The bHLH gene Hes1 as a repressor of the neuronal commitment of CNS stem cells

Journal of Neuroscience

Volumn 20, Issue 1, 2000, Pages 283-293

  Nakamura, Yuki ^a   Sakakibara, Shin Ichi ^a,b   Miyata, Takaki ^a   Ogawa, Masaharu ^c   Shimazaki, Takuya ^e   Weiss, Samuel ^e   Kageyama, Ryoichiro ^d   Okano, Hideyuki ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^c INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e UNIVERSITY OF CALGARY   (Canada)

Author keywords

Apoptosis; Basic helix loop helix (bHLH) transcription factor; Hes1; Multipotent progenitor cell; Neuronal commitment; Neurosphere assay

Indexed keywords

HELIX LOOP HELIX PROTEIN; NESTIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; CENTRAL NERVOUS SYSTEM; EMBRYO; FETUS; GENE REPRESSION; MOUSE; NEUROFILAMENT; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STEM CELL;

EID: 0033993524     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-01-00283.2000     Document Type: Article

References (68)

1. Akazawa C, Sasai Y, Nakanishi S, Kageyama R (1992) Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system. J Biol Chem 267:21879-21885.
2. Artavanis-Tsakonas S, Matsuno K, Fortini ME (1995) Notch signaling. Science 268:225-232.
3. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: cell fate control and signal integration in development. Science 284:770-776.
4. Bayer SA, Altman J (1991) Neocortical development. New York: Raven.
5. Blaschke AJ, Staley K, Chun J (1996) Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development 122:1165-1174.
6. Casarosa S, Fode C, Guillemot F (1999) Mash1 regulates neurogenesis in the ventral telencephalon. Development 126:525-534.
7. Cohen J, Wilkin GP (1995) Neural cell culture, New York: Oxford UP.
8. Crandall JE, Jacobson M, Kosik KS (1986) Ontogenesis of microtubule-associated protein 2 (MAP2) in embryonic mouse cortex. Dev Brain Res 28:127-133.
9. Debus E, Weber K, Osborn M (1983) Monoclonal antibodies specific for glial fibrillary acidic (GFA) protein and for each of the neurofilament triplet polypeptides. Differentiation 25:193-203.
10. DiCicco-Bloom E, Friedman WJ, Black IB (1993) NT-3 stimulates sympathetic neuroblast proliferation by promoting precursor survival. Neuron 11:1101-1111.
11. Frederiksen K, McKay RD (1988) Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J Neurosci 8:1144-1151.
12. Galand P, Degraef C (1989) Cyclin/PCNA immunostaining as an alternative to tritiated thymidine pulse labeling for marking S phase cells in paraffin sections from animal and human tissues. Cell Tissue Kinet 22:383-392.
13. Gerdes J, Schwab U, Lemke H, Stein H (1983) Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation. Int J Cancer 31:13-20.
14. Ghosh A, Greenberg ME (1995) Distinct roles for bFGF and NT-3 in the regulation of cortical neurogenesis. Neuron 15:89-103.
15. Ghosh A, Carnahan J, Greenberg ME (1994) Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263:1618-1623.
16. Guo M, Jan LY, Jan YN (1996) Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17:27-41.
17. Guillemot F, Joyner AL (1993) Dynamic expression of the murine Achacte-scute homolog Mash1 in the developing nervous system. Mech Dev 42:171-185.
18. Hockfield S, McKay RD (1985) Identification of major cell classes in the developing mammalian nervous system. J Neurosci 5:3310-3328.
19. Hulspas R, Tiarks C, Reilly J, Hsieh CC, Recht L, Quesenberry PJ (1997) In vitro cell density-dependent clonal growth of EGF-responsive murine neural progenitor cells under serum-free conditions. Exp Neurol 148:147-156.
20. Ingham PW, Howard KR, Ish-Horowicz D (1985) Transcription pattern of the Drosophila segmentation gene hairy. Nature 318:439-445.
21. Ishibashi M, Moriyoshi K, Sasai 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.
22. Ishibashi M, Siew-Lan A, 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. Izant JG, McIntosh JR (1980) Microtubule-associated proteins: a monoclonal antibody to MAP2 binds to differentiated neurons. Proc Natl Acad Sci USA 77:4741-4745.
24. Jan YN, Jan LY (1998) Asymmetric cell division. Nature 392:775-778.
25. Johnson GVW, Jope RS (1992) The role of microtubule-associated protein 2 (MAP2) in neuronal growth, plasticity, and degeneration. J Neurosci Res 33:505-512.
26. Johnson JE, Birren SJ, Anderson DJ (1990) Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 346:858-861.
27. Jones KR, Farinas I, Backus C, Reichardt LF (1994) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76:989-999.
28. Kageyama R, Nakanishi S (1997) Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system. Curr Opin Genet Dev 7:659-665.
29. Kageyama R, Sasai Y, Akazawa C, Ishibashi M, Takebayashi K, Shimizu C, Tomita K, Nakanishi S (1995) Regulation of mammalian neural development by helix-loop-helix transcription factors. Crit Rev Neurobiol 9:177-188.
30. Kaneko Y, Sakakibara S, Imai T, Suzuki A, Nakamura Y, Sawamoto K, Ogawa Y, Toyama Y, Miyata T, Okano H (2000) Musashil: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev Neurosci 22:138-152.
31. Klämbt C, Knust E, Tietze K, Campos-Ortega JA (1989) Closely related transcripts encoded by the neurogcnic gene complex Enhancer of split of Drosophila melanogaster. EMBO J 8:203-210.
32. Lee JE (1997) Basic helix-loop-helix genes in neural development. Curr Opin Neurobiol 7:13-20.
33. Lee JE, Hollenberg SM, Snider L, Turner D, Lipnick N, Weintraub H (1995) Conservation of Xenopus Ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268:836-844.
34. Lee MK, Tittle JB, Rebhun LI, Cleveland DW, Frankfurter A (1990) The expression and posttranslational modification of a neuron-specific β-tubulin isotype during chick embryogenesis. Cell Motil Cytoskel 17:117-132.
35. Lendahl U, Zimmerman LB, McKay RDG (1990) CNS stem cells express a new class of intermediate filament protein. Cell 60:585-595.
36. Lillien L (1998) Neural progenitors and stem cells: mechanisms of progenitor heterogeneity. Curr Opin Neurobiol 8:37-44.
37. Lo LC, Johnson JE, Wuenschell CW, Saito T, Anderson DJ (1991) Mammalian achaete-scute homolog 1 is transiently expressed by spatially-restricted subsets of early neuroepithelial and neural crest cells. Genes Dev 5:1524-1537.
38. Luskin MB, Pearlman AL, Sanes JR (1988) Cell lineage in the cerebral cortex of the mouse studied in vivo and in vitro with a recombinant retrovirus. Neuron 1:635-647.
39. Marusich MF, Furneasx HM, Henion PD, Weston JA (1994) Hu neuronal proteins are expressed in proliferating neurogenic cells. J Neurobiol 25:143-155.
40. Mayer-Proschel M, Kalyani AJ, Mujtaba T, Rao MS (1997) Isolation of lineage-restricted neuronal precursors from multipotent neuroepithelial stem cells. Neuron 19:773-785.
41. McAllister AK, Lo DC, Kats LC (1995) Neurotrophins regulate dendritic growth in developing visual cortex. Neuron 15:791-803.
42. McConnell SK (1995) Constructing the cerebral cortex: neurogenesis and fate determination. Neuron 15:761-768.
43. Menezes JR, Luskin MB (1994) Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J Neurosci 14:5399-5416.
44. Miyata T, Ogawa M (1994) Developmental potentials of early telencephalic neuroepithelial cells: a study with microexplant culture. Dev Growth Differ 36:319-331.
45. Morrow EM, Furukawa T, Lee JE, Cepko CL (1999) NeuroD regulates multiple functions in the developing neural retina in rodent. Development 126:23-36.
46. Nakao K, Campos-Ortega JA (1996) Persistent expression of genes of the Enhancer of Split complex suppresses neural development in Drosophila. Neuron 16:275-286.
47. Nawa H, Pelleymounter MA, Carnahan J (1994) Intraventricular administration of BDNF increases neuropeptide expression in newborn rat brain. J Neurosci 14:3751-3765.
48. Niinobe M, Maeda N, Ino H, Mikoshiba K (1988) Characterization of microtubule-associated protein 2 from mouse brain and its localization in the cerebellar cortex. J Neurochem 51:1132-1139.
49. Ohtsuka T, Ishihashi M, Gradwohl G, Nakanishi S, Guillemot F, Kageyama R (1999) Hes1 and Hes5 as Notch effectors in mammalian neuronal differentiation. EMBO J 18:2196-2207.
50. Okano HJ, Darnell RB (1997) A hierarchy of Hu RNA binding proteins in developing and adult neurons. J Neurosci 17:3024-3037.
51. Qian X, Goderic SK, Shen Q, Stern JH, Temple S (1998) Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125:3143-3152.
52. Rakic P (1988) Specification of cerebral cortical areas. Science 241:170-176.
53. Reynolds BA, Weiss S (1996) Clonal and population analyses demonstrate that an EGF-responsivc mammalian embryonic CNS precursor is a stem cell. Dev Biol 175:1-13.
54. Reynolds BA, Tetzlaff W, Weiss S (1992) A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565-4574.
55. Sakakibara S, Okano H (1997) Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J Neurosci 17:8300-8312.
56. Sakakibara S, Imai T, Hamaguchi K, Okabe M, Aruga J, Nakajima K, Yasutomi D, Nagata T, Kurihara Y, Uesugi S, Miyata T, Ogawa M, Mikoshiba K, Okano H (1996) Mouse-Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev Biol 176:230-242.
57. 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.
58. Schlüter C, Duchrow M, Wohlenberg C, Becker MHG, Key G, Flad HD, Gerdes J (1993) The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol 123:513-522.
59. Ström A, Castella P, Rockwood J, Wagner J, Caudy M (1997) Mediation of NGF signaling by post-translational inhibition of HES-1, a basic helix-loop-helix repressor of neuronal differentiation. Genes Dev 11:3168-3181.
60. Takebayashi K, Sasai Y, Sakai Y, Watanabe T, Nakanishi S, Kageyama R (1994) Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES1: negative autoregulation through the multiple N box elements. J Biol Chem 269:5150-5156.
61. Tanabe Y, Jessell TM (1996) Diversity and pattern in the developing spinal cord. Science 274:1115-1123.
62. Temple S (1989) Division and differentiation of isolated CNS blast cells in microculture. Nature 340:471-473.
63. Thomson JA, Marshall VS, Trojanowski JQ (1998) Neural differentiation of rhesus embryonic stem cells. APMIS 106:149-157.
64. Torii M, Matsuzaki F, Osumi N, Kaibuchi K, Nakamura S, Casarosa S, Guillemot F, Nakafuku M (1999) Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development 126:443-456.
65. Tropepe V, Sibilia M, Ciruna BG, Rossant J, Wagner EF, van der Kooy D (1999) Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telcncephalon. Dev Biol 208:166-188.
66. Vescovi AL, Reynolds BA, Fraser DD, Weiss S (1993) bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11:951-966.
67. Wakamatsu Y, Weston JA (1997) Sequential expression and role of Hu RNA-binding proteins during neurogenesis. Development 124:3449-3460.
68. Wang S, Sdrulla AD, duSibio G, Bush G, Nofziger D, Hicks C, Weinmaster G, Barres BA (1998) Notch recepter activation inhibits oligodendrocyte differentiation. Neuron 21:63-75.