. Difilippantonio, O. Fernandez-Capetillo, D.R. Pilch, O.A. Sedelnikova, M. Eckhaus, T. Ried, W.M. Bonner, and A. Nussenzweig H2AX haploinsufficiency modifies genomic stability and tumor susceptibility Cell 114 2003 371 383
51. T.T. Paull, E.P. Rogakou, V. Yamazaki, C.U. Kirchgessner, M. Gellert, and W.M. Bonner A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage Curr. Biol. 10 2000 886 895
52. National Center for Environmental Assessment-Washington Office, U.S. Environmental Protection Agency, Chemical and radiation leukemogenesis in humans and rodents and the value of rodent models for assessing risks of lymphohematopoietic cancers, EPA/600/R-97/090, May 1997.
53. B. Melendez, J. Santos, and J. Fernandez-Piqueras Loss of heterozygosity at the proximal-mid part of mouse chromosome 4 defines two novel tumour suppressor gene loci in T-cell lymphomas Oncogene 18 1999 4166 4169
54. H. Okano, Y. Saito, T. Miyazawa, T. Shinbo, D. Chou, S. Kosugi, Y. Takahashi, S. Odani, O. Niwa, and R. Kominami Homozygous deletions and point mutations of the Ikaros gene in -ray-induced mouse thymic lymphomas Oncogene 18 1999 6677 6683
55. H. Tsuji, H. Ishii-Ohba, H. Ukai, T. Katsube, and T. Ogiu Radiation-induced deletions in the 5′ end region of Notch1 lead to the formation of truncated proteins and are involved in the development of mouse thymic lymphomas Carcinogenesis 24 2003 1257 1268
56. H. Tsuji, H. Ishii-Ohba, T. Katsube, H. Ukai, S. Aizawa, M. Doi, K. Hioki, and T. Ogiu Involvement of illegitimate V(D) J recombination or microhomology-mediated nonhomologous end-joining in the formation of intragenic deletions of the Notch1 gene in mouse thymic lymphomas Cancer Res. 64 2004 8882 8890
57. J. Sakata, J. Inoue, H. Ohi, H. Kosugi-Okano, Y. Mishima, K. Hatakeyama, O. Niwa, and R. Kominami Involvement of V(D)J recombinase in the generation of intragenic deletions in the Rit1/Bcl11b tumor suppressor gene in gamma-ray-induced thymic lymphomas and in normal thymus of the mouse Carcinogenesis 25 2004 1069 1075
58. K. Yoshida, K. Nemoto, M. Nishimura, and M. Seki Exacerbating factors of radiation-induced myeloid leukemogenesis Leuk. Res. 17 1993 437 440
59. A.V. Guizard, O. Boutou, D. Pottier, X. Troussard, D. Pheby, G. Launoy, R. Slama, and A. Spira The incidence of childhood leukemia around the La Hague nuclear waste reprocessing plant (France): a survey for the years 1978-1998 J. Epidemiol. Community Health 55 2001 469 474
60. A.G. Noshchenko, K.B. Moysich, A. Bondar, P.V. Zamostyan, V.D. Drosdova, and A.M. Michalek Patterns of acute leukemia occurrence among children in the Chernobyl region Int. J. Epidemiol. 30 2001 125 129