Lack of extracellular superoxide dismutase (EC-SOD) in the microenvironment impacts radiation-induced changes in neurogenesis

Free Radical Biology and Medicine

Volumn 42, Issue 8, 2007, Pages 1133-1145

  Rola, Radoslaw ^a,b   Zou, Yani ^c   Huang, Ting Ting ^c,d   Fishman, Kelly ^a   Baure, Jennifer ^a   Rosi, Susanna ^a,e   Milliken, Heather ^e   Limoli, Charles L ^f   Fike, John R ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MEDICAL UNIVERSITY OF LUBLIN   (Poland)

^c STANFORD UNIVERSITY   (United States)

^d VA PALO ALTO HEALTH CARE SYSTEM   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain; Extracellular SOD; Inflammation; Neurogenesis; Oxidative stress; Radiation

Indexed keywords

EXTRACELLULAR SUPEROXIDE DISMUTASE; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; GENOTYPE; HIPPOCAMPUS; KNOCKOUT MOUSE; MALE; MICROENVIRONMENT; MOUSE; NERVE CELL; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEPLETION; QUANTITATIVE ANALYSIS; RADIATION DOSE; RADIATION INJURY; RADIATION RESPONSE; WILD TYPE;

ANIMALS; CEREBRAL CORTEX; COGNITION DISORDERS; HIPPOCAMPUS; MALE; MICE; MICE, KNOCKOUT; MICROGLIA; NEURONS; OXIDATIVE STRESS; RADIATION, IONIZING; SUPEROXIDE DISMUTASE;

MUS;

EID: 33947193944     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.01.020     Document Type: Article

References (83)

1. Hopewell J.W. Radiation injury to the central nervous system. Med. Pediatr. Oncol. Suppl. 1 (1998) 1-9
2. Tofilon P.J., and Fike J.R. The radioresponse of the central nervous system: A dynamic process. Radiat. Res. 153 (2000) 357-370
3. Fike J.R., and Gobbel G.T. Central nervous system radiation injury in large animal models. In: Sheline G.E. (Ed). Radiation injury to the nervous system (1991), Raven Press, New York 113-135
4. van der Kogel A.J. Central nervous system radiation injury in small animal models. In: Sheline G.E. (Ed). Radiation injury to the nervous system (1991), Raven Press, New York 91-111
5. Abayomi O.K. Pathogenesis of irradiation-induced cognitive dysfunction. Acta Oncol. 35 (1996) 659-663
6. Crossen J.R., Garwood D., Glatstein E., and Neuwelt E.A. Neurobehavioral sequelae of cranial irradiation in adults: a review of radiation-induced encephalopathy. J. Clin. Oncol. 12 (1994) 627-642
7. Lee P.W., Hung B.K., Woo E.K., Tai P.T., and Choi D.T. Effects of radiation therapy on neuropsychological functioning in patients with nasopharyngeal carcinoma. J. Neurol. Neurosurg. Psychiatry 52 (1989) 488-492
8. Roman D.D., and Sperduto P.W. Neuropsychological effects of cranial radiation: current knowledge and future directions. Int. J. Radiat. Oncol. Biol. Phys. 31 (1995) 983-998
9. Surma-aho O., Niemela M., Vilkki J., Kouri M., Brander A., Salonen O., Paetau A., Kallio M., Pyykkonen J., and Jaaskelainen J. Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients. Neurology 56 (2001) 1285-1290
10. Monje M.L., Mizumatsu S., Fike J.R., and Palmer T.D. Irradiation induces neural precursor-cell dysfunction. Nat. Med. 8 (2002) 955-962
11. Mizumatsu S., Monje M.L., Morhardt D.R., Rola R., Palmer T.D., and Fike J.R. Extreme sensitivity of adult neurogenesis to low doses of X-irradiation. Cancer Res. 63 (2003) 4021-4027
12. Madsen T.M., Kristjansen P.E., Bolwig T.G., and Wortwein G. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience 119 (2003) 635-642
13. Rola R., Raber J., Rizk A., Otsuka S., VandenBerg S.R., Morhardt D.R., and Fike J.R. Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp. Neurol. 188 (2004) 316-330
14. Raber J., Rola R., LeFevour A., Morhardt D., Curley J., Mizumatsu S., VandenBerg S.R., and Fike J.R. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat. Res. 162 (2004) 39-47
15. Suhonen J.O., Peterson D.A., Ray J., and Gage F.H. Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383 (1996) 624-627
16. Luskin M. Neuroblasts of the postnatal mammalian forebrain: their phenotype and fate. J. Neurobiol. 36 (1998) 221-233
17. Palmer T.D., Willhoite A.R., and Gage F.H. Vascular niche for adult hippocampal neurogenesis. J. Comp. Neurol. 425 (2000) 479-494
18. Song H., Stevens C.F., and Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature 417 (2002) 39-44
19. Smith M.A., Nunomura A., Zhu X., Takeda A., and Perry G. Metabolic, metallic, and mitotic sources of oxidative stress in Alzheimer disease. Antioxid. Redox Signal. 2 (2000) 413-420
20. Smith K.J., Kapoor R., and Felts P.A. Demyelination: the role of reactive oxygen and nitrogen species. Brain Pathol. 9 (1999) 69-92
21. Peuchen S., Bolanos J.P., Heales S.J., Almeida A., Duchen M.R., and Clark J.B. Interrelationships between astrocyte function, oxidative stress and antioxidant status within the central nervous system. Prog. Neurobiol. 52 (1997) 261-281
22. Lin M.T., and Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 443 (2006) 787-795
23. Forster M.J., Dubey A., Dawson K.M., Stutts W.A., Lal H., and Sohal R.S. Age-related losses of cognitive function and motor skills in mice are associated with oxidative protein damage in the brain. Proc. Natl. Acad. Sci. USA 93 (1996) 4765-4769
24. Juurlink B.H., and Paterson P.G. Review of oxidative stress in brain and spinal cord injury: suggestions for pharmacological and nutritional management strategies. J. Spinal Cord Med. 21 (1998) 309-334
25. Love S. Oxidative stress in brain ischemia. Brain Pathol. 9 (1999) 119-131
26. Schnell L., Fearn S., Klassen H., Schwab M.E., and Perry V.H. Acute inflammatory responses to mechanical lesions in the CNS: differences between brain and spinal cord. Eur. J. Neurosci. 11 (1999) 3648-3658
27. Schultheiss T.E., and Stephens L.C. Invited review: permanent radiation myelopathy. Br. J. Radiol. 65 (1992) 737-753
28. Limoli C.L., Giedzinski E., Rola R., Otsuka S., Palmer T.D., and Fike J.R. Radiation response of neural precursor cells: linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress. Radiat. Res. 161 (2004) 17-27
29. Limoli C.L., Rola R., Giedzinski E., Mantha S., Huang T.T., and Fike J.R. Cell-density-dependent regulation of neural precursor cell function. Proc. Natl. Acad. Sci. USA 101 (2004) 16052-16057
30. Lonergan P.E., Martin D.S., Horrobin D.F., and Lynch M.A. Neuroprotective effect of eicosapentaenoic acid in hippocampus of rats exposed to gamma-irradiation. J. Biol. Chem 277 (2002) 20804-20811
31. Riley P.A. Free radicals in biology: oxidative stress and the effects of ionizing radiation. Int. J. Radiat. Biol. 65 (1994) 27-33
32. Huang T.T., Carlson E.J., Raineri I., Gillespie A.M., Kozy H., and Epstein C.J. The use of transgenic and mutant mice to study oxygen free radical metabolism. Ann. N. Y. Acad. Sci. 893 (1999) 95-112
33. Thiels E., Urban N.N., Gonzalez-Burgos G.R., Kanterewicz B.I., Barrionuevo G., Chu C.T., Oury T.D., and Klann E. Impairment of long-term potentiation and associative memory in mice that overexpress extracellular superoxide dismutase. J. Neurosci. 20 (2000) 7631-7639
34. Levin E.D., Brady T.C., Hochrein E.C., Oury T.D., Jonsson L.M., Marklund S.L., and Crapo J.D. Molecular manipulations of extracellular superoxide dismutase: functional importance for learning. Behav. Genet. 28 (1998) 381-390
35. Carlsson L.M., Jonsson J., Edlund T., and Marklund S.L. Mice lacking extracellular superoxide dismutase are more sensitive to hyperoxia. Proc. Natl. Acad. Sci. USA 92 (1995) 6264-6268
36. Huang T.T., Raineri I., Eggerding F., and Epstein C.J. Transgenic and mutant mice for oxygen free radical studies. Methods Enzymol. 349 (2002) 191-213
37. Slotnick B.M., and Leonard C.M. A stereotaxic atlas of the albino mouse forebrain (1975), U.S. Dept. of Health Education and Welfare Public Health Service Alcohol Drug Abuse and Mental Health Administration, Rockville, MD
38. Shinohara C., Gobbel G.T., Lamborn K.R., Tada E., and Fike J.R. Apoptosis in the subependyma of young adult rats after single and fractionated doses of X-rays. Cancer Res. 57 (1997) 2694-2702
39. Tada E., Parent J.M., Lowenstein D.H., and Fike J.R. X-irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 99 (2000) 33-41
40. Fisher B.J., Naumova E., Leighton C.C., Naumov G.N., Kerklviet N., Fortin D., Macdonald D.R., Cairncross J.G., Bauman G.S., and Stitt L. Ki-67: a prognostic factor for low-grade glioma?. Int. J. Radiat. Oncol. Biol. Phys. 52 (2002) 996-1001
41. Kee N., Sivalingam S., Boonstra R., and Wojtowicz J.M. The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J. Neurosci. Methods 115 (2002) 97-105
42. Mizuguchi M., Qin J., Yamada M., Ikeda K., and Takashima S. High expression of doublecortin and KIAA0369 protein in fetal brain suggests their specific role in neuronal migration. Am. J. Pathol. 155 (1999) 1713-1721
43. Nacher J., Crespo C., and McEwen B.S. Doublecortin expression in the adult rat telencephalon. Eur. J. Neurosci. 14 (2001) 629-644
44. Englund U., Bjorklund A., and Wictorin K. Migration patterns and phenotypic differentiation of long-term expanded human neural progenitor cells after transplantation into the adult rat brain. Brain Res. Dev. Brain Res. 134 (2002) 123-141
45. Kempermann G., Gast D., Kronenberg G., Yamaguchi M., and Gage F.H. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130 (2003) 391-399
46. Jessberger S., and Kempermann G. Adult-born hippocampal neurons mature into activity-dependent responsiveness. Eur. J. Neurosci. 18 (2003) 2707-2712
47. Tada E., Yang C., Gobbel G.T., Lamborn K.R., and Fike J.R. Long-term impairment of subependymal repopulation following damage by ionizing irradiation. Exp. Neurol. 160 (1999) 66-77
48. Parent J.M., Tada E., Fike J.R., and Lowenstein D.H. Inhibition of dentate granule cell neurogenesis with brain irradiation does not prevent seizure-induced mossy fiber synaptic reorganization in the rat. J. Neurosci. 19 (1999) 4508-4519
49. Rola R., Mizumatsu S., Otsuka S., Morhardt D.R., Noble-Haeusslein L.J., Fishman K., Potts M.B., and Fike J.R. Alterations in hippocampal neurogenesis following traumatic brain injury in mice. Exp. Neurol. 202 (2006) 189-199
50. Abercrombie M. Estimation of nuclear population from microtomic sections. Anat. Rec. 94 (1946) 239-247
51. Rosi S., Ramirez-Amaya V., Vazdarjanova A., Worley P.F., Barnes C.A., and Wenk G.L. Neuroinflammation alters the hippocampal pattern of behaviorally induced Arc expression. J. Neurosci. 25 (2005) 723-731
52. Halliwell B.G.J. Free radicals in biology and medicine (1999), Oxford University Press, London
53. Bu J., Akhtar N., and Nishiyama A. Transient expression of the NG2 proteoglycan by a subpopulation of activated macrophages in an excitotoxic hippocampal lesion. Glia 34 (2001) 296-310
54. Jones L.L., Yamaguchi Y., Stallcup W.B., and Tuszynski M.H. NG2 is a major chondroitin sulfate proteoglycan produced after spinal cord injury and is expressed by macrophages and oligodendrocyte progenitors. J. Neurosci. 22 (2002) 2792-2803
55. Abayomi O.K. Pathogenesis of cognitive decline following therapeutic irradiation for head and neck tumors. Acta Oncol. 41 (2002) 346-351
56. Monje M.L., Toda H., and Palmer T.D. Inflammatory blockade restores adult hippocampal neurogenesis. Science 302 (2003) 1760-1765
57. Raber J., Fan Y., Matsumori Y., Liu Z., Weinstein P.R., Fike J.R., and Liu J. Irradiation attenuates neurogenesis and exacerbates ischemia-induced deficits. Ann. Neurol. 55 (2004) 381-389
58. Winocur G., Wojtowicz J.M., Sekeres M., Snyder J.S., and Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16 (2006) 296-304
59. Rola R., Sarkissian V., Obenaus A., Nelson G.A., Otsuka S., Limoli C.L., and Fike J.R. High-LET radiation induces inflammation and persistent changes in markers of hippocampal neurogenesis. Radiat. Res. 164 (2005) 556-560
60. Otsuka S., Coderre J.A., Micca P.L., Morris G.M., Hopewell J.W., Rola R., and Fike J.R. Depletion of neural precursor cells after local brain irradiation is due to radiation dose to the parenchyma, not the vasculature. Radiat. Res. 165 (2006) 582-591
61. Giedzinski E., Rola R., Fike J.R., and Limoli C.L. Efficient production of reactive oxygen species in neural precursor cells after exposure to 250 MeV protons. Radiat. Res. 164 (2005) 540-544
62. Oury T.D., Card J.P., and Klann E. Localization of extracellular superoxide dismutase in adult mouse brain. Brain Res. 850 (1999) 96-103
63. Hu D., Serrano F., Oury T.D., and Klann E. Aging-dependent alterations in synaptic plasticity and memory in mice that overexpress extracellular superoxide dismutase. J. Neurosci. 26 (2006) 3933-3941
64. Benzie I.F., and Strain J.J. Ferric reducing/antioxidant power assay: direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol. 299 (1999) 15-27
65. Kempermann G. Why new neurons? Possible functions for adult hippocampal neurogenesis. J. Neurosci. 22 (2002) 635-638
66. Kempermann G. Neuronal stem cells and adult neurogenesis. Ernst Schering Res. Found Workshop (2002) 17-28
67. Kempermann G., Kuhn H.G., and Gage F.H. More hippocampal neurons in adult mice living in an enriched environment. Nature 386 (1997) 493-495
68. van Praag H., Schinder A.F., Christie B.R., Toni N., Palmer T.D., and Gage F.H. Functional neurogenesis in the adult hippocampus. Nature 415 (2002) 1030-1034
69. Schaller B., and Graf R. Cerebral ischemic preconditioning. An experimental phenomenon or a clinical important entity of stroke prevention?. J. Neurol. 249 (2002) 1503-1511
70. Gori T., and Forconi S. The role of reactive free radicals in ischemic preconditioning-clinical and evolutionary implications. Clin. Hemorheol. Microcirc. 33 (2005) 19-28
71. Pespeni M., Hodnett M., and Pittet J.F. In vivo stress preconditioning. Methods 35 (2005) 158-164
72. Scharfman H., Goodman J., Macleod A., Phani S., Antonelli C., and Croll S. Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192 (2005) 348-356
73. Cao L., Jiao X., Zuzga D.S., Liu Y., Fong D.M., Young D., and During M.J. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat. Genet. 36 (2004) 827-835
74. Cardenas A., Moro M.A., Hurtado O., Leza J.C., and Lizasoain I. Dual role of nitric oxide in adult neurogenesis. Brain Res. Brain Res. Rev. 50 (2005) 1-6
75. Gibbs S.M. Regulation of neuronal proliferation and differentiation by nitric oxide. Mol. Neurobiol. 27 (2003) 107-120
76. Battista D., Ferrari C.C., Gage F.H., and Pitossi F.J. Neurogenic niche modulation by activated microglia: transforming growth factor beta increases neurogenesis in the adult dentate gyrus. Eur. J. Neurosci. 23 (2006) 83-93
77. Butovsky O., Ziv Y., Schwartz A., Landa G., Talpalar A.E., Pluchino S., Martino G., and Schwartz M. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol. Cell. Neurosci. 31 (2006) 149-160
78. Seri B., Garcia-Verdugo J.M., McEwen B.S., and Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21 (2001) 7153-7160
79. Baydas G., and Tuzcu M. Protective effects of melatonin against ethanol-induced reactive gliosis in hippocampus and cortex of young and aged rats. Exp. Neurol. 194 (2005) 175-181
80. Calvo W., Hopewell J.W., Reinhold H.S., and Yeung T.K. Time- and dose-related changes in the white matter of the rat brain after single doses of X-rays. Br. J. Radiol. 61 (1988) 1043-1052
81. Seki T. Microenvironmental elements supporting adult hippocampal neurogenesis. Anat. Sci. Int. 78 (2003) 69-78
82. Ekdahl C.T., Claasen J.H., Bonde S., Kokaia Z., and Lindvall O. Inflammation is detrimental for neurogenesis in adult brain. Proc. Natl. Acad. Sci. USA 100 (2003) 13632-13637
83. Schwartz M., Butovsky O., Bruck W., and Hanisch U.K. Microglial phenotype: is the commitment reversible?. Trends Neurosci. 29 (2006) 68-74