Unintended effects of cranial irradiation on cognitive function

Toxicologic Pathology

Volumn 38, Issue 1, 2010, Pages 198-202

  Raber, Jacob ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Fear conditioning; Hippocampus; Irradiation; Mice; Neurogenesis; Oxidative stress; Water maze

Indexed keywords

ANTINEOPLASTIC AGENT; MICROTUBULE ASSOCIATED PROTEIN 2;

ACUTE LYMPHOBLASTIC LEUKEMIA; ATTENTION DISTURBANCE; BRAIN RADIATION; COGNITIVE DEFECT; GENETIC SUSCEPTIBILITY; HEAD AND NECK CANCER; HEREDITY; HUMAN; INTELLECTUAL IMPAIRMENT; MEMORY DISORDER; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RADIATION EXPOSURE; REVIEW; SEX DIFFERENCE; WORKING MEMORY; ANIMAL; COGNITION; FEMALE; GENETIC PREDISPOSITION; MALE; MOUSE; SEXUAL DEVELOPMENT; SKULL IRRADIATION;

MUS;

ANIMALS; ANTINEOPLASTIC AGENTS; COGNITION; CRANIAL IRRADIATION; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MALE; MICE; NEUROGENESIS; OXIDATIVE STRESS; SEX CHARACTERISTICS;

EID: 77952294421     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623309352003     Document Type: Review

References (70)

1. Acevedo, S., Gardell, L., Bradley, S. R., Piu, F., and Raber, J. (2008). Selective androgens receptor modulators antagonize apolipoprotein E4-induced cognitive impairments. Lett Drug Design Discovery 5, 271-276
2. Acevedo, S., Tittle, S., and Raber, J. (2008). Transgenic expression of androgen receptors improves spatial memory retention of sham-irradiated and 137Cesium irradiated female mice. Radiat Res 170, 161-167
3. Alexander, G., Packard, M., and Hines, M. (1994). Testosterone has rewarding affective properties in male rats. Behav Neurosci 108, 424-428
4. Anderson, V., Godber, T., Smibert, E., and Ekert, H. (1997). Neurobehavioural sequelae following cranial irradiation and chemotherapy in children: an analysis of risk factors. Pediatr Rehabil 1, 63-76.
5. Beatty, W. W. (1979). Gonadal hormones and sex differences in nonreproductive behaviors in rodents: organizational and activational influences. Horm Behav 12, 112-163
6. Benice, T., and Raber, J. (2009). Testosterone and dihydrotestosterone differentially improve cognition in aged female mice. Learn Mem 16, 479-485
7. Benice, T., Rizk, A., Pfankuch, T., Kohama, S., and Raber, J. (2006). Sex differences in age-related cognitive decline in C57BL/6J mice associated with increased brain microtubule-associated protein 2 and synaptophysin immunoreactivity. Neuroscience 137, 413-423
8. Bretsky, P., Guralnik, J. M., Launer, L., Albert, M., and Seeman, T. E. (2003). Studies of successful aging. The role of APOE-epsilon 4 in longitudinal cognitive decline: MacArthur Studies of Successful Aging. Neurology 60, 1077-1081
9. Brown, R.,Madan-Swain, A.,Walco, G., Cherrick, I., Ievers, C., Conte, P., Vega, R., Bell, B., and Lauer, S. (1998). Cognitive and academic late effects among children previously treated for acute lymphocytic leukemia receiving chemotherapy as CNS prophylaxis. J Pediatr Psychol 23, 333-340
10. Butler, R., and Mulhern, R. (2005). Neurocognitive interventions for children and adolescents surviving cancer. J Pediatr Psychol 30, 65-78.
11. Buttini, M., Orth, M., Bellosta, S., Akeefe, H., Pitas, R. E., Wyss-Coray, T., Mucke, L., and Mahley, R. W. (1999). Expression of human apolipoprotein E3 or E4 in the brains of Apoe-/-mice: Isoform-specific effects on neurodegeneration. J Neurosci 19, 4867-4880
12. Collier, T. J., Quirk, G. J., and Routtenberg, A. (1987). Separable roles of hippocampal granule cells in forgetting and pyramidal cells in remembering spatial information. Brain Res 409, 316-328
13. Copeland, D., Moore, B., Francis, D., Jaffe, N., and Culbert, S. (1996). Neuropsychologic effects of chemotherapy on children with cancer: a longitudinal study. J Clin Oncol 14, 2826-2835
14. Deary, I., Whiteman, M. C., Pattie, A., Starr, J. M., Hayward, C., Wright, A. F., Carothers, A., and Whalley, L. J. (2002). Cognitive change and the APOE epsilon 4 allele. Nature 418, 932.
15. Farrer, L. A., Cupples, L. A., Haines, J. L., Hyman, B., Kukull, W. A., Mayeux, R., Myers, R. H., Pericak-Vance, M. A., Risch, N., and van Duijn, C. M. (1997). Effects of age, sex, and ethnicity on the association between apolipoprotein E genotype and Alzheimer disease. A meta-analysis. J Am Med Assoc 278, 1349-1356
16. Flood, J., and Roberts, E. (1988). Dehydroepiandrosterone sulfate improves memory in aging mice. Brain Res 118, 178-181
17. Gao, S., Hendrie, H. C., Hall, K. S., and Hui, S. (1998). The relationships between age, sex, and the incidence of dementia and Alzheimer disease: A meta-analysis. Arch Gen Psychiatry 55, 809-815
18. Glauser, T. A., and Packer, R. J. (1991). Cognitive deficits in long-term survivors of childhood brain tumors. Child's Nerv Syst 7, 2-12.
19. Goff, J., Anderson, H., and Cooper, P. (1980). Distractability and memory deficits in long-term survivors of acute lymphoblastic leukemia. J Dev Behav Perdiatr 1, 158-163
20. Gould, E., Beylin, A., Tanapat, P., Reeves, A., and Shors, T. J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2, 260-265 (Pubitemid 30491297)
21. Habib, M., and Sirigu, A. (1987). Pure topographical disorientation: a definition and anatomical basis. Cortex 23, 73-85.
22. Harada, A., Teng, J., Takei, Y., Oguchi, K., and Hirokawa, N. (2002). MAP-2 is required for dendrite elongation, PKA anchoring in dendrites, and proper PKA signal transduction. J Cell Biol 158, 541-549
23. Higuchi, Y., Nelson, G. A., Vazquez, M., Laskowitz, D. T., Slater, J. M., and Pearlstein, R. D. (2002). Apolipoprotein E expression and behavioral toxicity of high charge, high energy (HZE) particle radiation. J Radiat Res 43 Suppl, S219-S224.
24. Hörtnagl, H., Hansen, L., Kindel, G., Schneider, B., Tamer, A. E., and Hanin, I. (1993). Sex differences and estrous cycle-variations in the AF64A-induced cholinergic deficit in the rat hippocampus. Brain Res Bull 31, 129-134
25. Janowsky, J. S., Oviatt, S. K., and Orwoll, E. S. (1994). Testosterone influences spatial cognition in older men. Behav Neuroscience 108, 325-332
26. Joseph, R., Hess, S., and Birecree, E. (1978). Effects of hormone manipulations and exploration on sex differences in maze learning. Behav Biol 24, 364-377
27. Kolb, B., and Cioe, J. (1996). Sex-related differences in cortical function after medial frontal lesions in rats. Behav Neurosci 110, 1271-1281
28. Lomnitski, L., Chapman, S., Hochman, A., Kohen, R., Shohami, E., Chen, Y., Trembovler, V., and Michaelson, D. M. (1999). Antioxidant mechanisms in apolipoprotein E deficient mice prior to and following closed head injury. Biochim Biophys Acta Mol Basis Dis 1453, 359-368
29. MacLusky, N. J., Clark, A. S., Naftolin, F., and Goldman-Rakic, P. S. (1987). Estrogen formation in the mammalian brain: possible role of aromatase in sexual differentiation of the hippocampus and neocortex. Steroids 50, 4-6.
30. Madsen, T. M., Kristjansen, P. E. G., Bolwig, T. G., and Wortwein, G. (2003). Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119, 635-642
31. Maguire, E. A., and Cipolotti, L. (1998). Selective sparing of topographical memory. J Neurol Neurosurg Psych 65, 903-909
32. Mahley, R. W. (1988). Apolipoprotein E: cholesterol transport protein with expanding role in cell biology. Science 240, 622-630
33. Maren, S. (1995). Sexually dimorphic perforant path long-term potentiation (LTP) in urethane-anesthetized rats. Neurosci Lett 196, 177-180
34. Maren, S., De Oca, B., and Fanselow, M. (1994). Sex differences in hippocampal long-term potentiation (LTP) and Pavlovian fear conditioning in rats: positive correlation between LTP and contextual learning. Brain Res 661, 25-34.
35. McCarthy, R. A., Evans, J. J., and Hodges, J. R. (1996). Topographical amnesia: spatial memory disorder, perceptual dysfunction, or categoric specific semantic memory impairment? J Neurol Neurosurg Psychiatry 60, 318-325
36. Mickley, G. A., Ferguson, J. L., Mulvihill, M. A., and Nemeth, T. J. (1989). Progressive behavioral changes during the maturation of rats with early radiation-induced hypoplasia of fascia dentata granule cells. Neurotoxicol Teratol 11, 385-393
37. Mizumatsu, S., Monje, M., Morhardt, D., Rola, R., Palmer, T. D., and Fike, J. R. (2003). Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res 63, 4021-4027
38. Monje, M. L., Mizumatsu, S., Fike, J. R., and Palmer, T. D. (2002). Irradiation induces neural precursor-cell dysfunction. Nat Med 8, 955-962
39. Moreira, R. C. M., Moreira, M. V., Bueno, J. L. O., and Xavier, G. F. (1997). Hippocampal lesions induced by ionizing radiation: a parametric study. J Neurosci Meth 75, 41-47.
40. Mukaetova-Ladinska, E., Garcia-Sierra, F., Hurt, J., Gertz, H., Xuereb, J., Hills, R., Brayne, C., Huppert, F. A., Paykel, E. S., McGee, M., Jakes, R., Honer, W., Harrington, C., and Wischik, C. (2000). Staging of cytoskeletal and B-amyloid changs in human isocortex reveals biphasic synaptic protein response during progression of Alzheimer's disease. Am J Pathol 157, 623-636
41. Mulhern, R., and Butler, R. (2004). Neurocognitive sequelae of childhood cancers and their treatment. Pediatr Rehabil 7, 1-14. (Pubitemid 38160053)
42. O'Brien, J., Desmond, P., Ames, D., Schweitzer, I., and Tress, B. (1997). Magnetic resonance imaging correlates of memory impairment in the healthy elderly: association with medical temporal lobe atrophy but not white matter lesions. Int J Geriatr Psychiatr 12, 369-374
43. O'Keefe, J. A., Li, Y., Burgess, L. H., and Handa, R. J. (1995). Estrogen receptor mRNA alterations in the developing rat hippocampus. Mol Brain Res 30, 115-124
44. Packer, R., Sutton, L., and Atkins, T. (1989). A prospective study of cognitive functioning in children receiving whole-brain radiatherapy and chemotherapy: two year results. J Neurosurg 7079, 707-713
45. Raber, J. (2004). Differential gene actions of polymorphic alleles at the APOE locus; potential role of androgens and androgen receptor-mediated signaling. Science of Aging Knowledge Environ 11, re2.
46. Raber, J. (2008). AR, apoE, and cognitive function. Horm Behav 53, 706-715
47. Raber, J., Bongers, G., LeFevour, A., Buttini, M., and Mucke, L. (2002). Androgens protect against apolipoprotein E4-induced cognitive deficits. J Neurosci 22, 5204-5209
48. Raber, J., Fan, Y., Matsumori, Y.,Weistein, P. R., Fike, J. R., and Liu, J. (2004). Irradation attenuates neurogenesis in the dentate gyrus and exacerbates ischemia-induced functional deficits. Ann Neurol 55, 381-390
49. Raber, J., Rola, R., LeFevour, A., Morhardt, D., Curley, J., Mizumatsu, S., VandenBerg, S., and Fike, J. R. (2004). Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiation Res 162, 39-47. (Pubitemid 39044717)
50. Raber, J., Wong, D., Buttini, M., Orth, M., Bellosta, S., Pitas, R. E., Mahley, R. W., and Mucke, L. (1998). Isoform-specific effects of human apolipoprotein E on brain function revealed in ApoE knockout mice: increased susceptibility of females. Proc Natl Acad Sci U S A 95, 10914-10919
51. Raber, J., Wong, D., Yu, G.-Q., Buttini, M., Mahley, R. W., Pitas, R. E., and Mucke, L. (2000). Alzheimer's disease: apolipoprotein E and cognitive performance. Nature 404, 352-354
52. Resnick, S., Pham, D., Kraut, M., Zonderman, A., and Davatzikos, C. (2003). Longitudinal magnetic resonance imaging studies of older adults: a shrinking brain. J Neurosci 23, 3295-3301
53. Ris, M., Packer, R., Goldwein, J., Jones-Wallace, D., and Boyett, J. (2001). Intellectual outcome after reduced-dose radiation therapy plus adjuvant chemotherapy for medulloblastoma a children's cancer group study. J Clin Oncol 19, 3470-3476
54. Rola, R. (2004). High LET irradiation induced inflammation and persistent changes in markers of hippocampal neurogenesis. Rad Res:in press.
55. Rola, R., Otsuka, S., Obenaus, A., Nelson, G. A., Limoli, C. L., VandenBerg, S. R., and Fike, J. R. (2004). Indicators of hippocampal neurogenesis are altered by 56Fe irradiation in a dose-dependent manner. Rad Res 142, 442-446
56. Rola, R., Raber, J., Rizk, A., Otsuka, S., VandenBerg, S. R., Morhardt, D. R., and Fike, J. R. (2004). Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp Neurol 188, 316-330 (Pubitemid 38891593)
57. Rola, R., Zou, Y., Huang, T.-T., Fishman, K., Baure, J., Rosi, S., Milliken, H., Limoli, C. L., and Fike, J. R. (2007). Lack of extracellular superoxide dismutase (EC-SOD) in the microenvironment impacts radiation-induced changes in neurogenesis. Free Radic Biol Med 42, 1133-1145
58. Roman, D. D., and Sperduto, P. W. (1995). Neuropsychological effects of cranial radiation: current knowledge and future directions. Int J Radiat Oncol Biol Phys 31, 983-998
59. Sabo, T., Lomnitski, L., Nyska, A., Beni, S., Maronpot, R., Shohami, E., Roses, A. D., and Michaelson, D. (2000). Susceptibility of transgenic mice expressing human apolipoprotein E to closed head injury: the allele E3 is neuroprotective whereas E4 increases fatalities. Neuroscience 191, 879-884
60. Saxe, M., Battaglia, F., Wang, J.-W., Malleret, G., David, D., Monckton, J., Garcia, A., Sofroniew, M., Kandel, E., Santarelli, L., Hen, R., and Drew, M. (2006). Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Nat Acad Sci U S A 14, 17501-17506
61. Selkoe, D. K., and Schenk, D. (2003). Alzheimer's disease: molecular understanding predicts amyloid-based therapeutics. Annu Rev Pharmacol Toxicol 43, 545-584
62. Shukitt-Hale, B., Casadesus, G., McEwen, J., Rabin, B., and Joseph, J. (2000). Spatial learning and memory deficits induced by exposure to iron-56-particle radiation. Radiat Res 154, 28-33.
63. Small, G., La Rue, A., Komo, S., Kaplan, A., and Mandelkern, M. (1995). Predictors of cognitive change in middle-aged and older adults with memory loss. Am J Psychiatr 152, 1757-1764
64. Tada, E., Parent, J. M., Lowenstein, D. H., and Fike, J. R. (2000). X-irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 99, 33-41.
65. Tisserand, D., and Jolles, J. (2003). On the involvement of prefrontal networks in cognitive ageing. Cortex 39, 1107-1128
66. Vazquez-Pereyra, F., Rivas-Arancibia, S., and Castillo, A. L. D. (1995). Modulation of short-term and long-term memory by steroid sexual hormones. Life Sci 56, 255-260
67. Villasana, L., Acevedo, S., Poage, C., and Raber, J. (2006). Sex- and ApoE isoform-dependent effects of radiation on cognitive function. Radiat Res 166, 883-891
68. Villasana, L., Rosenberg, J., and Raber, J. (2009). Sex-dependent effects of 56Fe Irradiation on contextual fear conditioning in C56BL/6J mice. Hippocampus [in press].
69. Wallace, R. B., Graziadei, R., and Werboff, J. (1981). Behavioral correlates of focal hippocampal x-irradiation in rats. II. Behavior related to adaptive function in a natural setting. Exp Brain Res 43, 207-212
70. Yang, D., Pan, B., Han, T., and Xie, W. (2004). Sexual dimorphism in the induction of LTP: critical role of tetanizing stimulation. Life Sci 21, 119-127