Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system

Current Opinion in Genetics and Development

Volumn 7, Issue 5, 1997, Pages 659-665

  Kageyama, Ryoichiro ^a   Nakanishi, Shigetada ^a  

^a KYOTO UNIVERSITY FACULTY OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HELIX LOOP HELIX PROTEIN;

DROSOPHILA; GENE; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE REPRESSION; MITOSIS; MORPHOGENESIS; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; VERTEBRATE; XENOPUS;

VERTEBRATA;

EID: 0030727631     PISSN: 0959437X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-437X(97)80014-7     Document Type: Article

References (56)

1. Lewis J. Neurogenic genes and vertebrate neurogenesis. Curr Opin Neurobiol. 6:1996;3-10.
2. Lee JE. Basic helix-loop-helix genes in neural development. of outstanding interest Curr Opin Neurobiol. 7:1997;13-20 An excellent comprehensive review of neural HLH genes. The author categorizes the HLH genes into two groups, determination genes and differentiation genes, on the basis of their expression and function. The former genes may determine the neuronal fate and induce the latter, which then can promote terminal differentiation.
3. Tanabe Y, Jessel TM. Diversity and pattern in the developing spinal cord. Science. 274:1996;1115-1123.
4. Jan YN, Jan LY. HLH proteins, fly neurogenesis, and vertebrate myogenesis. Cell. 75:1993;827-830.
5. Artavanis-Tsakonas S, Matsuno K, Fortini ME. Notch signaling. Science. 268:1995;225-232.
6. Ma Q, Kintner C, Anderson DJ. Identification of neurogenin, a vertebrate neuronal determination gene. of outstanding interest Cell. 87:1996;43-52 The HLH gene neuronal (ngn) determines the neuronal fate in the ectoderm and induces another HLH gene, NeuroD. NeuroD and ngn constitute a unidiretional cascade. Interestingly, expressions and functions of ngn are negatively regulated by the Delta/Notch pathway, analogous to Drosophila proneural genes.
7. Johnson JE, Birren SJ, Anderson DJ. Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature. 346:1990;858-861.
8. Akazawa C, Ishibashi M, Shimizu C, Nakanishi S, Kageyama R. 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. 270:1995;8730-8738.
9. Ben-Arie N, McCall AE, Berkman S, Eichele G, Bellen HJ, Zoghbi HY. Evolutionary conservation of sequence and expression of the bHLH protein Atonal suggests a conserved role in neurogenesis. Hum Mol Genet. 5:1996;1207-1216.
10. Gradwohl G, Fode C, Guillemot F. Restricted expression of a novel murine atonal-related bHLH protein in undifferentiated neural precursors. Dev Biol. 180:1996;227-241.
11. Cau E, Gradwohl G, Fode C, Guillemot F. Mash1 activates a cascade of bHLH regulators in olfactory neuron progenitors. of special interest Development. 124:1997;1611-1621 HLH genes, Mash1, Math4Clngn, and NeuroD, are expressed in this sequence at distinct stages of olfactory neurogenesis. In the absence of Mash1, expresssion of the latter two genes disappear and olfactory neurons are not generated, indicating that a cascade of HLH genes regulates neuronal differentiation.
12. Lee JE, Hollenberg SM, Snider L, Turner DL, Lipnick N, Weintraub H. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science. 268:1995;836-844.
13. Bartholomä A, Nave KA. NEX-1: a novel brain-specific helix-loop-helix protein with autoregulation and sustained expression in mature cortical neuron. Mech Dev. 48:1994;217-228.
14. Shimizu C, Akazawa C, Nakanishi S, Kageyama R. 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. 229:1995;239-248.
15. McCormick MB, Tamimi RM, Snider L, Asakura A, Bergstrom D, Tapscott SJ. neuroD2 and neuroD3: distinct expression patterns and transcriptional activation potentials within the neuroD gene family. of special interest Mol Cell Biol. 16:1996;5792-5800 Two new members of neuroD family, neuroD2 and neuroD3, are differentially expressed in the developing nervous system. Interestingly, closely related NeuroD and NeuroD2 - both of which can induce ectopic neurons in Xenopus embryos - show distinct specificity for transcriptional activation.
16. Guillemot F, Lo LC, Johnson JE, Auerbach A, Anderson DJ, Joyner AL. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell. 75:1993;463-476.
17. Sommer L, Shah N, Rao M, Anderson DJ. The cellular function of MASH1 in autonomic neurogenesis. Neuron. 15:1995;1245-1258.
18. Blaugrund E, Pham TD, Tennyson VM, Lo L, Sommer L, Anderson DJ, Gershon MD. Distinct subpopulations of enteric neuronal progenitors defined by time of development, sympathoadrenal lineage markers and Mash-1-dependence. Development. 122:1996;309-320.
19. Tomita K, Nakanishi S, Guillemot F, Kageyama R. Mash1 promotes neuronal differentiation in the retina. Genes Cells. 1:1996;765-774.
20. Ferreiro B, Kintner C, Zimmerman K, Anderson D, Harris WA. XASH genes promote neurogenesis in Xenopus embryos. Development. 120:1994;3649-3655.
21. Turner DL, Weintraub H. Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 8:1994;1434-1447.
22. Takebayashi K, Takahashi C, Yokota C, Tsuda H, Nakanishi S, Asashima M, Kageyama R. Conversion of extoderm into a neural fate by ATH-3, a vertebrate basic helix-loop-helix gene homologous to Drosophila proneural gene atonal. of special interest EMBO J. 16:1997;384-395 The HLH gene ATH-3 can convert ectodermal cells into neurons with anterior features. Interestingly, a single amino acid change in the basic region from Ser to Asp, which mimics phosphorylation, still keeps the general neurogenic activity but severely impairs the anterior features.
23. Henrique D, Tyler D, Kintner C, Heath JK, Lewis JH, Ish-Horowicz D, Storey KG. cash4, a novel achaete-scute homolog induced by Hensen's node during generation of the posterior nervous system. of special interest Genes Dev. 11:1997;603-615 The chick achaete-scute homologue cash4 is expressed in the prospective posterior nervous system in response to signals from Hensen's node. cash4 can promote neuronal differentiation in the ectoderm of both Drosophila and Xenopus embryos, suggesting that cash4 functions as a proneural gene.
24. Sasai Y, Kageyama R, Tagawa Y, Shigemoto R, Nakanishi S. Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 6:1992;2620-2634.
25. Akazawa C, Sasai Y, Nakanishi S, Kageyama R. Molecular characterization of a rat negative regulator with a basic helix-loop-helix structure predominantly expressed in the developing nervous system. J Biol Chem. 267:1992;21879-21885.
26. Benezra R, Davis RL, Lockshon D, Turner DL, Weintraub H. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell. 61:1990;49-59.
27. Brown NL, Sattler CA, Paddock SW, Carroll SB. Hairy and emc negatively regulate morphogenetic furrow progression in the Drosophila eye. Cell. 80:1995;879-887.
28. Ishibashi M, Ang SL, Shiota K, Nakanishi S, Kageyama R, Guillemot F. Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (itHES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis and severe neural tube defects. Genes Dev. 9:1995;3136-3148.
29. Tomita K, Ishibashi M, Nakahara K, Ang SL, Nakanishi S, Guillemot F, Kageyama R. Mammalian hairy and Enhancer of split homolog 1 regulates differentiation of retinal neurons and is essential for eye morphogenesis. of outstanding interest Neuron. 16:1996;723-734 Retinal progenitors forced to express Hes1 via a retrovirus fail to differentiate and remain as progenitors. Conversely, Hes1-null retinal cells differentiate prematurely and non-uniformly, which results in small-sized eyes, altered ratios of neuronal types, and disruption of the laminar structure of the retina. Thus, Hes1 regulates the timing of differentiation and is essential for eye morphogenesis.
30. Ishibashi M, Moriyoshi K, Sasai Y, Shiota K, Nakanishi S, Kageyama R. Persistent expression of helix-loop-helix factor HES-1 prevents mammalian neural differentiation in the central nervous system. EMBO J. 13:1994;1799-1805.
31. Ohsako S, Hyer J, Panganiban G, Oliver I, Caudy M. hairy function as a DNA-binding helix-loop-helix repressor of Drosophila sensory organ formation. Genes Dev. 8:1994;2743-2755.
32. Van Doren M, Bailey AM, Esnayra J, Ede K, Posakony JW. Negative regulation of proneural gene activity: hairy is a direct transcriptional repressor of achaete. Genes Dev. 8:1994;2729-2742.
33. Chen H, Thiagalingam A, Chopra H, Borges MW, Feder JN, Nelkin BD, Baylin SB, Ball DW. Conservation of the Drosophila lateral inhibition pathway in human lung cancer: a hairy-related protein (HES-1) directly represses achaete-scute homolog-1 expression. of outstanding interest Proc Natl Acad Sci USA. 94:1997;5355-5360 The authors found an inverse correlation of Hes1 and Mash1 expression in lung cancer cell lines. In vitro studies indicated that Hes1 can bind directly to the N-box-related sequence in the human Mash1 promoter. In addition, induction of Hes1 expression represses the endogenous Mash1 transcription in lung cancer cells. Thus, Hes1 represses Mash1 expression in an analogue way to Drosophila Hairy, which inhibits achaete expression by directly binding to its promoter.
34. D: a dominant mutation of Drosophila, and its use in the study of functional domains of a helix-loop-helix protein. Proc Natl Acad Sci USA. 89:1992;6152-6156.
35. Wainwright SM, Ish-Horowicz D. Point mutations in the Drosophila hairy gene demonstrate in vivo requirements for basic, helix-loop-helix, and WRPW domains. Mol Cell Biol. 12:1992;2475-2483.
36. Paroush Z, Finley RL Jr, Kidd T, Wainwright SM, Ingham PW, Brent R, Ish-Horowicz D. Groucho is required for Drosophila neurogenesis, segmentation, and sex determination and interacts directly with hairy-related bHLH proteins. Cell. 79:1994;805-815.
37. Dawson SR, Turner DL, Weintraub H, Parkhurst SM. 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. 15:1995;6923-6931.
38. Fisher AL, Ohsako S, Caudy M. The WRPW motif of the Hairy-related basic helix-loop-helix repressor proteins acts as a 4-amino-acid transcription repression and protein - protein interaction domain. Mol Cell Biol. 16:1996;2670-2677.
39. Coffman CR, Skoglund P, Harris WA, Kintner CR. Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell. 73:1993;659-671.
40. Kopan R, Nye JS, Weintraub H. The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Development. 120:1994;2385-2396.
41. Nye JS, Kopan R, Axel R. An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development. 120:1994;2421-2430.
42. Chitnis A, Henrique D, Lewis J, Ish-Horowicz D, Kintner C. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature. 375:1995;761-766.
43. Dorsky RI, Rapaport DH, Harris WA. Xotch inhibits cell differentiation in the Xenopus retina. Neuron. 14:1995;487-496.
44. Austin CP, Feldman DE, Ida JA Jr, Cepko CL. Ganglion cells in the vertebrate retina are selected from an equivalence group regulated by Notch. Development. 121:1995;3637-3650.
45. Lardelli M, Williams R, Mitsiadis T, Lendahl U. Expression of the Notch 3 intracellular domain in mouse central nervous system progenitor cells is lethal and leads to disturbed neural tube development. Mech Dev. 59:1996;177-190.
46. Jarriault S, Brou C, Logeat F, Shroeter EH, Kopan R, Israel A. Signalling downstream of activated mammalian Notch. Nature. 377:1995;355-358.
47. Kopan R, Schroeter EH, Weintraub H, Nye JS. Signal transduction by activated mNotch: importance of proteolytic processing and its regulation by the extracellular domain. Proc Natl Acad Sci USA. 93:1996;1683-1688.
48. Honjo T. The shortest path from the surface to the nucleus: RBP-J κ/Su(H) transcription factor. Genes Cells. 1:1996;1-9.
49. Hsieh JJ-D, Nofziger DE, Weinmaster G, Hayward SD. Epstein - Barr virus immortalization: Notch2 interacts with CBF1 and blocks differentiation. J Virol. 71:1997;1938-1945.
50. Takebayashi K, Sasai Y, Sakai Y, Watanabe T, Nakanishi S, Kageyama R. Structure, chromosomal locus, and promoter analysis of the gene encoding the mouse helix-loop-helix factor HES-1: autoregulation through the multiple N box elements. J Biol Chem. 269:1994;5150-5156.
51. Bao ZZ, Cepko CL. The expression and function of Notch pathway genes in the developing rat eye. J Neurosci. 17:1997;1425-1434.
52. Shawber C, Notziger D, Hsieh JJD, Lindsell C, Bögler O, Hayward D, Weinmaster G. Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. of outstanding interest Development. 122:1996;3765-3773 The constitutively active form of Notch inhibits muscle cell fusion of C2C12 myoblasts without inducing Hes1. In addition, the ankyrin repeats of Notch are sufficient for this inhibitory activity, indicating that the region interacting with CBF1/RBP-J is not necessary. Thus, Notch can regulate cell differentiation through the CBF1-Hes1-independent pathway.
53. De la Pompa JL, Wakeham A, Correia KM, Samper E, Brown S, Aguilera RJ, Nakano T, Honjo T, Mak TW, Rossant J, Conlon RA. Conservation of the Notch signalling pathway in mammalian neurogenesis. of outstanding interest Development. 124:1997;1139-1148 In the absence if Notch1 or RBP-J, expression of the E(spl) homologue Hes5 is downregulated and that of the AS-C homologue Mash1 and the Delta homologue DII is upregulated, suggesting that the downstream pathway of Notch is well conserved between mammals and Drosophila. Surprisingly, Hes1 expression is not altered in Notch1 or RBP-J mutant embryos, suggesting the genetic redundancy of mammalian Notch and RBP-J.
54. Wettstein DA, Turner DL, Kintner C. The Xenopus homolog of Drosophila Suppressor of Hairless mediates Notch signaling during primary neurogenesis. of outstanding interest Development. 124:1997;693-702 In Xenopus, activation of Notch1 induces expression of ESR1, a Xenopus homologue of E(spl); this induction is mediated by Xenopus Su(H). Interestingly, expression of a dominant negative form of Su(H) increases Delta and ngnr expressions in Xenopus embryos, suggesting that Su(H) mediates Notch-induced suppression of neuronal differentiation.
55. Chitnis A, Kintner C. Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurons in Xenopus embryos. of special interest Development. 122:1996;2295-2301 The determination gene Xash3 is much more sensitive to the inhibitory activity of the Delta-Notch pathway than the differentiation gene NeuroD. As a result, Xash3 generates a scattered pattern of neurons whereas NeuroD forms a dense pattern of neurons. Thus, once NeuroD is expressed, neuronal differentiation is stabilized.
56. Dorsky RI, Chang WS, Rapaport DH, Harris WA. Regulation of neuronal diversity in the Xenopus retina by Delta signalling. Nature. 385:1997;67-70.