Precursors with glial fibrillary acidic protein promoter activity transiently generate GABA interneurons in the postnatal cerebellum

Stem Cells

Volumn 27, Issue 5, 2009, Pages 1152-1163

  Silbereis, John ^a   Cheng, Elise ^a   Ganat, Yosif M ^a   Ment, Laura R ^b   Vaccarino, Flora M ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Astrocytes; Cerebellum; GABA interneurons; Neural differentiation; Neural stem cells; Progenitor cell; Tissue specific stem cell; Transgenic mouse

Indexed keywords

4 AMINOBUTYRIC ACID; BETA GALACTOSIDASE; CRE RECOMBINASE; ENHANCED GREEN FLUORESCENT PROTEIN; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMATE DECARBOXYLASE 67; INHIBITOR PROTEIN; MOLECULAR LAYER; PROTEIN P2; PROTEIN P50; PROTEIN S100B; TAMOXIFEN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LEX; TRANSCRIPTION FACTOR MASH1; TRANSCRIPTION FACTOR MUSASHI1; TRANSCRIPTION FACTOR PAX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FATE; CELL MIGRATION; CELL POPULATION; CEREBELLUM; CEREBELLUM CORTEX; ENZYME ACTIVITY; GABAERGIC SYSTEM; GENETIC RECOMBINATION; GLIA; IN VIVO STUDY; INTERNEURON; MOUSE; NERVE CELL MEMBRANE POTENTIAL; NERVE REGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; POSTNATAL DEVELOPMENT; PROMOTER REGION; PROTEIN EXPRESSION; REPORTER GENE; SINGLE DRUG DOSE; STELLATE CELL; STEM CELL; WHITE MATTER;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; BIOLOGICAL MARKERS; CELL LINEAGE; CEREBELLUM; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION REGULATION; GENES, REPORTER; GLIAL FIBRILLARY ACIDIC PROTEIN; INTEGRASES; INTERNEURONS; MICE; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; RECOMBINATION, GENETIC; STEM CELLS; TAMOXIFEN; TIME FACTORS;

MUS; MUS MUSCULUS;

EID: 66149170085     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.18     Document Type: Article

References (66)

1. Ramon Y, Cajal S. Histology of the Nervous System. New York, NY:Oxford University Press, 1995.
2. Palay SL, Chan-Palay V. Cerebellar Cortex: Cytology and Organization. Vol. xii. Berlin:Springer, 1974:348.
3. Miale IL, Sidman RL. An autoradiographic analysis of histogenesis in the mouse cerebellum. Exp Neurol 1961;4:277-296.
4. Altman J, Bayer SA. Prenatal development of the cerebellar system in the rat. I. Cytogenesis and histogenesis of the deep nuclei and the cortex of the cerebellum. J Comp Neurol 1978;179:23-48.
5. Gould BB, Rakic P. The total number, time or origin and kinetics of proliferation of neurons comprising the deep cerebellar nuclei in the rhesus monkey. Exp Brain Res 1981;44:195-206. (Pubitemid 12227574)
6. Carletti B, Rossi F. Neurogenesis in the cerebellum. Neuroscientist 2008;14:91-100.
7. Hoshino M. Molecular machinery governing GABAergic neuron specification in the cerebellum. Cerebellum 2006;5:193-198. (Pubitemid 44451610)
8. Maricich SM, Herrup K. Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 1999;41:281-294. (Pubitemid 29494153)
9. Zhang L, Goldman JE. Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron 1996;16:47-54. (Pubitemid 26044728)
10. Milosevic A, Goldman JE. Potential of progenitors from postnatal cerebellar neuroepithelium and white matter: Lineage specified vs. multipotent fate. Mol Cell Neurosci 2004;26:342-353. (Pubitemid 38781090)
11. Weisheit G, Gliem M, Endl E et al. Postnatal development of the murine cerebellar cortex: Formation and early dispersal of basket, stellate and Golgi neurons. Eur J Neurosci 2006;24:466-478. (Pubitemid 44100338)
12. Hallonet ME, Teillet MA, Le Douarin NM. A new approach to the development of the cerebellum provided by the quail-chick marker system. Development 1990;108:19-31. (Pubitemid 20041690)
13. Alder J, Cho NK, Hatten ME. Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity. Neuron 1996;17:389-399. (Pubitemid 26322211)
14. Ben-Arie N, Bellen HJ, Armstrong DL et al. Math1 is essential for genesis of cerebellar granule neurons. Nature 1997;390:169-172. (Pubitemid 27507985)
15. Wingate RJ, Hatten ME. The role of the rhombic lip in avian cerebellum development. Development 1999;126:4395-4404.
16. Lin JC, Cai L, Cepko CL. The external granule layer of the developing chick cerebellum generates granule cells and cells of the isthmus and rostral hindbrain. J Neurosci 2001;21:159-168. (Pubitemid 32098738)
17. Machold R, Fishell G. Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 2005;48:17-24. (Pubitemid 41384162)
18. Altman J, Bayer S. Development of the Cerebellar System: In Relation to Its Evolution, Structure, and Function. Boca Raton, FL: CRC Press, 1997:783.
19. Hatten ME, Heintz N. Mechanisms of neural patterning and specification in the developing cerebellum. Annu Rev Neurosci 1995;18:385-408.
20. Wang VY, Zoghbi HY. Genetic regulation of cerebellar development. Nat Rev Neurosci 2001;2:484-491. (Pubitemid 33676583)
21. Komuro H, Yacubova E, Rakic P. Mode and tempo of tangential cell migration in the cerebellar external granular layer. J Neurosci 2001;21:527-540. (Pubitemid 32107442)
22. Lee A, Kessler JD, Read TA et al. Isolation of neural stem cells from the postnatal cerebellum. Nat Neurosci 2005;8:723-729. (Pubitemid 43085837)
23. Klein C, Butt SJ, Machold RP et al. Cerebellum- and forebrain-derived stem cells possess intrinsic regional character. Development 2005;132:4497-4508. (Pubitemid 41632228)
24. Leto K, Carletti B, Williams IM et al. Different types of cerebellar GABAergic interneurons originate from a common pool of multipotent progenitor cells. J Neurosci 2006;26:11682-11694.
25. Feil R, Brochard J, Mascrez B et al. Ligand-activated site-specific recombination in mice. Proc Natl Acad Sci USA 1996;93:10887-10890. (Pubitemid 26333086)
26. Metzger D, Clifford J, Chiba H et al. Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre recombinase. Proc Natl Acad Sci USA 1995;92:6991-6995.
27. Capela A, Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron 2002;35:865-875.
28. Graham V, Khudyakov J, Ellis P et al. SOX2 functions to maintain neural progenitor identity. Neuron 2003;39:749-765. (Pubitemid 37088088)
29. Seri B, Garcia-Verdugo JM, McEwen BS et al. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 2001;21:7153-7160. (Pubitemid 32846963)
30. Bani-Yaghoub M, Tremblay RG, Lei JX et al. Role of Sox2 in the development of the mouse neocortex. Dev Biol 2006;295:52-66. (Pubitemid 44041325)
31. Garcia AD, Doan NB, Imura T et al. GFAP-expressing progenitors are the principal source of constitutive neurogenesis in adult mouse forebrain. Nat Neurosci 2004;7:1233-1241. (Pubitemid 39426243)
32. Ganat YM, Silbereis J, Cave C et al. Early postnatal astroglial cells produce multilineage precursors and neural stem cells in vivo. J Neurosci 2006;26:8609-8621. (Pubitemid 44316190)
33. Brenner M, Kisseberth WC, Su Y et al. GFAP promoter directs astrocyte-specific expression in transgenic mice. J Neurosci 1994;14:1030-1037. (Pubitemid 24081901)
34. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nature Gen 1999;21:70-71. (Pubitemid 29036285)
35. Nakamura T, Colbert MC, Robbins J. Neural crest cells retain multipotential characteristics in the developing valves and label the cardiac conduction system. Circ Res 2006;98:1547-1554. (Pubitemid 44297078)
36. Gundersen HJ, Bagger P, Bendtsen TF et al. The new stereological tools: Disector, fractionator, nucleator, and point sampled intercepts and their use in pathological research and diagnosis. APMIS 1988;96:857-881. (Pubitemid 18270672)
37. West MJ. New stereological methods for counting neurons. Neurobiol Aging 1993;14:275-285. (Pubitemid 23214693)
38. Schmitz C, Hof PR. Design-based stereology in neuroscience. Neuroscience 2005;130:813-831. (Pubitemid 40094616)
39. Yamanaka H, Yanagawa Y, Obata K. Development of stellate and basket cells and their apoptosis in mouse cerebellar cortex. Neurosci Res 2004;50:13-22. (Pubitemid 39024297)
40. Fode C, Ma Q, Casarosa S et al. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 2000;14:67-80. (Pubitemid 30051580)
41. Ma Q, Sommer L, Cserjesi P et al. Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. J Neurosci 1997;17:3644-3652. (Pubitemid 27200591)
42. Zordan P, Croci L, Hawkes R et al. Comparative analysis of proneural gene expression in the embryonic cerebellum. Dev Dyn 2008;237:1726-1735.
43. Kim EJ, Battiste J, Nakagawa Y et al. Ascl1 (Mash1) lineage cells contribute to discrete cell populations in CNS architecture. Mol Cell Neurosci 2008;38:595-606.
44. Zhu X, Bergles DE, Nishiyama A. NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 2008;135:145-157.
45. Pringle NP, Richardson WD. A singularity of PDGF alpha-receptor expression in the dorsoventral axis of the neural tube may define the origin of the oligodendrocyte lineage. Development 1993;117:525-533. (Pubitemid 23103162)
46. Nishiyama A, Lin XH, Giese N et al. Co-localization of NG2 proteoglycan and PDGF alpha-receptor on O2A progenitor cells in the developing rat brain. J Neurosci Res 1996;43:299-314. (Pubitemid 26054018)
47. Redwine JM, Armstrong RC. In vivo proliferation of oligodendrocyte progenitors expressing PDGFalphaR during early remyelination. J Neurobiol 1998;37:413-428.
48. Fruttiger M, Karlsson L, Hall AC et al. Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development 1999;126:457-467. (Pubitemid 29082033)
49. Weyer A, Schilling K. Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J Neurosci Res 2003;73:400-409. (Pubitemid 36918103)
50. Altman J. Postnatal development of the cerebellar cortex in the rat. I. The external germinal layer and the transitional molecular layer. J Comp Neurol 1972;145:353-397.
51. 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)
52. Laywell E, Rakic P, Kukekov VG et al. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 2000;97:13883-13888.
53. Ellis P, Fagan BM, Magness ST et al. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci 2004;26:148-165. (Pubitemid 40867972)
54. Wegner M, Stolt CC. From stem cells to neurons and glia: A Soxist's view of neural development. Trends Neurosci 2005;28:583-588. (Pubitemid 41476688)
55. Sakakibara S, Nakamura Y, Satoh H et al. RNA-binding protein Musashi2: Developmentally regulated expression in neural precursor cells and subpopulations of neurons in mammalian CNS. J Neurosci 2001;21:8091-8107. (Pubitemid 32952766)
56. Imura T, Nakano I, Kornblum HI et al. Phenotypic and functional heterogeneity of GFAP-expressing cells in vitro: Differential expression of LeX/CD15 by GFAP-expressing multipotent neural stem cells and non-neurogenic astrocytes. Glia 2006;53:277-293. (Pubitemid 43224226)
57. Kamei Y, Inagaki N, Nishizawa M et al. Visualization of mitotic radial glial lineage cells in the developing rat brain by Cdc2 kinase-phosphorylated vimentin. Glia 1998;23:191-199. (Pubitemid 28259717)
58. Malatesta P, Hack MA, Hartfuss E et al. Neuronal or glial progeny: Regional differences in radial glia fate. Neuron 2003;37:751-764. (Pubitemid 36288548)
59. Kimelberg HK. The problem of astrocyte identity. Neurochem Int 2004;45:191-202. (Pubitemid 38625613)
60. Episkopou V. SOX2 functions in adult neural stem cells. Trends Neurosci 2005;28:219-221. (Pubitemid 41556906)
61. Kaneko Y, Sakakibara S, Imai T et al. Musashi1: An evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 2000;22:139-153. (Pubitemid 30098914)
62. Miyagi S, Nishimoto M, Saito T et al. The Sox2 regulatory region 2 functions as a neural stem cell-specific enhancer in the telencephalon. J Biol Chem 2006;281:13374-13381. (Pubitemid 43855248)
63. Mori T, Tanaka K, Buffo A et al. Inducible gene deletion in astroglia and radial glia - A valuable tool for functional and lineage analysis. Glia 2006;54:21-34. (Pubitemid 43980031)
64. Matthias K, Kirchhoff F, Seifert G et al. Segregated expression of AMPA-type glutamate receptors and glutamate transporters defines distinct astrocyte populations in the mouse hippocampus. J Neurosci 2003;23:1750-1758. (Pubitemid 36314730)
65. Sottile V, Li M, Scotting PJ. Stem cell marker expression in the Bergmann glia population of the adult mouse brain. Brain Res 2006;1099:8-17. (Pubitemid 44080085)
66. Snyder EY, Deitcher DL, Walsh C et al. Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 1992;68:33-51.