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Original Articles

Early- and late-occurring damage in bone marrow cells of male CBA/Ca mice exposed whole-body to 1 GeV/n 48Ti ions

ORCID Icon, , , , &
Pages 517-528 | Received 19 Mar 2020, Accepted 21 Jan 2021, Published online: 08 Mar 2021

References

  • Acharya MM, Baddour AAD, Kawashita T, Allen BD, Syage AR, Nguyen TH, Yoon N, Giedzinski E, Yu L, Parihar VK, et al. 2017. Epigenetic determinants of space radiation-induced cognitive dysfunction. Sci Rep. 7:42885–42885.
  • Baulch JE. 2019. Radiation-induced genomic instability, epigenetic mechanisms and the mitochondria: a dysfunctional ménage a trois? Int J Radiat Biol. 95:516–525.
  • Becker BV, Kaatsch L, Obermair R, Schrock G, Port M, Ullmann R. 2019. X-ray irradiation induces subtle changes in the genome-wide distribution of DNA hydroxymethylation with opposing trends in genic and intergenic regions. Epigenetics. 14:81–93.
  • Bonassi S, Znaor A, Ceppi M, Lando C, Chang WP, Holland N, Kirsch-Volders M, Zeiger E, Ban S, Barale R, et al. 2007. An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans. Carcinogenesis. 28:625–631.
  • Booth MJ, Ost TW, Beraldi D, Bell NM, Branco MR, Reik W, Balasubramanian S. 2013. Oxidative bisulfite sequencing of 5-methylcytosine and 5-hydroxymethylcytosine. Nat Protoc. 8:1841–1851.
  • Buscarlet M, Tessier A, Provost S, Mollica L, Busque L. 2016. Human blood cell levels of 5-hydroxymethylcytosine (5hmC) decline with age, partly related to acquired mutations in TET2. Exp Hematol. 44:1072–1084.
  • Ceppi M, Gallo F, Bonassi S. 2011. Study design and statistical analysis of data in human population studies with the micronucleus assay. Mutagenesis. 26:247–252.
  • Channarayappa Nath J, Ong T. 1992. Immunofluorescent staining of kinetochores in micronucleus for detection of aneuploidy inducing agents. J Tissue Cult Methods. 14:125–131.
  • Cucinotta FA. 2014. Space radiation risks for astronauts on multiple international space station missions. PLoS One. 9:e96099.
  • Dainiak N. 2002. Hematologic consequences of exposure to ionizing radiation. Exp Hematol. 30:513–528.
  • Dzitoyeva S, Chen H, Manev H. 2012. Effect of aging on 5-hydroxymethylcytosine in brain mitochondria. Neurobiol Aging. 33:2881–2891.
  • French JE, Gatti DM, Morgan DL, Kissling GE, Shockley KR, Knudsen GA, Shepard KG, Price HC, King D, Witt KL, et al. 2015. Diversity Outbred mice identify population-based exposure thresholds and genetic factors that influence benzene-induced genotoxicity. Environ Health Perspect. 123:237–245.
  • Gudi R, S. Sandhu S, Athwal RS. 1990. Kinetochore identification in micronuclei in mouse bone-marrow erythrocytes: an assay for the detection of aneuploidy-inducing agents. Mutat Res. 234:263–268.
  • Hahn MA, Li AX, Wu X, Pfeifer GP. 2015. Single base resolution analysis of 5-methylcytosine and 5-hydroxymethylcytosine by RRBS and TAB-RRBS. Methods Mol Biol. 1238:273–287.
  • Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell. 144:646–674.
  • Hayashi M, Sofuni T, Ishidate M. 1983. An application of Acridine Orange fluorescent staining to the micronucleus test. Mutat Res. 120:241–247.
  • Hayes J, Doherty AT, Adkins DJ, Oldman K, O'Donovan MR. 2009. The rat bone marrow micronucleus test-study design and statistical power. Mutagenesis. 24:419–424.
  • Heddle JA, Hite M, Kirkhart B, Mavournin K, MacGregor JT, Newell GW, Salamone MF. 1983. The induction of micronuclei as a measure of genotoxicity. A report of the United States Environmental Protection Agency Gene-Tox Program. Mutat Res. 123:61–118.
  • Hryciw G, Grygoryev D, Lasarev M, Ohlrich A, Dan C, Madhira R, Eckelmann B, Gauny S, Kronenberg A, Turker MS. 2015. Accelerated 48Ti ions induce autosomal mutations in mouse kidney epithelium at low dose and fluence. Radiat Res. 184:367–377.
  • 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. 17:10.
  • Jain MR, Li M, Chen W, Liu T, de Toledo SM, Pandey BN, Li H, Rabin BM, Azzam EI. 2011. In vivo space radiation-induced non-targeted responses: late effects on molecular signaling in mitochondria. Curr Mol Pharmacol. 4:106–114.
  • Jangiam W, Tungjai M, Rithidech K. 2015. Induction of chronic oxidative stress, chronic inflammation and aberrant patterns of DNA methylation in the liver of titanium-exposed CBA/CaJ mice. Int J Radiat Biol. 91:389–398.
  • Jangiam W, Udomtanakunchai C, Reungpatthanaphong P, Tungjai M, Honikel L, Gordon CR, Rithidech KN. 2018. Late effects of low-dose radiation on the bone marrow, lung, and testis collected from the same exposed BALB/cJ mice. Dose Response. 16:1559325818815031.
  • Jiang D, Wei S, Chen F, Zhang Y, Li J. 2017. TET3-mediated DNA oxidation promotes ATR-dependent DNA damage response. EMBO Rep. 18:781–796.
  • Kafer GR, Li X, Horii T, Suetake I, Tajima S, Hatada I, Carlton PM. 2016. 5-Hydroxymethylcytosine marks sites of DNA damage and promotes genome stability. Cell Rep. 14:1283–1292.
  • Kharat SS, Ding X, Swaminathan D, Suresh A, Singh M, Sengodan SK, Burkett S, Marks H, Pamala C, He Y, et al. 2020. Degradation of 5hmC-marked stalled replication forks by APE1 causes genomic instability. Sci Signal. 13:eaba8091.
  • Kissling GE, Dertinger SD, Hayashi M, MacGregor JT. 2007. Sensitivity of the erythrocyte micronucleus assay: dependence on number of cells scored and inter-animal variability. Mutat. Res. 634:235–240.
  • Kochmanski J, Marchlewicz EH, Cavalcante RG, Sartor MA, Dolinoy DC. 2018. Age-related epigenome-wide DNA methylation and hydroxymethylation in longitudinal mouse blood. Epigenetics. 13:779–792.
  • Kriaucionis S, Heintz N. 2009. The nuclear DNA base 5-hydroxymethylcytosine is present in purkinje neurons and the brain. Science. 324:929–930.
  • Krishna G, Hayashi M. 2000. In vivo rodent micronucleus assay: protocol, conduct and data interpretation. Mutat Res. 455:155–166.
  • Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, et al. 2007. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature. 448:553–560.
  • Moore F. 1992. Radiation burdens for humans on prolonged exomagnetospheric voyages. Faseb J. 6:2338–2343.
  • Morgan WF. 2003. Non-targeted and delayed effects of exposure to ionizing radiation: II. Radiation-induced genomic instability and bystander effects in vivo, clastogenic and transgenerational effects. Radiat Res. 159:581–596.
  • Norbury JW, Schimmerling W, Slaba TC, Azzam EI, Badavi FF, Baiocco G, Benton E, Bindi V, Blakely EA, Blattnig SR, et al. 2016. Galactic cosmic ray simulation at the NASA Space Radiation Laboratory. Life Sci Space Res (Amst). 8:38–51.
  • OECD. 2014. OECD guideline for the testing of chemicals; Mammalian erythrocytes micronucelus Test. OECD Environment, Health and Safety Publications (EHS), Series on Testing and Assessmnet. Paris (France): OECD.
  • Parihar VK, Allen BD, Caressi C, Kwok S, Chu E, Tran KK, Chmielewski NN, Giedzinski E, Acharya MM, Britten RA, et al. 2016. Cosmic radiation exposure and persistent cognitive dysfunction. Sci Rep. 6:34774.
  • Pawelec G, Goldeck D, Derhovanessian E. 2014. Inflammation, ageing and chronic disease. Curr Opin Immunol. 29:23–28.
  • Pfeifer GP, Xiong W, Hahn MA, Jin SG. 2014. The role of 5-hydroxymethylcytosine in human cancer. Cell Tissue Res. 356:631–641.
  • Prasanna PGS, Moroni M, Pellmar TC. 2010. Triage dose assessment for partial-body exposure: dicentric analysis. Health Phys. 98:244–251.
  • Rabin BM, Shukitt-Hale B, Joseph JA, Carrihill-Knoll KL, Carey AN, Cheng V. 2007. Relative effectiveness of different particles and energies in disrupting behavioral performance. Radiat Environ Biophys. 46:173–177.
  • Rithidech K, Au WW, Ramanujam VM, Whorton EB Jr, Legator MS. 1988. Persistence of micronuclei in peripheral blood normochromatic erythrocytes of subchronically benzene-treated male mice. Environ Mol Mutagen. 12:319–329.
  • Rithidech K, Bond VP, Cronkite EP, Thompson MH, Bullis JE. 1995. Hypermutability of mouse chromosome 2 during the development of x-ray-induced murine myeloid leukemia. Proc Natl Acad Sci U S A. 92:1152–1156.
  • Rithidech K, Reungpatthanaphong P, Honikel L, Rusek A, Simon S. 2010. Dose-rate effects of protons on in vivo activation of nuclear factor-kappa B and cytokines in mouse bone marrow cells. Radiat Environ Biophys. 49:405–419.
  • Rithidech K, Supanpaiboon W, Honikel L, Whorton EB. 2007. Analysis of chromosomal damage after in vivo exposure to 56Fe ions by means of mFISH and micronucleus methods. Adv Space Res. 40:491–500.
  • Rithidech K, Tungjai M, Arbab E, Simon SR. 2005. Activation of NF-kappaB in bone marrow cells of BALB/cJ mice following exposure in vivo to low doses of (137)Cs gamma-rays. Radiat Environ Biophys. 44:139–143.
  • Rithidech K, Tungjai M, Jangiam W, Honikel L, Gordon C, Lai X, Witzmann F. 2015a. Proteomic profiling of hematopoietic stem/progenitor cells after a whole body exposure of CBA/CaJ mice to titanium (48Ti) ions. Proteomes. 3:132–158.
  • Rithidech K, Udomtanakunchai C, Honikel L, Whorton E. 2013a. Lack of genomic instability in bone marrow cells of SCID mice exposed whole-body to low-dose radiation. Int J Environ Res Public Health. 10:1356–1377.
  • Rithidech KN, Golightly M, Whorton E. 2008. Analysis of cell cycle in mouse bone marrow cells following acute in vivo exposure to 56Fe ions. JRR. 49:437–443.
  • Rithidech KN, Honikel LM, Reungpathanaphong P, Tungjai M, Jangiam W, Whorton EB. 2015b. Late-occurring chromosome aberrations and global DNA methylation in hematopoietic stem/progenitor cells of CBA/CaJ mice exposed to silicon (28Si) ions. Mutat Res. 781:22–31.
  • Rithidech KN, Honikel LM, Reungpatthanaphong P, Tungjai M, Golightly M, Whorton EB. 2013b. Effects of 100 MeV protons delivered at 0.5 or 1 cGy/min on the in vivo induction of early and delayed chromosomal damage. Mutat Res. 756:127–140.
  • Rithidech KN, Jangiam W, Tungjai M, Gordon C, Honikel L, Whorton EB. 2016a. Induction of chronic inflammation and altered levels of DNA hydroxymethylation in somatic and germinal tissues of CBA/CaJ mice exposed to 48Ti Ions. Front Oncol. 6:155–155.
  • Rithidech KN, Jangiam W, Tungjai M, Gordon C, Honikel L, Whorton EB. 2016b. Induction of chronic inflammation and altered levels of DNA hydroxymethylation in somatic and germinal tissues of CBA/CaJ mice exposed to (48)Ti ions. Front Oncol. 6:155.
  • Rithidech KN, Supanpaiboon W, Honikel L, Whorton EB. 2009. Induction of genomic instability after an acute whole-body exposure of mice to 56Fe ions. Adv. in Space Res. 44:895–906.
  • Rithidech KN, Udomtanakunchai C, Honikel LM, Whorton EB. 2012. No evidence for the in vivo induction of genomic instability by low doses of 137Cs gamma rays in bone marrow cells of BALB/CJ and C57BL/6J mice. Dose Response. 10:11–36.
  • Rosin MP, German J. 1985. Evidence for chromosome instability in vivo in Bloom syndrome: increased numbers of micronuclei in exfoliated cells. Hum Genet. 71:187–191.
  • Rothfuss A, Schutz P, Bochum S, Volm T, Eberhardt E, Kreienberg R, Vogel W, Speit G. 2000. Induced micronucleus frequencies in peripheral lymphocytes as a screening test for carriers of a BRCA1 mutation in breast cancer families. Cancer Res. 60:390–394.
  • Rudd NL, Hoar DI, Greentree CL, Dimnik LS, Hennig UG. 1988. Micronucleus assay in human fibroblasts: a measure of spontaneous chromosomal instability and mutagen hypersensitivity. Environ Mol Mutagen. 12:3–13.
  • Schlegel R, MacGregor JT. 1984. The persistence of micronucleated erythrocytes in the peripheral circulation of normal and splenectomized Fischer 344 rats: implications for cytogenetic screening. Mutat Res. 127:169–174.
  • Schmid W. 1975. The micronucleus test. Mutat Res. 31:9–15.
  • Scott D, Barber JB, Levine EL, Burrill W, Roberts SA. 1998. Radiation-induced micronucleus induction in lymphocytes identifies a high frequency of radiosensitive cases among breast cancer patients: a test for predisposition? Br J Cancer. 77:614–620.
  • Shukla A, Sehgal M, Singh TR. 2015. Hydroxymethylation and its potential implication in DNA repair system: a review and future perspectives. Gene. 564:109–118.
  • Simonsen LC, Slaba TC, Guida P, Rusek A. 2020. NASA’s first ground-based Galactic Cosmic Ray Simulator: enabling a new era in space radiobiology research. PLoS Biol. 18:e3000669.
  • Slapšytė G, Jankauskienė A, Mierauskienė J, Lazutka JR. 2002. Cytogenetic analysis of peripheral blood lymphocytes of children treated with nitrofurantoin for recurrent urinary tract infection. Mutagenesis. 17:31–35.
  • Snedecor GW, Cochran WG. 1989. Statistical methods. 8th ed. Ames (IA): Iowa State University Press.
  • Soeteman-Hernández LG, Johnson GE, Slob W. 2016. Estimating the carcinogenic potency of chemicals from the in vivo micronucleus test. Mutagenesis. 31:347–358.
  • Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, et al. 2009. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 324:930–935.
  • Tice RR, Erexson GL, Shelby MD. 1990. The induction of micronucleated polychromatic erythrocytes in mice using single and multiple treatments. Mutat Res. 234:187–193.
  • Toraño EG, Bayón GF, del Real Á, Sierra MI, García MG, Carella A, Belmonte T, Urdinguio RG, Cubillo I, García-Castro J, et al. 2016. Age-associated hydroxymethylation in human bone-marrow mesenchymal stem cells. J Transl Med. 14:207.
  • Tungjai M, Whorton E, Rithidech K. 2013. Persistence of apoptosis and inflammatory responses in the heart and bone marrow of mice following whole-body exposure to 28Silicon (28Si) ions. Radiat Environ Biophys. 52:339–350.
  • Van Putten LM, Croon F. 1958. The life span of red cells in the rat and the mouse as determined by labeling with DFP32 in vivo. Blood. 13:789–794.
  • Whorton EB. 1985. Some experimental design and analysis considerations for cytogenetics studies. Environ Mutagen. 7 :9–15.
  • Witt KL, Livanos E, Kissling GE, Torous DK, Caspary W, Tice RR, Recio L. 2008. Comparison of flow cytometry- and microscopy-based methods for measuring micronucleated reticulocyte frequencies in rodents treated with nongenotoxic and genotoxic chemicals. Mutat Res. 649:101–113.
  • Yu M, Hon GC, Szulwach KE, Song CX, Jin P, Ren B, He C. 2012. Tet-assisted bisulfite sequencing of 5-hydroxymethylcytosine. Nat Protoc. 7:2159–2170.

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