Subventricular zone localized irradiation affects the generation of proliferating neural precursor cells and the migration of neuroblasts

Stem Cells

Volumn 30, Issue 11, 2012, Pages 2548-2560

  Achanta, Pragathi ^a   Capilla Gonzalez, Vivian ^a   Purger, David ^a   Reyes, Juvenal ^a   Sailor, Kurt ^a   Song, Hongjun ^a   Garcia Verdugo, Jose Manuel ^b   Gonzalez Perez, Oscar ^c   Ford, Eric ^a   Quinones Hinojosa, Alfredo ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VALENCIA   (Spain)

^c UNIVERSIDAD DE COLIMA   (Mexico)

Author keywords

Migrating neuroblasts; Neural stem cells; Radiation therapy; Subventricular zone

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL MIGRATION; CELL PROLIFERATION; CELL STRUCTURE; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; IRRADIATION; MALE; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEUROBLAST; NONHUMAN; SIGNAL TRANSDUCTION; STEM CELL NICHE; SUBVENTRICULAR ZONE;

ANIMALS; ASTROCYTES; CELL COUNT; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CEREBRAL VENTRICLES; MALE; MICE; MICE, INBRED C57BL; NEURAL STEM CELLS; OLFACTORY BULB; SPHEROIDS, CELLULAR;

EID: 84867909513     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1214     Document Type: Article

References (78)

1. Stupp R, Hegi ME, Mason WP et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol 2009;10:459-466.
2. Stupp R, Mason WP, van den Bent MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 2005;352:987-996. (Pubitemid 40349501)
3. Calabrese P, Schlegel U. Neurotoxicity of treatment. Recent Results Cancer Res 2009;171:165-174.
4. Marazziti D, Baroni S, Catena-Dell'osso M et al. Cognitive, psychological and psychiatric effects of ionizing radiation exposure. Curr Med Chem 2012;19:1864-1869
5. Silber JH, Radcliffe J, Peckham V et al. Whole-brain irradiation and decline in intelligence: The influence of dose and age on IQ score. J Clin Oncol 1992;10:1390-1396. (Pubitemid 23059921)
6. Walter AW, Mulhern RK, Gajjar A et al. Survival and neurodevelopmental outcome of young children with medulloblastoma at St Jude Children's Research Hospital. J Clin Oncol 1999;17:3720-3728.
7. Achanta P, Fuss M, Martinez JL, Jr. Ionizing radiation impairs the formation of trace fear memories and reduces hippocampal neurogenesis. Behav Neurosci 2009;123:1036-1045.
8. Fike JR, Rola R, Limoli CL. Radiation response of neural precursor cells. Neurosurg Clin N Am 2007;18:115-127, x. (Pubitemid 46161195)
9. McGinn MJ, Sun D, Colello RJ. Utilizing X-irradiation to selectively eliminate neural stem/progenitor cells from neurogenic regions of the mammalian brain. J Neurosci Methods 2008;170:9-15.
10. Monje ML, Mizumatsu S, Fike JR et al. Irradiation induces neural precursor-cell dysfunction. Nat Med 2002;8:955-962. (Pubitemid 35033699)
11. Tada E, Yang C, Gobbel GT et al. Long-term impairment of subependymal repopulation following damage by ionizing irradiation. Exp Neurol 1999;160:66-77.
12. Abrous DN, Koehl M, Le Moal M. Adult neurogenesis: From precursors to network and physiology. Physiol Rev 2005;85:523-569. (Pubitemid 40404636)
13. Alvarez-Buylla A, Garcia-Verdugo JM. Neurogenesis in adult subventricular zone. J Neurosci 2002;22:629-634. (Pubitemid 34141742)
14. Ming GL, Song H. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 2005;28:223-250. (Pubitemid 41098905)
15. Menn B, Garcia-Verdugo JM, Yaschine C et al. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 2006;26:7907-7918. (Pubitemid 44315160)
16. Glass R, Synowitz M, Kronenberg G et al. Glioblastoma-induced attraction of endogenous neural precursor cells is associated with improved survival. J Neurosci 2005;25:2637-2646. (Pubitemid 40365175)
17. Aboody KS, Brown A, Rainov NG et al. Neural stem cells display extensive tropism for pathology in adult brain: Evidence from intracranial gliomas. Proc Natl Acad Sci USA 2000;97:12846-12851.
18. Achanta P, Sedora Roman NI, Quinones-Hinojosa A. Gliomagenesis and the use of neural stem cells in brain tumor treatment. Anticancer Agents Med Chem 2010;10:121-130.
19. Ahmed AU, Thaci B, Alexiades NG et al. Neural stem cell-based cell carriers enhance therapeutic efficacy of an oncolytic adenovirus in an orthotopic mouse model of human glioblastoma. Mol Ther 2011;19:1714-1726.
20. Frank RT, Edmiston M, Kendall SE et al. Neural stem cells as a novel platform for tumor-specific delivery of therapeutic antibodies. PLoS One 2009;4:e8314.
21. Lee EX, Lam DH, Wu C et al. Glioma gene therapy using induced pluripotent stem cell derived neural stem cells. Mol Pharm 2011;8:1515-1524.
22. Quinones-Hinojosa A, Sanai N, Soriano-Navarro M et al. Cellular composition and cytoarchitecture of the adult human subventricular zone: A niche of neural stem cells. J Comp Neurol 2006;494:415-434. (Pubitemid 41794059)
23. Sanai N, Tramontin AD, Quinones-Hinojosa A et al. Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 2004;427:740-744. (Pubitemid 38294593)
24. Mirzadeh Z, Merkle FT, Soriano-Navarro M et al. Neural stem cells confer unique pinwheel architecture to the ventricular surface in neurogenic regions of the adult brain. Cell Stem Cell 2008;3:265-278.
25. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A. Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 1997;17:5046-5061. (Pubitemid 27263818)
26. Lois C, Alvarez-Buylla A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci USA 1993;90:2074-2077. (Pubitemid 23070000)
27. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A. Chain migration of neuronal precursors. Science 1996;271:978-981. (Pubitemid 26066393)
28. Curtis MA, Kam M, Nannmark U et al. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 2007;315:1243-1249. (Pubitemid 46364256)
29. Marsh JC, Godbole R, Diaz AZ et al. Sparing of the hippocampus, limbic circuit and neural stem cell compartment during partial brain radiotherapy for glioma: A dosimetric feasibility study. J Med Imaging Radiat Oncol 2011;55:442-449.
30. Redmond KJ, Achanta P, Grossman SA et al. A radiotherapy technique to limit dose to neural progenitor cell niches without compromising tumor coverage. J Neurooncol 2011;104:579-587.
31. Wong J, Armour E, Kazanzides P et al. High-resolution, small animal radiation research platform with x-ray tomographic guidance capabilities. Int J Radiat Oncol Biol Phys 2008;71:1591-1599. (Pubitemid 351978175)
32. Ford EC, Achanta P, Purger D et al. Localized CT-guided irradiation inhibits neurogenesis in specific regions of the adult mouse brain. Radiat Res 2011;175:774-783.
33. Mirzadeh Z, Doetsch F, Sawamoto K et al. The subventricular zone en-face: Wholemount staining and ependymal flow. J Vis Exp 2010;6:1938.
34. Ferron SR, Andreu-Agullo C, Mira H et al. A combined ex/in vivo assay to detect effects of exogenously added factors in neural stem cells. Nat Protoc 2007;2:849-859.
35. Ge S, Goh EL, Sailor KA et al. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 2006;439:589-593. (Pubitemid 43185382)
36. Belvindrah R, Lazarini F, Lledo PM. Postnatal neurogenesis: From neuroblast migration to neuronal integration. Rev Neurosci 2009;20:331-346.
37. Hellstrom NA, Bjork-Eriksson T, Blomgren K et al. Differential recovery of neural stem cells in the subventricular zone and dentate gyrus after ionizing radiation. Stem Cells 2009;27:634-641.
38. Panagiotakos G, Alshamy G, Chan B et al. Long-term impact of radiation on the stem cell and oligodendrocyte precursors in the brain. PLoS One 2007;2:e588.
39. Tada E, Parent JM, Lowenstein DH et al. X-irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 2000;99:33-41. (Pubitemid 30495550)
40. Shi L, Molina DP, Robbins ME et al. Hippocampal neuron number is unchanged 1 year after fractionated whole-brain irradiation at middle age. Int J Radiat Oncol Biol Phys 2008;71:526-532. (Pubitemid 351636200)
41. Jirak D, Namestkova K, Herynek V et al. Lesion evolution after gamma knife irradiation observed by magnetic resonance imaging. Int J Radiat Biol 2007;83:237-244. (Pubitemid 46399006)
42. Santarelli L, Saxe M, Gross C et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003;301:805-809. (Pubitemid 36962615)
43. Saxe MD, Battaglia F, Wang JW et al. Ablation of hippocampal neurogenesis impairs contextual fear conditioning and synaptic plasticity in the dentate gyrus. Proc Natl Acad Sci USA 2006;103:17501-17506. (Pubitemid 44788998)
44. Rogakou EP, Nieves-Neira W, Boon C et al. Initiation of DNA fragmentation during apoptosis induces phosphorylation of H2AX histone at serine 139. J Biol Chem 2000;275:9390-9395. (Pubitemid 30185164)
45. Doetsch F, Caille I, Lim DA et al. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 1999;97:703-716. (Pubitemid 29278045)
46. Morshead CM, Craig CG, van der Kooy D. In vivo clonal analyses reveal the properties of endogenous neural stem cell proliferation in the adult mammalian forebrain. Development 1998;125:2251-2261. (Pubitemid 28336386)
47. Capilla-Gonzalez V, Gil-Perotin S, Ferragud A et al. Exposure to N-ethyl- N-nitrosourea in adult mice alters structural and functional integrity of neurogenic sites. PLoS One 2012;7:e29891.
48. Capilla-Gonzalez V, Gil-Perotin S, Garcia-Verdugo JM. Postnatal exposure to N-ethyl-N-nitrosurea disrupts the subventricular zone in adult rodents. Eur J Neurosci 2010;32:1789-1799.
49. Snyder EY, Park KI. Limitations in brain repair. Nat Med 2002;8:928-930. (Pubitemid 35033685)
50. Monje ML, Palmer T. Radiation injury and neurogenesis. Curr Opin Neurol 2003;16:129-134. (Pubitemid 36521196)
51. Shen Q, Goderie SK, Jin L et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 2004;304:1338-1340. (Pubitemid 38697433)
52. Shen Q, Wang Y, Kokovay E et al. Adult SVZ stem cells lie in a vascular niche: A quantitative analysis of niche cell-cell interactions. Cell Stem Cell 2008;3:289-300.
53. Tavazoie M, Van der Veken L, Silva-Vargas V et al. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 2008;3:279-288.
54. Brown WR, Thore CR, Moody DM et al. Vascular damage after fractionated whole-brain irradiation in rats. Radiat Res 2005;164:662-668. (Pubitemid 41532562)
55. Li YQ, Chen P, Haimovitz-Friedman A et al. Endothelial apoptosis initiates acute blood-brain barrier disruption after ionizing radiation. Cancer Res 2003;63:5950-5956. (Pubitemid 37187496)
56. Ljubimova NV, Levitman MK, Plotnikova ED et al. Endothelial cell population dynamics in rat brain after local irradiation. Br J Radiol 1991;64:934-940.
57. Otsuka S, Coderre JA, Micca PL et al. Depletion of neural precursor cells after local brain irradiation is due to radiation dose to the parenchyma, not the vasculature. Radiat Res 2006;165:582-591.
58. Andreu-Agullo C, Morante-Redolat JM, Delgado AC et al. Vascular niche factor PEDF modulates Notch-dependent stemness in the adult subependymal zone. Nat Neurosci 2009;12:1514-1523.
59. Ramirez-Castillejo C, Sanchez-Sanchez F, Andreu-Agullo C et al. Pigment epithelium-derived factor is a niche signal for neural stem cell renewal. Nat Neurosci 2006;9:331-339. (Pubitemid 43290962)
60. Wittko IM, Schanzer A, Kuzmichev A et al. VEGFR-1 regulates adult olfactory bulb neurogenesis and migration of neural progenitors in the rostral migratory stream in vivo. J Neurosci 2009;29:8704-8714.
61. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003;302:1760-1765. (Pubitemid 37505739)
62. Reynolds BA, Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992;255:1707-1710.
63. Mu Y, Lee SW, Gage FH. Signaling in adult neurogenesis. Curr Opin Neurol 2010;20:416-423.
64. Arvidsson A, Collin T, Kirik D et al. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002;8:963-970. (Pubitemid 35033700)
65. Goings GE, Sahni V, Szele FG. Migration patterns of subventricular zone cells in adult mice change after cerebral cortex injury. Brain Res 2004;996:213-226. (Pubitemid 38022018)
66. Aboody K, Capela A, Niazi N et al. Translating stem cell studies to the clinic for CNS repair: Current state of the art and the need for a Rosetta Stone. Neuron 2011;70:597-613.
67. 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. (Pubitemid 38891593)
68. Craig CG, D'sa R, Morshead CM et al. Migrational analysis of the constitutively proliferating subependyma population in adult mouse forebrain. Neuroscience 1999;93:1197-1206.
69. Gritti A, Bonfanti L, Doetsch F et al. Multipotent neural stem cells reside into the rostral extension and olfactory bulb of adult rodents. J Neurosci 2002;22:437-445. (Pubitemid 34049081)
70. Hack MA, Saghatelyan A, de Chevigny A et al. Neuronal fate determinants of adult olfactory bulb neurogenesis. Nat Neurosci 2005;8:865-872.
71. Diaz D, Recio JS, Baltanas FC et al. Long-lasting changes in the anatomy of the olfactory bulb after ionizing irradiation and bone marrow transplantation. Neuroscience 2011;173:190-205.
72. Martoncikova M, Racekova E, Orendacova J. The number of proliferating cells in the rostral migratory stream of rat during the first postnatal month. Cell Mol Neurobiol 2006;26:1453-1461. (Pubitemid 44924058)
73. Hallbergson AF, Gnatenco C, Peterson DA. Neurogenesis and brain injury: Managing a renewable resource for repair. J Clin Invest 2003;112:1128-1133. (Pubitemid 38056287)
74. Catchpole T, Henkemeyer M. EphB2 tyrosine kinase-dependent forward signaling in migration of neuronal progenitors that populate and form a distinct region of the dentate niche. J Neurosci 2011;31:11472-11483.
75. Connor B, Gordon RJ, Jones KS et al. Deviating from the well travelled path: Precursor cell migration in the pathological adult mammalian brain. J Cell Biochem 2011;112:1467-1474.
76. Kaneko N, Marin O, Koike M et al. New neurons clear the path of astrocytic processes for their rapid migration in the adult brain. Neuron 2010;67:213-223.
77. Nie K, Molnar Z, Szele FG. Proliferation but not migration is associated with blood vessels during development of the rostral migratory stream. Dev Neurosci 2010;32:163-172.
78. Wang Y, Kaneko N, Asai N et al. Girdin is an intrinsic regulator of neuroblast chain migration in the rostral migratory stream of the postnatal brain. J Neurosci 2011;31:8109-8122.