Neonatal hypoxic/ischemic brain injury induces production of calretinin-expressing interneurons in the striatum

Journal of Comparative Neurology

Volumn 511, Issue 1, 2008, Pages 19-33

  Yang, Zhengang ^a   You, Yan ^a   Levison, Steven W ^b  

^a FUDAN UNIVERSITY   (China)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Calretinin; Medium spiny neurons; Neural stem cells; Neurogenesis; Stroke; Subventricular zone

Indexed keywords

CALRETININ; CHOLINE ACETYLTRANSFERASE; PARVALBUMIN; PHOSPHOPROTEIN DARPP 32; SOMATOSTATIN; BIOLOGICAL MARKER; CALBINDIN; DOUBLECORTIN PROTEIN; MICROTUBULE ASSOCIATED PROTEIN; NEUROPEPTIDE; PPP1R1B PROTEIN, RAT; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN HYPOXIA; BRAIN INJURY; BRAIN ISCHEMIA; CELL FATE; CONTROLLED STUDY; CORPUS STRIATUM; FEMALE; GENE MAPPING; IMMUNOREACTIVITY; INTERNEURON; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETROVIRUS; SUBVENTRICULAR ZONE; ANIMAL; CYTOLOGY; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; PREGNANCY; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL MARKERS; CALCIUM-BINDING PROTEIN, VITAMIN D-DEPENDENT; CORPUS STRIATUM; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; FEMALE; HUMANS; HYPOXIA-ISCHEMIA, BRAIN; INTERNEURONS; MICROTUBULE-ASSOCIATED PROTEINS; NEUROPEPTIDES; PREGNANCY; RATS; RATS, WISTAR; TYROSINE 3-MONOOXYGENASE;

EID: 56149114293     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21819     Document Type: Article

References (80)

1. Alvarez-Buylla A, Lim DA. 2004. For the long run: maintaining germinal niches in the adult brain. Neuron 41:683-686.
2. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. 2002. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963-970.
3. Back SA, Han BH, Luo NL, Chricton CA, Xanthoudakis S, Tam J, Arvin KL, Holtzman DM. 2002. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 22:455-463.
4. Batista-Brito R, Close J, Machold R, Fishell G. 2008a. The distinct temporal origins of olfactory bulb interneuron subtypes. J Neurosci 28:3966-3975.
5. Batista-Brito R, Machold R, Klein C, Fishell G. 2008b. Gene expression in cortical Interneuron precursors is prescient of their mature function. Cereb Cortex doi:10.1093/cercor/bhm258.
6. Betarbet R, Zigova T, Bakay RA, Luskin MB. 1996. Dopaminergic and GABAergic interneurons of the olfactory bulb are derived from the neonatal subventricular zone. Int J Dev Neurosci 14:921-930.
7. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG. 2003. Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1-10.
8. Butt SJ, Fuccillo M, Nery S, Noctor S, Kriegstein A, Corbin JG, Fishell G. 2005. The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48:591-604.
9. Chen J, Magavi SS, Macklis JD. 2004. Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc Natl Acad Sci U S A 101:16357-16362.
10. Chmielnicki E, Benraiss A, Economides AN, Goldman SA. 2004. Adenovirally expressed noggin and brain-derived neurotrophic factor cooperate to induce new medium spiny neurons from resident progenitor cells in the adult striatal ventricular zone. J Neurosci 24:2133-2142.
11. Cho SR, Benraiss A, Chmielnicki E, Samdani A, Economides A, Goldman SA. 2007. Induction of neostriatal neurogenesis slows disease progression in a transgenic murine model of Huntington disease. J Clin Invest 117:2889-2902.
12. Clarke DJ, Dunnett SB, Isacson O, Sirinathsinghji DJ, Björklund A. 1988. Striatal grafts in rats with unilateral neostriatal lesions - I. Ultrastructural evidence of afferent synaptic inputs from the host nigrostriatal pathway. Neuroscience 24:791-801.
13. Collin T, Arvidsson A, Kokaia Z, Lindvall O. 2005. Quantitative analysis of the generation of different striatal neuronal subtypes in the adult brain following excitotoxic injury. Exp Neurol 195:71-80.
14. Curtis MA, Kam M, Nannmark U, Anderson MF, Axell MZ, Wikkelso C, Holtas S, van Roon-Mom WM, Bjork-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.
15. Dayer AG, Cleaver KM, Abouantoun T, Cameron HA. 2005. New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168:415-427.
16. De Marchis S, Bovetti S, Carletti B, Hsieh YC, Garzotto D, Peretto P, Fasolo A, Puche AC, Rossi F. 2007. Generation of distinct types of periglomerular olfactory bulb interneurons during development and in adult mice: implication for intrinsic properties of the subventricular zone progenitor population. J Neurosci 27:657-664.
17. Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH. 1998. Neurogenesis in the adult human hippocampus. Nat Med 4:1313-1317.
18. Felling RJ, Snyder MJ, Romanko MJ, Rothstein RP, Ziegler AN, Yang Z, Givogri MI, Bongarzone ER, Levison SW. 2006. Neural stem/progenitor cells participate in the regenerative response to perinatal hypoxia/ ischemia. J Neurosci 26:4359-4369.
19. Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marin O. 2007. Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci 27:9682-9695.
20. Fogarty M, Grist M, Gelman D, Marin O, Pachnis V, Kessaris N. 2007. Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J Neurosci 27: 10935-10946.
21. Friedman B, Hockfield S, Black JA, Woodruff KA, Waxman SG. 1989. In situ demonstration of mature oligodendrocytes and their processes: an immunocytochemical study with a new monoclonal antibody, rip. Glia 2:380-390.
22. Hsieh J, Aimone JB, Kaspar BK, Kuwabara T, Nakashima K, Gage FH. 2004. IGF-I instructs multipotent adult neural progenitor cells to become oligodendrocytes. J Cell Biol 164:111-122.
23. Ito D, Imai Y, Ohsawa K, Nakajima K, Fukuuchi Y, Kohsaka S. 1998. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res 57:1-9.
24. Jankovski A, Garcia C, Soriano E, Sotelo C. 1998. Proliferation, migration and differentiation of neuronal progenitor cells in the adult mouse subventricular zone surgically separated from its olfactory bulb. Eur J Neurosci 10:3583-3568.
25. Jin K, Sun Y, Xie L, Peel A, Mao XO, Batteur S, Greenberg DA. 2003. Directed migration of neuronal precursors into the ischemic cerebral cortex and striatum. Mol Cell Neurosci 24:171-189.
26. Jin K, Sun Y, Xie L, Childs J, Mao XO, Greenberg DA. 2004. Post-ischemic administration of heparin-binding epidermal growth factor-like growth factor (HB-EGF) reduces infarct size and modifies neurogenesis after focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 24:399-408.
27. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC. 1992. Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18:527-535.
28. Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A. 1999. Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J Neurosci 19:2171-2180.
29. Kohwi M, Petryniak MA, Long JE, Ekker M, Obata K, Yanagawa Y, Rubenstein JL, Alvarez-Buylla A. 2007. A subpopulation of olfactory bulb GABAergic interneurons is derived from Emx1- and Dlx5/6-expressing progenitors. J Neurosci 27:6878-6891.
30. Leker RR, Soldner F, Velasco I, Gavin DK, Androutsellis-Theotokis A, McKay RD. 2007. Long-lasting regeneration after ischemia in the cerebral cortex. Stroke 38:153-161.
31. Levison SW, Goldman JE. 1993. Both oligodendrocytes and astrocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 10:201-212.
32. Liu FC, Graybiel AM. 1992. Heterogeneous development of calbindin-D28K expression in the striatal matrix. J Comp Neurol 320:304-322.
33. Luskin MB. 1993. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173-189.
34. Magavi SS, Leavitt BR, Macklis JD. 2000. Induction of neurogenesis in the neocortex of adult mice. Nature 405:951-955.
35. Marin O, Rubenstein JL. 2001. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2:780-790.
36. Marin O, Anderson SA, Rubenstein JL. 2000. Origin and molecular specification of striatal interneurons. J Neurosci 20:6063-6076.
37. Merkle FT, Alvarez-Buylla A. 2006. Neural stem cells in mammalian development. Curr Opin Cell Biol 18:704-709.
38. Merkle FT, Mirzadeh Z, Alvarez-Buylla A. 2007. Mosaic organization of neural stem cells in the adult brain. Science 317:381-384.
39. Ming GL, Song H. 2005. Adult neurogenesis in the mammalian central nervous system. Annu Rev Neurosci 28:223-250.
40. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116:201-211.
41. Nacher J, Crespo C, McEwen BS. 2001. Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14:629-644.
42. Nakatomi H, Kuriu T, Okabe S, Yamamoto S, Hatano O, Kawahara N, Tamura A, Kirino T, Nakafuku M. 2002. Regeneration of hippocampal pyramidal neurons after ischemic brain injury by recruitment of endogenous neural progenitors. Cell 110:429-441.
43. Ness JK, Romanko MJ, Rothstein RP, Wood TL, Levison SW. 2001. Perinatal hypoxia-ischemia induces apoptotic and excitotoxic death of periventricular white matter oligodendrocyte progenitors. Dev Neurosci 23:203-208.
44. Ong J, Plane JM, Parent JM, Silverstein FS. 2005. Hypoxic-ischemic injury stimulates subventricular zone proliferation and neurogenesis in the neonatal rat. Pediatr Res 58:600-606.
45. Ouimet CC, Langley-Gullion KC, Greengard P. 1998. Quantitative immunocytochemistry of DARPP-32-expressing neurons in the rat caudatoputamen. Brain Res 808:8-12.
46. Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM. 2002. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 52:802-813.
47. Partida GJ, Lee SC, Haft-Candell L, Nichols GS, Ishida AT. 2004. DARPP-32-like immunoreactivity in aII amacrine cells of rat retina. J Comp Neurol 480:251-263.
48. Pasteels B, Miki N, Hatakenaka S, Pochet R. 1987. Immunohistochemical cross-reactivity and electrophoretic comigration between calbindin D-27 kDa and visinin. Brain Res 412:107-113.
49. Pinaud R, Saldanha CJ, Wynne RD, Lovell PV, Mello CV. 2007. The excitatory thalamo-"cortical" projection within the song control system of zebra finches is formed by calbindin-expressing neurons. J Comp Neurol 504:601-608.
50. Plane JM, Liu R, Wang TW, Silverstein FS, Parent JM. 2004. Neonatal hypoxic-ischemic injury increases forebrain subventricular zone neurogenesis in the mouse. Neurobiol Dis 16:585-595.
51. Redmond L, Hockfield S, Morabito MA. 1996. The divergent homeobox gene PBX1 is expressed in the postnatal subventricular zone and interneurons of the olfactory bulb. J Neurosci 16:2972-2982.
52. Rice JE 3rd, Vannucci RC, Brierley JB. 1981. The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 9:131-141.
53. Rushlow W, Flumerfelt BA, Naus CC. 1995. Colocalization of somatostatin, neuropeptide Y, and NADPH-diaphorase in the caudate-putamen of the rat. J Comp Neurol 351:499-508.
54. Rymar VV, Sasseville R, Luk KC, Sadikot AF. 2004. Neurogenesis and stereological morphometry of calretinin-immunoreactive GABAergic interneurons of the neostriatum. J Comp Neurol 469:325-339.
55. Schlosser B, Klausa G, Prime G, Ten Bruggencate G. 1999. Postnatal development of calretinin- and parvalbumin-positive interneurons in the rat neostriatum: an immunohistochemical study. J Comp Neurol 405:185-198.
56. Song H, Stevens CF, Gage FH. 2002. Astroglia induce neurogenesis from adult neural stem cells. Nature 417:39-44.
57. Stenman J, Toresson H, Campbell K. 2003. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J Neurosci 23:167-174.
58. Suzuki S, Gerhold LM, Bottner M, Rau SW, Dela Cruz C, Yang E, Zhu H, Yu J, Cashion AB, Kindy MS, Merchenthaler I, Gage FH, Wise PM. 2007. Estradiol enhances neurogenesis following ischemic stroke through estrogen receptors alpha and beta. J Comp Neurol 500:1064-1075.
59. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663-676.
60. Tansey FA, Cammer W. 1991. A pi form of glutathione-S-transferase is a myelin- and oligodendrocyte-associated enzyme in mouse brain. J Neurochem 57:95-102.
61. Teramoto T, Qiu J, Plumier JC, Moskowitz MA. 2003. EGF amplifies the replacement of parvalbumin-expressing striatal interneurons after ischemia. J Clin Invest 111:1125-1132.
62. Thal LJ, Gilbertson E, Armstrong DM, Gage FH. 1992. Development of the basal forebrain cholinergic system: phenotype expression prior to target innervation. Neurobiol Aging 13:67-72.
63. Thored P, Arvidsson A, Cacci E, Ahlenius H, Kallur T, Darsalia V, Ekdahl CT, Kokaia Z, Lindvall O. 2006. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24:739-747.
64. Toma JG, Akhavan M, Fernandes KJ, Barnabe-Heider F, Sadikot A, Kaplan DR, Miller FD. 2001. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 3:778-784.
65. Toresson H, Parmar M, Campbell K. 2000. Expression of Meis and Pbx genes and their protein products in the developing telencephalon: implications for regional differentiation. Mech Dev 94:183-187.
66. Vannucci RC, Vannucci SJ. 1997. A model of perinatal hypoxic-ischemic brain damage. Ann N Y Acad Sci 835:234-249.
67. Vannucci SJ, Hagberg H. 2004. Hypoxia-ischemia in the immature brain. J Exp Biol 207:3149-3154.
68. Ventura RE, Goldman JE. 2007. Dorsal radial glia generate olfactory bulb interneurons in the postnatal murine brain. J Neurosci 27:4297-4302.
69. Volpe JJ. 1997. Brain injury in the premature infant - from pathogenesis to prevention. Brain Dev 19:519-534.
70. Waclaw RR, Allen ZJn, Bell SM, Erdelyi F, Szabo G, Potter S, Campbell K. 2006. The zinc finger transcription factor Sp8 regulates the generation and diversity of olfactory bulb interneurons. Neuron 49:503-516.
71. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A. 2001. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128: 3759-3771.
72. Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA. 2004. Origins of cortical interneuron subtypes. J Neurosci 24:2612-2622.
73. Yamashita T, Ninomiya M, Hernandez Acosta P, Garcia-Verdugo JM, Sunabori T, Sakaguchi M, Adachi K, Kojima T, Hirota Y, Kawase T, Araki N, Abe K, Okano H, Sawamoto K. 2006. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 26:6627-6636.
74. Yang HKC, Sundholm-Peters NL, Goings GE, Walker AS, Hyland K, Szele FG. 2004. Distribution of doublecortin expressing cells near the lateral ventricles in the adult mouse brain. J Neurosci Res 76:282-295.
75. Yang Z. 2008. Postnatal subventricular zone progenitors give rise not only to granular and periglomerular interneurons but also to interneurons in the external plexiform layer of the rat olfactory bulb. J Comp Neurol 506:347-358.
76. Yang Z, Levison SW. 2006. Hypoxia/ischemia expands the regenerative capacity of progenitors in the perinatal subventricular zone. Neuroscience 139:555-564.
77. Yang Z, Levison SW. 2007. Perinatal hypoxic/ischemic brain injury induces persistent production of striatal neurons from subventricular zone progenitors. Dev Neurosci 29:331-340.
78. Yang Z, Covey M, Bitel C, Ni L, Jonakait G, Levison SW. 2007. Sustained neocortical neurogenesis after neonatal hypoxic/ischemic injury. Ann Neurol 61:199-208.
79. Young KM, Fogarty M, Kessaris N, Richardson WD. 2007. Subventricular zone stem cells are heterogeneous with respect to their embryonic origins and neurogenic fates in the adult olfactory bulb. J Neurosci 27:8286-8296.
80. Zhao C, Deng W, Gage FH. 2008. Mechanisms and functional implications of adult neurogenesis. Cell 132:645-660.