The hippocampal neurovascular niche during normal development and after irradiation to the juvenile mouse brain

References

• Achanta P, Capilla-Gonzalez V, Purger D, Reyes J, Sailor K, Song H, Garcia-Verdugo JM, Gonzalez-Perez O, Ford E, Quinones-Hinojosa A. 2012. Subventricular zone localized irradiation affects the generation of proliferating neural precursor cells and the migration of neuroblasts. Stem Cells 30:2548–2560.
   PubMed Web of Science ®Google Scholar
• Allt G, Lawrenson JG. 2001. Pericytes: Cell biology and pathology. Cells Tissues Organs 169:1–11.
   PubMed Web of Science ®Google Scholar
• Altman J, Das GD. 1965. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335.
   PubMed Web of Science ®Google Scholar
• Armulik A, Abramsson A, Betsholtz C. 2005. Endothelial/pericyte interactions. Circ Res 97:512–523.
   PubMed Web of Science ®Google Scholar
• Armulik A, Genove G, Betsholtz C. 2011. Pericytes: Developmental, physiological, and pathological perspectives, problems, and promises. Dev Cell 21:193–215.
   PubMed Web of Science ®Google Scholar
• Armulik A, Genove G, Mae M, Nisancioglu MH, Wallgard E, Niaudet C, He L, Norlin J, Lindblom P, Strittmatter K, Johansson BR, Betsholtz C. 2010. Pericytes regulate the blood-brain barrier. Nature 468:557–561.
   PubMed Web of Science ®Google Scholar
• Bell RD, Winkler EA, Sagare AP, Singh I, Larue B, Deane R, Zlokovic BV. 2010. Pericytes control key neurovascular functions and neuronal phenotype in the adult brain and during brain aging. Neuron 68:409–427.
   PubMed Web of Science ®Google Scholar
• Ben Abdallah NM, Slomianka L, Vyssotski AL, Lipp HP. 2010. Early age-related changes in adult hippocampal neurogenesis in C57 mice. Neurobiol Aging 31:151–161.
   PubMedGoogle Scholar
• Bergers G, Song S. 2005. The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol 7:452–464.
   PubMed Web of Science ®Google Scholar
• Boström M, Kalm M, Karlsson N, Hellström Erkenstam N, Blomgren K. 2013. Irradiation to the young mouse brain caused long-term, progressive depletion of neurogenesis but did not disrupt the neurovascular niche. J Cereb Blood Flow Metab 33:935–943.
   PubMed Web of Science ®Google Scholar
• Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, Van Roon-Mom WM, Björk-Eriksson T, Nordborg C, Frisen J, Dragunow M, Faull RL, Eriksson PS. 2007. Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249.
   PubMed Web of Science ®Google Scholar
• Dore-Duffy P, Katychev A, Wang X, Van Buren E. 2006. CNS microvascular pericytes exhibit multipotential stem cell activity. J Cereb Blood Flow Metab 26:613–624.
   PubMed Web of Science ®Google Scholar
• Dranovsky A, Picchini AM, Moadel T, Sisti AC, Yamada A, Kimura S, Leonardo ED, Hen R. 2011. Experience dictates stem cell fate in the adult hippocampus. Neuron 70:908–923.
   Google Scholar
• Ellenberg L, Liu Q, Gioia G, Yasui Y, Packer RJ, Mertens A, Donaldson SS, Stovall M, Kadan-Lottick N, Armstrong G, Robison LL, Zeltzer LK. 2009. Neurocognitive status in long-term survivors of childhood CNS malignancies: A report from the Childhood Cancer Survivor Study. Neuropsychology 23:705–717.
   PubMed Web of Science ®Google Scholar
• Eriksson PS, Perfilieva E, Björk-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317.
   PubMed Web of Science ®Google Scholar
• Farkas E, Luiten PG. 2001. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog Neurobiol 64:575–611.
   PubMed Web of Science ®Google Scholar
• Filippov V, Kronenberg G, Pivneva T, Reuter K, Steiner B, Wang LP, Yamaguchi M, Kettenmann H, Kempermann G. 2003. Subpopulation of nestin-expressing progenitor cells in the adult murine hippocampus shows electrophysiological and morphological characteristics of astrocytes. Mol Cell Neurosci 23:373–382.
   PubMed Web of Science ®Google Scholar
• Fouladi M, Gilger E, Kocak M, Wallace D, Buchanan G, Reeves C, Robbins N, Merchant T, Kun LE, Khan R, Gajjar A, Mulhern R. 2005. Intellectual and functional outcome of children 3 years old or younger who have CNS malignancies. J Clin Oncol 23:7152–7160.
   PubMed Web of Science ®Google Scholar
• Fukuda H, Fukuda A, Zhu C, Korhonen L, Swanpalmer J, Hertzman S, Leist M, Lannering B, Lindholm D, Björk-Eriksson T, Marky I, Blomgren K. 2004. Irradiation-induced progenitor cell death in the developing brain is resistant to erythropoietin treatment and caspase inhibition. Cell Death Differ 11:1166–1178.
   PubMed Web of Science ®Google Scholar
• Garthe A, Behr J, Kempermann G. 2009. Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One 4:e5464.
   PubMed Web of Science ®Google Scholar
• Greenberg DA, Jin K. 2005. From angiogenesis to neuropathology. Nature 438:954–959.
   PubMed Web of Science ®Google Scholar
• Guo S, Kim WJ, Lok J, Lee SR, Besancon E, Luo BH, Stins MF, Wang X, Dedhar S, Lo EH. 2008. Neuroprotection via matrix-trophic coupling between cerebral endothelial cells and neurons. Proc Natl Acad Sci USA 105:7582–7587.
   PubMed Web of Science ®Google Scholar
• Hellström M, Gerhardt H, Kalen M, Li X, Eriksson U, Wolburg H, Betsholtz C. 2001. Lack of pericytes leads to endothelial hyperplasia and abnormal vascular morphogenesis. J Cell Biol 153:543–553.
   PubMed Web of Science ®Google Scholar
• Hellström NA, Björk-Eriksson T, Blomgren K, Kuhn HG. 2009. Differential recovery of neural stem cells in the subventricular zone and dentate gyrus after ionizing radiation. Stem Cells 27:634–641.
   PubMed Web of Science ®Google Scholar
• Huo K, Sun Y, Li H, Du X, Wang X, Karlsson N, Zhu C, Blomgren K. 2012. Lithium reduced neural progenitor apoptosis in the hippocampus and ameliorated functional deficits after irradiation to the immature mouse brain. Mol Cell Neurosci 51:32–42.
   PubMed Web of Science ®Google Scholar
• Jiao Q, Xie WL, Wang YY, Chen XL, Yang PB, Zhang PB, Tan J, Lu HX, Liu Y. 2013. Spatial relationship between NSCs/NPCs and microvessels in rat brain along prenatal and postnatal development. Int J Dev Neurosci 31:280–285.
   PubMedGoogle Scholar
• Kalm M, Karlsson N, Nilsson MK, Blomgren K. 2013. Loss of hippocampal neurogenesis, increased novelty-induced activity, decreased home cage activity, and impaired reversal learning one year after irradiation of the young mouse brain. Exp Neurol 247:402–409.
   PubMed Web of Science ®Google Scholar
• Kempermann G, Gage FH. 2002. Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. Eur J Neurosci 16:129–136.
   PubMed Web of Science ®Google Scholar
• Kuhn HG, Blomgren K. 2011. Developmental dysregulation of adult neurogenesis. Eur J Neurosci 33:1115–1122.
   PubMed Web of Science ®Google Scholar
• Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033.
   PubMed Web of Science ®Google Scholar
• Kuo JR, Lo CJ, Chang CP, Lin HJ, Lin MT, Chio CC. 2010. Brain cooling-stimulated angiogenesis and neurogenesis attenuated traumatic brain injury in rats. J Trauma 69:1467–1472.
   PubMedGoogle Scholar
• Lannering B, Marky I, Lundberg A, Olsson E. 1990. Long-term sequelae after pediatric brain tumors: Their effect on disability and quality of life. Med Pediatr Oncol 18:304–310.
   PubMedGoogle Scholar
• Lee HS, Han J, Bai HJ, Kim KW. 2009. Brain angiogenesis in developmental and pathological processes: regulation, molecular and cellular communication at the neurovascular interface. FEBS J 276:4622–4635.
   PubMed Web of Science ®Google Scholar
• Lee SW, Clemenson GD, Gage FH. 2012. New neurons in an aged brain. Behav Brain Res 227:497–507.
   PubMedGoogle Scholar
• Lindahl P, Johansson BR, Leveen P, Betsholtz C. 1997. Pericyte loss and microaneurysm formation in PDGF-B-deficient mice. Science 277:242–245.
   PubMed Web of Science ®Google Scholar
• Monje ML, Mizumatsu S, Fike JR, Palmer TD. 2002. Irradiation induces neural precursor-cell dysfunction. Nat Med 8:955–962.
   PubMed Web of Science ®Google Scholar
• Naylor AS, Bull C, Nilsson MK, Zhu C, Björk-Eriksson T, Eriksson PS, Blomgren K, Kuhn HG. 2008. Voluntary running rescues adult hippocampal neurogenesis after irradiation of the young mouse brain. Proc Natl Acad Sci USA 105:14632–14637.
   PubMed Web of Science ®Google Scholar
• Palmer TD, Willhoite AR, Gage FH. 2000. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 425:479–494.
   PubMed Web of Science ®Google Scholar
• Peissner W, Kocher M, Treuer H, Gillardon F. 1999. Ionizing radiation-induced apoptosis of proliferating stem cells in the dentate gyrus of the adult rat hippocampus. Brain Res Mol Brain Res 71:61–68.
   PubMedGoogle Scholar
• Peppiatt CM, Howarth C, Mobbs P, Attwell D. 2006. Bidirectional control of CNS capillary diameter by pericytes. Nature 443:700–704.
   PubMed Web of Science ®Google Scholar
• Persson A, Lindwall C, Curtis MA, Kuhn HG. 2010. Expression of ezrin radixin moesin proteins in the adult subventricular zone and the rostral migratory stream. Neuroscience 167:312–322.
   PubMedGoogle Scholar
• Piatti VC, Esposito MS, Schinder AF. 2006. The timing of neuronal development in adult hippocampal neurogenesis. Neuroscientist 12:463–468.
   PubMed Web of Science ®Google Scholar
• Raber J, Allen AR, Rosi S, Sharma S, Dayger C, Davis MJ, Fike JR. 2013. Effects of (56)Fe radiation on hippocampal function in mice deficient in chemokine receptor 2 (CCR2). Behav Brain Res 246:69–75.
   PubMedGoogle Scholar
• Raber J, Rola R, Lefevour A, Morhardt D, Curley J, Mizumatsu S, Vandenberg SR, Fike JR. 2004. Radiation-induced cognitive impairments are associated with changes in indicators of hippocampal neurogenesis. Radiat Res 162:39–47.
   PubMed Web of Science ®Google Scholar
• Robertson PL, Du Bois M, Bowman PD, Goldstein GW. 1985. Angiogenesis in developing rat brain: An in vivo and in vitro study. Brain Res 355:219–223.
   PubMed Web of Science ®Google Scholar
• Roof RL. 1993. The dentate gyrus is sexually dimorphic in prepubescent rats: Testosterone plays a significant role. Brain Res 610:148–151.
   PubMedGoogle Scholar
• Roughton K, Kalm M, Blomgren K. 2012. Sex-dependent differences in behavior and hippocampal neurogenesis after irradiation to the young mouse brain. Eur J Neurosci 36:2763–2772.
   PubMed Web of Science ®Google Scholar
• Semple BD, Blomgren K, Gimlin K, Ferriero DM, Noble-Haeusslein LJ. 2013. Brain development in rodents and humans: Identifying benchmarks of maturation and vulnerability to injury across species. Prog Neurobiol 106–107:1–16.
   PubMed Web of Science ®Google Scholar
• Shen Q, Goderie SK, Jin L, Karanth N, Sun Y, Abramova N, Vincent P, Pumiglia K, Temple S. 2004. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 304:1338–1340.
   PubMed Web of Science ®Google Scholar
• Sims DE, Westfall JA. 1983. Analysis of relationships between pericytes and gas exchange capillaries in neonatal and mature bovine lungs. Microvasc Res 25:333–342.
   PubMedGoogle Scholar
• Soussain C, Ricard D, Fike JR, Mazeron JJ, Psimaras D, Delattre JY. 2009. CNS complications of radiotherapy and chemotherapy. Lancet 374:1639–1651.
   PubMed Web of Science ®Google Scholar
• Stewart PA, Vinters HV, Wong CS. 1995. Blood-spinal cord barrier function and morphometry after single doses of x-rays in rat spinal cord. Int J Radiat Oncol Biol Phys 32:703–711.
   PubMedGoogle Scholar
• Tada E, Parent JM, Lowenstein DH, Fike JR. 2000. X-irradiation causes a prolonged reduction in cell proliferation in the dentate gyrus of adult rats. Neuroscience 99:33–41.
   PubMed Web of Science ®Google Scholar
• Tavazoie M, Van Der Veken L, Silva-Vargas V, Louissaint M, Colonna L, Zaidi B, Garcia-Verdugo JM, Doetsch F. 2008. A specialized vascular niche for adult neural stem cells. Cell Stem Cell 3:279–288.
   PubMed Web of Science ®Google Scholar
• Warrington JP, Csiszar A, Johnson DA, Herman TS, Ahmad S, Lee YW, Sonntag WE. 2011. Cerebral microvascular rarefaction induced by whole brain radiation is reversible by systemic hypoxia in mice. Am J Physiol Heart Circ Physiol 300:H736–744.
   Google Scholar
• Villacampa N, Almolda B, Gonzalez B, Castellano B. 2013. Tomato lectin histochemistry for microglial visualization. Methods Mol Biol 1041:261–279.
   PubMedGoogle Scholar
• Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, Stan TM, Fainberg N, Ding Z, Eggel A, Lucin KM, Czirr E, Park JS, Couillard-Despres S, Aigner L, Li G, Peskind ER, Kaye JA, Quinn JF, Galasko DR, Xie XS, Rando TA, Wyss-Coray T. 2011. The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477:90–94.
   PubMed Web of Science ®Google Scholar
• Zlokovic BV. 2008. The blood-brain barrier in health and chronic neurodegenerative disorders. Neuron 57:178–201.
   PubMed Web of Science ®Google Scholar