Hes1 but not Hes5 regulates an astrocyte versus oligodendrocyte fate choice in glial restricted precursors

Developmental Dynamics

Volumn 226, Issue 4, 2003, Pages 675-689

  Wu, Yuanyuan ^a   Liu, Ying ^a,b   Levine, Edward M ^a   Rao, Mahendra S ^b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Astrocyte; Development; Differentiation; GRP; Hes1; Hes5; Notch1; Oligodendrocyte; Promotion

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE; BIOLOGICAL MARKER; GLIAL FIBRILLARY ACIDIC PROTEIN; NOTCH RECEPTOR; PROTEOLIPID PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; ASTROCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM CELL; GENE; GENE EXPRESSION; HES1 GENE; HES5 GENE; NEUROEPITHELIUM; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STEM CELL; UPREGULATION;

ANIMALS; ASTROCYTES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINEAGE; DNA-BINDING PROTEINS; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; OLIGODENDROGLIA; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, NOTCH1; RECEPTORS, CELL SURFACE; REPRESSOR PROTEINS; SPINAL CORD; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 0037382649     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/dvdy.10278     Document Type: Article

References (63)

1. Alfei L, Alta M, Caronti B, De Vita R, Margotta V, Medolago Albani L, Valente AM. 1999. Hyaluronate receptor CD44 is expressed by astrocytes in the adult chicken and in astrocyte cell precursors in early development of the chick spinal cord. Eur J Histochem 43:29-38.
2. Artavanis-Tsakonas S, Matsuno K, Fortini ME. 1995. Notch signaling. Science 268:225-232.
3. Bailey AM, Posakony JW. 1995. Suppressor of hairless directly activates transcription of enhancer of split complex genes in response to Notch receptor activity. Genes Dev 9:2609-2622.
4. Bettenhausen B, Hrabe de Angelis M, Simon D, Guenet JL, Gossler A. 1995. Transient and restricted expression during mouse embryogenesis of DII1, a murine gene closely related to Drosophila Delta. Development 121:2407-2418.
5. Bonni A, Sun Y, Nadal-Vicens M, Bhatt A, Frank DA, Rozovsky I, Stahl N, Yancopoulos GD, Greenberg ME. 1997. Regulation of gliogenesis in the central nervous system by the JAK-STAT signaling pathway. Science 278:477-483
6. Castella P, Wagner JA, Caudy M. 1999. Regulation of hippocampal neuronal differentiation by the basic helix-loop-helix transcription factors HES-1 and MASH-1. J Neurosci Res 56:229-240.
7. Dawson SR, Turner DL, Weintraub H, Parkhurst SM. 1995. Specificity for the hairy/enhancer of split basic helix-loop-helix (bHLH) proteins maps outside the bHLH domain and suggests two separable modes of transcriptional repression. Mol Cell Biol 15:6923-6931.
8. de la Pompa JL, Wakeham A, Correia KM, Samper E, Brown S, Aguilera RJ, Nakano T, Honjo T, Mak TW, Rossant J, Conlon RA. 1997. Conservation of the Notch signalling pathway in mammalian neurogenesis. Development 124:1139-1148.
9. Dunwoodie SL, Henrique D, Harrison SM, Beddington RS. 1997. Mouse DII3: a novel divergent Delta gene which may complement the function of other Delta homologues during early pattern formation in the mouse embryo. Development 124:3065-3076.
10. Eddison M, Le Roux I, Lewis J. 2000. Notch signaling in the development of the inner ear: lessons from Drosophila. Proc Natl Acad Sci U S A 97:11692-11699.
11. Feder JN, Jan LY, Jan YN. 1993. A rat gene with sequence homology to the Drosophila gene hairy is rapidly induced by growth factors known to influence neuronal differentiation. Mol Cell Biol 13:105-113.
12. Frisen J, Lendahl U. 2001. Oh no, Notch again! Bioessays 23:3-7.
13. Fruttiger M, Karlsson L, Hall AC, Abramsson A, Calver AR, Bostrom H, Willetts K, Bertold CH, Heath JK, Betsholtz C, Richardson WD. 1999. Defective oligodendrocyte development and severe hypomyelination in PDGF-A knockout mice. Development 126:457-467.
14. Furukawa T, Mukherjee S, Bao ZZ, Morrow EM, Cepko CL. 2000. rax, Hes1, and notch1 promote the formation of Muller glia by postnatal retinal progenitor cells. Neuron 26:383-394.
15. Gage FH. 2000. Mammalian neural stem cells. Science 287:1433-1438.
16. Gaiano N, Nye JS, Fishell G. 2000. Radial glial identity is promoted by Notch1 signaling in the murine forebrain. Neuron 26:395-404.
17. Giebel B, Campos-Ortega JA. 1997. Functional dissection of the Drosophila enhancer of split protein, a suppressor of neurogenesis. Proc Natl Acad Sci U S A 94:6250-6254.
18. Gregori N, Proschel C, Noble M, Mayer-Proschel M. 2002. The tripotential glialrestricted precursor (GRP) cell and glial development in the spinal cord: generation of bipotential oligodendrocyte-type-2 astrocyte progenitor cells and dorsal-ventral differences in GRP cell function. J Neurosci 22:248-256.
19. Gross RE, Mehler MF, Mable PC, Zang Z, Santschi L, Kessler JA. 1996. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17:595-606.
20. Herrera J, Yang H, Zhang SC, Proschel C, Tresco P, Duncan ID, Luskin M, MayerProschel M. 2001. Embryonic-derived glial-restricted precursor cells (GRP cells) can differentiate into astrocytes and oligodendrocytes in vivo. Exp Neurol 171:11-21.
21. Hojo M, Ohtsuka T, Hashimoto N, Gradwohl G, Guillemot F, Kageyama R. 2000. Glial cell fate specification modulated by the bHLH gene Hes5 in mouse retina. Development 127:2515-2522.
22. Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F. 1995. Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev 9:3136-3148.
23. Ishibashi M, Moriyoshi K, Sasal Y, Shiota K, Nakanishi S, Kageyama R. 1994. Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J 13:1799-1805.
24. Issack PS, Ziff EB. 1998. Genetic elements regulating HES-1 induction in Wnt-1-transformed PC12 cells. Cell Growth Differ 9:827-836.
25. Jarriault S, Brou C, Logeat F, Schroeter EH, Kopan R, Israel A. 1995. Signalling downstream of activated mammalian Notch. Nature 377:355-358.
26. Jarriault S, Le Bail O, Hirsinger E, Pourqule O, Logeat F, Strong CF, Brou C, Seidah NG, Isra LA. 1998. Delta-1 activation of notch-1 signaling results in HES-1 transactivation. Mol Ceil Biol 18:7423-7431.
27. Kalyani A, Hobson K, Rao MS. 1997. Neuroepithelial stem cells from the embryonic spinal cord: isolation, characterization, and clonal analysis. Dev Biol 186:202-223.
28. Kondo T, Raff M. 2000. Basic helix-loop-helix proteins and the timing of oligodendrocyte differentiation. Development 127:2989-2998.
29. Lecourtois M, Schweisguth F. 1995. The neurogenic suppressor of hairless DNA-binding protein mediates the transcriptional activation of the enhancer of split complex genes triggered by Notch signaling. Genes Dev 9:2598-2608.
30. Lee JC, Mayer-Proschel M, Rao MS. 2000. Gliogenesis in the central nervous system. Glia 30:105-121.
31. Lee JC, Wu Y, Qi Y, Xue H, Liu Y, Cai J, Guillemot F, Qiu M, Rao MS. 2003. Neurogenin 3 participates in gliogenesis in the developing vertebrate spinal cord. Dev Biol 253:84-98.
32. Lendahl U. 1998. A growing family of Notch ligands. Bioessays 20:103-10.
33. Lewis J. 1996. Neurogenic genes and vertebrate neurogenesis. Curr Opin Neurobiol 6:3-10.
34. Lindsell CE, Shawber CJ, Boulter J, Weinmaster G. 1995. Jagged: a mammalian ligand that activates Notch1. Cell 80:909-917.
35. Lindsell CE, Boulter J, diSibio G, Gossler A, Weinmaster G. 1996. Expression patterns of Jagged, Delta1, Notch1, Notch2, and Notch3 genes identify ligand-receptor pairs that may function in neural development. Mol Cell Neurosci 8:14-27.
36. Lu QR, Yuk D, Alberta JA, Zhu Z, Pawlitzky J, Chan J, McMahon AP, Stiles CD, Rowitch DH. 2000. Sonic hedgehog-regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25:317-329.
37. Mayer-Proschel M, Kalyani AJ, Mujtaba T, Rao MS. 1997. Isolation of lineage-restricted neuronal precursors from multipotent neuroepithetial stem cells. Neuron 19:773-785.
38. Morrison SJ, Perez SE, Qiao Z, Verdi JM, Hicks C, Weinmaster G, Anderson DJ. 2000. Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101:499-510.
39. Nakashima K, Yanagisawa M, Arakawa H, Kimura N, Hisatsune T, Kawabata M, Miyazono K, Taga T. 1999. Synergistic signaling in fetal brain by STAT3-Smad1 complex bridged by p300. Science 284:479-482.
40. Nakashima K, Takizawa T, Ochiai W, Yanagisawa M, Hisatsune T, Nakafuku M, Miyazono K, Kishimoto T, Kageyama R, Taga T. 2001. BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis. Proc Natl Acad Sci U S A 98:5868-5873.
41. Nye JS, Kopan R, Axel R. 1994. An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development 120:2421-2430.
42. Ohtsuka T, Ishibashi M, Gradwohi G, Nakanishi S, Guillemot F, Kageyama R. 1999. Hes1 and Hes5 as notch effectors in mammalian neuronal differentiation. EMBO J 18:2196-2207.
43. Ohtsuka T, Sakamoto M, Guillemot F, Kageyama R. 2001. Roles of the basic helix-loop-helix genes Hes1 and Hes5 in expansion of neural stem cells of the developing brain. J Biol Chem 276:30467-30474.
44. Qi Y, Cai J, Wu Y, Wu R, Lee J, Fu H, Rao M, Sussel L, Rubenstein J, Qiu M. 2001. Control of oligodendrocyte differentiation by the Nkx2.2 homeodomain transcription factor. Development 128:2723-2733.
45. Rao MS, Mayer-Proschel M. 1997. Glial-restricted precursors are derived from multipotent neuroepithelial stem cells. Dev Biol 188:48-63.
46. Rao MS, Noble M, Mayer-Proschel M. 1998. A tripotential glial precursor cell is present in the developing spinal cord. Proc Natl Acad Sci U S A 95:3996-4001.
47. Sakagami T, Sakurada K, Sakai Y, Watanabe T, Nakanishi S, Kageyama R. 1994. Structure and chromosomal locus of the mouse gene encoding a cerebellar Purkinje cell-specific helix-loop-helix factor Hes-3. Biochem Biophys Res Commun 203:594-601.
48. Sasai Y, Kageyama R, Tagawa Y, Shigemoto R, Nakanishi S. 1992. Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev 6:2620-2634.
49. Schweisguth F. 1995. Suppressor of Hairless is required for signal reception during lateral inhibition in the Drosophila pupal notum. Development 121:1875-1884.
50. Shawber C, Boulter J, Lindsell CE, Weinmaster G. 1996a. Jagged2: a serrate-like gene expressed during rat embryogenesis. Dev Biol 180:370-376.
51. Shawber C, Nofziger D, Hsieh JJ, Lindsell C, Bogler O, Hayward D, Weinmaster G. 1996b. Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. Development 122:3765-3773.
52. Soula C, Danesin C, Kan P, Grob M, Poncet C, Cochard P. 2001. Distinct sites of origin of oligodendrocytes and somatic motoneurons in the chick spinal cord: oligodendrocytes arise from Nkx2.2-expressing progenitors by a Shh-dependent mechanism. Development 128:1369-1379.
53. Sun Y, Nadal-Vicens M, Misono S, Lin MZ, Zubiaga A, Hua X, Fan G, Greenberg ME. 2001. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104:365-376.
54. Takebayashi K, Akazawa C, Nakanishi S, Kageyama R. 1995. Structure and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-5. Identification of the neural precursor cell-specific promoter element. J Biol Chem 270:1342-1349.
55. Takke C, Dornseifer P, v Weizsacker E, Campos-Ortega JA. 1999. her4, a zebrafish homologue of the Drosophila neurogenic gene E(spl), is a target of NOTCH signalling. Development 126:1811-1821.
56. Tanigaki K, Nogaki F, Takahashi J, Tashiro K, Kurooka H, Honjo T. 2001. Notch1 and Notch3 instructively restrict bFGF-responsive multipotent neural progenitor cells to an astroglial fate. Neuron 29:45-55.
57. Vartanian T, Fischbach G, Miller R. 1999. Failure of spinal cord oligodendrocyte development in mice lacking neuregulin. Proc Natl Acad Sci U S A 96:731-735.
58. Wang S, Sdrulla AD, diSibio G, Bush G, Nofziger D, Hicks C, Weinmaster G, Barres BA. 1998. Notch receptor activation inhibits oligodendrocyte differentiation. Neuron 21:63-75.
59. Weissman IL, Anderson DJ, Gage F. 2001. Stem and progenitor cells: origins, phenotypes, lineage commitments, and transdifferentiations. Annu Rev Cell Dev Biol 17:387-403.
60. Xu X, Cai J, Fu H, Wu R, Qi Y, Modderman G, Liu R, Qiu M. 2000. Selective expression of Nkx-2.2 transcription factor in chicken oligodendrocyte progenitors and implications for the embryonic origin of oligodendrocytes. Mol Cell Neurosci 16:740-753.
61. Zhou Q, Anderson DJ. 2002. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109:61-73.
62. Zhou Q, Wang S, Anderson DJ. 2000. Identification of a novel family of oligodendrocyte lineage-specific basic helix-loop-helix transcription factors. Neuron 25:331-343.
63. Zhou Q, Choi G, Anderson DJ. 2001. The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31:791-807.