Exposure to low-dose 56Fe-ion radiation induces long-term epigenetic alterations in mouse bone marrow hematopoietic progenitor and stem cells

Radiation Research

Volumn 182, Issue 1, 2014, Pages 92-101

  Miousse, Isabelle R ^a   Shao, Lijian ^a   Chang, Jianhui ^a   Feng, Wei ^a   Wang, Yingying ^a   Allen, Antiño R ^a,b   Turner, Jennifer ^c   Stewart, Blair ^c   Raber, Jacob ^c,d,e   Zhou, Daohong ^a   Koturbash, Igor ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Departments of Behavioral Neuroscience   (United States)

^d Departments of Behavioral Neuroscience ^*  (United States)

^e OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; DNA; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; HEAVY ION; IRON; LINE1 PROTEIN; PROTEIN; REACTIVE OXYGEN METABOLITE; SINE B1 PROTEIN; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; APOPTOSIS; ARTICLE; CELL AGING; CELL DAMAGE; CELL ISOLATION; CONTROLLED STUDY; COPY NUMBER VARIATION; COSMIC RADIATION; DNA METHYLATION; DNA STRAND BREAKAGE; DOSIMETRY; EPIGENETICS; FLOW CYTOMETRY; GENE EXPRESSION; GENOMIC INSTABILITY; HEAVY ION RADIATION; HEMATOPOIETIC STEM CELL; IRRADIATION; LINEAR ENERGY TRANSFER; LOW ENERGY RADIATION; MALE; MONONUCLEAR CELL; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN EXPRESSION; WHOLE BODY RADIATION;

ANIMALS; APOPTOSIS; CELL AGING; DNA DAMAGE; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, RADIATION; EPIGENESIS, GENETIC; GENE DOSAGE; HEMATOPOIETIC STEM CELLS; IRON; MALE; MICE; MICE, INBRED C57BL; REACTIVE OXYGEN SPECIES; REPETITIVE SEQUENCES, NUCLEIC ACID; TIME FACTORS;

EID: 84904098214     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR13580.1     Document Type: Article

References (53)

1. Suzuki M, Piao C, Hall EJ, Hei TK. Cell killing and chromatid damage in primary human bronchial epithelial cells irradiated with accelerated 56Fe ions. Radiat Res 2001; 155:432-9.
2. Aypar U, Morgan WF, Baulch JE. Radiation-induced epigenetic alterations after low and high LET irradiations. Mutat Res 2011; 707:24-33.
3. Durante M, Cucinotta FA. Heavy ion carcinogenesis and human space exploration. Nat Rev Cancer 2008; 8:465-72.
4. Durante M, Snigiryova G, Akaeva E, Bogomazova A, Druzhinin S, Fedorenko B, et al. Chromosome aberration dosimetry in cosmonauts after single or multiple space flights. Cytogenet Genome Res 2003; 103:40-6.
5. Mothersill C, Seymour C. Implications for human and environmental health of low doses of ionising radiation. J Environ Radioact 2013; DOI 10.1016/j.jenvrad.2013.04.002.
6. Shimizu Y, Kato H, Schull WJ. Risk of cancer among atomic bomb survivors. J Radiat Res 1991; 32 Suppl 2:54-63.
7. Weil MM, Bedford JS, Bielefeldt-Ohmann H, Ray FA, Genik PC, Ehrhart EJ, et al. Incidence of acute myeloid leukemia and hepatocellular carcinoma in mice irradiated with 1 GeV/nucleon (56)Fe ions. Radiat Res 2009; 172:213-9.
8. Steffen LS, Bacher JW, Peng Y, Le PN, Ding LH, Genik PC, et al. Molecular characterisation of murine acute myeloid leukaemia induced by 56Fe ion and 137Cs gamma ray irradiation. Mutagenesis 2013; 28:71-9.
9. Koturbash I, Pogribny I, Kovalchuk O. Stable loss of global DNA methylation in the radiation-target tissue-a possible mechanism contributing to radiation carcinogenesis? Biochem Biophys Res Commun 2005; 337:526-33.
10. Loree J, Koturbash I, Kutanzi K, Baker M, Pogribny I, Kovalchuk O. Radiation-induced molecular changes in rat mammary tissue: possible implications for radiation-induced carcinogenesis. Int J Radiat Biol 2006; 82:805-15.
11. Ehrlich M, Lacey M. DNA methylation and differentiation: silencing, upregulation and modulation of gene expression. Epigenomics 2013; 5:553-68.
12. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012; 13:484-92.
13. Jones PA, Liang G. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 2009; 10:805-11.
14. Howard G, Eiges R, Gaudet F, Jaenisch R, Eden A. Activation and transposition of endogenous retroviral elements in hypomethylation induced tumors in mice. Oncogene 2008; 27:404-8.
15. Hajkova H, Markova J, Haskovec C, Sarova I, Fuchs O, Kostecka A, et al. Decreased DNA methylation in acute myeloid leukemia patients with DNMT3A mutations and prognostic implications of DNA methylation. Leuk Res 2012; 36:1128-33.
16. Chung YR, Schatoff E, Abdel-Wahab O. Epigenetic alterations in hematopoietic malignancies. Int J Hematol 2012; 96:413-27.
17. Giotopoulos G, McCormick C, Cole C, Zanker A, Jawad M, Brown R, et al. DNA methylation during mouse hemopoietic differentiation and radiation-induced leukemia. Exp Hematol 2006; 34:1462-70.
18. Holz-Schietinger C, Matje DM, Reich NO. Mutations in DNA methyltransferase (DNMT3A) observed in acute myeloid leukemia patients disrupt processive methylation. J Biol Chem 2012; 287:30941-51.
19. Scholz B, Marschalek R. Epigenetics and blood disorders. Br J Haematol 2012; 158:307-22.
20. Shih AH, Abdel-Wahab O, Patel JP, Levine RL. The role of mutations in epigenetic regulators in myeloid malignancies. Nat Rev Cancer 2012; 12:599-612.
21. Wakita S, Yamaguchi H, Omori I, Terada K, Ueda T, Manabe E, et al. Mutations of the epigenetics-modifying gene (DNMT3a, TET2, IDH1/2) at diagnosis may induce FLT3-ITD at relapse in de novo acute myeloid leukemia. Leukemia 2013; 27:1044-52.
22. Yamazaki J, Estecio MR, Lu Y, Long H, Malouf GG, Graber D, et al. The epigenome of AML stem and progenitor cells. Epigenetics 2013; 8:92-104.
23. Saied MH, Marzec J, Khalid S, Smith P, Down TA, Rakyan VK, et al. Genome wide analysis of acute myeloid leukemia reveal leukemia specific methylome and subtype specific hypomethylation of repeats. PLoS One 2012; 7:e33213.
24. Thol F, Damm F, Ludeking A, Winschel C, Wagner K, Morgan M, et al. Incidence and prognostic influence of DNMT3A mutations in acute myeloid leukemia. J Clin Oncol 2011; 29:2889-96.
25. Cross M, Bach E, Tran T, Krahl R, Jaekel N, Niederwieser D, et al. Pretreatment long interspersed element (LINE)-1 methylation levels, not early hypomethylation under treatment, predict hematological response to azacitidine in elderly patients with acute myeloid leukemia. Onco Targets Ther 2013; 6:741-8.
26. Koturbash I, Boyko A, Rodriguez-Juarez R, McDonald RJ, Tryndyak VP, Kovalchuk I, et al. Role of epigenetic effectors in maintenance of the long-term persistent bystander effect in spleen in vivo. Carcinogenesis 2007; 28:1831-8.
27. Tamminga J, Kathiria P, Koturbash I, Kovalchuk O. DNA damage-induced upregulation of miR-709 in the germline downregulates BORIS to counteract aberrant DNA hypomethylation. Cell Cycle 2008; 7:3731-6.
28. Goetz W, Morgan MN, Baulch JE. The effect of radiation quality on genomic DNA methylation profiles in irradiated human cell lines. Radiat Res 2011; 175:575-87.
29. Martens JH, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, Steinlein P, et al. The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J 2005; 24:800-812.
30. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 2008; 3:1101-8.
31. Vitullo P, Sciamanna I, Baiocchi M, Sinibaldi-Vallebona P, Spadafora C. LINE-1 retrotransposon copies are amplified during murine early embryo development. Mol Reprod Dev 2012; 79:118-27.
32. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, Agarwal P, et al. Initial sequencing and comparative analysis of the mouse genome. Nature 2002; 420:520-62.
33. Hogart A, Lichtenberg J, Ajay SS, Anderson S, Margulies EH, Bodine DM. Genome-wide DNA methylation profiles in hematopoietic stem and progenitor cells reveal overrepresentation of ETS transcription factor binding sites. Genome Res 2012; 22:1407-18.
34. Gridley DS, Pecaut MJ. Genetic background and lymphocyte populations after total-body exposure to iron ion radiation. Int J Radiat Biol 2011; 87:8-23.
35. Perepelitsa-Belancio V, Deininger P. RNA truncation by premature polyadenylation attenuates human mobile element activity. Nat Genet 2003; 35:363-6.
36. Han JS, Szak ST, Boeke JD. Transcriptional disruption by the L1 retrotransposon and implications for mammalian transcriptomes. Nature 2004; 429:268-74.
37. Jurka J, Kapitonov VV, Kohany O, Jurka MV. Repetitive sequences in complex genomes: structure and evolution. Annu Rev Genomics Hum Genet 2007; 8:241-59.
38. Mistry H, Tamblyn L, Butt H, Sisgoreo D, Gracias A, Larin M, et al. UHRF1 is a genome caretaker that facilitates the DNA damage response to gamma-irradiation. Genome Integr 2010; 1:7.
39. Wang Y, Liu L, Pazhanisamy SK, Li H, Meng A, Zhou D. Total body irradiation causes residual bone marrow injury by induction of persistent oxidative stress in murine hematopoietic stem cells. Free Radic Biol Med 2010; 48:348-56.
40. Maksakova IA, Mager DL, Reiss D. Keeping active endogenous retroviral-like elements in check: the epigenetic perspective. Cell Mol Life Sci 2008; 65:3329-47.
41. Cowley M, Oakey RJ. Transposable elements re-wire and finetune the transcriptome. PLoS Genet 2013; 9:e1003234.
42. Ehrlich M, Lacey M. DNA hypomethylation and hemimethylation in cancer. Adv Exp Med Biol 2013; 754:31-56.
43. Koturbash I, Beland FA, Pogribny IP. Role of epigenetic events in chemical carcinogenesis-a justification for incorporating epigenetic evaluations in cancer risk assessment. Toxicol Mech Methods 2011; 21:289-97.
44. Pogribny IP, Beland FA. DNA hypomethylation in the origin and pathogenesis of human diseases. Cell Mol Life Sci 2009; 66:2249-61.
45. Bollati V, Baccarelli A, Hou L, Bonzini M, Fustinoni S, Cavallo D, et al. Changes in DNA methylation patterns in subjects exposed to low-dose benzene. Cancer Res 2007; 67:876-80.
46. Ji Z, Zhang L, Peng V, Ren X, McHale CM, Smith MT. A comparison of the cytogenetic alterations and global DNA hypomethylation induced by the benzene metabolite, hydroquinone, with those induced by melphalan and etoposide. Leukemia 2010; 24:986-91.
47. Muotri AR, Marchetto MC, Coufal NG, Oefner R, Yeo G, Nakashima K, et al. L1 retrotransposition in neurons is modulated by MeCP2. Nature 2010; 468:443-6.
48. Prise KM, Pinto M, Newman HC, Michael BD. A review of studies of ionizing radiation-induced double-strand break clustering. Radiat Res 2001; 156:572-6.
49. Pogribny I, Koturbash I, Tryndyak V, Hudson D, Stevenson SM, Sedelnikova O, et al. Fractionated low-dose radiation exposure leads to accumulation of DNA damage and profound alterations in DNA and histone methylation in the murine thymus. Mol Cancer Res 2005; 3:553-61.
50. Arand J, Spieler D, Karius T, Branco MR, Meilinger D, Meissner A, et al. In vivo control of CpG and non-CpG DNA methylation by DNA methyltransferases. PLoS Genet 2012; 8:e1002750.
51. Pogribny IP, Tryndyak VP, Bagnyukova TV, Melnyk S, Montgomery B, Ross SA, et al. Hepatic epigenetic phenotype predetermines individual susceptibility to hepatic steatosis in mice fed a lipogenic methyl-deficient diet. J Hepatol 2009; 51:176-86.
52. Koturbash I, Kutanzi K, Hendrickson K, Rodriguez-Juarez R, Kogosov D, Kovalchuk O. Radiation-induced bystander effects in vivo are sex specific. Mutat Res 2008; 642:28-36.
53. Koturbash I, Zemp F, Kolb B, Kovalchuk O. Sex-specific radiation-induced microRNAome responses in the hippocampus, cerebellum and frontal cortex in a mouse model. Mutat Res 2011; 722:114-8.