Regionalization and fate specification in neurospheres: The role of Olig2 and Pax6

Molecular and Cellular Neuroscience

Volumn 25, Issue 4, 2004, Pages 664-678

  Hack, M A ^a   Sugimori, M ^b   Lundberg, C ^c   Nakafuku, M ^b   Gotz M ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGODENDROCYTE TRANSCRIPTION FACTOR 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR OLIG1; TRANSCRIPTION FACTOR PAX6; UNCLASSIFIED DRUG;

ADULTHOOD; ANIMAL CELL; ARTICLE; BRAIN REGION; CELL FATE; CELL SPECIFICITY; CENTRAL NERVOUS SYSTEM; DOWN REGULATION; EMBRYO; GENE EXPRESSION REGULATION; MOUSE; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN FUNCTION; UPREGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BODY PATTERNING; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELLS, CULTURED; DOWN-REGULATION; EYE PROTEINS; GROWTH SUBSTANCES; HOMEODOMAIN PROTEINS; MICE; MICE, NEUROLOGIC MUTANTS; NERVE TISSUE PROTEINS; NEURONS; OLIGODENDROGLIA; PAIRED BOX TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; SPHEROIDS, CELLULAR; STEM CELLS; TELENCEPHALON; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 1842689282     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2003.12.012     Document Type: Article

References (75)

1. Alvarez-Buylla A., Garcia-Verdugo J.M., Tramontin A.D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev., Neurosci. 2:2001;287-293.
2. Anderson S.A., Eisenstat D.D., Shi L., Rubenstein J.L. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science. 278:1997;474-476.
3. Anderson S.A., Qiu M., Bulfone A., Eisenstat D.D., Meneses J., Pedersen R., Rubenstein J.L. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron. 19:1997;27-37.
4. Arvidsson A., Collin T., Kirik D., Kokaia Z., Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat. Med. 8:2002;963-970.
5. Bertrand N., Castro D.S., Guillemot F. Proneural genes and the specification of neural cell types. Nat. Rev., Neurosci. 3:2002;517-530.
6. Briata P., Di Blas E., Gulisano M., Mallamaci A., Iannone R., Boncinelli E., Corte G. EMX1 homeoprotein is expressed in cell nuclei of the developing cerebral cortex and in the axons of the olfactory sensory neurons. Mech. Dev. 57:1996;169-180.
7. Campbell K., Götz M. Radial glia: multi-purpose cells for vertebrate brain development. Trends Neurosci. 25:2002;235-238.
8. Capela A., Temple S. LeX/ssea-1 is expressed by adult mouse CNS stem cells, identifying them as nonependymal. Neuron. 35:2002;865-875.
9. Chojnacki A., Shimazaki T., Gregg C., Weinmaster G., Weiss S. Glycoprotein 130 signaling regulates Notch1 expression and activation in the self-renewal of mammalian forebrain neural stem cells. J. Neurosci. 23:2003;1730-1741.
10. Ciccolini F., Collins T.J., Sudhoelter J., Lipp P., Berridge M.J., Bootman M.D. Local and global spontaneous calcium events regulate neurite outgrowth and onset of GABAergic phenotype during neural precursor differentiation. J. Neurosci. 23:2003;103-111.
11. Decker L., Durbec P., Rougon G., Evercooren A.B. Loss of polysialic residues accelerates CNS neural precursor differentiation in pathological conditions. Mol. Cell Neurosci. 19:2002;225-238.
12. Diez del Corral R., Olivera-Martinez I., Goriely A., Gale E., Maden M., Storey K. Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron. 40:2003;65-79.
13. Doetsch F., Caille I., Lim D.A., Garcia-Verdugo J.M., Alvarez-Buylla A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell. 97:1999;703-716.
14. Doetsch F., Petreanu L., Caille I., Garcia-Verdugo J.M., Alvarez-Buylla A. EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron. 36:2002;1021-1034.
15. Fricker R.A., Carpenter M.K., Winkler C., Greco C., Gates M.A., Bjorklund A. Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J. Neurosci. 19:1999;5990-6005.
16. Gabay L., Lowell S., Rubin L., Anderson D. Deregulation of dorsoventral patterning by FGF confers trilineage differentiation capacity on CNS stem cells in vitro. Neuron. 40:2003;485-499.
17. Ghattas I.R., Sanes J.R., Majors J.E. The encephalomyocarditis virus internal ribosome entry site allows efficient coexpression of two genes from a recombinant provirus in cultured cells and in embryos. Mol. Cell. Biol. 11:1991;5848-5859.
18. Götz M. How are neurons specified: master or positional control? Trends Neurosci. 21:1998;135-136.
19. Götz M. Glial cells generate neurons - master control within CNS regions: developmental perspectives on neural stem cells. Neuroscientist. 9:2003;379-397.
20. Götz M., Stoykova A., Gruss P. Pax6 controls radial glia differentiation in the cerebral cortex. Neuron. 21:1998;1031-1044.
21. Götz M., Hartfuss E., Malatesta P. Radial glial cells as neuronal precursors: a new perspective on the correlation of morphology and lineage restriction in the developing cerebral cortex of mice. Brain Res. Bull. 57:2002;777-788.
22. Grandbarbe L., Bouissac J., Rand M., Hrabe de Angelis M., Artavanis-Tsakonas S., Mohier E. Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process. Development. 130:2003;1391-1402.
23. Grove E.A., Williams B.P., Li D.Q., Hajihosseini M., Friedrich A., Price J. Multiple restricted lineages in the embryonic rat cerebral cortex. Development. 117:1993;553-561.
24. Hartfuss E., Galli R., Heins N., Götz M. Characterization of CNS precursor subtypes and radial glia. Dev. Biol. 229:2001;15-30.
25. Heins N., Malatesta P., Cecconi F., Nakafuku M., Tucker K.L., Hack M.A., Chapouton P., Barde Y.A., Götz M. Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5:2002;308-315.
26. Herrera D.G., Garcia-Verdugo J.M., Alvarez-Buylla A. Adult-derived neural precursors transplanted into multiple regions in the adult brain. Ann. Neurol. 46:1999;867-877.
27. Hevner R.F., Neogi T., Englund C., Daza R.A., Fink A. Cajal-Retzius cells in the mouse: transcription factors, neurotransmitters, and birthdays suggest a pallial origin. Brain Res. Dev. Brain Res. 141:2003;39-53.
28. Hill R.E., Favor J., Hogan B.L., Ton C.C., Saunders G.F., Hanson I.M., Prosser J., Jordan T., Hastie N.D., van Heyningen V. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature. 354:1991;522-525.
29. Hitoshi S., Alexson T., Tropepe V., Donoviel D., Elia A.J., Nye J.S., Conlon R.A., Mak T.W., Bernstein A., van der Kooy D. Notch pathway molecules are essential for the maintenance, but not the generation, of mammalian neural stem cells. Genes Dev. 16:2002;846-858.
30. Hitoshi S., Tropepe V., Ekker M., van der Kooy D. Neural stem cell lineages are regionally specified, but not committed, within distinct compartments of the developing brain. Development. 129:2002;233-244.
31. Imura T., Kornblum H.I., Sofroniew M.V. The predominant neural stem cell isolated from postnatal and adult forebrain but not early embryonic forebrain expresses GFAP. J. Neurosci. 23:2003;2824-2832.
32. Kilpatrick T.J., Bartlett P.F. Cloned multipotential precursors from the mouse cerebrum require FGF-2, whereas glial restricted precursors are stimulated with either FGF-2 or EGF. J. Neurosci. 15:1995;3653-3661.
33. Klein C., Bueler H., Mulligan R.C. Comparative analysis of genetically modified dendritic cells and tumor cells as therapeutic cancer vaccines. J. Exp. Med. 191:2000;1699-1708.
34. Lim D.A., Tramontin A.D., Trevejo J.M., Herrera D.G., Garcia-Verdugo J.M., Alvarez-Buylla A. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron. 28:2000;713-726.
35. Lo L., Tiveron M.C., Anderson D.J. MASH1 activates expression of the paired homeodomain transcription factor Phox2a, and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development. 125:1998;609-620.
36. Lu Q.R., Sun T., Zhu Z., Ma N., Garcia M., Stiles C.D., Rowitch D.H. Common developmental requirement for Olig function indicates a motor neuron/oligodendrocyte connection. Cell. 109:2002;75-86.
37. Luskin M.B., Pearlman A.L., Sanes J.R. Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron. 1:1988;635-647.
38. Luskin M.B., Parnavelas J.G., Barfield J.A. Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J. Neurosci. 13:1993;1730-1750.
39. Malatesta P., Hack M.A., Hartfuss E., Kettenmann H., Klinkert W., Kirchhoff F., Götz M. Neuronal or glial progeny: regional differences in radial glia fate. Neuron. 37:2003;751-764.
40. Menezes J.R., Smith C.M., Nelson K.C., Luskin M.B. The division of neuronal progenitor cells during migration in the neonatal mammalian forebrain. Mol. Cell Neurosci. 6:1995;496-508.
41. Mizuguchi R., Sugimori M., Takebayashi H., Kosako H., Nagao M., Yoshida S., Nabeshima Y., Shimamura K., Nakafuku M. Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of pan-neuronal and subtype-specific properties of motoneurons. Neuron. 31:2001;757-771.
42. Molofsky A.V., Pardal R., Iwashita T., Park I.K., Clarke M.F., Morrison S.J. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature. 425:2003;962-967.
43. Morshead C.M., Garcia A.D., Sofroniew M.V., Van Der Kooy D. The ablation of glial fibrillary acidic protein-positive cells from the adult central nervous system results in the loss of forebrain neural stem cells but not retinal stem cells. Eur. J. Neurosci. 18:2003;76-84.
44. Nakamura Y., Sakakibara S., Miyata T., Ogawa M., Shimazaki T., Weiss S., Kageyama R., Okano H. The bHLH gene hes1 as a repressor of the neuronal commitment of CNS stem cells. J. Neurosci. 20:2000;283-293.
45. Nosaka T., Kawashima T., Misawa K., Ikuta K., Mui A.L., Kitamura T. STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J. 18:1999;4754-4765.
46. Novitch B.G., Chen A.I., Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron. 31:2001;773-789.
47. Ostenfeld T., Joly E., Tai Y.T., Peters A., Caldwell M., Jauniaux E., Svendsen C.N. Regional specification of rodent and human neurospheres. Brain Res. Dev. Brain Res. 134:2002;43-55.
48. Park H.C., Appel B. Delta-Notch signaling regulates oligodendrocyte specification. Development. 130:2003;3747-3755.
49. Parmar M., Skogh C., Bjorklund A., Campbell K. Regional specification of neurosphere cultures derived from subregions of the embryonic telencephalon. Mol. Cell Neurosci. 21:2002;645-656.
50. Pear W.S., Nolan G.P., Scott M.L., Baltimore D. Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. U. S. A. 90:1993;8392-8396.
51. Price J. Retroviruses and the study of cell lineage. Development. 101:1987;409-419.
52. Price J., Thurlow L. Cell lineage in the rat cerebral cortex: a study using retroviral-mediated gene transfer. Development. 104:1988;473-482.
53. Qian X., Davis A.A., Goderie S.K., Temple S. FGF2 concentration regulates the generation of neurons and glia from multipotent cortical stem cells. Neuron. 18:1997;81-93.
54. Ramalho-Santos M., Yoon S., Matsuzaki Y., Mulligan R.C., Melton D.A. "Stemness": transcriptional profiling of embryonic and adult stem cells. Science. 298:2002;597-600.
55. Reid C.B., Walsh C.A. Evidence of common progenitors and patterns of dispersion in rat striatum and cerebral cortex. J. Neurosci. 22:2002;4002-4014.
56. Reynolds B.A., Weiss S. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175:1996;1-13.
57. Rubenstein J.L., Puelles L. Homeobox gene expression during development of the vertebrate brain. Curr. Top. Dev. Biol. 29:1994;1-63.
58. Sadowski I., Ma J., Triezenberg S., Ptashne M. GAL4-VP16 is an unusually potent transcriptional activator. Nature. 335:1988;563-564.
59. Santa-Olalla J., Baizabal J.M., Fregoso M., del Carmen Cardenas M., Covarrubias L. The in vivo positional identity gene expression code is not preserved in neural stem cells grown in culture. Eur. J. Neurosci. 18:2003;1073-1084.
60. Schmahl W., Knoedlseder M., Favor J., Davidson D. Defects of neuronal migration and the pathogenesis of cortical malformations are associated with Small eye (Sey) in the mouse, a point mutation at the Pax-6-locus. Acta Neuropathol. (Berl.). 86:1993;126-135.
61. Seri B., Garcia-Verdugo J.M., McEwen B.S., Alvarez-Buylla A. Astrocytes give rise to new neurons in the adult mammalian hippocampus. J. Neurosci. 21:2001;7153-7160.
62. Song H., Stevens C.F., Gage F.H. Astroglia induce neurogenesis from adult neural stem cells. Nature. 417:2002;39-44.
63. Stoykova A., Treichel D., Hallonet M., Gruss P. Pax6 modulates the dorsoventral patterning of the mammalian telencephalon. J. Neurosci. 20:2000;8042-8050.
64. Takebayashi H., Yoshida S., Sugimori M., Kosako H., Kominami R., Nakafuku M., Nabeshima Y. Dynamic expression of basic helix-loop-helix Olig family members: implication of Olig2 in neuron and oligodendrocyte differentiation and identification of a new member, Olig3. Mech. Dev. 99:2000;143-148.
65. Tekki-Kessaris N., Woodruff R., Hall A.C., Gaffield W., Kimura S., Stiles C.D., Rowitch D.H., Richardson W.D. Hedgehog-dependent oligodendrocyte lineage specification in the telencephalon. Development. 128:2001;2545-2554.
66. Toresson H., Potter S.S., Campbell K. Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development. 127:2000;4361-4371.
67. Walsh C., Cepko C.L. Clonal dispersion in proliferative layers of developing cerebral cortex. Nature. 362:1993;632-635.
68. Walther C., Gruss P. Pax-6, a murine paired box gene, is expressed in the developing CNS. Development. 113:1991;1435-1449.
69. Williams B.P., Price J. Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron. 14:1995;1181-1188.
70. Williams B.P., Read J., Price J. The generation of neurons and oligodendrocytes from a common precursor cell. Neuron. 7:1991;685-693.
71. Winkler C., Fricker R.A., Gates M.A., Olsson M., Hammang J.P., Carpenter M.K., Bjorklund A. Incorporation and glial differentiation of mouse EGF-responsive neural progenitor cells after transplantation into the embryonic rat brain. Mol. Cell Neurosci. 11:1998;99-116.
72. Yan J., Studer L., McKay R.D. Ascorbic acid increases the yield of dopaminergic neurons derived from basic fibroblast growth factor expanded mesencephalic precursors. J. Neurochem. 76:2001;307-311.
73. Yee J.K., Friedmann T., Burns J.C. Generation of high-titer pseudotyped retroviral vectors with very broad host range. Methods Cell Biol. 43(Pt A):1994;99-112.
74. Zhou Q., Anderson D.J. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell. 109:2002;61-73.
75. Zhou Q., Choi G., Anderson D.J. The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron. 31:2001;791-807.