Dose rate dependent reduction in chromatin accessibility at transcriptional start sites long time after exposure to gamma radiation

References

• ICRP. The 2007 recommendations of the international commission on radiological protection. ICRP Publication. 2007;103:0146–17. Contract No: 2-4.
   Google Scholar
• Preston DL, Ron E, Tokuoka S, et al. Solid cancer incidence in atomic bomb survivors: 1958-1998. Radiat Res. 2007;168(1):1–64.
   PubMed Web of Science ®Google Scholar
• Folley JH, Borges W, Yamawaki T. Incidence of leukemia in survivors of the atomic bomb in Hiroshima and Nagasaki, Japan. Am j med. 1952;13(3):311–321.
   PubMed Web of Science ®Google Scholar
• NAS. Health risks from exposure to low levels of ionizing radiation; BEIR VII. Washington, DC: The National Academies Press; 2006p. 422.
   Google Scholar
• Little MP, Tawn EJ, Tzoulaki I, et al. A systematic review of epidemiological associations between low and moderate doses of ionizing radiation and late cardiovascular effects, and their possible mechanisms. Radiat Res. 2008;169(1):99–109, 11.
   PubMed Web of Science ®Google Scholar
• Shimizu Y, Kodama K, Nishi N, et al. Radiation exposure and circulatory disease risk: hiroshima and Nagasaki atomic bomb survivor data, 1950-2003. BMJ (Clin Res Ed). 2010;340:b5349.
   PubMed Web of Science ®Google Scholar
• Gillies M, Richardson DB, Cardis E, et al. Mortality from circulatory diseases and other non-cancer outcomes among nuclear workers in France, the United Kingdom and the United States (INWORKS). Radiat Res. 2017;188(3):276–290. DOI:10.1667/rr14608.1
   PubMed Web of Science ®Google Scholar
• Akahoshi M, Amasaki Y, Soda M, et al. Effects of radiation on fatty liver and metabolic coronary risk factors among atomic bomb survivors in Nagasaki. Hypertens Res. 2003;26(12):965–970.
   PubMed Web of Science ®Google Scholar
• Tapio S, Little MP, Kaiser JC, et al. Ionizing radiation-induced circulatory and metabolic diseases. Environ Int. 2021;146:106235.
   PubMed Web of Science ®Google Scholar
• Minamoto A, Taniguchi H, Yoshitani N, et al. Cataract in atomic bomb survivors. Int J Radiat Biol. 2004;80(5):339–345. DOI:10.1080/09553000410001680332
   PubMed Web of Science ®Google Scholar
• Ozasa K, Cullings HM, Ohishi W, et al. Epidemiological studies of atomic bomb radiation at the radiation effects research foundation. Int J Radiat Biol. 2019;95(7):879–891.
   PubMed Web of Science ®Google Scholar
• WHO. Health effects of the chernobyl accidents and special health care programmes; report of the UN chernobyl forum expert group “health”. WHO Press. 2006;9241594179.
   Google Scholar
• WHO. Health risk assessment from the nuclear accident after the 2011 Great East Japan earthquake and tsunami, based on a preliminary dose estimation. 2013 978 92 4 150513 0.
   Google Scholar
• Rühm W, Azizova TV, Bouffler SD, et al. Dose-rate effects in radiation biology and radiation protection. Ann ICRP. 2016;45(1_suppl):262–279. DOI:10.1177/0146645316629336
   PubMedGoogle Scholar
• Little MP. Evidence for dose and dose rate effects in human and animal radiation studies. Ann ICRP. 2018;47(3–4):97–112.
   PubMedGoogle Scholar
• SSK. Dose- and dose-rate-effectiveness factor (DDREF), recommendation by the German commission on radiological protection with scientific grounds. Bonn, Germany: German Commission on Radiological Protection; 2014.
   Google Scholar
• UNSCEAR. Biological mechanisms of radiation actions at low doses; a white paper to guide the scientific committee’s future programme of work. United Nations Publications. 2012;45.
   Google Scholar
• Reisz JA, Bansal N, Qian J, et al. Effects of ionizing radiation on biological molecules–mechanisms of damage and emerging methods of detection. Antioxidants & Redox Signaling. 2014;21(2):260–292.
   PubMed Web of Science ®Google Scholar
• Mavragani IV, Nikitaki Z, Mp S, et al. Complex DNA damage: a route to radiation-induced genomic instability and carcinogenesis. Cancers (Basel). 2017;9(7):91. DOI:10.3390/cancers9070091
   PubMed Web of Science ®Google Scholar
• Azzam EI, Jay-Gerin JP, Pain D. Ionizing radiation-induced metabolic oxidative stress and prolonged cell injury. Cancer Lett. 2012;327(1–2):48–60.
   PubMed Web of Science ®Google Scholar
• Huang R, Zhou P-K. DNA damage repair: historical perspectives, mechanistic pathways and clinical translation for targeted cancer therapy. Signal Transduct Target Ther. 2021;6(1):254.
   PubMed Web of Science ®Google Scholar
• Aleksandrov R, Hristova R, Stoynov S, et al. The chromatin response to double-strand DNA breaks and their repair. Cells. 2020;9(8):1853. PubMed PMID: rayyan-676545108. 10.3390/cells9081853.
   PubMed Web of Science ®Google Scholar
• Pandita T, Kumar R, Horikoshi N, et al. Chromatin modifications and the DNA damage response to ionizing radiation. Front Oncol. 2013;2. DOI:10.3389/fonc.2012.00214.
   PubMedGoogle Scholar
• Tsompana M, Buck MJ. Chromatin accessibility: a window into the genome. Epigenetics & Chromatin. 2014;7(1):33.
   PubMedGoogle Scholar
• Stadler J, Richly H. Regulation of DNA repair mechanisms: how the chromatin environment regulates the DNA damage response. Int J Mol Sci. 2017;18(8):1715.
   PubMed Web of Science ®Google Scholar
• Merrifield M, Kovalchuk O. Epigenetics in radiation biology: a new research frontier. Front Genet. 2013;4:40.
   PubMedGoogle Scholar
• Tharmalingam S, Sreetharan S, Kulesza AV, et al. Low-dose ionizing radiation exposure, oxidative stress and epigenetic programing of health and disease. Radiat Res. 2017;188(4.2):525–538.
   PubMed Web of Science ®Google Scholar
• Belli M, Tabocchini MA. Ionizing radiation-induced epigenetic modifications and their relevance to radiation protection. Int J Mol Sci. 2020;21(17):5993.
   PubMed Web of Science ®Google Scholar
• Miousse IR, Kutanzi KR, Koturbash I. Effects of ionizing radiation on DNA methylation: from experimental biology to clinical applications. Int J Radiat Biol. 2017;93(5):457–469. PubMed PMID: rayyan-676545029. 10.1080/09553002.2017.1287454.
   PubMed Web of Science ®Google Scholar
• Pogribny I, Koturbash I, Tryndyak V, 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(10):553–561. PubMed PMID: rayyan-676545057.
   PubMed Web of Science ®Google Scholar
• Friedl A, Mazurek B, Seiler D. Radiation-induced alterations in histone modification patterns and their potential impact on short-term radiation effects. Front Oncol. 2012;2. DOI:10.3389/fonc.2012.00117
   PubMedGoogle Scholar
• Van HT, Santos MA. Histone modifications and the DNA double-strand break response. cell cycle (georgetown, tex). 2018;17(21–22):2399–2410. DOI:10.1080/15384101.2018.1542899
   Google Scholar
• Klemm SL, Shipony Z, Greenleaf WJ. Chromatin accessibility and the regulatory epigenome. Nat Rev Genet. 2019;20(4):207–220.
   PubMed Web of Science ®Google Scholar
• Jafer A, Sylvius N, Adewoye AB, et al. The long-term effects of exposure to ionising radiation on gene expression in mice. Mutat Res. 2020;821:111723.
   PubMed Web of Science ®Google Scholar
• Jain V, Das B. Global transcriptome profile reveals abundance of DNA damage response and repair genes in individuals from high level natural radiation areas of Kerala coast. PLoS ONE. 2017;12(11):e0187274.
   PubMed Web of Science ®Google Scholar
• Dahl H, Eide DM, Tengs T, et al. Perturbed transcriptional profiles after chronic low dose rate radiation in mice. PLoS ONE. 2021;16(8):e0256667. DOI:10.1371/journal.pone.0256667
   PubMed Web of Science ®Google Scholar
• Uehara Y, Ito Y, Taki K, et al. Gene expression profiles in mouse liver after long-term low-dose-rate irradiation with gamma rays. Radiat Res. 2010;174(5):611–617. DOI:10.1667/rr2195.1
   PubMed Web of Science ®Google Scholar
• Burgio E, Piscitelli P, Migliore L. Ionizing radiation and human health: reviewing models of exposure and mechanisms of cellular damage an epigenetic perspective. Int J Environ Res Public Health. 2018;15(9):1971.
   PubMed Web of Science ®Google Scholar
• Paunesku T, Stevanović A, Popović J, et al. Effects of low dose and low dose rate low linear energy transfer radiation on animals - review of recent studies relevant for carcinogenesis. Int J Radiat Biol. 2021;97(6):757–768.
   PubMed Web of Science ®Google Scholar
• Brooks AL, Hoel DG, Preston RJ. The role of dose rate in radiation cancer risk: evaluating the effect of dose rate at the molecular, cellular and tissue levels using key events in critical pathways following exposure to low LET radiation. Int J Radiat Biol. 2016;92(8):405–426.
   PubMed Web of Science ®Google Scholar
• Bae MJ, Kang MK, Kye YU, et al. Differential effects of low and high radiation dose rates on mouse spermatogenesis. Int J Mol Sci. 2021;22(23). DOI:10.3390/ijms222312834
   Web of Science ®Google Scholar
• Tanaka K, Kohda A, Satoh K, et al. Dose-rate effectiveness for unstable-type chromosome aberrations detected in mice after continuous irradiation with low-dose-rate gamma rays. Radiat Res. 2009;171(3):290–301.
   PubMed Web of Science ®Google Scholar
• Flavahan WA, Gaskell E, Bernstein BE. Epigenetic plasticity and the hallmarks of cancer. Science. 2017;357(6348): PubMed PMID: rayyan-676545096. DOI:10.1126/science.aal2380
   PubMed Web of Science ®Google Scholar
• Buenrostro JD, Wu B, Chang HY, et al. ATAC-seq: a method for assaying chromatin accessibility genome-wide. Curr Protoc Mol Biol. 2015;109(1):.21.9.1–.9.9.
   Google Scholar
• Buenrostro JD, Giresi PG, Zaba LC, et al. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods. 2013;10(12):1213–1218.
   PubMed Web of Science ®Google Scholar
• Corces MR, Trevino AE, Hamilton EG, et al. An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nat Methods. 2017;14(10):959–962. DOI:10.1038/nmeth.4396
   PubMed Web of Science ®Google Scholar
• Duale N, Eide DM, Amberger ML, et al. Using prediction models to identify miRNA-based markers of low dose rate chronic stress. Sci Total Environ. 2020;717:137068.
   PubMed Web of Science ®Google Scholar
• Graupner A, Eide DM, Brede DA, et al. Genotoxic effects of high dose rate X-ray and low dose rate gamma radiation in Apc(Min/+) mice. Environ Mol Mutagenesis. 2017;58(8):560–569.
   PubMed Web of Science ®Google Scholar
• E. Lindbo Hansen POH. Air kerma measurements with landauer nanoDots in Cs-137 and Co-60 beams. Part I - SSDL exposures free in air. Teqnical document no. 8. Norwegian Radiation Protection Authority, Østerås, Oslo: NRPA, 2017 2017-12-07. Report No.: Contract No.: 8.
   Google Scholar
• Graupner A, Eide DM, Instanes C, et al. Gamma radiation at a human relevant low dose rate is genotoxic in mice. Sci Rep. 2016;6(1):32977. DOI:10.1038/srep32977
   PubMedGoogle Scholar
• Lind OC, Helen Oughton D, Salbu B. The NMBU FIGARO low dose irradiation facility. Int J Radiat Biol. 2018;95(1):1–6.
   Web of Science ®Google Scholar
• Li H, Durbin R. Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics. 2009;25(14):1754–1760.
   PubMed Web of Science ®Google Scholar
• Ewels PA, Peltzer A, Fillinger S, et al. The nf-core framework for community-curated bioinformatics pipelines. Nat Biotechnol. 2020;38(3):276–278.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liu T, Meyer CA, et al. Model-based analysis of ChIP-Seq (MACS). Genome Bio. 2008;9(9):R137. DOI:10.1186/gb-2008-9-9-r137
   PubMed Web of Science ®Google Scholar
• Carroll TS, Liang Z, Salama R, et al. Impact of artifact removal on ChIP quality metrics in ChIP-seq and ChIP-exo data. Front Genet. 2014;5:75.
   PubMed Web of Science ®Google Scholar
• Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Bio. 2014;15(12):550.
   PubMed Web of Science ®Google Scholar
• Kane AE, Sinclair DA. Epigenetic changes during aging and their reprogramming potential. Critical reviews in biochemistry and molecular biology. 2019;54(1):61–83. DOI:10.1080/10409238.2019.1570075
   Google Scholar
• Yu G, Wang LG, He QY. ChIPseeker: an R/Bioconductor package for ChIP peak annotation, comparison and visualization. Bioinformatics. 2015;31(14):2382–2383.
   PubMed Web of Science ®Google Scholar
• Carlson M. org.Mm.eg.db: Available from. Genome wide annotation for mouse bioconductor2019. Genome wide annotation for mouse, primarily based on mapping using entrez gene identifiers.]. https://bioconductor.org/packages/release/data/annotation/html/org.Mm.eg.db.html.
   Google Scholar
• Zhou Y, Zhou B, Pache L, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019;10(1):1523. DOI:10.1038/s41467-019-09234-6
   PubMed Web of Science ®Google Scholar
• Heberle H, Meirelles GV, da Silva FR, et al. InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinf. 2015;16(1):169.
   PubMed Web of Science ®Google Scholar
• Yates AD, Achuthan P, Akanni W, et al. Ensembl 2020. Nucleic Acids Res. 2020;48(D1):D682–8. DOI:10.1093/nar/gkz966
   PubMed Web of Science ®Google Scholar
• Song Y, Xie L, Lee Y, et al. Integrative assessment of low-dose gamma radiation effects on Daphnia magna reproduction: toxicity pathway assembly and AOP development. Sci Total Environ. 2020;705:135912.
   PubMed Web of Science ®Google Scholar
• Vaiserman A, Cuttler JM, Socol Y. Low-dose ionizing radiation as a hormetin: experimental observations and therapeutic perspective for age-related disorders. Biogerontology. 2021;22(2):145–164.
   PubMed Web of Science ®Google Scholar
• Ray-Jones H, Spivakov M. Transcriptional enhancers and their communication with gene promoters. Cell Mol Life Sci. 2021;78(19):6453–6485.
   PubMed Web of Science ®Google Scholar
• Lysek-Gladysinska M, Wieczorek A, Walaszczyk A, et al. Long-term effects of low-dose mouse liver irradiation involve ultrastructural and biochemical changes in hepatocytes that depend on lipid metabolism. Radiat Environ Biophys. 2018;57(2):123–132. DOI:10.1007/s00411-018-0734-9
   PubMed Web of Science ®Google Scholar
• Golla S, Golla JP, Krausz KW, et al. Metabolomic analysis of mice exposed to gamma radiation reveals a systemic understanding of total-body exposure. Radiat Res. 2017;187(5):612–629. DOI:10.1667/rr14592.1
   PubMed Web of Science ®Google Scholar
• Rajbhandari P, Thomas BJ, Feng AC, et al. IL-10 signaling remodels adipose chromatin architecture to limit thermogenesis and energy expenditure. Cell. 2018;172(1–2):218–33.e17.
   PubMed Web of Science ®Google Scholar
• Starks RR, Biswas A, Jain A, et al. Combined analysis of dissimilar promoter accessibility and gene expression profiles identifies tissue-specific genes and actively repressed networks. Epigenetics & Chromatin. 2019;12(1):16.
   PubMedGoogle Scholar
• Corces MR, Granja JM, Shams S, et al. The chromatin accessibility landscape of primary human cancers. Science. 2018;362(6413).
   PubMed Web of Science ®Google Scholar
• Lara-Astiaso D, Weiner A, Lorenzo-Vivas E, et al. Immunogenetics. Chromatin state dynamics during blood formation. Science. 2014;345(6199):943–949. DOI:10.1126/science.1256271
   PubMed Web of Science ®Google Scholar
• Zheng S, Papalexi E, Butler A, et al. Molecular transitions in early progenitors during human cord blood hematopoiesis. Mol Syst Biol. 2018;14(3):e8041.
   PubMed Web of Science ®Google Scholar
• Li X, Chen Y, Fu C, et al. Characterization of epigenetic and transcriptional landscape in infantile hemangiomas with ATAC-seq and RNA-seq. Epigenomics. 2020;12(11):893–905. DOI:10.2217/epi-2020-0060
   PubMed Web of Science ®Google Scholar
• de la Torre-Ubieta L, Stein JL, Won H, et al. The dynamic landscape of open chromatin during human cortical neurogenesis. Cell. 2018;172(1–2):289–304.e18.
   PubMed Web of Science ®Google Scholar
• Minnoye L, Marinov GK, Krausgruber T, et al. Chromatin accessibility profiling methods. Nat Rev Dis Primers. 2021;1(1):10. DOI:10.1038/s43586-020-00008-9
   Google Scholar
• Rühm W, Woloschak GE, Shore RE, et al. Dose and dose-rate effects of ionizing radiation: a discussion in the light of radiological protection. Radiat Environ Biophys. 2015;54(4):379–401. DOI:10.1007/s00411-015-0613-6
   PubMed Web of Science ®Google Scholar
• Lomax ME, Folkes LK, O’neill P. Biological consequences of radiation-induced DNA damage: relevance to radiotherapy. Clin Oncol. 2013;25(10):578–585.
   PubMed Web of Science ®Google Scholar
• Dabin J, Fortuny A, Polo Sophie E. Epigenome maintenance in response to DNA damage. Molecular Cell. 2016;62(5):712–727.
   PubMed Web of Science ®Google Scholar
• Brambilla F, Garcia-Manteiga JM, Monteleone E, et al. Nucleosomes effectively shield DNA from radiation damage in living cells. Nucleic Acids Res. 2020;48(16):8993–9006. PubMed PMID: rayyan-676545021.
   PubMed Web of Science ®Google Scholar
• Elia MC, Bradley MO. Influence of chromatin structure on the induction of DNA double strand breaks by ionizing radiation. Cancer Res. 1992;52(6): 1580–1586. PubMed PMID: 1540967.
   PubMed Web of Science ®Google Scholar
• Falk M, Lukášová E, Kozubek S. Chromatin structure influences the sensitivity of DNA to γ-radiation. Biochim Biophys Acta, Mol Cell Res. 2008;1783(12):2398–2414.
   PubMed Web of Science ®Google Scholar
• Takata H, Hanafusa T, Mori T, et al. Chromatin compaction protects genomic DNA from radiation damage. PLoS ONE. 2013;8(10):e75622. DOI:10.1371/journal.pone.0075622
   PubMed Web of Science ®Google Scholar
• Healy S, Khan P, Davie JR. Immediate early response genes and cell transformation. Pharmacol Ther. 2013;137(1):64–77.
   PubMed Web of Science ®Google Scholar
• Sherman ML, Datta R, Hallahan DE, et al. Ionizing radiation regulates expression of the c-jun protooncogene. Proc Natl Acad Sci USA. 1990;87(15):5663–5666.
   PubMed Web of Science ®Google Scholar
• Bejjani F, Evanno E, Zibara K, et al. The AP-1 transcriptional complex: local switch or remote command? Biochim Biophys Acta Rev Cancer. 2019;1872(1):11–23.
   PubMed Web of Science ®Google Scholar
• Atlasi Y, Stunnenberg HG. The interplay of epigenetic marks during stem cell differentiation and development. Nat Rev Genet. 2017;18(11):643–658.
   PubMed Web of Science ®Google Scholar
• Bernstein BE, Mikkelsen TS, Xie X, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125(2):315–326. DOI:10.1016/j.cell.2006.02.041
   PubMed Web of Science ®Google Scholar
• Ilnytskyy Y, Kovalchuk O. Non-targeted radiation effects-an epigenetic connection. Mutat Res. 2011;714(1–2):113–125.
   PubMed Web of Science ®Google Scholar
• Lindeman LC, Kamstra JH, Ballangby J, et al. Gamma radiation induces locus specific changes to histone modification enrichment in zebrafish and Atlantic salmon. PLoS ONE. 2019;14(2):e0212123. PubMed PMID: rayyan-676545106.
   PubMed Web of Science ®Google Scholar
• Kovalchuk O, Burke P, Besplug J, et al. Methylation changes in muscle and liver tissues of male and female mice exposed to acute and chronic low-dose X-ray-irradiation. Mutat Res. 2004;548(1–2):75–84.
   PubMed Web of Science ®Google Scholar
• Bahrami S, Drabløs F. Gene regulation in the immediate-early response process. Adv Biol Regul. 2016;62:37–49.
   PubMedGoogle Scholar
• Rye M, Sandve GK, Daub CO, et al. Chromatin states reveal functional associations for globally defined transcription start sites in four human cell lines. BMC Genomics. 2014;15(1):120. DOI:10.1186/1471-2164-15-120
   PubMedGoogle Scholar
• Chereji RV, Eriksson PR, Ocampo J, et al. Accessibility of promoter DNA is not the primary determinant of chromatin-mediated gene regulation. Genome Res. 2019;29(12):1985–1995.
   PubMed Web of Science ®Google Scholar
• Zhu W, Zhang X, Yu M, et al. Radiation-induced liver injury and hepatocyte senescence. Cell Death Discovery. 2021;7(1):244.
   PubMed Web of Science ®Google Scholar
• Baratta JL, Ngo A, Lopez B, et al. Cellular organization of normal mouse liver: a histological, quantitative immunocytochemical, and fine structural analysis. Histochem Cell Biol. 2009;131(6):713–726.
   PubMed Web of Science ®Google Scholar