Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2016, Article ID 1243527, 17 pages
http://dx.doi.org/10.1155/2016/1243527
Review Article

Current Evidence for Developmental, Structural, and Functional Brain Defects following Prenatal Radiation Exposure

Radiobiology Unit, Laboratory of Molecular and Cellular Biology, Institute for Environment, Health and Safety, Belgian Nuclear Research Centre, SCK•CEN, 2400 Mol, Belgium

Received 4 February 2016; Accepted 12 May 2016

Academic Editor: Feng Ru Tang

Copyright © 2016 Tine Verreet et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. N. Han, V. I. Kesic, K. Van Calsteren, S. Petkovic, and F. Amant, “Cancer in pregnancy: a survey of current clinical practice,” European Journal of Obstetrics & Gynecology and Reproductive Biology, vol. 167, no. 1, pp. 18–23, 2013. View at Publisher · View at Google Scholar
  2. R. Smith-Bindman, D. L. Miglioretti, and E. B. Larson, “Rising use of diagnostic medical imaging in a large integrated health system,” Health Affairs, vol. 27, no. 6, pp. 1491–1502, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Mercuri, T. Sheth, and M. K. Natarajan, “Radiation exposure from medical imaging: a silent harm?” Canadian Medical Association Journal, vol. 183, no. 4, pp. 413–414, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. O. Holmberg, J. Malone, M. Rehani, D. McLean, and R. Czarwinski, “Current issues and actions in radiation protection of patients,” European Journal of Radiology, vol. 76, no. 1, pp. 15–19, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Otake and W. J. Schull, “Radiation-related brain damage and growth retardation among the prenatally exposed atomic bomb survivors,” International Journal of Radiation Biology, vol. 74, no. 2, pp. 159–171, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. Y. Kameyama and M. Inouye, “Irradiation injury to the developing nervous system: mechanisms of neuronal injury,” NeuroToxicology, vol. 15, no. 1, pp. 75–80, 1994. View at Google Scholar · View at Scopus
  7. D. A. Giussani, “The vulnerable developing brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 7, pp. 2641–2642, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Rice and S. Barone Jr., “Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models,” Environmental Health Perspectives, vol. 108, supplement 3, pp. 511–533, 2000. View at Publisher · View at Google Scholar · View at Scopus
  9. J. L. Ronan, W. Wu, and G. R. Crabtree, “From neural development to cognition: unexpected roles for chromatin,” Nature Reviews Genetics, vol. 14, no. 5, pp. 347–359, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. L. Goldstein and D. P. Murphy, “Etiology of ill-health in children born after maternal pelvic irradiation. II. Defecitve children born after postconception pelvic irradiation,” American Journal of Roentgenology, vol. 22, pp. 322–331, 1929. View at Google Scholar
  11. D. L. Preston, H. Cullings, A. Suyama et al., “Solid cancer incidence in atomic bomb survivors exposed in utero or as young children,” Journal of the National Cancer Institute, vol. 100, no. 6, pp. 428–436, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. W. J. Schull and M. Otake, “Cognitive function and prenatal exposure to ionizing radiation,” Teratology, vol. 59, no. 4, pp. 222–226, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Otake, W. J. Schull, and S. Lee, “Threshold for radiation-related severe mental retardation in prenatally exposed A-bomb survivors: a re-analysis,” International Journal of Radiation Biology, vol. 70, no. 6, pp. 755–763, 1996. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Ikenoue, T. Ikeda, S. Ibara, M. Otake, and W. J. Schull, “Effects of environmental factors on perinatal outcome: neurological development in cases of intrauterine growth retardation and school performance of children perinatally exposed to ionizing radiation,” Environmental Health Perspectives, vol. 101, supplement 2, pp. 53–57, 1993. View at Google Scholar · View at Scopus
  15. K. S. Heiervang, S. Mednick, K. Sundet, and B. R. Rund, “The psychological well-being of Norwegian adolescents exposed in utero to radiation from the Chernobyl accident,” Child and Adolescent Psychiatry and Mental Health, vol. 5, article 12, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Busby, E. Lengfelder, S. Pflugbeil, and I. Schmitz-Feuerhake, “The evidence of radiation effects in embryos and fetuses exposed to Chernobyl fallout and the question of dose response,” Medicine, Conflict, and Survival, vol. 25, no. 1, pp. 20–40, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. K. S. Heiervang, S. Mednick, K. Sundet, and B. R. Rund, “Effect of low dose ionizing radiation exposure in utero on cognitive function in adolescence,” Scandinavian Journal of Psychology, vol. 51, no. 3, pp. 210–215, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. K. S. Heiervang, S. Mednick, K. Sundet, and B. R. Rund, “The Chernobyl accident and cognitive functioning: a study of norwegian adolescents exposed in utero,” Developmental Neuropsychology, vol. 35, no. 6, pp. 643–655, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. T. K. Loganovskaja and K. N. Loganovsky, “EEG, cognitive and psychopathological abnormalities in children irradiated in utero,” International Journal of Psychophysiology, vol. 34, no. 3, pp. 213–224, 1999. View at Publisher · View at Google Scholar · View at Scopus
  20. K. N. Loganovsky, T. K. Loganovskaja, S. Y. Nechayev, Y. Y. Antipchuk, and M. A. Bomko, “Disrupted development of the dominant hemisphere following prenatal irradiation,” Journal of Neuropsychiatry and Clinical Neurosciences, vol. 20, no. 3, pp. 274–291, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. A. I. Nyagu, K. N. Loganovsky, and T. K. Loganovskaja, “Psychophysiologic aftereffects of prenatal irradiation,” International Journal of Psychophysiology, vol. 30, no. 3, pp. 303–311, 1998. View at Publisher · View at Google Scholar · View at Scopus
  22. A. C. Nordenskjöld, M. Palme, and M. Kaijser, “X-ray exposure in utero and school performance: a population-based study of X-ray pelvimetry,” Clinical Radiology, vol. 70, no. 8, pp. 830–834, 2015. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Verheyde and M. A. Benotmane, “Unraveling the fundamental molecular mechanisms of morphological and cognitive defects in the irradiated brain,” Brain Research Reviews, vol. 53, no. 2, pp. 312–320, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. J. F. Cryan and A. Holmes, “Model organisms: the ascent of mouse: advances in modelling human depression and anxiety,” Nature Reviews Drug Discovery, vol. 4, no. 9, pp. 775–790, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Nouspikel, “DNA repair in differentiated cells: some new answers to old questions,” Neuroscience, vol. 145, no. 4, pp. 1213–1221, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Fukuda, H. Fukuda, J. Swanpalmer et al., “Age-dependent sensitivity of the developing brain to irradiation is correlated with the number and vulnerability of progenitor cells,” Journal of Neurochemistry, vol. 92, no. 3, pp. 569–584, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. M. O'Driscoll and P. A. Jeggo, “The role of the DNA damage response pathways in brain development and microcephaly: insight from human disorders,” DNA Repair, vol. 7, no. 7, pp. 1039–1050, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Gisone, E. Robello, J. Sanjurjo et al., “Reactive species and apoptosis of neural precursor cells after γ-irradiation,” NeuroToxicology, vol. 27, no. 2, pp. 253–259, 2006. View at Publisher · View at Google Scholar · View at Scopus
  29. C. Ikonomidou and A. M. Kaindl, “Neuronal death and oxidative stress in the developing brain,” Antioxidants and Redox Signaling, vol. 14, no. 8, pp. 1535–1550, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. K. F. S. Bell, B. Al-Mubarak, M.-A. Martel et al., “Neuronal development is promoted by weakened intrinsic antioxidant defences due to epigenetic repression of Nrf2,” Nature Communications, vol. 6, article 7066, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Nowak, O. Etienne, P. Millet et al., “Radiation-induced H2AX phosphorylation and neural precursor apoptosis in the developing brain of mice,” Radiation Research, vol. 165, no. 2, pp. 155–164, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Barazzuol, N. Rickett, L. Ju, and P. A. Jeggo, “Low levels of endogenous or X-ray-induced DNA double-strand breaks activate apoptosis in adult neural stem cells,” Journal of Cell Science, vol. 128, no. 19, pp. 3597–3606, 2015. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Saha, L. Woodbine, J. Haines et al., “Increased apoptosis and DNA double-strand breaks in the embryonic mouse brain in response to very low-dose X-rays but not 50 Hz magnetic fields,” Journal of the Royal Society Interface, vol. 11, no. 100, article 0783, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. Z. Mao, M. Bozzella, A. Seluanov, and V. Gorbunova, “Comparison of nonhomologous end joining and homologous recombination in human cells,” DNA Repair, vol. 7, no. 10, pp. 1765–1771, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. K. Rothkamm and M. Löbrich, “Evidence for a lack of DNA double-strand break repair in human cells exposed to very low x-ray doses,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 9, pp. 5057–5062, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. S. A. Gatz, L. Ju, R. Gruber et al., “Requirement for DNA ligase IV during embryonic neuronal development,” Journal of Neuroscience, vol. 31, no. 27, pp. 10088–10100, 2011. View at Publisher · View at Google Scholar · View at Scopus
  37. B. Rydberg, “Radiation-induced heat-labile sites that convert into DNA double-strand breaks,” Radiation Research, vol. 153, no. 6, pp. 805–812, 2000. View at Publisher · View at Google Scholar · View at Scopus
  38. T. Roque, C. Haton, O. Etienne et al., “Lack of a p21waf1/cip-dependent G1/S checkpoint in neural stem and progenitor cells after DNA damage in vivo,” STEM CELLS, vol. 30, no. 3, pp. 537–547, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. T. Verreet, R. Quintens, D. Van Dam et al., “A multidisciplinary approach unravels early and persistent effects of X-ray exposure at the onset of prenatal neurogenesis,” Journal of Neurodevelopmental Disorders, vol. 7, no. 1, article 3, 2015. View at Publisher · View at Google Scholar
  40. Y. Lee, M. J. Chong, and P. J. McKinnon, “Ataxia telangiectasia mutated-dependent apoptosis after genotoxic stress in the developing nervous system is determined by cellular differentiation status,” Journal of Neuroscience, vol. 21, no. 17, pp. 6687–6693, 2001. View at Google Scholar · View at Scopus
  41. C. D'Sa-Eipper, J. R. Leonard, G. Putcha et al., “DNA damage-induced neural precursor cell apoptosis requires p53 and caspase 9 but neither Bax nor caspase 3,” Development, vol. 128, no. 1, pp. 137–146, 2001. View at Google Scholar · View at Scopus
  42. Y. Kubota, S. Takahashi, X.-Z. Sun, H. Sato, S. Aizawa, and K. Yoshida, “Radiation-induced tissue abnormalities in fetal brain are related to apoptosis immediately after irradiation,” International Journal of Radiation Biology, vol. 76, no. 5, pp. 649–659, 2000. View at Publisher · View at Google Scholar · View at Scopus
  43. L. Rousseau, O. Etienne, T. Roque et al., “In vivo importance of homologous recombination DNA repair for mouse neural stem and progenitor cells,” PLoS ONE, vol. 7, no. 5, article e37194, 2012. View at Publisher · View at Google Scholar · View at Scopus
  44. O. Etienne, T. Roque, C. Haton, and F. D. Boussin, “Variation of radiation-sensitivity of neural stem and progenitor cell populations within the developing mouse brain,” International Journal of Radiation Biology, vol. 88, no. 10, pp. 694–702, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Norton and B. F. Kimler, “Early effects of low doses of ionizing radiation on the fetal cerebral cortex in rats,” Radiation Research, vol. 124, no. 2, pp. 235–241, 1990. View at Publisher · View at Google Scholar · View at Scopus
  46. S. Bolaris, E. Bozas, A. Benekou, H. Philippidis, and F. Stylianopoulou, “In utero radiation-induced apoptosis and p53 gene expression in the developing rat brain,” International Journal of Radiation Biology, vol. 77, no. 1, pp. 71–81, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Deckbar, P. A. Jeggo, and M. Löbrich, “Understanding the limitations of radiation-induced cell cycle checkpoints,” Critical Reviews in Biochemistry and Molecular Biology, vol. 46, no. 4, pp. 271–283, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. A. Semont, E. B. Nowak, C. Silva Lages et al., “Involvement of p53 and Fas/CD95 in murine neural progenitor cell response to ionizing irradiation,” Oncogene, vol. 23, no. 52, pp. 8497–8508, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. T. Kato, Y. Kanemura, K. Shiraishi, J. Miyake, S. Kodama, and M. Hara, “Early response of neural stem/progenitor cells after X-ray irradiation in vitro,” NeuroReport, vol. 18, no. 9, pp. 895–900, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. D. K. Jeppesen, V. A. Bohr, and T. Stevnsner, “DNA repair deficiency in neurodegeneration,” Progress in Neurobiology, vol. 94, no. 2, pp. 166–200, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. P. J. McKinnon, “Maintaining genome stability in the nervous system,” Nature Neuroscience, vol. 16, no. 11, pp. 1523–1529, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. S. Katyal and P. J. McKinnon, “DNA strand breaks, neurodegeneration and aging in the brain,” Mechanisms of Ageing and Development, vol. 129, no. 7-8, pp. 483–491, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. P.-O. Frappart and P. J. McKinnon, “Mouse models of DNA double-strand break repair and neurological disease,” DNA Repair, vol. 7, no. 7, pp. 1051–1060, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. G. K. Alderton, L. Galbiati, E. Griffith et al., “Regulation of mitotic entry by microcephalin and its overlap with ATR signalling,” Nature Cell Biology, vol. 8, no. 7, pp. 725–733, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. A. P. Jackson, H. Eastwood, S. M. Bell et al., “Identification of microcephalin, a protein implicated in determining the size of the human brain,” American Journal of Human Genetics, vol. 71, no. 1, pp. 136–142, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. K. E. Orii, Y. Lee, N. Kondo, and P. J. McKinnon, “Selective utilization of nonhomologous end-joining and homologous recombination DNA repair pathways during nervous system development,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 26, pp. 10017–10022, 2006. View at Publisher · View at Google Scholar · View at Scopus
  57. B. Deans, C. S. Griffin, M. Maconochie, and J. Thacker, “Xrcc2 is required for genetic stability, embryonic neurogenesis and viability in mice,” The EMBO Journal, vol. 19, no. 24, pp. 6675–6685, 2000. View at Publisher · View at Google Scholar · View at Scopus
  58. D. E. Barnes, G. Stamp, I. Rosewell, A. Denzel, and T. Lindahl, “Targeted disruption of the gene encoding DNA ligase IV leads to lethality in embryonic mice,” Current Biology, vol. 8, no. 25, pp. 1395–1398, 1998. View at Publisher · View at Google Scholar · View at Scopus
  59. K. M. Frank, J. M. Sekiguchi, K. J. Seidl et al., “Late embryonic lethality and impaired V(D)J recombination in mice lacking DNA ligase IV,” Nature, vol. 396, no. 6707, pp. 173–177, 1998. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Gao, Y. Sun, K. M. Frank et al., “A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis,” Cell, vol. 95, no. 7, pp. 891–902, 1998. View at Publisher · View at Google Scholar · View at Scopus
  61. J. Essers, H. Van Steeg, J. De Wit et al., “Homologous and non-homologous recombination differentially affect DNA damage repair in mice,” The EMBO Journal, vol. 19, no. 7, pp. 1703–1710, 2000. View at Publisher · View at Google Scholar · View at Scopus
  62. L. Schneider, M. Fumagalli, and F. d'Adda di Fagagna, “Terminally differentiated astrocytes lack DNA damage response signaling and are radioresistant but retain DNA repair proficiency,” Cell Death and Differentiation, vol. 19, no. 4, pp. 582–591, 2012. View at Publisher · View at Google Scholar · View at Scopus
  63. A. Barzilai, S. Biton, and Y. Shiloh, “The role of the DNA damage response in neuronal development, organization and maintenance,” DNA Repair, vol. 7, no. 7, pp. 1010–1027, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. S. L. Rulten and K. W. Caldecott, “DNA strand break repair and neurodegeneration,” DNA Repair, vol. 12, no. 8, pp. 558–567, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. M. L. Fishel, M. R. Vasko, and M. R. Kelley, “DNA repair in neurons: so if they don't divide what's to repair?” Mutation Research, vol. 614, no. 1-2, pp. 24–36, 2007. View at Publisher · View at Google Scholar · View at Scopus
  66. L. A. Cocas, P. A. Georgala, J.-M. Mangin et al., “Pax6 is required at the telencephalic pallial-subpallial boundary for the generation of neuronal diversity in the postnatal limbic system,” The Journal of Neuroscience, vol. 31, no. 14, pp. 5313–5324, 2011. View at Publisher · View at Google Scholar · View at Scopus
  67. M. Kohwi, M. A. Petryniak, J. E. Long et al., “A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors,” Journal of Neuroscience, vol. 27, no. 26, pp. 6878–6891, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. K.-H. Herzog, M. J. Chong, M. Kapsetaki, J. I. Morgan, and P. J. McKinnon, “Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system,” Science, vol. 280, no. 5366, pp. 1089–1091, 1998. View at Publisher · View at Google Scholar · View at Scopus
  69. R. Quintens, T. Verreet, A. Janssen et al., “Identification of novel radiation-induced p53-dependent transcripts extensively regulated during mouse brain development,” Biology Open, vol. 4, no. 3, pp. 331–344, 2015. View at Publisher · View at Google Scholar
  70. J. Verheyde, L. De Saint-Georges, L. Leyns, and M. A. Benotmane, “The role of Trp53 in the transcriptional response to ionizing radiation in the developing brain,” DNA Research, vol. 13, no. 2, pp. 65–75, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. M. D. Johnson, H. Xiang, S. London et al., “Evidence for involvement of Bax and p53, but not caspases, in radiation-induced cell death of cultured postnatal hippocampal neurons,” Journal of Neuroscience Research, vol. 54, no. 6, pp. 721–733, 1998. View at Publisher · View at Google Scholar · View at Scopus
  72. M. J. Chong, M. R. Murray, E. C. Gosink et al., “Atm and Bax cooperate in ionizing radiation-induced apoptosis in the central nervous system,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 2, pp. 889–894, 2000. View at Publisher · View at Google Scholar · View at Scopus
  73. I. Ferrer, “Role of caspases in ionizing radiation-induced apoptosis in the developing cerebellum,” Journal of Neurobiology, vol. 41, no. 4, pp. 549–558, 1999. View at Publisher · View at Google Scholar · View at Scopus
  74. G. A. Mickley, J. L. Ferguson, and T. J. Nemeth, “Serial injections of MK 801 (Dizocilpine) in neonatal rats reduce behavioral deficits associated with X-ray-induced hippocampal granule cell hypoplasia,” Pharmacology, Biochemistry and Behavior, vol. 43, no. 3, pp. 785–793, 1992. View at Publisher · View at Google Scholar · View at Scopus
  75. F. Alaoui, J. Pratt, S. Trocherie, L. Court, and J.-M. Stutzmann, “Acute effects of irradiation on the rat brain: protection by glutamate blockade,” European Journal of Pharmacology, vol. 276, no. 1-2, pp. 55–60, 1995. View at Publisher · View at Google Scholar · View at Scopus
  76. N. Samari, L. De Saint-Georges, G. Pani, S. Baatout, L. Leyns, and M. A. Benotmane, “Non-conventional apoptotic response to ionising radiation mediated by N-methyl D-aspartate receptors in immature neuronal cells,” International Journal of Molecular Medicine, vol. 31, no. 3, pp. 516–524, 2013. View at Publisher · View at Google Scholar · View at Scopus
  77. J. W. Olney, “New insights and new issues in developmental neurotoxicology,” NeuroToxicology, vol. 23, no. 6, pp. 659–668, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. M. Zhang, B. Ji, H. Zou et al., “Vitamin A depletion alters sensitivity of motor behavior to MK-801 in C57BL/6J mice,” Behavioral and Brain Functions, vol. 6, article 7, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. S. Miyamoto, J. N. Leipzig, J. A. Lieberman, and G. E. Duncan, “Effects of ketamine, MK-801, and amphetamine on regional brain 2-deoxyglucose uptake in freely moving mice,” Neuropsychopharmacology, vol. 22, no. 4, pp. 400–412, 2000. View at Publisher · View at Google Scholar · View at Scopus
  80. I. M. Najm, C. Q. Tilelli, and R. Oghlakian, “Pathophysiological mechanisms of focal cortical dysplasia: a critical review of human tissue studies and animal models,” Epilepsia, vol. 48, supplement 2, pp. 21–32, 2007. View at Publisher · View at Google Scholar · View at Scopus
  81. S. Fushiki, Y. Hyodo-Taguchi, C. Kinoshita, Y. Ishikawa, and T. Hirobe, “Short- and long-term effects of low-dose prenatal X-irradiation in mouse cerebral cortex, with special reference to neuronal migration,” Acta Neuropathologica, vol. 93, no. 5, pp. 443–449, 1997. View at Publisher · View at Google Scholar · View at Scopus
  82. X.-Z. Sun, M. Inouye, Y. Takagishi, S. Hayasaka, and H. Yamamura, “Follow-up study on histogenesis of microcephaly associated with ectopic gray matter induced by prenatal γ-irradiation in the mouse,” Journal of Neuropathology and Experimental Neurology, vol. 55, no. 3, pp. 357–365, 1996. View at Publisher · View at Google Scholar · View at Scopus
  83. X.-Z. Sun, S. Takahashi, Y. Fukui et al., “Different patterns of abnormal neuronal migration in the cerebral cortex of mice prenatally exposed to irradiation,” Developmental Brain Research, vol. 114, no. 1, pp. 99–108, 1999. View at Publisher · View at Google Scholar · View at Scopus
  84. X.-Z. Sun, S. Takahashi, Y. Fukui et al., “Neurogenesis of heterotopic gray matter in the brain of the microcephalic mouse,” Journal of Neuroscience Research, vol. 66, no. 6, pp. 1083–1093, 2001. View at Publisher · View at Google Scholar · View at Scopus
  85. O. Marín, M. Valiente, X. Ge, and L.-H. Tsai, “Guiding neuronal cell migrations,” Cold Spring Harbor Perspectives in Biology, vol. 2, no. 2, Article ID a001834, 2010. View at Publisher · View at Google Scholar · View at Scopus
  86. M. Inouye, “Radiation-induced apoptosis and developmental disturbance of the brain,” Congenital Anomalies, vol. 35, no. 1, pp. 1–13, 1995. View at Publisher · View at Google Scholar · View at Scopus
  87. B. F. Kimler, “Prenatal irradiation: a major concern for the developing brain,” International Journal of Radiation Biology, vol. 73, no. 4, pp. 423–434, 1998. View at Publisher · View at Google Scholar · View at Scopus
  88. A. Fujimori, T. Yaoi, H. Ogi et al., “Ionizing radiation downregulates ASPM, a gene responsible for microcephaly in humans,” Biochemical and Biophysical Research Communications, vol. 369, no. 3, pp. 953–957, 2008. View at Publisher · View at Google Scholar · View at Scopus
  89. J. Bond, E. Roberts, G. H. Mochida et al., “ASPM is a major determinant of cerebral cortical size,” Nature Genetics, vol. 32, no. 2, pp. 316–320, 2002. View at Publisher · View at Google Scholar · View at Scopus
  90. M. Shimada and K. Komatsu, “Emerging connection between centrosome and DNA repair machinery,” Journal of Radiation Research, vol. 50, no. 4, pp. 295–301, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Barbelanne and W. Y. Tsang, “Molecular and cellular basis of autosomal recessive primary microcephaly,” BioMed Research International, vol. 2014, Article ID 547986, 13 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  92. A. M. Kaindl, S. Passemard, P. Kumar et al., “Many roads lead to primary autosomal recessive microcephaly,” Progress in Neurobiology, vol. 90, no. 3, pp. 363–383, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. D. L. Silver, D. E. Watkins-Chow, K. C. Schreck et al., “The exon junction complex component Magoh controls brain size by regulating neural stem cell division,” Nature Neuroscience, vol. 13, no. 5, pp. 551–558, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. L. Pilaz, J. McMahon, E. Miller et al., “Prolonged mitosis of neural progenitors alters cell fate in the developing brain,” Neuron, vol. 89, no. 1, pp. 83–99, 2016. View at Publisher · View at Google Scholar
  95. P. U. Devi, M. Hossain, and K. S. Bisht, “Effect of late fetal irradiation on adult behavior of mouse: dose-response relationship,” Neurotoxicology and Teratology, vol. 21, no. 2, pp. 193–198, 1999. View at Publisher · View at Google Scholar · View at Scopus
  96. S. Saito, I. Aoki, K. Sawada, and T. Suhara, “Quantitative assessment of central nervous system disorder induced by prenatal X-ray exposure using diffusion and manganese-enhanced MRI,” NMR in Biomedicine, vol. 25, no. 1, pp. 75–83, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Saito, K. Sawada, M. Hirose, Y. Mori, Y. Yoshioka, and K. Murase, “Diffusion tensor imaging of brain abnormalities induced by prenatal exposure to radiation in rodents,” PloS ONE, vol. 9, no. 9, Article ID e107368, 2014. View at Publisher · View at Google Scholar · View at Scopus
  98. M. Hossain, M. Chetana, and P. U. Devi, “Late effect of prenatal irradiation on the hippocampal histology and brain weight in adult mice,” International Journal of Developmental Neuroscience, vol. 23, no. 4, pp. 307–313, 2005. View at Publisher · View at Google Scholar · View at Scopus
  99. H.-P. Li, T. Miki, H. Gu et al., “The effect of the timing of prenatal X-irradiation on Purkinje cell numbers in rat cerebellum,” Developmental Brain Research, vol. 139, no. 2, pp. 159–166, 2002. View at Publisher · View at Google Scholar · View at Scopus
  100. R. W. F. Vitral, C. M. Vitral, and M. L. Dutra, “Callosal agenesis and absence of primary visual cortex induced by prenatal X rays impair navigation's strategy and learning in tasks involving visuo-spatial working but not reference memory in mice,” Neuroscience Letters, vol. 395, no. 3, pp. 230–234, 2006. View at Publisher · View at Google Scholar · View at Scopus
  101. W.-M. Gao, B. Wang, and X.-Y. Zhou, “Effects of prenatal low-dose beta radiation from tritiated water on learning and memory in rats and their possible mechanisms,” Radiation Research, vol. 152, no. 3, pp. 265–272, 1999. View at Publisher · View at Google Scholar · View at Scopus
  102. N. Kokošová, L. Tomášová, T. Kisková, and B. Šmajda, “Neuronal analysis and behaviour in prenatally gamma-irradiated rats,” Cellular and Molecular Neurobiology, vol. 35, no. 1, pp. 45–55, 2015. View at Publisher · View at Google Scholar
  103. A. Saito, H. Yamauchi, Y. Ishida, Y. Ohmachi, and H. Nakayama, “Defect of the cerebellar vermis induced by prenatal γ-ray irradiation in radiosensitive BALB/c mice,” Histology and Histopathology, vol. 23, no. 8, pp. 953–964, 2008. View at Google Scholar · View at Scopus
  104. C. Schmitz, N. Grolms, P. R. Hof, R. Boehringer, J. Glaser, and H. Korr, “Altered spatial arrangement of layer V pyramidal cells in the mouse brain following prenatal low-dose X-irradiation. A stereological study using a novel three-dimensional analysis method to estimate the nearest neighbor distance distributions of cells in thick sections,” Cerebral Cortex, vol. 12, no. 9, pp. 954–960, 2002. View at Publisher · View at Google Scholar · View at Scopus
  105. T. Miki, Y. Fukui, Y. Takeuchi, and M. Itoh, “A quantitative study of the effects of prenatal X-irradiation on the development of cerebral cortex in rats,” Neuroscience Research, vol. 23, no. 3, pp. 241–247, 1995. View at Publisher · View at Google Scholar · View at Scopus
  106. C. Schmitz, U. Otto, and H. Korr, “More cerebellar granule cells following prenatal low-dose X-irradiation,” Brain Research, vol. 872, no. 1-2, pp. 250–253, 2000. View at Publisher · View at Google Scholar · View at Scopus
  107. T. A. Ralcewicz and T. V. N. Persaud, “Purkinje and granule cells distribution in the cerebellum of the rat following prenatal exposure to low dose ionizing radiation,” Experimental and Toxicologic Pathology, vol. 46, no. 6, pp. 443–452, 1994. View at Publisher · View at Google Scholar · View at Scopus
  108. K. Aldridge, L. Wang, M. P. Harms et al., “A longitudinal analysis of regional brain volumes in macaques exposed to X-irradiation in early gestation,” PLoS ONE, vol. 7, no. 8, Article ID e43109, 2012. View at Publisher · View at Google Scholar · View at Scopus
  109. L. D. Selemon, L. Wang, M. B. Nebel, J. G. Csernansky, P. S. Goldman-Rakic, and P. Rakic, “Direct and indirect effects of fetal irradiation on cortical gray and white matter volume in the macaque,” Biological Psychiatry, vol. 57, no. 1, pp. 83–90, 2005. View at Publisher · View at Google Scholar · View at Scopus
  110. L. D. Selemon, C. Ceritoglu, J. T. Ratnanather et al., “Distinct abnormalities of the primate prefrontal cortex caused by ionizing radiation in early or midgestation,” Journal of Comparative Neurology, vol. 521, no. 5, pp. 1040–1053, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. O. Algan and P. Rakic, “Radiation-induced, lamina-specific deletion of neurons in the primate visual cortex,” Journal of Comparative Neurology, vol. 381, no. 3, pp. 335–352, 1997. View at Publisher · View at Google Scholar · View at Scopus
  112. B. F. Kimler and S. Norton, “Behavioral changes and structural defects in rats irradiated in utero,” International Journal of Radiation Oncology, Biology, Physics, vol. 15, no. 5, pp. 1171–1177, 1988. View at Publisher · View at Google Scholar · View at Scopus
  113. S. J. Franco and U. Müller, “Shaping our minds: stem and progenitor cell diversity in the mammalian neocortex,” Neuron, vol. 77, no. 1, pp. 19–34, 2013. View at Publisher · View at Google Scholar · View at Scopus
  114. J. B. Angevine Jr., “Time of neuron origin in the hippocampal region. An autoradiographic study in the mouse,” Experimental Neurology, Supplement, supplement 2, pp. 1–70, 1965. View at Google Scholar
  115. V. S. Caviness Jr., “Time of neuron origin in the hippocampus and dentate gyrus of normal and reeler mutant mice: an autoradiographic analysis,” Journal of Comparative Neurology, vol. 151, no. 2, pp. 113–120, 1973. View at Publisher · View at Google Scholar · View at Scopus
  116. B. B. Stanfield and W. M. Cowan, “The development of the hippocampus and dentate gyrus in normal and reeler mice,” Journal of Comparative Neurology, vol. 185, no. 3, pp. 423–459, 1979. View at Publisher · View at Google Scholar · View at Scopus
  117. N. Takai, X.-Z. Sun, K. Ando, K. Mishima, and S. Takahashi, “Ectopic neurons in the hippocampus may be a cause of learning disability after prenatal exposure to X-rays in rats,” Journal of Radiation Research, vol. 45, no. 4, pp. 563–569, 2004. View at Publisher · View at Google Scholar · View at Scopus
  118. X.-Z. Sun, S. Takahashi, Y. Kubota et al., “Types and three-dimensional distribution of neuronal ectopias in the brain of mice prenatally subjected to X-irradiation,” Journal of Radiation Research, vol. 43, no. 1, pp. 89–98, 2002. View at Publisher · View at Google Scholar · View at Scopus
  119. X.-Z. Sun, R. Zhang, C. Cui et al., “Expression of neural cell adhesion molecule L1 in the brain of rats exposed to X-irradiation in utero,” Journal of Medical Investigation, vol. 50, no. 3-4, pp. 187–191, 2003. View at Google Scholar · View at Scopus
  120. R. Zhang, X.-Z. Sun, C. Cui et al., “Spatial learning and expression of neural cell adhesion molecule L1 in rats X-irradiated prenatally,” The Journal of Medical Investigation, vol. 54, no. 3-4, pp. 322–330, 2007. View at Publisher · View at Google Scholar · View at Scopus
  121. H. Ochiai, S. Miyahara, and S. Wakisaka, “Developmental abnormalities of corticospinal tract neurons in prenatally irradiated rats: a study using retrograde labeling with fast blue and intracellular lucifer yellow staining,” Brain Research, vol. 603, no. 1, pp. 129–133, 1993. View at Publisher · View at Google Scholar · View at Scopus
  122. S. Sajikumar and H. C. Goel, “Podophyllum hexandrum prevents radiation-induced neuronal damage in postnatal rats exposed in utero,” Phytotherapy Research, vol. 17, no. 7, pp. 761–766, 2003. View at Publisher · View at Google Scholar · View at Scopus
  123. Y. Fukui, K. Hoshino, I. Hayasaka, M. Inouye, and Y. Kameyama, “Developmental disturbance of rat cerebral cortex following prenatal low-dose γ-irradiation: a quantitative study,” Experimental Neurology, vol. 112, no. 3, pp. 292–298, 1991. View at Publisher · View at Google Scholar · View at Scopus
  124. T. Miki, K. Sawada, X.-Z. Sun, S. Hisano, Y. Takeuchi, and Y. Fukui, “Abnormal distribution of hippocampal mossy fibers in rats exposed to X-irradiation in utero,” Developmental Brain Research, vol. 112, no. 2, pp. 275–280, 1999. View at Publisher · View at Google Scholar · View at Scopus
  125. F.-W. Zhou and S. N. Roper, “Altered firing rates and patterns in interneurons in experimental cortical Dysplasia,” Cerebral Cortex, vol. 21, no. 7, pp. 1645–1658, 2011. View at Publisher · View at Google Scholar · View at Scopus
  126. F.-W. Zhou and S. N. Roper, “Densities of glutamatergic and GABAergic presynaptic terminals are altered in experimental cortical dysplasia,” Epilepsia, vol. 51, no. 8, pp. 1468–1476, 2010. View at Publisher · View at Google Scholar · View at Scopus
  127. K. M. Jacobs, V. N. Kharazia, and D. A. Prince, “Mechanisms underlying epileptogenesis in cortical malformations,” Epilepsy Research, vol. 36, no. 2-3, pp. 165–188, 1999. View at Publisher · View at Google Scholar · View at Scopus
  128. K. Nakanishi, K. Watanabe, M. Kawabata, A. Fukuda, and A. Oohira, “Altered synaptic activities in cultures of neocortical neurons from prenatally X-irradiated rats,” Neuroscience Letters, vol. 355, no. 1-2, pp. 61–64, 2004. View at Publisher · View at Google Scholar · View at Scopus
  129. S. J. Kempf, C. von Toerne, S. M. Hauck, M. J. Atkinson, M. A. Benotmane, and S. Tapio, “Long-term consequences of in utero irradiated mice indicate proteomic changes in synaptic plasticity related signalling,” Proteome Science, vol. 13, no. 1, article 26, 2015. View at Publisher · View at Google Scholar
  130. S. N. Roper, “In utero irradiation of rats as a model of human cerebrocortical dysgenesis: a review,” Epilepsy Research, vol. 32, no. 1-2, pp. 63–74, 1998. View at Publisher · View at Google Scholar · View at Scopus
  131. S. Momosaki, X.-Z. Sun, N. Takai, R. Hosoi, O. Inoue, and S. Takahashi, “Changes in histological construction and decrease in 3H-QNB binding in the rat brain after prenatal X-irradiation,” Journal of Radiation Research, vol. 43, no. 3, pp. 277–282, 2002. View at Publisher · View at Google Scholar · View at Scopus
  132. R. P. Jensh, L. M. Eisenman, and R. L. Brent, “Postnatal neurophysiologic effects of prenatal X-irradiation,” International Journal of Radiation Biology, vol. 67, no. 2, pp. 217–227, 1995. View at Publisher · View at Google Scholar · View at Scopus
  133. C. C. Filgueiras and A. C. Manhães, “Increased lateralization in rotational side preference in male mice rendered acallosal by prenatal gamma irradiation,” Behavioural Brain Research, vol. 162, no. 2, pp. 289–298, 2005. View at Publisher · View at Google Scholar · View at Scopus
  134. H. M. Aolad, M. Inouye, W. Darmanto, S. Hayasaka, and Y. Murata, “Hydrocephalus in mice following X-irradiation at early gestational stage: possibly due to persistent deceleration of cell proliferation,” Journal of Radiation Research, vol. 41, no. 3, pp. 213–226, 2000. View at Publisher · View at Google Scholar · View at Scopus
  135. S. Saito, K. Sawada, Y. Mori, Y. Yoshioka, and K. Murase, “Brain and arterial abnormalities following prenatal X-ray irradiation in mice assessed by magnetic resonance imaging and angiography,” Congenital Anomalies, vol. 55, no. 2, pp. 103–106, 2015. View at Publisher · View at Google Scholar · View at Scopus
  136. L. Tomášová, B. Šmajda, and J. Ševc, “Effects of prenatal irradiation on behaviour and hippocampal neurogenesis in adult rats,” Acta Physiologica Hungarica, vol. 99, no. 2, pp. 126–132, 2012. View at Publisher · View at Google Scholar
  137. M. Hossain and P. Uma Devi, “Effect of irradiation at the early fetal stage on adult brain function in the mouse: locomotor activity,” International Journal of Radiation Biology, vol. 76, no. 10, pp. 1397–1402, 2000. View at Publisher · View at Google Scholar · View at Scopus
  138. M. Hossain and P. Uma Devi, “Effect of irradiation at the early foetal stage on adult brain function of mouse: learning and memory,” International Journal of Radiation Biology, vol. 77, no. 5, pp. 581–585, 2001. View at Publisher · View at Google Scholar · View at Scopus
  139. Z. J. Sienkiewicz, R. G. E. Haylock, and R. D. Saunders, “Prenatal irradiation and spatial memory in mice: investigation of dose-response relationship,” International Journal of Radiation Biology, vol. 65, no. 5, pp. 611–618, 1994. View at Publisher · View at Google Scholar · View at Scopus
  140. J. Kisková and B. Šmajda, “Behavioural changes in prenatal rats irradiated with low dosage of γ-rays,” Bulletin of the Veterinary Institute in Pulawy, vol. 50, no. 4, pp. 595–598, 2006. View at Google Scholar · View at Scopus
  141. R. Baskar and P. U. Devi, “Influence of gestational age to low-level gamma irradiation on postnatal behavior in mice,” Neurotoxicology and Teratology, vol. 22, no. 4, pp. 593–602, 2000. View at Publisher · View at Google Scholar · View at Scopus
  142. Z. J. Sienkiewicz, R. G. E. Haylock, and R. D. Saunders, “Differential learning impairments produced by prenatal exposure to ionizing radiation in mice,” International Journal of Radiation Biology, vol. 75, no. 1, pp. 121–127, 1999. View at Publisher · View at Google Scholar · View at Scopus
  143. R. L. Brent, “Counseling patients exposed to ionizing radiation during pregnancy,” Pan American Journal of Public Health, vol. 20, no. 2-3, pp. 198–204, 2006. View at Publisher · View at Google Scholar · View at Scopus
  144. K. Nakagawa, Y. Aoki, T. Kusama, N. Ban, S. Nakagawa, and Y. Sasaki, “Radiotherapy during pregnancy: effects on fetuses and neonates,” Clinical Therapeutics, vol. 19, no. 4, pp. 770–777, 1997. View at Publisher · View at Google Scholar · View at Scopus
  145. K. Van Calsteren and F. Amant, “Cancer during pregnancy,” Acta Obstetricia et Gynecologica Scandinavica, vol. 93, no. 5, pp. 443–446, 2014. View at Publisher · View at Google Scholar · View at Scopus
  146. T. D. Jacquin, Q. Xie, T. Miki, I. Satriotomo, M. Itoh, and Y. Takeuchi, “Prenatal X-irradiation increases GFAP- and calbindin D28k-immunoreactivity in the medial subdivision of the nucleus of solitary tract in the rat,” Journal of the Autonomic Nervous System, vol. 80, no. 1-2, pp. 8–13, 2000. View at Publisher · View at Google Scholar · View at Scopus
  147. S. Saito, I. Aoki, K. Sawada et al., “Quantitative and noninvasive assessment of prenatal X-ray-induced CNS abnormalities using magnetic resonance imaging,” Radiation Research, vol. 175, no. 1, pp. 1–9, 2011. View at Publisher · View at Google Scholar · View at Scopus
  148. M. van Vulpen, H. B. Kal, M. J. B. Taphoorn, and S. Y. El Sharouni, “Changes in blood-brain barrier permeability induced by radiotherapy: implications for timing of chemotherapy? (Review),” Oncology Reports, vol. 9, no. 4, pp. 683–688, 2002. View at Google Scholar · View at Scopus
  149. N. R. Saunders, S. A. Liddelow, and K. M. Dziegielewska, “Barrier mechanisms in the developing brain,” Frontiers in Pharmacology, vol. 3, pp. 1–18, 2012. View at Publisher · View at Google Scholar · View at Scopus
  150. M. Murga, S. Bunting, M. F. Montãa et al., “A mouse model of ATR-Seckel shows embryonic replicative stress and accelerated aging,” Nature Genetics, vol. 41, no. 8, pp. 891–898, 2009. View at Publisher · View at Google Scholar · View at Scopus
  151. O. Fernandez-Capetillo, “Intrauterine programming of ageing,” EMBO Reports, vol. 11, no. 1, pp. 32–36, 2010. View at Publisher · View at Google Scholar · View at Scopus
  152. C. López-Otín, M. A. Blasco, L. Partridge, M. Serrano, and G. Kroemer, “The hallmarks of aging,” Cell, vol. 153, no. 6, pp. 1194–1217, 2013. View at Publisher · View at Google Scholar
  153. B. F. Pachkowski, K. Z. Guyton, and B. Sonawane, “DNA repair during in utero development: a review of the current state of knowledge, research needs, and potential application in risk assessment,” Mutation Research—Reviews in Mutation Research, vol. 728, no. 1-2, pp. 35–46, 2011. View at Publisher · View at Google Scholar · View at Scopus
  154. R. Madabhushi, L. Pan, and L.-H. Tsai, “DNA damage and its links to neurodegeneration,” Neuron, vol. 83, no. 2, pp. 266–282, 2014. View at Publisher · View at Google Scholar · View at Scopus
  155. L. Li, W. Wang, S. Welford, T. Zhang, X. Wang, and X. Zhu, “Ionizing radiation causes increased tau phosphorylation in primary neurons,” Journal of Neurochemistry, vol. 131, no. 1, pp. 86–93, 2014. View at Publisher · View at Google Scholar · View at Scopus
  156. M.-A. Seol, U. Jung, H. S. Eom, S.-H. Kim, H.-R. Park, and S.-K. Jo, “Prolonged expression of senescence markers in mice exposed to gamma-irradiation,” Journal of Veterinary Science, vol. 13, no. 4, pp. 331–338, 2012. View at Publisher · View at Google Scholar · View at Scopus
  157. N. L. Le Oanh, F. Rodier, F. Fontaine et al., “Ionizing radiation-induced long-term expression of senescence markers in mice is independent of p53 and immune status,” Aging Cell, vol. 9, no. 3, pp. 398–409, 2010. View at Publisher · View at Google Scholar · View at Scopus
  158. S. J. Kempf, O. Azimzadeh, M. J. Atkinson, and S. Tapio, “Long-term effects of ionising radiation on the brain: cause for concern?” Radiation and Environmental Biophysics, vol. 52, no. 1, pp. 5–16, 2013. View at Publisher · View at Google Scholar · View at Scopus
  159. N. Begum, B. Wang, M. Mori, and G. Vares, “Does ionizing radiation influence Alzheimer's disease risk?” Journal of Radiation Research, vol. 53, no. 6, pp. 815–822, 2012. View at Publisher · View at Google Scholar · View at Scopus
  160. S. M. Poulose, D. F. Bielinski, K. Carrihill-Knoll, B. M. Rabin, and B. Shukitt-Hale, “Exposure to 16O-particle radiation causes aging-like decrements in rats through increased oxidative stress, inflammation and loss of autophagy,” Radiation Research, vol. 176, no. 6, pp. 761–769, 2011. View at Publisher · View at Google Scholar · View at Scopus
  161. S. Suman, O. C. Rodriguez, T. A. Winters, A. J. Fornace, C. Albanese, and K. Datta, “Therapeutic and space radiation exposure of mouse brain causes impaired dna repair response and premature senescence by chronic oxidant production,” Aging, vol. 5, no. 8, pp. 607–622, 2013. View at Publisher · View at Google Scholar · View at Scopus
  162. S. Norton, B. F. Kimler, and P. J. Mullenix, “Progressive behavioral changes in rats after exposure to low levels of ionizing radiation in utero,” Neurotoxicology and Teratology, vol. 13, no. 2, pp. 181–188, 1991. View at Publisher · View at Google Scholar · View at Scopus
  163. H. R. Friedman and L. D. Selemon, “Fetal irradiation interferes with adult cognition in the nonhuman primate,” Biological Psychiatry, vol. 68, no. 1, pp. 108–111, 2010. View at Publisher · View at Google Scholar · View at Scopus
  164. A. M. Polyukhov, I. V. Kobsar, V. I. Grebelnik, and V. P. Voitenko, “The accelerated occurrence of age-related changes of organism in Chernobyl workers: a radiation-induced progeroid syndrome?” Experimental Gerontology, vol. 35, no. 1, pp. 105–115, 2000. View at Publisher · View at Google Scholar · View at Scopus
  165. Y. Socol and L. Dobrzyński, “Atomic bomb survivors life-span study: insufficient statistical power to select radiation carcinogenesis model,” Dose-Response, vol. 13, no. 1, 2015. View at Publisher · View at Google Scholar · View at Scopus
  166. D. B. Richardson, S. Wing, and S. R. Cole, “Missing doses in the life span study of Japanese atomic bomb survivors,” American Journal of Epidemiology, vol. 177, no. 6, pp. 562–568, 2013. View at Publisher · View at Google Scholar · View at Scopus
  167. Y. Dincer and Z. Sezgin, “Medical radiation exposure and human carcinogenesis-genetic and epigenetic mechanisms,” Biomedical and Environmental Sciences, vol. 27, no. 9, pp. 718–728, 2014. View at Publisher · View at Google Scholar · View at Scopus
  168. R. Fazel, H. M. Krumholz, Y. Wang et al., “Exposure to low-dose ionizing radiation from medical imaging procedures,” The New England Journal of Medicine, vol. 361, no. 9, pp. 849–857, 2009. View at Publisher · View at Google Scholar · View at Scopus
  169. R. Doll and R. Wakeford, “Risk of childhood cancer from fetal irradiation,” British Journal of Radiology, vol. 70, pp. 130–139, 1997. View at Publisher · View at Google Scholar · View at Scopus
  170. E. C. Lin, “Radiation risk from medical imaging,” Mayo Clinic Proceedings, vol. 85, no. 12, pp. 1142–1146, 2010. View at Publisher · View at Google Scholar · View at Scopus
  171. L. Mullenders, M. Atkinson, H. Paretzke, L. Sabatier, and S. Bouffler, “Assessing cancer risks of low-dose radiation,” Nature Reviews Cancer, vol. 9, no. 8, pp. 596–604, 2009. View at Publisher · View at Google Scholar · View at Scopus
  172. D. J. Brenner, R. Doll, D. T. Goodhead et al., “Cancer risks attributable to low doses of ionizing radiation: assessing what we really know,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 24, pp. 13761–13766, 2003. View at Publisher · View at Google Scholar
  173. H. B. Kal and H. Struikmans, “Radiotherapy during pregnancy: fact and fiction,” Lancet Oncology, vol. 6, no. 5, pp. 328–333, 2005. View at Publisher · View at Google Scholar · View at Scopus
  174. C. P. Nguyen and L. H. Goodman, “Fetal risk in diagnostic radiology,” Seminars in Ultrasound, CT and MRI, vol. 33, no. 1, pp. 4–10, 2012. View at Publisher · View at Google Scholar · View at Scopus
  175. R. S. Groen, J. Y. Bae, and K. J. Lim, “Fear of the unknown: ionizing radiation exposure during pregnancy,” American Journal of Obstetrics and Gynecology, vol. 206, no. 6, pp. 456–462, 2012. View at Publisher · View at Google Scholar · View at Scopus
  176. E. K. Osei and K. Faulkner, “Radiation risks from exposure to diagnostic X-rays during pregnancy,” Radiography, vol. 6, no. 2, pp. 131–144, 2000. View at Publisher · View at Google Scholar · View at Scopus
  177. K. N. Prasad, W. C. Cole, and G. M. Haase, “Radiation protection in humans: extending the concept of as low as reasonably achievable (ALARA) from dose to biological damage,” British Journal of Radiology, vol. 77, no. 914, pp. 97–99, 2004. View at Publisher · View at Google Scholar · View at Scopus
  178. M. Tubiana, A. Aurengo, D. Averbeck, and R. Masse, “Recent reports on the effect of low doses of ionizing radiation and its dose-effect relationship,” Radiation and Environmental Biophysics, vol. 44, no. 4, pp. 245–251, 2006. View at Publisher · View at Google Scholar · View at Scopus
  179. M. Tubiana, L. E. Feinendegen, C. Yang, and J. M. Kaminski, “The linear no-threshold relationship is inconsistent with radiation biologic and experimental data,” Radiology, vol. 251, no. 1, pp. 13–22, 2009. View at Publisher · View at Google Scholar · View at Scopus
  180. M. Sokolov and R. Neumann, “Effects of low doses of ionizing radiation exposures on stress-responsive gene expression in human embryonic stem cells,” International Journal of Molecular Sciences, vol. 15, no. 1, pp. 588–604, 2014. View at Publisher · View at Google Scholar · View at Scopus
  181. F. Ballarini, M. Biaggi, A. Ottolenghi, and O. Sapora, “Cellular communication and bystander effects: a critical review for modelling low-dose radiation action,” Mutation Research—Fundamental and Molecular Mechanisms of Mutagenesis, vol. 501, no. 1-2, pp. 1–12, 2002. View at Publisher · View at Google Scholar · View at Scopus
  182. E. J. Calabrese and L. A. Baldwin, “Hormesis: U-shaped dose responses and their centrality in toxicology,” Trends in Pharmacological Sciences, vol. 22, no. 6, pp. 285–291, 2001. View at Publisher · View at Google Scholar · View at Scopus