Sensitivity to radiation-induced apoptosis and neuron loss declines rapidly in the postnatal mouse neocortex

International Journal of Radiation Biology

Volumn 81, Issue 7, 2005, Pages 545-554

  Nakaya, K ^a   Hasegawa, T ^b   Flickinger, J C ^a   Kondziolka, D S ^a   Fellows Mayle, W ^a   Gobbel, G T ^a,c  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b NAGOYA UNIVERSITY   (Japan)

^c PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

Author keywords

Age; Apoptosis; Brain; Infant; Neocortex; Neonate; Radiation

Indexed keywords

CASPASE 3;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN RADIATION; CONTROLLED STUDY; FEMALE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEOCORTEX; NERVE CELL; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIVITY; X IRRADIATION;

ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CHILD; CHILD DEVELOPMENT; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; NEOCORTEX; NEURONS; RADIATION INJURIES; RISK FACTORS;

ANIMALIA;

EID: 28044456108     PISSN: 09553002     EISSN: 13623095     Source Type: Journal    
DOI: 10.1080/09553000500280492     Document Type: Article

References (44)

1. Abayomi OK. 1996. Pathogenesis of irradiation-induced cognitive dysfunction. Acta Oncologica 35: 659-663.
2. Anderson VA, Godber T, Smibert E, Weiskop S, Ekert H. 2000. Cognitive and academic outcome following cranial irradiation and chemotherapy in children: a longitudinal study. British Journal of Cancer 82: 255-262.
3. Burek MJ, Oppenheim RW. 1996. Programmed cell death in the developing nervous system. Brain Pathology 6: 427-446.
4. Calvo W, Hopewell JW, Reinhold HS, Yeung TK. 1988. Time- and dose-related changes in the white matter of the rat brain after single doses of X rays. British Journal of Radiology 61: 1043-1052.
5. Chaillan FA, Devigne C, Diabira D, Khrestchatisky M, Roman FS, Ben-Ari Y, Soumireu-Mourat B. 1997. Neonatal gamma-ray irradiation impairs learning and memory of an olfactory associative task in adult rats. European Journal of Neuroscience 9: 884-894.
6. Chong MJ, Murray MR, Gosink EC, Russell HR, Srinivasan A, Kapsetaki M, Korsmeyer SJ, McKinnon PJ. 2000. Atm and Bax cooperate in ionizing radiation-induced apoptosis in the central nervous system. Proceedings of the National Academy of Sciences, USA, 97: 889-894.
7. Crossen JR, Garwood D, Glatstein E, Neuwelt EA. 1994. Neurobehavioral sequelae of cranial irradiation in adults: a review of radiation-induced encephalopathy. Journal of Clinical Oncology 12: 627-642.
8. Dessi F, Represa A, Ben-Ari Y. 1991. Effects of neonatal gamma-ray irradiation on rat hippocampus-II. Development of excitatory amino acid binding sites. Neuroscience 42: 151-157.
9. Duffner PK, Cohen ME, Anderson SW, Voorhess ML, MacGillivray MH, Panahon A, Brecher ML. 1983. Long-term effects of treatment on endocrine function in children with brain tumors. Annals of Neurology 14: 528-532.
10. Ellenberg L, McComb JG, Siegel SE, Stowe S. 1987. Factors affecting intellectual outcome in pediatric brain tumor patients. Neurosurgery 21: 638-644.
11. Ferrer I. 1992. The effect of cycloheximide on natural and X-ray-induced cell death in the developing cerebral cortex. Brain Research, 588: 351-357.
12. Ferrer I. 1996. Cell death in the normal developing brain, and following ionizing radiation, methyl-azoxymethanol acetate, and hypoxia-ischaemia in the rat. Neuropathology and Applied Neurobiology 22: 489-494.
13. Ferrer I, Serrano T, Alcantara S, Tortosa A, Graus F. 1993. X-ray-induced cell death in the developing hippocampal complex involves neurons and requires protein synthesis. Journal of Neuropathology and Experimental Neurology 52: 370-378.
14. Fike J, Gobbel G. 1991. Central nervous system radiation injury in large animal models. In: Gutin P, Leibel S, Sheline G, editors. Radiation injury to the nervous system. New York, NY: Raven, p. 113-135.
15. Gobbel GT, Bellinzona M, Vogt AR, Gupta N, Fike JR, Chan PH. 1998. Response of postmitotic neurons to X-irradiation: implications for the role of DNA damage in neuronal apoptosis. Journal of Neuroscience 18: 147-155.
16. Hagberg H, Bona E, Gilland E, Puka-Sundvall M. 1997. Hypoxia-ischaemia model in the 7-day-old rat: possibilities and short-comings. Acta Paediatrica 422(Suppl.):85-88.
17. Hall P, Adami HO, Trichopoulos D, Pedersen NL, Lagiou P, Ekbom A, Ingvar M, Lundell M, Granath F. 2004. Effect of low doses of ionising radiation in infancy on cognitive function in adulthood: Swedish population based cohort study. British Medical Journal 328: 19-23.
18. Herzog K-H, Chong MJ, Kapsetaki M, Morgan JI, McKinnon PJ. 1998. Requirement for Atm in ionizing radiation-induced cell death in the developing central nervous system. Science 280: 1089-1091.
19. Hirsch JF, Renier D, Czernichow P, Benveniste L, Pierre-Kahn A. 1979. Medulloblastoma in childhood. Survival and functional results. Acta Neurochirurgica 48: 1-15.
20. Hunter SF, Leavitt JA, Rodriguez M. 1997. Direct observation of myelination in vivo in the mature human central nervous system. A model for the behaviour of oligodendrocyte progenitors and their progeny. Brain 120: 2071-2082.
21. Johnson MD, Kinoshita Y, Xiang H, Ghatan S, Morrison RS. 1999. Contribution of p53-dependent caspase activation to neuronal cell death declines with neuronal maturation. Journal of Neuroscience 19: 2996-3006.
22. Khong PL, Kwong DL, Chan GC, Sham JS, Chan FL, Ooi GC. 2003. Diffusion-tensor imaging for the detection and quantification of treatment-induced white matter injury in children with medulloblastoma: a pilot study. American Journal of Neuroradiology 24: 734-740.
23. Korr H, Thorsten Rohde H, Benders J, Dafotakis M, Grolms N, Schmitz C. 2001. Neuron loss during early adulthood following prenatal low-dose X-irradiation in the mouse brain. International Journal of Radiation Biology 77: 567-580.
24. Lee PW, Hung BK, Woo EK, Tai PT, Choi DT. 1989. Effects of radiation therapy on neuropsychological functioning in patients with nasopharyngeal carcinoma. Journal of Neurology, Neurosurgery and Psychiatry 52: 488-492.
25. Madsen TM, Kristjansen PE, Bolwig TG, Wortwein G. 2003. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119: 635-642.
26. Monje ML, Mizumatsu S, Fike JR, Palmer TD. 2002. Irradiation induces neural precursor-cell dysfunction. Nature Medicine 8: 955-962.
27. Monje ML, Toda H, Palmer TD. 2003. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302: 1760-1765.
28. Moreira RCM, Bueno JL. 2003. Conditional discrimination learning and negative patterning in rats with neonatal hippocampal lesion induced by ionizing radiation. Behavioral Brain Research 138: 29-44.
29. Mulhern RK, Reddick WE, Palmer SL, Glass JO, Elkin TD, Kun LE, Taylor J, Langston J, Gajjar A. 1999. Neurocognitive deficits in medulloblastoma survivors and white matter loss. Annals of Neurology 46: 834-841.
30. Reddick WE, Russell JM, Glass JO, Xiong X, Mulhern RK, Langston JW, Merchant TE, Kun LE, Gajjar A. 2000. Subtle white matter volume differences in children treated for medulloblastoma with conventional or reduced dose craniospinal irradiation. Magnetic Resonance Imaging 18: 787-793.
31. Rice D, Barone S, Jr. 2000. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environmental Health Perspectives 3(Suppl. 108): 511-533.
32. Rola R, Raber J, Rizk A, Otsuka S, VandenBerg SR, Morhardt DR, Fike JR. 2004. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Experimental Neurology 188: 316-330.
33. Roman DD, Sperduto PW. 1995. Neuropsychological effects of cranial radiation: current knowledge and future directions. International Journal of Radiation Oncology, Biology, and Physics 31: 983-998.
34. Schroeter M, Kury P, Jander S. 2003. Inflammatory gene expression in focal cortical brain ischemia: differences between rats and mice. Brain Research. Molecular Brain Research 117: 1-7.
35. Shinohara C, Gobbel GT, Lamborn KR, Tada E, Fike JR. 1997. Apoptosis in the subependyma of young adult rats after single and fractionated doses of X-rays. Cancer Research 57: 2694-2702.
36. Sienkiewicz ZJ, Saunders RD, Butland BK. 1992. Prenatal irradiation and spatial memory in mice: investigation of critical period. International Journal of Radiation Biology 62: 211-219.
37. Silber JH, Radcliffe J, Peckham V, Perilongo G, Kishnani P, Fridman M, Goldwein JW, Meadows AT. 1992. Whole-brain irradiation and decline in intelligence: the influence of dose and age on IQ score. Journal of Clinical Oncology 10: 1390-1396.
38. Silverman CL, Palkes H, Talent B, Kovnar E, Clouse JW, Thomas PR. 1984. Late effects of radiotherapy on patients with cerebellar medulloblastoma. Cancer 54: 825-829.
39. Sinz EH, Kochanek PM, Dixon CE, Clark RS, Carcillo JA, Schiding JK, Chen M, Wisniewski SR, Carlos TM, Williams D, DeKosky ST, Watkins SC, Marion DW, Billiar TR. 1999. Inducible nitric oxide synthase is an endogenous neuroprotectant after traumatic brain injury in rats and mice. Journal of Clinical Investigation 104: 647-656.
40. Surma-aho O, Niemela M, Vilkki J, Kouri M, Brander A, Salonen O, Paetau A, Kallio M, Pyykkonen J, Jaaskelainen J. 2001. Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients. Neurology 56: 1285-1290.
41. Utz PJ, Anderson P. 2000. Life and death decisions: regulation of apoptosis by proteolysis of signaling molecules. Cell Death and Differentiation 7: 589-602.
42. Van der Kogel A. 1991. Central nervous system radiation injury in small animal models. In: Gutin P, Leibel S, Sheline G, editors. Radiation injury to the nervous system. New York, NY: Raven. p. 113-135.
43. Xiang H, Kinoshita Y, Knudson CM, Korsmeyer SJ, Schwartzkroin PA, Morrison RS. 1998. Bax involvement in p53-mediated neuronal cell death. Journal of Neuroscience 18: 1363-1373.
44. Yoshida T, Waeber C, Huang Z, Moskowitz MA. 1995. Induction of nitric oxide synthase activity in rodent brain following middle cerebral artery occlusion. Neuroscience Letters 194: 214-218.