462
Views
7
CrossRef citations to date
0
Altmetric
Original Articles

Fractionated exposure to low doses of ionizing radiation results in accumulation of DNA damage in mouse spleen tissue and activation of apoptosis in a p53/Atm-independent manner

, &
Pages 148-155 | Received 30 Dec 2015, Accepted 28 Aug 2016, Published online: 19 Oct 2016

References

  • Barcellos-Hoff MH, Brenner DJ, Brooks AL, Formenti S, Hlatky L, Locke PA, Shore R, Tenforde T, Travis EL, Williams J. 2011. Low-dose radiation knowledge worth the cost. Science. 332:305–306.
  • Basnakian AG, James SJ. 1996. Quantification of 3′OH DNA breaks by random oligonucleotide-primed synthesis (ROPS) assay. DNA Cell Biol. 15:255–262.
  • Bulavin DV, Amundson SA, Fornace AJ. 2002. p38 and Chk1 kinases: different conductors for the G(2)/M checkpoint symphony. Curr Opin Genet Dev. 12:92–97.
  • Calabrese EJ, O’Connor MK. 2014. Estimating risk of low radiation doses – a critical review of the BEIR VII report and its use of the linear no-threshold (LNT) hypothesis. Radiat Res. 182:463–474.
  • Elmore S. 2007. Apoptosis: a review of programmed cell death. Toxicol Pathol. 35:495–516.
  • Georgakilas A. 2011. Detection of clustered DNA lesions: biological and clinical applications. World J Biol Chem. 2:173–176.
  • Hyun SJ, Yoon MY, Kim TH, Kim JH. 1997. Enhancement of mitogen-stimulated proliferation of low dose radiation-adapted mouse splenocytes. Anticancer Res. 17:225–229.
  • Iliakis G, Wang Y, Guan J, Wang H. 2003. DNA damage checkpoint control in cells exposed to ionizing radiation. Oncogene. 22:5834–5847.
  • Ilnytskyy Y, Kovalchuk O. 2011. Non-targeted radiation effects – an epigenetic connection. Mutat Res. 714:113–125.
  • Jeggo P, Löbrich M. 2006. Radiation-induced DNA damage responses. Radiat Prot Dosimetry. 122:124–127.
  • Kamiya K, Ozasa K, Akiba S, Niwa O, Kodama K, Takamura N, Zaharieva EK, Kimura Y, Wakeford R. 2015. Long-term effects of radiation exposure on health. Lancet. 386:469–478.
  • Klokov D, Macphail SM, Banath JP, Byrne JP, Olive PL. 2006. Phosphorylated histone H2AX in relation to cell survival in tumor cells and xenografts exposed to single and fractionated doses of X-rays. Radiother Oncol. 80:223–229.
  • Koturbash I, Kutanzi K, Hendrickson K, Rodriguez-Juarez R, Kogosov D, Kovalchuk O. 2008a. Radiation-induced bystander effects in vivo are sex specific. Mutat Res. 642:28–36.
  • Koturbash I, Loree J, Kutanzi K, Koganow C, Pogribny I, Kovalchuk O. 2008b. In vivo bystander effect: cranial X-irradiation leads to elevated DNA damage, altered cellular proliferation and apoptosis, and increased p53 levels in shielded spleen. Int J Radiat Oncol Biol Phys. 70:554–562.
  • Koturbash I, Zemp FJ, Kutanzi K, Luzhna L, Loree J, Kolb B, Kovalchuk O. 2008c. Sex-specific microRNAome deregulation in the shielded bystander spleen of cranially exposed mice. Cell Cycle. 7:1658–1667.
  • Kovalchuk O, Baulch JE. 2008. Epigenetic changes and nontargeted radiation effects – is there a link? Environ Mol Mutagen. 49:16–25.
  • Langie SA, Koppen G, Desaulniers D, Al-Mulla F, Al-Temaimi R, Amedei A, Azqueta A, Bisson WH, Brown DG, Brunborg G, et al. 2015. Causes of genome instability: the effect of low dose chemical exposures in modern society. Carcinogenesis. 36(Suppl. 1):S61–S88.
  • Laposa RR, Huang EJ, Cleaver JE. 2007. Increased apoptosis, p53 up-regulation, and cerebellar neuronal degeneration in repair-deficient Cockayne syndrome mice. Proc Natl Acad Sci USA. 104:1389–1394.
  • Li W, Wang G, Cui J, Xue L, Cai L. 2004. Low-dose radiation (LDR) induces hematopoietic hormesis: LDR-induced mobilization of hematopoietic progenitor cells into peripheral blood circulation. Exp Hematol. 32:1088–1096.
  • Majer M, Knezevic Z, Saveta M. 2014. Current trends in estimating risk of cancer from exposure to low doses of ionising radiation. Arh Hig Rada Toksikol. 65:251–257.
  • Martin LM, Marples B, Lynch TH, Hollywood D, Marignol L. 2013. Exposure to low dose ionising radiation: molecular and clinical consequences. Cancer Lett. 338:209–218.
  • Merrifield M, Kovalchuk O. 2013. Epigenetics in radiation biology: a new research frontier. Front Genet. 4:40.
  • Mikhailov A, Shinohara M, Rieder CL. 2005. The p38-mediated stress-activated checkpoint. A rapid response system for delaying progression through antephase and entry into mitosis. Cell Cycle. 4:57–62.
  • Moertl S, Karras GI, Wismuller T, Ahne F, Eckardt-Schupp F. 2008. Regulation of double-stranded DNA gap repair by the RAD6 pathway. DNA Repair (Amst). 7:1893–1906.
  • Morgan WF. 2003a. Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation? Oncogene. 22:7094–7099.
  • Morgan WF. 2003b. Non-targeted and delayed effects of exposure to ionizing radiation: I. Radiation-induced genomic instability and bystander effects in vitro. Radiat Res. 159:567–580.
  • Morgan WF. 2003c. 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. Radiat Res. 159:581–596.
  • Mothersill C, Seymour CB. 2004. Radiation-induced bystander effects – implications for cancer. Nat Rev Cancer. 4:158–164.
  • Pearce AK, Humphrey TC. 2001. Integrating stress-response and cell-cycle checkpoint pathways. Trends Cell Biol. 11:426–433.
  • 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. 3:553–561.
  • Pouliliou S, Koukourakis MI. 2014. Gamma histone 2AX (gamma-H2AX) as a predictive tool in radiation oncology. Biomarkers. 19:167–180.
  • Redon CE, Dickey JS, Bonner WM, Sedelnikova OA. 2009. gamma-H2AX as a biomarker of DNA damage induced by ionizing radiation in human peripheral blood lymphocytes and artificial skin. Adv Space Res. 43:1171–1178.
  • Saito A, Yamauchi H, Ishida Y, Ohmachi Y, Nakayama H. 2008. Defect of the cerebellar vermis induced by prenatal gamma-ray irradiation in radiosensitive BALB/c mice. Histol Histopathol. 23:953–964.
  • Seymour CB, Mothersill C. 2000. Relative contribution of bystander and targeted cell killing to the low-dose region of the radiation dose-response curve. Radiat Res. 153:508–511.
  • Suchowerska N, Ebert MA, Zhang M, Jackson M. 2005. In vitro response of tumour cells to non-uniform irradiation. Phys Med Biol. 50:3041–3051.
  • Tice RR, Strauss GH. 1995. The single cell gel electrophoresis/comet assay: a potential tool for detecting radiation-induced DNA damage in humans. Stem Cells. 13(Suppl. 1):207–214.
  • Vyas D, Robertson CM, Stromberg PE, Martin JR, Dunne WM, Houchen CW, Barrett TA, Ayala A, Perl M, Buchman TG, Coopersmith CM. 2007. Epithelial apoptosis in mechanistically distinct methods of injury in the murine small intestine. Histol Histopathol. 22:623–630.
  • Xue L, Furusawa Y, Yu D. 2015. ATR signaling cooperates with ATM in the mechanism of low dose hypersensitivity induced by carbon ion beam. DNA Repair (Amst). 34:1–8.
  • Xue L, Yu D, Furusawa Y, Cao J, Okayasu R, Fan S. 2009. ATM-dependent hyper-radiosensitivity in mammalian cells irradiated by heavy ions. Int J Radiat Oncol Biol Phys. 75:235–243.
  • Yoshida N, Imada H, Kunugita N, Norimura T. 1993. Low dose radiation-induced adaptive survival response in mouse spleen T-lymphocytes in vivo. J Radiat Res (Tokyo). 34:269–276.

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.