Impact of medical imaging on the epigenome – low-dose exposure in the course of computed tomography does not induce detectable changes of DNA-methylation profiles in peripheral blood cells

References

• Andrews S. 2010. FastQC: a quality control tool for high throughput sequence data. Cambridge (UK): Babraham Bioinformatics, Babraham Institute.
   Google Scholar
• Antwih DA, Gabbara KM, Lancaster WD, Ruden DM, Zielske SP. 2013. Radiation-induced epigenetic DNA methylation modification of radiation-response pathways. Epigenetics. 8(8):839–848.
   PubMed Web of Science ®Google Scholar
• Aypar U, Morgan WF, Baulch JE. 2011. Radiation-induced epigenetic alterations after low and high LET irradiations. Mutat Res. 707(1–2):24–33.
   PubMed Web of Science ®Google Scholar
• Boo SH, Kim YK. 2020. The emerging role of RNA modifications in the regulation of mRNA stability. Exp Mol Med. 52(3):400–408.
   PubMed Web of Science ®Google Scholar
• Charles MW. 2008. ICRP Publication 103: Recommendations of the ICRP. Radiat Prot Dosim. 129(4):500–507.
   Google Scholar
• Goetz W, Morgan MN, Baulch JE. 2011. The effect of radiation quality on genomic DNA methylation profiles in irradiated human cell lines. Radiat Res. 175(5):575–587.
   PubMed Web of Science ®Google Scholar
• Hall EJ, Brenner DJ. 2008. Cancer risks from diagnostic radiology. Br J Radiol. 81(965):362–378.
   PubMed Web of Science ®Google Scholar
• Hansen KD, Langmead B, Irizarry RA. 2012. BSmooth: from whole genome bisulfite sequencing reads to differentially methylated regions. Genome Biol. 13(10):R83.
   PubMed Web of Science ®Google Scholar
• Impey S, Pelz C, Tafessu A, Marzulla T, Turker MS, Raber J. 2016. Proton irradiation induces persistent and tissue-specific DNA methylation changes in the left ventricle and hippocampus. BMC Genomics. 17(1):1.
   PubMed Web of Science ®Google Scholar
• Jones PA. 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet. 13(7):484–492.
   PubMed Web of Science ®Google Scholar
• Kaatsch HL, Becker BV, Schüle S, Ostheim P, Nestler K, Jakobi J, Schäfer B, Hantke T, Brockmann MA, Abend M, et al. 2021. Gene expression changes and DNA damage after ex vivo exposure of peripheral blood cells to various CT photon spectra. Sci Rep. 11(1):12060.
   PubMed Web of Science ®Google Scholar
• Kaatsch HL, Majewski M, Schrock G, Obermair R, Seidel J, Nestler K, Abend M, Waldeck S, Port M, Ullmann R, et al. 2020. CT irradiation-induced changes of gene expression within peripheral blood cells. Health Phys. 119(1):44–51.
   PubMed Web of Science ®Google Scholar
• Kalinich JF, Catravas GN, Snyder SL. 1989. The effect of γ radiation on DNA methylation. Radiat Res. 117(2):185–197.
   PubMed Web of Science ®Google Scholar
• Kamstra JH, Hurem S, Martin LM, Lindeman LC, Legler J, Oughton D, Salbu B, Brede DA, Lyche JL, Aleström P. 2018. Ionizing radiation induces transgenerational effects of DNA methylation in zebrafish. Sci Rep. 8(1):15373.
   PubMed Web of Science ®Google Scholar
• 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. Mutat Res. 597(1):87–97.
   PubMed Web of Science ®Google Scholar
• Kim JG, Park MT, Heo K, Yang KM, Yi JM. 2013. Epigenetics meets radiation biology as a new approach in cancer treatment. Int J Mol Sci. 14(7):15059–15073.
   PubMed Web of Science ®Google Scholar
• Korthauer K, Chakraborty S, Benjamini Y, Irizarry RA. 2019. Detection and accurate false discovery rate control of differentially methylated regions from whole genome bisulfite sequencing. Biostatistics. 20(3):367–383.
   PubMed Web of Science ®Google Scholar
• 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? Biochem Biophys Res Commun. 337(2):526–533.
   PubMed Web of Science ®Google Scholar
• Krueger F, Andrews SR. 2011. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics. 27(11):1571–1572.
   PubMed Web of Science ®Google Scholar
• Krueger F. 2015. Trim galore. A wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files 516, 517
   Google Scholar
• Kumar A, Rai PS, Upadhya R, Vishwanatha Shama Prasada K, Satish Rao B, Satyamoorthy K. 2011. γ-radiation induces cellular sensitivity and aberrant methylation in human tumor cell lines. Int J Radiat Biol. 87(11):1086–1096.
   PubMed Web of Science ®Google Scholar
• Laanen P, Saenen E, Mysara M, Van de Walle J, Van Hees M, Nauts R, Van Nieuwerburgh F, Voorspoels S, Jacobs G, Cuypers A, et al. 2021. Changes in DNA methylation in Arabidopsis thaliana plants exposed over multiple generations to gamma radiation. Front Plant Sci. 12:611783.
   PubMed Web of Science ®Google Scholar
• Lee Y, Kim YJ, Choi YJ, Lee JW, Lee S, Cho YH, Chung HW. 2015. Radiation-induced changes in DNA methylation and their relationship to chromosome aberrations in nuclear power plant workers. Int J Radiat Biol. 91(2):142–149.
   PubMed Web of Science ®Google Scholar
• Li E, Beard C, Jaenisch R. 1993. Role for DNA methylation in genomic imprinting. Nature. 366(6453):362–365.
   PubMed Web of Science ®Google Scholar
• Li H. 2013. Seqtk: a fast and lightweight tool for processing FASTA or FASTQ sequences; [accessed 2021 Apr]. https://github.com/lh3/seqtk/.
   Google Scholar
• Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA, Johnson ND, Lucero J, Huang Y, Dwork AJ, Schultz MD, et al. 2013. Global epigenomic reconfiguration during mammalian brain development. Science. 341(6146):1237905.
   PubMed Web of Science ®Google Scholar
• Maierhofer A, Flunkert J, Dittrich M, Müller T, Schindler D, Nanda I, Haaf T. 2017. Analysis of global DNA methylation changes in primary human fibroblasts in the early phase following X-ray irradiation. PLoS One. 12(5):e0177442.
   PubMed Web of Science ®Google Scholar
• Mettler FA, Mahesh M, Bhargavan-Chatfield M, Chambers CE, Elee JG, Frush DP, Miller DL, Royal HD, Milano MT, Spelic DC, et al. 2020. Patient exposure from radiologic and nuclear medicine procedures in the United States: procedure volume and effective dose for the period 2006–2016. Radiology. 295(2):418–427.
   PubMed Web of Science ®Google Scholar
• Miousse IR, Kutanzi KR, Koturbash I. 2017. Effects of ionizing radiation on DNA methylation: from experimental biology to clinical applications. Int J Radiat Biol. 93(5):457–469.
   PubMed Web of Science ®Google Scholar
• Nekolla E, Schegerer A, Griebel J, Brix G. 2017. Frequency and doses of diagnostic and interventional X-ray applications: trends between 2007 and 2014. Radiologe. 57(7):555–562.
   PubMed Web of Science ®Google Scholar
• Newman MR, Sykes PJ, Blyth BJ, Bezak E, Lawrence MD, Morel KL, Ormsby RJ. 2014. A single whole-body low dose X-irradiation does not affect L1, B1 and IAP repeat element DNA methylation longitudinally. PLOS One. 9(3):e93016.
   PubMed Web of Science ®Google Scholar
• 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(3):247–257.
   PubMed Web of Science ®Google Scholar
• Organisation for Economic Co-operation and Development. 2018. Computed tomography (CT) exams (indicator). [accessed on 2021 July 1 2021]. https://doi.org/https://doi.org/10.1787/3c994537-en.
   Google Scholar
• Park Y, Figueroa ME, Rozek LS, Sartor MA. 2014. MethylSig: a whole genome DNA methylation analysis pipeline. Bioinformatics. 30(17):2414–2422.
   PubMed Web of Science ®Google Scholar
• 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. Mol Cancer Res. 3(10):553–561.
   PubMed Web of Science ®Google Scholar
• Pogribny I, Raiche J, Slovack M, Kovalchuk O. 2004. Dose-dependence, sex- and tissue-specificity, and persistence of radiation-induced genomic DNA methylation changes. Biochem Biophys Res Commun. 320(4):1253–1261.
   PubMed Web of Science ®Google Scholar
• R Core Team. 2013. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.
   Google Scholar
• Riggs AD. 1975. X inactivation, differentiation, and DNA methylation. Cytogenet Cell Genet. 14(1):9–25.
   PubMedGoogle Scholar
• Robinson JT, Thorvaldsdóttir H, Winckler W, Guttman M, Lander ES, Getz G, Mesirov JP. 2011. Integrative genomics viewer. Nat Biotechnol. 29(1):24–26.
   PubMed Web of Science ®Google Scholar
• Schaefke B, Sun W, Li YS, Fang L, Chen W. 2018. The evolution of posttranscriptional regulation. Wiley Interdiscip Rev RNA. 9(5):e1485.
   PubMed Web of Science ®Google Scholar
• Slotkin RK, Martienssen R. 2007. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet. 8(4):272–285.
   PubMed Web of Science ®Google Scholar
• Thaulow J, Song Y, Lindeman LC, Kamstra JH, Lee Y, Xie L, Aleström P, Salbu B, Tollefsen KE. 2020. Epigenetic, transcriptional and phenotypic responses in Daphnia magna exposed to low-level ionizing radiation. Environ Res. 190:109930.
   PubMed Web of Science ®Google Scholar