674
Views
69
CrossRef citations to date
0
Altmetric
Radiation-Induced Genomic Instability and Epigentics

Radiation-induced genomic instability: Are epigenetic mechanisms the missing link?

, &
Pages 179-191 | Received 01 Jul 2010, Accepted 07 Sep 2010, Published online: 02 Nov 2010

References

  • Ayoub N, Jeyasekharan AD, Bernal JA, Venkitaraman AR. 2008. HP1-beta mobilization promotes chromatin changes that initiate the DNA damage response. Nature 453:682–686.
  • Barres R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, Krook A, Zierath JR. 2009. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metabolism 10:189–198.
  • Bestor TH. 2005. Transposons reanimated in mice. Cell 122:322–325.
  • Bestor TH. 2009. The DNA methyltransferases of mammals. Human Molecular Genetics 9:2395–2402.
  • Brock MV, Herman JG, Baylin SB. 2007. Cancer as a manifestation of aberrant chromatin structure. Cancer Journal 13:3–8.
  • Cai X, Hagedorn CH, Cullen BR. 2004. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10:1957–1966.
  • Cerda S, Weitzman SA. 1997. Influence of oxygen radical injury on DNA methylation. Mutation Research 386:141–152.
  • Cha HJ, Seong KM, Bae S, Jung JH, Kim CS, Yang KH, Jin YW, An S. 2009a. Identification of specific microRNAs responding to low and high dose gamma-irradiation in the human lymphoblast line IM9. Oncology Reports 22:863–868.
  • Cha HJ, Shin S, Yoo H, Lee EM, Bae S, Yang KH, Lee SJ, Park IC, Jin YW, An S. 2009b. Identification of ionizing radiation-responsive microRNAs in the IM9 human B lymphoblastic cell line. International Journal of Oncology 34:1661–1668.
  • Clutton SM, Townsend KM, Walker C, Ansell JD, Wright EG. 1996. Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis 17:1633–1639.
  • Cowland JB, Hother C, Grønbæk K. 2007. MicroRNAs and cancer. Acta Pathologica, Microbiologica et Immunologica Scandinavica 115:1090–1106.
  • Davidson-Moncada J, Papavasiliou FN, Tam W. 2010. MicroRNAs of the immune system: Roles in inflammation and cancer. Annals of the New York Academy of Sciences 1183:183–194.
  • Dayal D, Martin SM, Limoli CL, Spitz DR. 2008. Hydrogen peroxide mediates the radiation-induced mutator phenotype in mammalian cells. Biochemical Journal 413:185–191.
  • Dayal D, Martin SM, Owens KM, Aykin-Burns N, Zhu Y, Boominathan A, Pain D, Limoli CL, Goswami PC, Domann FE, Spitz DR. 2009. Mitochondrial complex II dysfunction can contribute significantly to genomic instability after exposure to ionizing radiation. Radiation Research 172:737–745.
  • Falk M, Lukasova E, Gabrielova B, Ondrej V, Kozubek S. 2007. Chromatin dynamics during DSB repair. Biochimica et Biophysica Acta 1773:1534–1545.
  • Falk M, Lukasova E, Kozubek S. 2008. Chromatin structure influences the sensitivity of DNA to γ-radiation. Biochimica et Biophysica Acta 1783:2398–2414.
  • Feinberg AP, Cui H, Ohlsson R. 2002. DNA methylation and genomic imprinting: Insights from cancer into epigenetic mechanisms. Seminars in Cancer Biology 12:389–398.
  • Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A. 2004. H2AX: The histone guardian of the genome. DNA Repair 3:959–967.
  • Fillingham J, Keogh MC, Krogan NJ. 2006. GammaH2AX and its role in DNA double-strand break repair. Biochemistry and Cell Biology 84:568–577.
  • Franco R, Schoneveld O, Georgakilas AG, Panayiotidis MI. 2008. Oxidative stress, DNA methylation and carcinogenesis. Cancer Letters 266:6–11.
  • Goll MG, Kirpekar F, Maggert KA, Yoder JA, Hsieh CL, Zhang X, Golic KG, Jacobsen SE, Bestor TH. 2006. Methylation of tRNAAsp by the DNA methyltransferase homolog Dnmt2. Science 311:395–398.
  • Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Lobrich M, Jeggo PA. 2008. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Molecular Cell 31:167–177.
  • Grafstrom RH, Yuan R, Hamilton DL. 1985. The characteristics of DNA methylation in an in vitro DNA synthesizing system from mouse fibroblasts. Nucleic Acids Research 13:2827–2842.
  • Grønbæk K, Hother C, Jones PA. 2007. Epigenetic changes in cancer. Acta Pathologica, Microbiologica et Immunologica Scandinavica 115:1039–1059.
  • Guil S, Esteller M. 2009. DNA methylomes, histone codes and miRNAs: Tying it all together. International Journal of Biochemistry & Cell Biology 41:87–95.
  • Herman JG, Baylin SB. 2003. Gene silencing in cancer in association with promoter hypermethylation. New England Journal of Medicine 349:2042–2054.
  • Holmberg K, Falt S, Johansson A, Lambert B. 1993. Clonal chromosome aberrations and genomic instability in X-irradiated human T-lymphocyte cultures. Mutation Research 286:321–330.
  • Holmberg K, Meijer AE, Auer G, Lambert BO. 1995. Delayed chromosomal instability in human T-lymphocyte clones exposed to ionizing radiation. International Journal of Radiation Biology 68:245–255.
  • Hu H, Du L, Nagabayashi G, Seeger RC, Gatti RA. 2010. ATM is down-regulated by N-Myc-regulated microRNA-421. Proceedings of the National Academy of Sciences of the USA 107:1506–15011.
  • Ilnytskyy Y, Koturbash I, Kovalchuk O. 2009. Radiation-induced bystander effects in vivo are epigenetically regulation in a tissue-specific manner. Environmental and Molecular Mutagenesis 50:105–113.
  • Ishii H, Saito T. 2006. Radiation-induced response of micro RNA expression in murine embryonic stem cells. Journal of Medicinal Chemistry 2:555–563.
  • Jaklevic B, Uyetake L, Wichmann A, Bilak A, English CN, Su TT. 2008. Modulation of ionizing radiation-induced apoptosis by bantam microRNA in Drosophila. Developmental Biology 320:122–130.
  • Jirtle RL, Skinner MK. 2007. Environmental epigenomics and disease susceptibility. Nature Reviews Genetics 8:253–262.
  • Jones PA, Baylin SB. 2002. The fundamental role of epigenetic events in cancer. Nature Reviews Genetics 3:415–428.
  • Jones PA, Baylin SB. 2007. The epigenomics of cancer. Cell 128:683–692.
  • Kadhim MA, Lorimore SA, Hepburn MD, Goodhead DT, Buckle VJ, Wright EG. 1994. Alpha-particle-induced chromosomal instability in human bone marrow cells. The Lancet 344:987–988.
  • Kadhim MA, Macdonald DA, Goodhead DT, Lorimore SA, Marsden SJ, Wright EG. 1992. Transmission of chromosomal instability after plutonium alpha-particle irradiation. Nature 355:738–740.
  • Kalinich JF, Catravas GN, Snyder SL. 1989. The effect of γ irradiation on DNA methylation. Radiation Research 117:185–197.
  • Karagiannis TC, Harikrishnan KN, El-Osta A. 2007. Disparity of histone deacetylase inhibition on repair of radiation-induced DNA damage on euchromatin and constitutive heterochromatin compartments. Oncogene 26:3963–3971.
  • Kaup S, Grandjean V, Mukherjee R, Kapoor A, Keyes E, Seymour CB, Mothersill CE, Schofield PN. 2006. Radiation-induced genomic instability is associated with DNA methylation changes in cultured human keratinocytes. Mutation Research 597:87–97.
  • Kim GJ, Chandrasekaran K, Morgan WF. 2006a. Mitochondrial dysfunction, persistently elevated levels of reactive oxygen species and radiation-induced genomic instability: A review. Mutagenesis 21:361–367.
  • Kim GJ, Fiskum GM, Morgan WF. 2006b. A role for mitochondrial dysfunction in perpetuating radiation-induced genomic instability. Cancer Research 66:10377–10383.
  • Klarmann GJ, Decker A, Farrar WL. 2008. Epigenetic gene silencing in the Wnt pathway in breast cancer. Epigenetics 3:59–63.
  • Koturbash I, Baker M, Loree J, Kutanzi K, Hudson D, Pogribny I, Sedelnikova O, Bonner W, Kovalchuk O. 2006. Epigenetic dysregulation underlies radiation-induced transgenerational genome instability in vivo. International Journal of Radiation Oncology Biology Physics 66:327–330.
  • Koturbash I, Pogribny I, Kovalchuk O. 2005. Stable loss of global DNA methylation in the radiation-target tissue – a possible mechanism contributing to radiation carcinogenesis? Biochemical and Biophysical Research Communications 337:526–533.
  • Kovalchuk O, Baulch JE. 2008. Epigenetic changes and nontargeted radiation effects – is there a link? Environmental and Molecular Mutagenesis 49:16–25.
  • Kovalchuk O, Burke P, Arkhipov A, Kuchma N, James SJ, Kovalchuk I, Pogribny I. 2003. Genome hypermethylation in Pinus silvestris of Chernobyl – a mechanism for radiation adaptation? Mutation Research 529:13–20.
  • Kovalchuk O, Burke P, Besplug J, Slovack M, Filkowski J, Pogribny I. 2004. Methylation changes in muscle and liver tissues of male and female mice exposed to acute and chronic low-dose X-ray-irradiation. Mutation Research 548:75–84.
  • Kuo LJ, Yang LX. 2008. Gamma-H2AX – a novel biomarker for DNA double-strand breaks. In Vivo 22:305–309.
  • Lafon-Hughes L, Di Tomaso MV, Méndez-Acuña L, Martínez-López W. 2008. Chromatin-remodelling mechanisms in cancer. Mutation Research 658:191–214.
  • Laiakis EC, Baulch JE, Morgan WF. 2008. Interleukin 8 exhibits a pro-mitogenic and pro-survival role in radiation induced genomically unstable cells. Mutation Research 640:74–81.
  • Lambert B, Holmberg K, Hackman P, Wennborg A. 1998. Radiation induced chromosomal instability in human T-lymphocytes. Mutation Research 405:161–170.
  • Landthaler M, Yalcin A, Tuschl T. 2004. The human DiGeorge syndrome critical region gene 8 and its D. melanogaster homolog are required for miRNA biogenesis. Current Biology 14:2162–2167.
  • Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Rådmark O, Kim S, Kim VN. 2003. The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415–419.
  • Lee Y, Jeon K, Lee JT, Kim S, Kim VN. 2002. MicroRNA maturation: Stepwise processing and subcellular localization. EMBO Journal 21:4663–4670.
  • Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. 2004. MicroRNA genes are transcribed by RNA polymerase II. EMBO Journal 23:4051–4060.
  • Limoli CL, Giedzinski E, Morgan WF, Swarts SG, Jones GD, Hyun W. 2003. Persistent oxidative stress in chromosomally unstable cells. Cancer Research 63:3107–3111.
  • Limoli CL, Hartmann A, Shephard L, Yang C, Boothman DA, Bartholomew J, Morgan WF. 1998. Apoptosis, reproductive failure, and oxidative stress in Chinese hamster ovary cells with compromised genomic integrity. Cancer Research 58:3712–3718.
  • Limoli CL, Kaplan MI, Corcoran J, Meyers M, Boothman DA, Morgan WF. 1997a. Chromosomal instability and its relationship to other end points of genomic instability. Cancer Research 57:5557–5563.
  • Limoli CL, Kaplan MI, Giedzinski E, Morgan WF. 2001. Attenuation of radiation-induced genomic instability by free radical scavengers and cellular proliferation. Free Radical Biology & Medicine 31:10–19.
  • Limoli CL, Kaplan MI, Phillips JW, Adair GM, Morgan WF. 1997b. Differential induction of chromosomal instability by DNA strand-breaking agents. Cancer Research 57:4048–4056.
  • Limoli CL, Ponnaiya B, Corcoran JJ, Giedzinski E, Morgan WF. 2000. Chromosomal instability induced by heavy ion irradiation. International Journal of Radiation Biology 76:1599–1606.
  • Little JB. 2000. Radiation carcinogenesis. Carcinogenesis 21:397–404.
  • Loree J, Koturbash I, Kutanzi K, Baker M, Pogribny I, Kovalchuk O. 2006. Radiation-induced molecular changes in rat mammary tissue: Possible implications for radiation-induced carcinogenesis. International Journal of Radiation Biology 82:805–815.
  • Lorimore SA, Coates PJ, Scobie GE, Milne G, Wright EG. 2001. Inflammatory-type responses after exposure to ionizing radiation in vivo: A mechanism for radiation-induced bystander effects? Oncogene 20:7085–7095.
  • Lorimore SA, Coates PJ, Wright EG. 2003. Radiation-induced genomic instability and bystander effects: Inter-related nontargeted effects of exposure to ionizing radiation. Oncogene 22:7058–7069.
  • Lorimore SA, Wright EG. 2003. Radiation-induced genomic instability and bystander effects: Related inflammatory-type responses to radiation-induced stress and injury? A review. International Journal of Radiation Biology 79:15–25.
  • Maes OC, An J, Sarojini H, Wu H, Wang E. 2008. Changes in microRNA expression patterns in human fibroblasts after low-LET radiation. Journal of Cellular Biochemistry 105:824–834.
  • Marder BA, Morgan WF. 1993. Delayed chromosomal instability induced by DNA damage. Molecular and Cellular Biology 13:6667–6677.
  • Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. 2004. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs. Molecular Cell 15:185–197.
  • Miller JH, Jin S, Morgan WF, Yang A, Wan Y, Aypar U, Peters JS, Springer DL. 2008. Profiling mitochondrial proteins in radiation-induced genome-unstable cell lines with persistent oxidative stress by mass spectrometry. Radiation Research 169:700–706.
  • Morgan WF. 2003a. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiation Research 159:567–580.
  • Morgan WF. 2003b. Non-targeted and delayed effects of exposure to ionizing radiation: II. Radiation-induced genomic instability and bystander effects in vivo, clastogenic factors and transgenerational effects. Radiation Research 159:581–596.
  • Morgan WF, Corcoran J, Hartmann A, Kaplan MI, Limoli CL, Ponnaiya B. 1998. DNA double-strand breaks, chromosomal rerrangements, and genomic instability. Mutation Research 404:125–128.
  • Morgan WF, Day JP, Kaplan MI, McGhee EM, Limoli CL. 1996. Genomic instability induced by ionizing radiation. Radiation Research 146:247–258.
  • Morgan WF, Hartmann A, Limoli CL, Nagar S, Ponnaiya B. 2002. Bystander effects in radiation-induced genomic instability. Mutation Research 504:91–100.
  • Nagar S, Morgan WF. 2005. The death-inducing effect and genomic instability. Radiation Research 163:316–323.
  • Nagar S, Smith LE, Morgan WF. 2003. Characterization of a novel epigenetic effect of ionizing radiation: The death-inducing effect. Cancer Research 63:324–328.
  • Nakayama M, Wada H, Harada T, Nagayama J, Kusaba H, Ohshima K, Kozuru M, Komatsu H, Ueda R, Kuwano M. 1998. Hypomethylation status of CpG sites at the promoter region and overexpression of the human MDR1 gene in acute myeloid leukemias. Blood 92:4296–4307.
  • Nyce J, Liu L, Jones PA. 1986. Variable effects of DNA-synthesis inhibitors upon DNA methylation in mammalian cells. Nucleic Acids Research 14:4353–4367.
  • Okano M, Bell DW, Haber DA, Li E. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247–257.
  • Park JH, Park EJ, Lee HS, Kim SJ, Hur SK, Imbalzano AN, Kwon J. 2006. Mammalian SWI/SNF complexes facilitate DNA double-strand break repair by promoting gamma-H2AX induction. EMBO Journal 25:3986–3997.
  • Pendas-Franco N, Aguilera O, Pereira F, Gonzalez-Sancho JM, Munoz A. 2008. Vitamin D and Wnt/beta-catenin pathway in colon cancer: Role and regulation of DICKKOPF genes. Anticancer Research 28:2613–2623.
  • Pogribny I, Koturbash I, Tryndyak V, Hudson D, Stevenson SM, Sedelnikova O, Bonner W, Kovalchuk O. 2005. Fractionated low-dose radiation exposure leads to accumulation of DNA damage and profound alterations in DNA and histone methylation in the murine thymus. Molecular Cancer Research 3:553–561.
  • Pogribny I, Raiche J, Slovack M, Kovalchuk O. 2004. Dose-dependence, sex- and tissue-specificity and persistence of radiation-induced genomic DNA methylation changes. Biochemical and Biophysical Research Communications 320:1253–1261.
  • Pommier JP, Lebeau J, Ducray C, Sabatier L. 1995. Chromosomal instability and alteration of telomere repeat sequences. Biochimie 77:817–825.
  • Ponnaiya B, Limoli CL, Corcoran J, Kaplan MI, Hartmann A, Morgan WF. 1998. The evolution of chromosomal instability in Chinese hamster cells: A changing picture? International Journal of Radiation Biology 74:765–770.
  • Prochownik EV, Li Y. 2007. The ever expanding role for c-Myc in promoting genomic instability. Cell Cycle 6:1024–1029.
  • Raiche J, Rodriguez-Juarez R, Pogribny I, Kovalchuk O. 2004. Sex and tissue specific expression of maintenance and de novo DNA methyltransferases upon low dose X-irradiation in mice. Biochemical and Biophysical Research Communications 325:39–47.
  • Ramsahoye BH, Biniszkiewicz D, Lyko F, Clark V, Bird AP, Jaenisch R. 2000. Non-CpG methylation is prevalent in embryonic stem cells and may be mediated by DNA methyltransferase 3a. Proceedings of the National Academy of Sciences of the USA 97:5237–5242.
  • Reik W, Lewis A. 2005. Co-evolution of X-chromosome inactivation and imprinting in mammals. Nature Reviews Genetics 6:403–410.
  • Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. Journal of Biological Chemistry 273:5858–5868.
  • Romney CA, Paulauskis JD, Nagasawa H, Little JB. 2001. Multiple manifestations of X-ray-induced genomic instability in Chinese hamster ovary (CHO) cells. Molecular Carcinogenesis 32:118–127.
  • Roy K, Kodama S, Suzuki K, Fukase K, Watanabe M. 2000. Hypoxia relieves X-ray-induced delayed effects in normal human embryo cells. Radiation Research 154:659–666.
  • Salomon R, Kaye AM. 1970. Methylation of mouse DNA in vivo: Di- and tripyrimidine sequences containing 5-methylcytosine. Biochimica et Biophysica Acta 204:340–351.
  • Schickel R, Boyerinas B, Park SM, Peter ME. 2008. MicroRNAs: Key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 27:5959–5974.
  • Schuffenhauer S, Bartsch O, Stumm M, Buchholz T, Petropoulou T, Kraft S, Belohradsky B, Hinkel GK, Meitinger T, Wegner RD. 1995. DNA, FISH and complementation studies in ICF syndrome: DNA hypomethylation of repetitive and single copy loci and evidence for a trans acting factor. Human Genetics 96:562–571.
  • Schwarz DS, Hutvágner G, Du T, Xu Z, Aronin N, Zamore PD. 2003. Asymmetry in the assembly of the RNAi enzyme complex. Cell 115:199–208.
  • Shin S, Cha HJ, Lee EM, Jung JH, Lee SJ, Park IC, Jin YW, An S. 2009a. MicroRNAs are significantly influenced by p53 and radiation in HCT116 human colon carcinoma cells. International Journal of Oncology 34:1645–1652.
  • Shin S, Cha HJ, Lee EM, Lee SJ, Seo SK, Jin HO, Park IC, Jin YW, An S. 2009b. Alteration of miRNA profiles by ionizing radiation in A549 human non-small cell lung cancer cells. International Journal of Oncology 35:81–86.
  • Simone NL, Soule BP, Ly D, Saleh AD, Savage JE, Degraff W, Cook J, Harris CC, Gius D, Mitchell JB. 2009. Ionizing radiation-induced oxidative stress alters miRNA expression. PLoS One 4:e6377.
  • Snyder AR, Morgan WF. 2003. Persistent oxidative stress and gene expression changes in radiation-induced genomic instability. International Congress Series 1258:199–206.
  • Snyder AR, Morgan WF. 2004. Radiation-induced chromosomal instability and gene expression profiling: Searching for clues to initiation and perpetuation. Mutation Research 568:89–96.
  • Snyder AR, Morgan WF. 2005a. Differential induction and activation of NF-kB transcription complexes in radiation-induced chromosomally unstable cell lines. Environmental and Molecular Mutagenesis 45:177–187.
  • Snyder AR, Morgan WF. 2005b. Lack of consensus gene expression changes associated with radiation-induced chromosomal instability. DNA Repair (Amsterdam) 4:958–970.
  • Sonkoly E, Pivarcsi A. 2009. microRNAs in inflammation. International Reviews of Immunology 28:535–561.
  • Sowa Resat MB, Morgan WF. 2004. Radiation-induced genomic instability: A role for secreted soluble factors in communicating the radiation response to non-irradiated cells. Journal of Cellular Biochemistry 92:1013–1019.
  • Srivastava N, Gochhait S, de Boer P, Bamezai RN. 2009. Role of H2AX in DNA damage response and human cancers. Mutation Research 681:180–188.
  • Stark A, Brennecke J, Bushati N, Russell RB, Cohen SM. 2005. Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3′ UTR evolution. Cell 123:1133–1146.
  • Tamminga J, Kathiria P, Koturbash I, Kovalchuk O. 2008. DNA damage-induced upregulation of miR-709 in the germline downregulates BORIS to counteract aberrant DNA hypomethylation. Cell Cycle 7:3731–3736.
  • Taniguchi H, Yamamoto H, Hirata T, Miyamoto N, Oki M, Nosho K, Adachi Y, Endo T, Imai K, Shinomura Y. 2005. Frequent epigenetic inactivation of Wnt inhibitory factor-1 in human gastrointestinal cancers. Oncogene 24:7946–7952.
  • Tawa R, Kimura Y, Komura J, Miyamura Y, Kurishita A, Sasaki MS, Sakurai H, Ono T. 1998. Effects of X-ray irradiation on genomic DNA methylation levels in mouse tissues. Journal of Radiation Research 39:271–278.
  • Trani D, Datta K, Doiron K, Kallakury B, Fornace AJ Jr. 2010. Enhanced intestinal tumor multiplicity and grade in vivo after HZE exposure: Mouse models for space radiation risk estimates. Radiation and Environmental Biophysics 49:389–396.
  • Ullrich RL, Ponnaiya B. 1998. Radiation-induced instability and its relation to radiation carcinogenesis. International Journal of Radiation Biology 74:747–754.
  • Upton AC. 1986. Historical perspectives on radiation carcinogenesis. Radiation Carcinogenesis: 1–10.
  • Vasireddy RS, Karagiannis TC, El-Osta A. 2010. γ-radiation-induced γH2AX formation occurs preferentially in actively transcribing euchromatic loci. Cellular and Molecular Life Sciences 67:291–294.
  • Waldren CA. 2004. Classical radiation biology dogma, bystander effects and paradigm shifts. Human & Experimental Toxicology 23:95–100.
  • Wang GG, Allis CD, Chi P. 2007a. Chromatin remodeling and cancer, Part I: Covalent histone modifications. Trends in Molecular Medicine 13:363–372.
  • Wang GG, Allis CD, Chi P. 2007b. Chromatin remodeling and cancer, Part II: ATP-dependent chromatin remodeling. Trends in Molecular Medicine 13:373–380.
  • Watson GE, Lorimore SA, Macdonald DA, Wright EG. 2000. Chromosomal instability in unirradiated cells induced in vivo by a bystander effect of ionizing radiation. Cancer Research 60:5608–5611.
  • Wilkins JA, Sansom OJ. 2008. C-Myc is a critical mediator of the phenotypes of Apc loss in the intestine. Cancer Research 68:4963–4966.
  • Woodcock DM, Crowther PJ, Diver WP. 1987. The majority of methylated deoxycytidines in human DNA are not in the CpG dinucleotide. Biochemical and Biophysical Research Communications 145:888–894.
  • Wright EG. 2010. Manifestations and mechanisms of non-targeted effects of ionizing radiation. Mutation Research 687:28–33.
  • Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M, Hulten M, Qu X, Russo JJ, Viegas-Péquignot E. 1999. Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402:187–191.
  • Yi R, Qin Y, Macara IG, Cullen BR. 2003. Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes & Development 17:3011–3016.
  • Yin B, Bassing CH. 2008. The sticky business of histone H2AX in V(D)J recombination, maintenance of genomic stability, and suppression of lymphoma. Immunologic Research 42:29–40.
  • Zawia NH, Lahiri DK, Cardozo-Pelaez F. 2009. Epigenetics, oxidative stress, and Alzheimer disease. Free Radical Biology & Medicine 46:1241–1249.
  • Zhou W, Wang X, Rosenfeld MG. 2009. Histone H2A ubiquitination in transcriptional regulation and DNA damage repair. International Journal of Biochemistry & Cell Biology 41:12–15.
  • Ziv Y, Bielopolski D, Galanty Y, Lukas C, Taya Y, Schultz DC, Lukas J, Bekker-Jensen S, Bartek J, Shiloh Y. 2006. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway. Nature Cell Biology 8:870–876.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.