Seminars in Radiation Oncology
Volume 19, Issue 2 , Pages 122-132 , April 2009

Neural Precursor Cells and Central Nervous System Radiation Sensitivity

  • John R. Fike, PhD

      Affiliations

    • Brain and Spinal Injury Center, University of California, San Francisco, CA
    • Department of Neurological Surgery, University of California, San Francisco, CA
    • Radiation Oncology, University of California, San Francisco, CA
    • Corresponding Author InformationAddress reprint requests to John R. Fike, PhD, Brain and Spinal Injury Center, San Francisco General Hospital, Bldg 1, Rm 101, 1001 Potrero Ave, San Francisco, CA 94110-0899
  • ,
  • Susanna Rosi, PhD

      Affiliations

    • Brain and Spinal Injury Center, University of California, San Francisco, CA
    • Department of Neurological Surgery, University of California, San Francisco, CA
    • Physical Therapy and Rehabilitation Science, University of California, San Francisco, CA
  • ,
  • Charles L. Limoli, PhD

      Affiliations

    • Department of Radiation Oncology, University of California, Irvine, CA

References 

  1. Meyers CA, Brown PD. Role and relevance of neurocognitive assessment in clinical trials of patients with CNS tumors. J Clin Oncol. 2006;24:1305–1309
  2. Butler JM, Rapp SR, Shaw EG. Managing the cognitive effects of brain tumor radiation therapy. Curr Treat Options Oncol. 2006;7:517–523
  3. Yazlovitskaya EM, Edwards E, Thotala D, et al. Lithium treatment prevents neurocognitive deficit resulting from cranial irradiation. Cancer Res. 2006;66:11179–11186
  4. 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. 2007;67:6–9
  5. Tofilon PJ, Fike JR. The radioresponse of the central nervous system: A dynamic process. Radiat Res. 2000;153:357–370
  6. Sheline GE, Wara WM, Smith V. Therapeutic irradiation and brain injury. Int J Radiat Oncol Biol Phys. 1980;6:1215–1228
  7. Abayomi OK. Pathogenesis of irradiation-induced cognitive dysfunction. Acta Oncol. 1996;35:659–663
  8. Roman DD, Sperduto PW. Neuropsychological effects of cranial radiation: Current knowledge and future directions. Int J Radiat Oncol Biol Phys. 1995;31:983–998
  9. Surma-aho O, Niemela M, Vilkki J, et al. Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients. Neurology. 2001;56:1285–1290
  10. Raber J, Fan Y, Matsumori Y, et al. Irradiation attenuates neurogenesis and exacerbates ischemia-induced deficits. Ann Neurol. 2004;55:381–389
  11. Raber J, Rola R, LeFevour A, et al. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res. 2004;162:39–47
  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. 2004;188:316–330
  13. Madsen TM, Kristjansen PE, Bolwig TG, et al. Arrested neuronal proliferation and impaired hippocampal function following fractionated brain irradiation in the adult rat. Neuroscience. 2003;119:635–642
  14. Winocur G, Wojtowicz JM, Sekeres M, et al. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus. 2006;16:296–304
  15. Gage FH. Mammalian neural stem cells. Science. 2000;287:1433–1438
  16. Santarelli L, Saxe M, Gross C, et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science. 2003;301:805–809
  17. Monje ML, Vogel H, Masek M, et al. Impaired human hippocampal neurogenesis after treatment for central nervous system malignancies. Ann Neurol. 2007;62:515–520
  18. Fan Y, Liu Z, Weinstein PR, et al. Environmental enrichment enhances neurogenesis and improves functional outcome after cranial irradiation. Eur J Neurosci. 2007;25:38–46
  19. Shi L, Adams MM, Long A, et al. Spatial learning and memory deficits after whole-brain irradiation are associated with changes in NMDA receptor subunits in the hippocampus. Radiat Res. 2006;166:892–899
  20. Villasana L, Acevedo S, Poage C, et al. Sex- and APOE isoform-dependent effects of radiation on cognitive function. Radiat Res. 2006;166:883–891
  21. Fike JR, Rola R, Limoli CL. Radiation response of neural precursor cells. Neurosurg Clin North Am. 2007;18:115–127
  22. Mizumatsu S, Monje ML, Morhardt DR, et al. Extreme sensitivity of adult neurogenesis to low doses of x-irradiation. Cancer Res. 2003;63:4021–4027
  23. Monje ML, Mizumatsu S, Fike JR, et al. Irradiation induces neural precursor-cell dysfunction. Nat Med. 2002;8:955–962
  24. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science. 2003;302:1760–1765
  25. Rola R, Zou Z, Huang T-T, et al. Lack of EC-SOD in the microenvironment impacts radiation-induced changes in neurogenesis. Free Radic Biol Med. 2007;42:1133–1145
  26. Chojnacki A, Shimazaki T, Gregg C, et al. Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J Neurosci. 2003;23:1730–1741
  27. Gage FH, Kempermann G, Palmer TD, et al. Multipotent progenitor cells in the adult dentate gyrus. J Neurobiol. 1998;36:249–266
  28. Lu FG, Wong CS. Time-dependent neurosphere-forming ability of adult rat spinal cord after irradiation. Radiat Res. 2007;168:453–461
  29. Palmer TD, Ray J, Gage FH. FGF-2-responsive neuronal progenitors reside in proliferative and quiescent regions of the adult rodent brain. Mol Cell Neurosci. 1995;6:474–486
  30. Palmer TD, Schwartz PH, Taupin P, et al. Cell culture (Progenitor cells from human brain after death). Nature. 2001;411:42–43
  31. Tarasenko YI, Yu Y, Jordan PM, et al. Effect of growth factors on proliferation and phenotypic differentiation of human fetal neural stem cells. J Neurosci Res. 2004;78:625–636
  32. Louis SA, Rietze RL, Deleyrolle L, et al. Enumeration of neural stem and progenitor cells in the neural colony-forming cell assay. Stem Cells. 2008;26:988–996
  33. Lu F, Wong CS. A clonogenic survival assay of neural stem cells in rat spinal cord after exposure to ionizing radiation. Radiat Res. 2005;163:63–71
  34. Reynolds BA, Rietze RL. Neural stem cells and neurospheres—Re-evaluating the relationship. Nat Methods. 2005;2:333–336
  35. Limoli CL, Rola R, Giedzinski E, et al. Cell density dependent regulation of neural precursor cell function. Proc Natl Acad Sci U S A. 2004;101:16052–16057
  36. Giedzinski E, Rola R, Fike JR, et al. Efficient production of reactive oxygen species in neural precursor cells after exposure to 250 MeV protons. Radiat Res. 2005;164:540–544
  37. Limoli CL, Giedzinski E, Baure J, et al. Using superoxide dismutase/catalase mimetics to manipulate the redox environment of neural precursor cells. Radiat Prot Dosim. 2006;122:228–236
  38. Limoli CL, Giedzinski E, Baure J, et al. Altered growth and radiosensitivity in neural precursor cells subjected to oxidative stress. Int J Radiat Biol. 2006;82:640–647
  39. Limoli CL, Giedzinski E, Baure J, et al. Redox changes induced in hippocampal precursor cells by heavy ion irradiation. Radiat Environ Biophys. 2007;46:167–172
  40. Limoli CL, Giedzinski E, Rola R, et al. Radiation response of neural precursor cells: Linking cellular sensitivity to cell cycle checkpoints, apoptosis and oxidative stress. Radiat Res. 2004;161:17–27
  41. Mikkelsen RB, Wardman P. Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene. 2003;22:5734–5754
  42. King MP, Attardi G. Isolation of human cell lines lacking mitochondrial DNA. Methods Enzymol. 1996;264:304–313
  43. Clarke MF, Dick JE, Dirks PB, et al. Cancer stem cells—Perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res. 2006;66:9339–9344
  44. Dalerba P, Cho RW, Clarke MF. Cancer stem cells: Models and concepts. Annu Rev Med. 2007;58:267–284
  45. Hill RP, Perris R. “Destemming” cancer stem cells. J Natl Cancer Inst. 2007;99:1435–1440
  46. Nakano I, Kornblum HI. Brain tumor stem cells. Pediatr Rev. 2006;59:54R–58R
  47. Sanai N, Alvarez-Buylla A, Berger MS. Neural stem cells and the origin of gliomas. N Engl J Med. 2005;353:811–822
  48. Singh S, Dirks PB. Brain tumor stem cells: Identification and concepts. Neurosurg Clin North Am. 2007;18:31–38
  49. Bao S, Wu Q, McLendon RE, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–760
  50. Nakano I, Masterman-Smith M, Saigusa K, et al. Maternal embryonic leucine zipper kinase is a key regulator of the proliferation of malignant brain tumors, including brain tumor stem cells. J Neurosci Res. 2008;86:48–60
  51. Nakano I, Paucar AA, Bajpai R, et al. Maternal embryonic leucine zipper kinase (MELK) regulates multipotent neural progenitor proliferation. J Cell Biol. 2005;170:413–427
  52. Becq H, Jorquera I, Ben-Ari Y, et al. Differential properties of dentate gyrus and CA1 neural precursors. J Neurobiol. 2005;62:243–261
  53. Seaberg RM, van der Kooy D. Adult rodent neurogenic regions: The ventricular subependyma contains neural stem cells, but the dentate gyrus contains restricted progenitors. J Neurosci. 2002;22:1784–1793
  54. Prozorovski T, Schulze-Topphoff U, Glumm R, et al. Sirt1 contributes critically to the redox-dependent fate of neural progenitors. Nat Cell Biol. 2008;10:385–394
  55. Kempermann G, Gast D, Kronenberg G, et al. Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development. 2003;130:391–399
  56. Rola R, Fishman K, Baure J, et al. Hippocampal neurogenesis and neuroinflammation after cranial irradiation with (56)fe particles. Radiat Res. 2008;169:626–632
  57. Lewen A, Matz P, Chan PH. Free radical pathways in CNS injury. J Neurotrauma. 2000;17:871–890
  58. Smith KJ, Kapoor R, Felts PA. Demyelination: The role of reactive oxygen and nitrogen species. Brain Pathol. 1999;9:69–92
  59. Schultheiss TE, Stephens LC. Permanent radiation myelopathy. Br J Radiol. 1992;65:737–753
  60. Lonergan PE, Martin DS, Horrobin DF, et al. Neuroprotective effect of eicosapentaenoic acid in hippocampus of rats exposed to gamma-irradiation. J Biol Chem. 2002;277:20804–20811
  61. Huang TT, Carlson EJ, Raineri I, et al. The use of transgenic and mutant mice to study oxygen free radical metabolism. Ann N Y Acad Sci. 1999;893:95–112
  62. Levin ED, Brady TC, Hochrein EC, et al. Molecular manipulations of extracellular superoxide dismutase: Functional importance for learning. Behav Genet. 1998;28:381–390
  63. Thiels E, Urban NN, Gonzalez-Burgos GR, et al. Impairment of long-term potentiation and associative memory in mice that overexpress extracellular superoxide dismutase. J Neurosci. 2000;20:7631–7639
  64. Gori T, Forconi S. The role of reactive free radicals in ischemic preconditioning—Clinical and evolutionary implications. Clin Hemorheol Microcirc. 2005;33:19–28
  65. Yu BP, Chung HY. Adaptive mechanisms to oxidative stress during aging. Mech Ageing Dev. 2006;127:436–443
  66. Qutob SS, Multani AS, Pathak S, et al. Fractionated X-radiation treatment can elicit an inducible-like radioprotective response that is not dependent on the intrinsic cellular X-radiation resistance/sensitivity. Radiat Res. 2006;166:590–599
  67. Butovsky O, Ziv Y, Schwartz A, et al. Microglia activated by IL-4 or IFN-gamma differentially induce neurogenesis and oligodendrogenesis from adult stem/progenitor cells. Mol Cell Neurosci. 2006;31:149–160
  68. Schwartz M, Butovsky O, Bruck W, et al. Microglial phenotype: Is the commitment reversible?. Trends Neurosci. 2006;29:68–74
  69. Achanta P, Thompson KJ, Fuss M, et al. Gene expression changes in the rodent hippocampus following whole brain irradiation. Neurosci Lett. 2007;418:143–148
  70. Mahmoud-Ahmed AS, Atkinson S, Wong CS. Early gene expression profile in mouse brain after exposure to ionizing radiation. Radiat Res. 2006;165:142–154
  71. Lyford GL, Yamagata K, Kaufmann WE, et al. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron. 1995;14:433–445
  72. McIntyre CK, Miyashita T, Setlow B, et al. Memory-influencing intra-basolateral amygdala drug infusions modulate expression of arc protein in the hippocampus. Proc Natl Acad Sci U S A. 2005;102:10718–10723
  73. Guzowski JF, Lyford GL, Stevenson GD, et al. Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci. 2000;20:3993–4001
  74. Guzowski JF, Setlow B, Wagner EK, et al. Experience-dependent gene expression in the rat hippocampus after spatial learning: A comparison of the immediate-early genes arc, c-fos, and zif268. J Neurosci. 2001;21:5089–5098
  75. Plath N, Ohana O, Dammermann B, et al. Arc/Arg3. 1 Is essential for the consolidation of synaptic plasticity and memories. Neuron. 2006;52:437–444
  76. Guzowski JF, McNaughton BL, Barnes CA, et al. Environment-specific expression of the immediate-early gene arc in hippocampal neuronal ensembles. Nat Neurosci. 1999;2:1120–1124
  77. Ramirez-Amaya V, Vazdarjanova A, Mikhael D, et al. Spatial exploration-induced arc mRNA and protein expression: Evidence for selective, network-specific reactivation. J Neurosci. 2005;25:1761–1768
  78. Rosi S, Ramirez-Amaya V, Vazdarjanova A, et al. Neuroinflammation alters the hippocampal pattern of behaviorally induced arc expression. J Neurosci. 2005;25:723–731
  79. Kempermann G, Kuhn HG, Gage FH. Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci U S A. 1997;94:10409–10414
  80. Jung MW, McNaughton BL. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus. 1993;3:165–182
  81. Ramirez-Amaya V, Marrone DF, Gage FH, et al. Integration of new neurons into functional neural networks. J Neurosci. 2006;26:12237–12241
  82. Kee N, Teixeira CM, Wang AH, et al. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci. 2007;10:355–362

 Supported in part by NIH grant NS 46,051(JRF); NASA grants NNJ04HC90G (JRF), NNJ05HE33G (JRF), and NNA06CB37G (CLL); ACS grant RSG-00-036-04-CNE (CLL); and DOE Grant DE-FG02-07ER64349 (CLL).

PII: S1053-4296(08)00085-4

doi: 10.1016/j.semradonc.2008.12.003

Seminars in Radiation Oncology
Volume 19, Issue 2 , Pages 122-132 , April 2009