Generation of neurons by transient expression of neural bHLH proteins in mammalian cells

Development

Volumn 127, Issue 4, 2000, Pages 693-702

  Farah, Mohamed H ^a,b   Olson, James M ^c,d   Sucic, Holly B ^a   Hume, Richard I ^b,e   Tapscott, Stephen J ^d   Turner, David L ^a,b  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d USA   (United States)

^e UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Basic helix loop helix; Mouse; Neuron; p27; Transcription

Indexed keywords

CELL PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR; HELIX LOOP HELIX PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; CARCINOMA CELL; CELL CYCLE; CELL FATE; CELL STRUCTURE; CONTROLLED STUDY; DIMERIZATION; EMBRYONAL CARCINOMA; GENETIC TRANSFECTION; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL CYCLE; CELL CYCLE PROTEINS; CELL DIFFERENTIATION; CELL LINE; CYCLIN-DEPENDENT KINASE INHIBITOR P27; CYCLIN-DEPENDENT KINASES; DNA PRIMERS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VECTORS; HELIX-LOOP-HELIX MOTIFS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; NEURONS; NEUROPEPTIDES; TRANSCRIPTION FACTORS; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA; HEXAPODA; MAMMALIA;

EID: 0034051923     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (52)

1. Akazawa, C., Ishibashi, M., Shimizu, C., Nakanishi, S. and Kageyama, R. (1995). A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J. Biol. Chem. 270, 8730-8738.
2. Bain, G., Kitchens, D., Yao, M., Huettner, J. E. and Gottlieb, D. I. (1995). Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168, 342-357.
3. Bartholoma, A. and Nave, K. A. (1994). NEX-1: a novel brain-specific helix-loop-helix protein with autoregulation and sustained expression in mature cortical neurons. Mech. Dev. 48, 217-228.
4. Begley, C. G., Lipkowitz, S., Gobel, V., Mahon, K. A., Bertness, V., Green, A. R., Gough, N. M. and Kirsch, I. R. (1992). Molecular characterization of NSCL, a gene encoding a helix-loop-helix protein expressed in the developing nervous system. Proc. Natl. Acad. Sci. USA 89, 38-42.
5. Ben-Arie, N., Bellen, H. J., Armstrong, D. L., McCall, A. E., Gordadze, P. R., Guo, Q., Matzuk, M. M. and Zoghbi, H. Y. (1997). Math1 is essential for genesis of cerebellar granule neurons. Nature 390, 169-172.
6. Blader, P., Fischer, N., Gradwohl, G., Guillemont, F. and Strahle, U. (1997). The activity of neurogenin1 is controlled by local cues in the zebrafish embryo. Development 124, 4557-4569.
7. Boudjelal, M., Taneja, R., Matsubara, S., Bouillet, P., Dolle, P. and Chambon, P. (1997). Overexpression of Stra13, a novel retinoic acid-inducible gene of the basic helix-loop-helix family, inhibits mesodermal and promotes neuronal differentiation of P19 cells. Genes Dev. 11, 2052-2065.
8. 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.
9. Chen, C. and Okayama, H. (1987). High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell Biol. 7, 2745-2752.
10. Cserjesi, P., Brown, D., Lyons, G. E. and Olson, E. N. (1995). Expression of the novel basic helix-loop-helix gene eHAND in neural crest derivatives and extraembryonic membranes during mouse development. Dev. Biol. 170, 664-678.
11. Davis, R. L., Cheng, P. F., Lassar, A. B. and Weintraub, H. (1990). The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60, 733-746.
12. Easter, S. S., Jr., Ross, L. S. and Frankfurter, A. (1993). Initial tract formation in the mouse brain. J. Neurosci. 13, 285-299.
13. Fode, C., Gradwohl, G., Morin, X., Dierich, A., LeMeur, M., Goridis, C. and Guillemot, F. (1998). The bHLH protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. Neuron 20, 483-494.
14. Furukawa, T., Morrow, E. M. and Cepko, C. L. (1997). Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91, 531-541.
15. 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.
16. Halevy, O., Novitch, B. G., Spicer, D. B., Skapek, S. X., Rhee, J., Hannon, G. J., Beach, D. and Lassar, A. B. (1995). Correlation of terminal cell cycle arrest of skeletal muscle with induction of p21 by MyoD. Science 267, 1018-1021.
17. 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 125, 599-608.
18. Hollenberg, S. M., Sternglanz, R., Cheng, P. F. and Weintraub, H. (1995). Identification of a new family of tissue-specific basic helix-loop-helix proteins with a two-hybrid system. Mol. Cell Biol. 15, 3813-3822.
19. Itoh, F., Nakane, T. and Chiba, S. (1997). Gene expression of MASH-1, MATH-1, neuroD and NSCL-2, basic helix-loop-helix proteins, during neural differentiation in P19 embryonal carcinoma cells. Tohoku J. Exp. Med. 182, 327-336.
20. 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.
21. Johnson, J. E., Zimmerman, K., Saito, T. and Anderson, D. J. (1992). Induction and repression of mammalian achaete-scute homologue (MASH) gene expression during neuronal differentiation of P19 embryonal carcinoma cells. Development 114, 75-87.
22. Kanekar, S., Perron, M., Dorsky, R., Harris, W. A., Jan, L. Y., Jan, Y. N. and Vetter, M. L. (1997). Xath5 participates in a network of bHLH genes in the developing Xenopus retina. Neuron 19, 981-994.
23. Lee, J. E., Hollenberg, S. M., Snider, L., Turner, D. L., Lipnick, N. and Weintraub, H. (1995). Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268, 836-844.
24. 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.
25. Ma, Q., Chen, Z., del Barco Barrantes, I., de la Pompa, J. L. and Anderson, D. J. (1998). neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20, 469-482.
26. Ma, Q., Kintner, C. and Anderson, D. J. (1996). Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87, 43-52.
27. McBurney, M. W. (1993). P19 embryonal carcinoma cells. Int. J. Dev. Biol. 37, 135-140.
28. McBurney, M. W., Reuhl, K. R., Ally, A. I., Nasipuri, S., Bell, J. C. and Craig, J. (1988). Differentiation and maturation of embryonal carcinoma-derived neurons in cell culture. J. Neurosci. 8, 1063-1073.
29. McCormick, M. B., Tamimi, R. M., Snider, L., Asakura, A., Bergstrom, D. and Tapscott, S. J. (1996). neuroD2 and neuroD3: Distinct Expression Patterns and Transcriptional Activation Potentials within the neuroD Gene Family. Molec. Cell. Biol. 16, 5792-5800.
30. Miyata, T., Maeda, T. and Lee, J. E. (1999). NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev. 13, 1647-1652.
31. Molkentin, J. D. and Olson, E. N. (1996). Defining the regulatory networks for muscle development. Curr. Opin. Genet. Dev. 6, 445-453.
32. Morrow, E. M., Furukawa, T., Lee, J. E. and Cepko, C. L. (1999). NeuroD regulates multiple functions in the developing neural retina in rodent. Development 126, 23-36.
33. Murre, C., McCaw, P. S., Vaessin, H., Caudy, M., Jan, L. Y., Jan, Y. N., Cabrera, C. V., Buskin, J. N., Hauschka, S. D., Lassar, A. B. et al. (1989). Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58, 537-544.
34. Mutoh, H., Naya, F. J., Tsai, M. J. and Leiter, A. B. (1998). The basic helix-loop-helix protein BETA2 interacts with p300 to coordinate differentiation of secretin-expressing enteroendocrine cells. Genes Dev. 12, 820-830.
35. Otten, A. D., Firpo, E. J., Gerber, A. N., Brody, L. L., Roberts, J. M. and Tapscott, S. J. (1997). Inactivation of MyoD-mediated expression of p21 in tumor cell lines. Cell Growth Differ. 8, 1151-1160.
36. Perez, S. E., Rebelo, S. and Anderson, D. J. (1999). Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 126, 1715-1728.
37. Peyton, M., Stellrecht, C. M., Naya, F. J., Huang, H. P., Samora, P. J. and Tsai, M. J. (1996). BETA3, a novel helix-loop-helix protein, can act as a negative regulator of BETA2 and MyoD-responsive genes. Mol. Cell Biol. 16, 626-633.
38. Polyak, K., Lee, M. H., Erdjument-Bromage, H., Koff, A., Roberts, J. M., Tempst, P. and Massague, J. (1994). Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78, 59-66.
39. Robb, L., Mifsud, L., Hartley, L., Biben, C., Copeland, N. G., Gilbert, D. J., Jenkins, N. A. and Harvey, R. P. (1998). epicardin: A novel basic helix-loop-helix transcription factor gene expressed in epicardium, branchial arch myoblasts, and mesenchyme of developing lung, gut, kidney, and gonads. Dev. Dyn. 213, 105-113.
40. Rupp, R. A., Snider, L. and Weintraub, H. (1994). Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev. 8, 1311-1323.
41. Rupp, R. A. and Weintraub, H. (1991). Ubiquitous MyoD transcription at the midblastula transition precedes induction-dependent MyoD expression in presumptive mesoderm of X. laevis. Cell 65, 927-937.
42. Shimizu, C., Akazawa, C., Nakanishi, S. and Kageyama, R. (1995). MATH-2, a mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal, is specifically expressed in the nervous system. Eur. J. Biochem. 229, 239-248.
43. Sommer, L., Ma, Q. and Anderson, D. J. (1996). Neurogenins, a novel family of atonal-related bHLH transcription factors, are putative mammalian neuronal determination genes that reveal progenitor cell hetereogeneity in the developing CNS and PNS. Mol. Cell Neurosci. 8, 221-241.
44. Takebayashi, K., Takahashi, S., Yokota, C., Tsuda, H., Nakanishi, S., Asashima, M. and Kageyama, R. (1997). Conversion of ectoderm into a neural fate by ATH-3, a vertebrate basic helix-loop-helix gene homologous to Drosophila proneural gene atonal. EMBO J. 16, 384-395.
45. Tanabe, Y., William, C. and Jessell, T. M. (1998). Specification of motor neuron identity by the MNR2 homeodomain protein. Cell 95, 67-80.
46. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S., Waknitz, M. A., Swiergiel, J. J., Marshall, V. S. and Jones, J. M. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147.
47. Tontonoz, P., Hu, E. and Spiegelman, B. M. (1994). Stimulation of adipogenesis in fibroblasts by PPAR gamma 2, a lipid-activated transcription factor. Cell 79, 1147-1156.
48. Turner, D. L. and Weintraub, H. (1994). Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 8, 1434-1447.
49. Wakamatsu, Y. and Weston, J, A. (1997). Sequential expression and role of Hu RNA-binding proteins during neurogenesis. Development 124, 3449-3460.
50. Walker, M. D., Park, C. W., Rosen, A. and Aronheim, A. (1990). A cDNA from a mouse pancreatic beta cell encoding a putative transcription factor of the insulin gene. Nucleic Acids Res. 18, 1159-1166.
51. Weintraub, H., Davis, R., Tapscott, S., Thayer, M., Krause, M., Benezra, R., Blackwell, T. K., Turner, D., Rupp, R., Hollenberg, S. et al (1991). The myoD gene family: nodal point during specification of the muscle cell lineage. Science 251, 761-766.
52. Yan, Y., Narayanan, V. and Lagenaur, C. (1996). Expression of members of the proteolipid protein gene family in the developing murine central nervous system. J. Comp. Neurol. 370, 465-478.