Aging-Dependent Changes in the Radiation Response of the Adult Rat Brain

International Journal of Radiation Oncology Biology Physics

Volumn 70, Issue 3, 2008, Pages 826-834

  Schindler, Matthew K ^a   Forbes, M Elizabeth ^a   Robbins, Mike E ^a   Riddle, David R ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Hippocampus; Microglia; Neurogenesis; Whole brain irradiation

Indexed keywords

AGING OF MATERIALS; BRAIN; NEUROLOGY; RADIATION EFFECTS;

AGING; HIPPOCAMPUS; MICROGLIA; NEUROGENESIS; WHOLE-BRAIN IRRADIATION;

RADIOTHERAPY;

AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN NERVE CELL; BRAIN RADIATION; CELL ACTIVATION; CELL COUNT; CELL DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; DENTATE GYRUS; HIPPOCAMPUS; INFLAMMATION; MALE; MICROGLIA; NEUROBIOLOGY; NEUROBLAST; NONHUMAN; PRIORITY JOURNAL; RADIATION DOSE; RADIATION INJURY; RADIATION RESPONSE; RAT; SENSITIVITY ANALYSIS;

AGE FACTORS; AGING; ANIMALS; BRAIN; CELL COUNT; CELL PROLIFERATION; CRANIAL IRRADIATION; DENTATE GYRUS; MALE; MICROGLIA; NEURONS; RATS; RATS, INBRED F344;

EID: 39049086174     PISSN: 03603016     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijrobp.2007.10.054     Document Type: Article

References (62)

1. Crossen J.R., Garwood D., Glatstein E., et al. Neurobehavioral sequelae of cranial irradiation in adults: A review of radiation-induced encephalopathy. J Clin Oncol 12 (1994) 627-642
2. Johannesen T.B., Lien H.H., Hole K.H., et al. Radiological and clinical assessment of long-term brain tumour survivors after radiotherapy. Radiother Oncol 69 (2003) 169-176
3. Omuro A.M., Ben-Porat L.S., Panageas K.S., et al. Delayed neurotoxicity in primary central nervous system lymphoma. Arch Neurol 62 (2005) 1595-1600
4. Brandes A.A., Rigon A., and Monfardini S. Radiotherapy of the brain in elderly patients. Contra. Eur J Cancer 36 (2000) 447-451
5. Swennen M.H., Bromberg J.E., Witkamp T.D., et al. Delayed radiation toxicity after focal or whole brain radiotherapy for low-grade glioma. J Neurooncol 66 (2004) 333-339
6. Kortmann R.D., Timmermann B., Taylor R.E., et al. Current and future strategies in radiotherapy of childhood low-grade glioma of the brain. Part II: Treatment-related late toxicity. Strahlenther Onkol 179 (2003) 585-597
7. Jemal A., Siegel R., Ward E., et al. Cancer statistics. CA Cancer J Clin 2007 57 (2007) 43-66
8. Mizumatsu S., Monje M.L., Morhardt D.R., et al. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res 63 (2003) 4021-4027
9. Tada E., Parent J.M., Lowenstein D.H., et al. X-Irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 99 (2000) 33-41
10. Monje M.L., Toda H., and Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302 (2003) 1760-1765
11. Raber J., Rola R., LeFevour A., et al. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162 (2004) 39-47
12. Rola R., Raber J., Rizk A., et al. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp Neurol 188 (2004) 316-330
13. Monje M.L., Mizumatsu S., Fike J.R., et al. Irradiation induces neural precursor-cell dysfunction. Nat Med 8 (2002) 955-962
14. Gilmore S.A., Phillips N., Liu K.M., et al. Radiation-induced modulation of the microglial population in the normal and injured mature spinal cord. Exp Neurol 182 (2003) 169-179
15. Kuhn H.G., Dickinson-Anson H., and Gage F.H. Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. J Neurosci 16 (1996) 2027-2033
16. Lichtenwalner R.J., Forbes M.E., Bennett S.A., et al. Intracerebroventricular infusion of insulin-like growth factor-I ameliorates the age-related decline in hippocampal neurogenesis. Neuroscience 107 (2001) 603-613
17. Rao M.S., Hattiangady B., and Shetty A.K. The window and mechanisms of major age-related decline in the production of new neurons within the dentate gyrus of the hippocampus. Aging Cell 5 (2006) 545-558
18. Klempin F., and Kempermann G. Adult hippocampal neurogenesis and aging. Eur Arch Psychiatry Clin Neurosci 257 (2007) 271-280
19. Perry V.H., Matyszak M.K., and Fearn S. Altered antigen expression of microglia in the aged rodent CNS. Glia 7 (1993) 60-67
20. Griffin R., Nally R., Nolan Y., et al. The age-related attenuation in long-term potentiation is associated with microglial activation. J Neurochem 99 (2006) 1263-1272
21. Frank M.G., Barrientos R.M., Biedenkapp J.C., et al. mRNA up-regulation of MHC II and pivotal pro-inflammatory genes in normal brain aging. Neurobiol Aging 27 (2006) 717-722
22. Sierra A., Gottfried-Blackmore A.C., McEwen B.S., et al. Microglia derived from aging mice exhibit an altered inflammatory profile. Glia 55 (2007) 412-424
23. Yager J.Y., Shuaib A., and Thornhill J. The effect of age on susceptibility to brain damage in a model of global hemispheric hypoxia-ischemia. Brain Res Dev Brain Res 93 (1996) 143-154
24. Kyrkanides S., O'Banion M.K., Whiteley P.E., et al. Enhanced glial activation and expression of specific CNS inflammation-related molecules in aged versus young rats following cortical stab injury. J Neuroimmunol 119 (2001) 269-277
25. Conde J.R., and Streit W.J. Effect of aging on the microglial response to peripheral nerve injury. Neurobiol Aging 27 (2006) 1451-1461
26. Badan I., Buchhold B., Hamm A., et al. Accelerated glial reactivity to stroke in aged rats correlates with reduced functional recovery. J Cereb Blood Flow Metab 23 (2003) 845-854
27. Popa-Wagner A., Badan I., Walker L., et al. Accelerated infarct development, cytogenesis and apoptosis following transient cerebral ischemia in aged rats. Acta Neuropathol (Berl) 113 (2007) 277-293
28. Deng X.H., Bertini G., Xu Y.Z., et al. Cytokine-induced activation of glial cells in the mouse brain is enhanced at an advanced age. Neuroscience 141 (2006) 645-661
29. Lamproglou I., Chen Q.M., Boisserie G., et al. Radiation-induced cognitive dysfunction: An experimental model in the old rat. Int J Radiat Oncol Biol Phys 31 (1995) 65-70
30. Lamproglou I., Baillet F., Boisserie G., et al. [The influence of age on radiation-induced cognitive deficit: Experimental studies on brain irradiation of 30 Gy in 10 sessions and 12 hours in the Wistar rat at 1 1/2, 4 and 18 months age]. Can J Physiol Pharmacol 80 (2002) 679-685
31. Kee N., Sivalingam S., Boonstra R., et al. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Methods 115 (2002) 97-105
32. Damoiseaux J.G., Dopp E.A., Calame W., et al. Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1. Immunology 83 (1994) 140-147
33. Ito D., Imai Y., Ohsawa K., et al. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57 (1998) 1-9
34. Brown J.P., Couillard-Despres S., Cooper-Kuhn C.M., et al. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467 (2003) 1-10
35. Kempermann G., Kuhn H.G., and Gage F.H. Experience-induced neurogenesis in the senescent dentate gyrus. J Neurosci 18 (1998) 3206-3212
36. Gundersen H.J., Bagger P., Bendtsen T.F., et al. The new stereological tools: Disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96 (1988) 857-881
37. Sprott R.L., and Austad S.N. Animal models for aging research. In: Schneider E.L., and Rowe J.W. (Eds). Handbook of the biology of aging. 4th ed. (1995), Academic Press, San Diego 3-24
38. Clancy B., Darlington R.B., and Finlay B.L. Translating developmental time across mammalian species. Neuroscience 105 (2001) 7-17
39. Clancy B., Finlay B.L., Darlington R.B., et al. Extrapolating brain development from experimental species to humans. Neurotoxicology 28 (2007) 931-937
40. de Graaf-Peters V.B., and Hadders-Algra M. Ontogeny of the human central nervous system: What is happening when?. Early Hum Dev 82 (2006) 257-266
41. Rice D., and Barone Jr. S. Critical periods of vulnerability for the developing nervous system: Evidence from humans and animal models. Environ Health Perspect 108 Suppl. 3 (2000) 511-533
42. Arias E. United States life tables. Natl Vital Stat Rep 2006 54 (2003) 1-40
43. Fan Y., Liu Z., Weinstein P.R., et al. Environmental enrichment enhances neurogenesis and improves functional outcome after cranial irradiation. Eur J Neurosci 25 (2007) 38-46
44. Olariu A., Cleaver K.M., and Cameron H.A. Decreased neurogenesis in aged rats results from loss of granule cell precursors without lengthening of the cell cycle. J Comp Neurol 501 (2007) 659-667
45. Rao M.S., and Shetty A.K. Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19 (2004) 234-246
46. Couillard-Despres S., Winner B., Schaubeck S., et al. Doublecortin expression levels in adult brain reflect neurogenesis. Eur J Neurosci 21 (2005) 1-14
47. Plumpe T., Ehninger D., Steiner B., et al. Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 7 (2006) 77-90
48. Butler J.M., Rapp S.R., and Shaw E.G. Managing the cognitive effects of brain tumor radiation therapy. Curr Treat Options Oncol 7 (2006) 517-523
49. Lee P.W., Hung B.K., Woo E.K., et al. Effects of radiation therapy on neuropsychological functioning in patients with nasopharyngeal carcinoma. J Neurol Neurosurg Psychiatry 52 (1989) 488-492
50. Byrne T.N. Cognitive sequelae of brain tumor treatment. Curr Opin Neurol 18 (2005) 662-666
51. Shaw E.G., Rosdhal R., D'Agostino Jr. R.B., et al. Phase II study of donepezil in irradiated brain tumor patients: Effect on cognitive function, mood, and quality of life. J Clin Oncol 24 (2006) 1415-1420
52. Robbins M.E., and Diz D.I. Pathogenic role of the renin-angiotensin system in modulating radiation-induced late effects. Int J Radiat Oncol Biol Phys 64 (2006) 6-12
53. Zhao W., Payne V., Tommasi E., et al. Administration of the peroxisomal proliferator-activated receptor gamma agonist pioglitazone during fractionated brain irradiation prevents radiation-induced cognitive impairment. Int J Radiat Oncol Biol Phys 67 (2007) 6-9
54. Perry V.H., Cunningham C., and Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol 7 (2007) 161-167
55. Wilson C.J., Finch C.E., and Cohen H.J. Cytokines and cognition-The case for a head-to-toe inflammatory paradigm. J Am Geriatr Soc 50 (2002) 2041-2056
56. McGeer P.L., and McGeer E.G. Inflammation and neurodegeneration in Parkinson's disease. Parkinsonism Relat Disord 10 Suppl. 1 (2004) S3-S7
57. Long J.M., Kalehua A.N., Muth N.J., et al. Stereological analysis of astrocyte and microglia in aging mouse hippocampus. Neurobiol Aging 19 (1998) 497-503
58. Town T., Nikolic V., and Tan J. The microglial "activation" continuum: From innate to adaptive responses. J Neuroinflammation 2 (2005) 24-33
59. Sloane J.A., Hollander W., Moss M.B., et al. Increased microglial activation and protein nitration in white matter of the aging monkey. Neurobiol Aging 20 (1999) 395-405
60. Sheng J.G., Mrak R.E., and Griffin W.S. Enlarged and phagocytic, but not primed, interleukin-1 alpha-immunoreactive microglia increase with age in normal human brain. Acta Neuropathol (Berl) 95 (1998) 229-234
61. Nakajima K., Tohyama Y., Maeda S., et al. Neuronal regulation by which microglia enhance the production of neurotrophic factors for GABAergic, catecholaminergic, and cholinergic neurons. Neurochem Int 50 (2007) 807-820
62. Elkabes S., Cicco-Bloom E.M., and Black I.B. Brain microglia/macrophages express neurotrophins that selectively regulate microglial proliferation and function. J Neurosci 16 (1996) 2508-2521