Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system

Development

Volumn 126, Issue 3, 1999, Pages 443-456

  Torii, Masa Aki ^a   Matsuzaki, Fumio ^b   Osumi, Noriko ^b   Kaibuchi, Kozo ^c   Nakamura, Shun ^b   Casarosa, Simona ^d   Guillemot, François ^d   Nakafuku, Masato ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b National Institute of Neurology and Psychiatry   (Japan)

^c NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^d NONE

Author keywords

Glia; Mash 1; Neural development; Neuron; Prospero; Stem cell

Indexed keywords

NESTIN; TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; EMBRYO; MOUSE; MOUSE MUTANT; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; RAT; STEM CELL;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; DNA-BINDING PROTEINS; HELIX-LOOP-HELIX MOTIFS; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MICE; MICE, KNOCKOUT; RABBITS; RATS; STEM CELLS; TRANSCRIPTION FACTORS;

ANIMALIA; MAMMALIA; PROSPERO; VERTEBRATA;

EID: 0033063992     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Altman, J. and Bayer, S. A. (1995). Atlas of the prenatal rat brain development. CRC Press Inc, Ltd., Boca Raton.
2. Angevine, J. B. Jr. (1970). Time of neuron origin in the diencephalon of the mouse. An autoradiographic study. J. Com. Neurol. 139, 129-187.
3. Bhide, P. G. (1996). Cell cycle kinetics in the embryonic mouse corpus striatum. J. Comp. Neurol. 374, 506-522.
4. Boulder Committee (1970). Embryonic vertebrate central nervous system: revised terminology. Anat. Rec. 166, 257-261.
5. Bulfone, A., Puelles, L., Porteus, M. H., Frohman, M. A., Martin, G. R. and Rubenstein, J. L. (1993). Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2 and Wnt-3 in the embryonic day 12.5 mouse forebrain detines potential transverse and longitudinal segmental boundaries. J. Neurosci. 13, 3155-3172.
6. Casarosa, S., Fode, C. and Guillemot, F. (1999). Mash-1 regulates neurogenesis in the ventral telencephalon. Development 126, 525-534.
7. Cau, E., Gradwohl, G., Fode, C. and Guillemot, F. (1997). Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. Development 124, 1611-1621.
8. Cepko, C., Ryder, E. F., Austin, C. P., Walsh, C. and Fekete, D. M. (1995). Lineage analysis using retrovirus vectors. Methods Enzymol. 254, 387-419.
9. Davis, A. A. and Temple, S. (1994). A self-renewing multipolential stem cell in embryonic rat cerebral cortex. Nature 372, 263-266.
10. de la Pompa, J. L., Wakeham, A., Correia, K. M., Samper, E., Brown, S., Aguilera, R. J., Nakano, T., Honjo, T., Mak, T. W., Rossant, J. and Conlon, R. A. (1997). Conservation of the Notch signaling pathway in mammalian neurogenesis. Development 124, 1139-1148.
11. Doe, C. Q. and Technau, G. M. (1993). Identification and cell lineage of individual neural precursors in the Drosophila CNS. Trends Neurosci. 16, 510-514.
12. Frederiksen, K. and McKay, R. D. (1988). Proliferation and differentiation of rat neuroepithelial precursor cells in vivo. J. Neurosci. 8, 1144-1151.
13. Gordon, M. K., Mumm, J. S., Davis, R. A., Holcomb, J. D. and Calof, A. L. (1995). Dynamics of MASH1 expression in vitro and in vivo suggest a non-stem cell site of MASH1 action in the olfactory receptor neuron lineage. Mol. Cell. Neurosci. 6, 363-379.
14. Gradwohl, G., Fode, C. and Guillemot, F. (1996). Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors. Dev. Biol. 180, 227-241.
15. Gross, R. E., Mehler, M. F., Mabie, P. C., Zang, Z., Santschi, L. and Kessler, J. A. (1996). Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17, 595-606.
16. Guillemot, F. and Joyner, A. L. (1993). Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system. Mech. Dev. 42, 171-185.
17. Guillemot, F., Lo, L. C., Johnson, J. E., Auerbach, A., Anderson, D. J. and Joyner, A. L. (1993). Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463-476.
18. Hall, P. A. and Watt, F. M. (1989). Stem cells: the generation and maintenance of cellular diversity. Development 106, 619-633.
19. Hirata, J., Nakagoshi, H., Nabeshima, Y. and Matsuzaki, F. (1995). Asymmetric segregation of the homeodomain protein Prospero during Drosophila development. Nature 377, 627-630.
20. Hirsch, M. R., Tiveron, M. C., Guillemot, F., Brunet, J. F. and Goridis, C. (1998). Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development Suppl. 125, 599-608.
21. Jan, Y. N. and Jan, L. Y. (1993). HLH proteins, fly neurogenesis and vertebrate myogenesis. Cell 75, 827-830.
22. Johe, K. K., Hazel, T. G., Muller, T., Dugich-Djordjevic, M. M. and McKay, R. D. (1996). Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev. 10, 3129-3140.
23. Johnson, J. E., Birren, S. J. and Anderson, D. J. (1990). Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 346, 858-861.
24. Kageyama, R. and Nakanishi, S. (1997). Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system. Curr. Opin. Genet. Dev. 7, 659-665.
25. Kilpatrick, T. J. and Bartlett, P. F. (1993). Cloning and growth of multipotential neural precursors: requirements for proliferation and differentiation. Neuron 10, 255-265.
26. Kilpatrick, T. J., Richards, L. J. and Bartlett, P. F. (1995). The regulation of neural precursor cells within the mammalian brain. Mol. Cell. Neurosci. 6, 2-15.
27. Lee, J. E. (1997). Basic helix-loop-helix genes in neural development. Curr. Opin. Neurobiol. 7, 13-20.
28. Lendahl, U., Zimmerman, L. B. and McKay, R. D. (1990). CNS stem cells express a new class of intermediate filament protein. Cell 60, 585-595.
29. Lillien, L. (1998). Neural progenitors and stem cells: mechanisms of progenitor heterogeneity. Curr. Opin. Neurobiol. 8, 37-44.
30. Lo, L. and Anderson, D. J. (1995). Postmigratory neural crest cells expressing c-RET display restricted developmental and proliferative capacities. Neuron 15, 517-539.
31. Lo, L. C., Johnson, J. E., Wuenschell, C. W., Saito, T. and Anderson, D. J. (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.
32. Lo, L., Tiveron, M. C. and Anderson, D. J. (1998). MASH1 activates expression of the paired homeodomain transcription factor Phox2a and couples pan-neuronal and subtype-specific components of autonomic neuronal identity. Development 125, 609-620.
33. McConnell, S. K. (1995). Strategies for the generation of neuronal diversity in the developing central nervous system. J. Neurosci. 15, 6987-6998.
34. McKay, R. (1997). Stem cells in the central nervous system. Science 276, 66-71.
35. Nakafuku, M. and Nakamura, S. (1995). Establishment and characterization of a multipotential neural cell line that can conditionally generate neurons. astrocytes and oligodendrocytes in vitro. 3. Neurosci. Res. 41, 153-168.
36. Nakagawa, Y., Kaneko, T., Ogura, T., Suzuki, T., Torii, M., Kaibuchi, K., Arai, K., Nakamura, S. and Nakafuku, M. (1996). Roles of cell-autonomous mechanisms for differential expression of region-specific transcription factors in neuroepithelial cells. Development 122, 2449-2464.
37. Oliver, G., Sosa-Pineda, B., Geisendorf, S., Spana, E. P., Doe, C. Q. and Gruss, P. (1993). Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech. Dev. 44, 3-16.
38. Osumi, N., Hirota, A., Ohuchi, H., Nakafuku, M., Iimura, T., Kuratani, S., Fujiwara, M., Noji, S. and Eto, K. (1997). Pax-6 is involved in the specification of hindbrain motor neuron subtype. Development 124, 2961-2972.
39. Porteus, M. H., Bulfone, A., Liu, J. K., Puelles, L., Lo, L. C. and Rubenstein, J. L. (1994). DLX-2, MASH-1 and MAP-2 expression and bromodeoxyuridine incorporation define molecularly distinct cell populations in the embryonic mouse forebrain. J. Neurosci. 14, 6370-6383.
40. Puelles, L. and Rubenstein, J. L. (1993). Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci. 16, 472-479.
41. Qian, X., Goderie, S. K., Shen, Q., Stern, J. H. and Temple, S. (1998). Intrinsic programs of patterned cell lineages in isolated vertebrate CNS ventricular zone cells. Development 125, 3143-3152.
42. Redies, C., Lendahl, U. and McKay, R. D. (1991). Differentiation and heterogeneity in T-antigen immortalized precursor cell lines from mouse cerebellum. J. Neurosci Res. 30, 601-615.
43. Reynolds, B. A., Tetzlaff, W. and Weiss, S. (1992). A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12, 4565-4574.
44. Reynolds, B. A. and Weiss, S. (1996). Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev. Biol. 175, 1-13.
45. Saito, T., Lo, L., Anderson, D. J. and Mikoshiba, K. (1996). Identification of novel paired homeodomain protein related to C. elegans unc-4 as a potential downstream target of MASH1. Dev. Biol. 25, 143-155.
46. Shah, N. M., Groves, A. K. and Anderson, D. J. (1996) Alternative neural crest cell fates are instructively promoted by TGFbeta superfamily members. Cell 85, 331-343.
47. Sommer, L., Shah, N., Rao, M. and Anderson, D. J. (1995). The cellular function of MASH1 in autonomie neurogenesis. Neuron 15, 1245-1258.
48. Stoykova, A. and Gruss, P. (1994). Roles of Pax-genes in developing and adult brain as suggested by expression patterns. J. Neurosci. 14, 1395-1412.
49. Temple, S. and Qian, X. (1996). Vertebrate neural progenitor cells: subtypes and regulation. Curr. Opin. Neurobiol. 6, 11-17.
50. Verma-Kurvari, S., Savage, T., Smith, D. and Johnson, J. E. (1998). Multiple elements regulate Mash1 expression in the developing CNS. Dev. Biol. 197, 106-116.
51. Vescovi, A. L., Reynolds, B. A., Fraser, D. D. and Weiss, S. (1993). bFGF regulates the proliferative fate of unipotent (neuronal) and bipotent (neuronal/astroglial) EGF-generated CNS progenitor cells. Neuron 11, 951-966.
52. Williams, B. P. and Price, J. (1995). Evidence for multiple precursor cell types in the embryonic rat cerebral cortex. Neuron 14, 1181-1188.
53. Williams, B. P., Park, J. K., Alberta, J. A., Muhlebach, S. G., Hwang, G. Y., Roberts, T. M. and Stiles, C. D. (1997). A PDGF-regulated immediate early gene response initiates neuronal differentiation in ventricular zone progenitor cells. Neuron 18, 553-562.
54. Zimmerman, L., Parr, B., Lendahl, U., Cunningham, M., McKay, R., Gavin, B., Mann, J., Vassileva, G. and McMahon, A. (1994). Independent regulatory elements in the nestin gene direct transgene expression to neural stem cells or muscle precursors. Neuron 12, 11-24.