Conservation of neurogenic genes and mechanisms

Current Opinion in Neurobiology

Volumn 9, Issue 5, 1999, Pages 582-588

  Chan, Yee Ming ^a   Jan, Yuh Nung ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL FATE; CENTRAL NERVOUS SYSTEM; DROSOPHILA MELANOGASTER; GENE EXPRESSION; HOMEOBOX; INNER EAR; INVERTEBRATE; MOLECULAR EVOLUTION; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VERTEBRATE;

EID: 0032843919     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)00017-3     Document Type: Review

References (69)

1. Arendt D, Nübler-Jung K Comparison of early nerve cord development in insects and vertebrates. Development. 126:1999;2309-2325. This excellent, thought-provoking review discusses similarities and differences between the development of insect and vertebrate central nervous systems. The review focuses on findings from the major model organisms, but also reviews studies of gene expression in other organisms.
2. Rao Y, Vaessin H, Jan LY, Jan YN Neuroectoderm in Drosophila embryos is dependent on the mesoderm for positioning but not for formation. Genes Dev. 5:1991;1577-1588.
3. De Robertis EM, Sasai Y A common plan for dorsoventral patterning in Bilateria. Nature. 380:1996;37-40.
4. Villares R, Cabrera CV The achaete-scute gene complex of D. melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc. Cell. 50:1987;415-424.
5. Brand M, Jarman AP, Jan LY, Jan YN asense is a Drosophila neural precursor gene and is capable of initiating sense organ formation. Development. 119:1993;1-17.
6. Dominguez M, Campuzano S asense, a member of the Drosophila achaete-scute complex, is a proneural and neural differentiation gene. EMBO J. 12:1993;2049-2060.
7. Jarman AP, Grau Y, Jan LY, Jan YN atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell. 73:1993;1307-1321.
8. Zhao C, Emmons SW A transcription factor controlling development of peripheral sense organs in C. elegans. Nature. 373:1995;74-78.
9. Krause M, Park M, Zhang J-M, Yuan J, Harfe B, Xu S-Q, Greenwald I, Cole M, Paterson B, Fire A A C. elegans E/Daughterless bHLH protein marks neuronal but not striated muscle development. Development. 124:1997;2179-2189.
10. Lee JE Basic helix-loop-helix genes in neural development. Curr Opin Neurobiol. 7:1997;13-20.
11. Kageyama R, Nakanishi S Helix-loop-helix factors in growth and differentiation of the vertebrate nervous system. Curr Opin Genet Dev. 7:1997;659-665.
12. Jarman AP, Sun Y, Jan LY, Jan YN Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development. 121:1995;2019-2030.
13. Ben-Arie N, Bellen HJ, Armstrong DL, McCall AE, Gordadze PR, Guo Q, Matzuk MM, Zoghbi HY Math1 is essential for genesis of cerebellar granule neurons. Nature. 390:1997;169-172.
14. Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N, Eatock RA, Bellen HJ, Lysakowski A, Zoghbi HY Math1: an essential gene for the generation of inner ear hair cells. Science. 284:1999;1837-1841. This paper reports that Math1 knockout mice lack hair cells of the inner ear, possibly as a result of a transformation of hair cells to support cells.
15. Ma Q, Chen Z, del Barco Barrantes I, de la Pompa JL, Anderson DJ neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron. 20:1998;469-482.
16. Fode C, Gradwohl G, Morin X, Dierich A, LeMeur M, Goridis C, Guillemot F The bHLH protein NEUROGENIN 2 is a determination factor for epibranchial placode-derived sensory neurons. Neuron. 20:1998;483-494.
17. Guillemot F, Lo L-C, 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.
18. Hirsch M-R, Tiveron M-C, Guillemot F, Brunet J-F, Goridis C Control of noradrenergic differentiation and Phox2a expression by MASH1 in the central and peripheral nervous system. Development. 125:1998;599-608.
19. Casarosa S, Fode C, Guillemot F Mash1 regulates neurogenesis in the ventral telencephalon. Development. 126:1999;525-534. In Mash1 knockout mice, neural precursors in the medial ganglionic eminence of the ventral telencephalon fail to form. In the lateral ganglionic eminence of Mash1 knockout mice, neural precursors form but fail to express the Notch pathway genes Deltalike1, Deltalike3, and Hes5 and fail to restrict Mash1 expression, possibly as a result of a defect in lateral inhibition. Precursors in the lateral ganglionic eminence also express differentiation markers prematurely, though subsequent differentiation steps appear normal. Mash1, therefore, has multiple roles in the developing ventral telencephalon, including specification of neural precursors and timing of precursor differentation.
20. Tuttle R, Nakagawa Y, Johnson JE, O'Leary DDM Defects in thalamocortical axon pathfinding correlate with altered cell domains in Mash-1-deficient mice. Development. 126:1999;1903-1916. Expression of Mash1 in the developing brain defines cell domains that are important for proper pathfinding of axons through these domains. In Mash1 knockout mice, the thalamocortical axons, which normally project from the dorsal thalamus to the neocortex, exhibit pathfinding defects. Mash1 is not expressed in the developing dorsal thalamus or neocortex, so the loss of Mash1 does not affect neurons in these regions directly. Rather, the axonal pathfinding defects appear to be secondary to changes in Mash1-expressing brain regions that lie along the path of thalamocortical axons; these changes can be visualized by altered expression patterns of the homeobox gene Pax6 and the receptor protein phosphatase gene RPTPδ.
21. Torii M-a, Matsuzaki F, Osumi N, Kaibuchi K, Nakamura S, Casarosa S, Guillemot F, Nakafuku M Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development. 126:1999;443-456. The authors report that Mash1 and Prox1 are expressed in differentiating neural precursors in the developing spinal cord and thalamus and in MNS-70 cells, which resemble early neural precursors, that have been induced to differentiate. They also report an increased number of undifferentiated cells in Mash1 knockout mice. Thus, in these cells, Mash1 is required not for initial specification but for differentiation of neural precursors.
22. Campuzano S, Balcells L, Villares R, Carramolino L, Garcia-Alonso L, Modolell J Excess function Hairy-wing mutations caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila. Cell. 44:1986;303-312.
23. Rodríguez I, Hernández R, Modolell J, Ruiz-Gómez M Competence to develop sensory organs is temporally and spatially regulated in Drosophila epidermal primordia. EMBO J. 9:1990;3583-3592.
24. Jarman AP, Ahmed I The specificity of proneural genes in determining Drosophila sense organ identity. Mech Dev. 76:1998;117-125.
25. Chien C-T, Hsiao C-D, Jan LY, Jan YN Neuronal type information encoded in the basic-helix-loop-helix domain of proneural genes. Proc Natl Acad Sci USA. 93:1996;13239-13244.
26. Kanekar S, Perron M, Dorsky R, Harris WA, Jan LY, Jan YN, Vetter ML Xath5 participates in a network of bHLH genes in the developing Xenopus retina. Neuron. 19:1997;981-994.
27. Brown NL, Kanekar S, Vetter ML, Tucker PK, Gemza DL, Glaser T Math5 encodes a murine basic helix-loop-helix transcription factor expressed during early stages of retinal neurogenesis. Development. 125:1998;4821-4833. The newly identified mouse neural bHLH gene Math5 is expressed in the developing retina and in the developing tenth cranial ganglion. Math5 expression in the developing retina requires Pax6 and precedes expression of other neural bHLH genes. Ectopic Math5 and Mash1 expression results in increased formation of the same cell type (i.e. retinal bipolar cells), even though Math5 and Mash1 contain divergent basic domains.
28. Modolell J, Campuzano S The achaete-scute complex as an integrating device. Int J Dev Biol. 42:1998;275-282.
29. Sun Y, Jan LY, Jan YN Transcriptional regulation of atonal during development of the Drosophila peripheral nervous system. Development. 125:1998;3731-3740. Distinct 5′ and 3′ regulatory elements direct distinct locations and phases of atonal expression. For example, in the developing eye, different elements control the initial expression of atonal and its subsequent refinement.
30. Sato M, Kojima T, Michiue T, Saigo K Bar homeobox genes are latitudinal prepattern genes in the developing Drosophila notum whose expression is regulated by the concerted functions of decapentaplegic and wingless. Development. 126:1999;1457-1466. Bar homeobox genes are expressed in the anterior thorax, and this expression is regulated by the Decapentaplegic (Dpp) and Wingless (Wg) signaling pathways. Bar mutants lack expression of Achaete and, thus, do not form bristles in this region. Bar, therefore, links general patterning by Dpp and Wg to Achaete expression.
31. Grillenzoni N, van Helden J, Dambly-Chaudière C, Ghysen A The iroquois complex controls the somatotopy of Drosophila notum mechanosensory projections. Development. 125:1998;3563-3569.
32. Kehl BT, Cho K-O, Choi K-W mirror, a Drosophila homeobox gene in the iroquois complex, is required for sensory organ and alula formation. Development. 125:1998;1217-1227.
33. Leyns L, Gómez-Skarmeta J-L, Dambly-Chaudière C iroquois: a prepattern gene that controls the formation of bristles on the thorax of Drosophila. Mech Dev. 59:1996;63-72.
34. Gómez-Skarmeta J-L, del Corral RD, de la Calle-Mustienes E, Ferrés-Marcó D, Modolell J araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell. 85:1996;95-105.
35. Ramain P, Heitzler P, Haenlin M, Simpson P pannier, a negative regulator of achaete and scute in Drosophila, encodes a zinc finger protein with homology to the vertebrate transcription factor GATA-1. Development. 119:1993;1277-1291.
36. Cubadda Y, Heitzler P, Ray RP, Bourouis M, Ramain P, Gelbart W, Simpson P, Haenlin M u-shaped encodes a zinc finger protein that regulates the proneural genes achaete and scute during the formation of bristles in Drosophila. Genes Dev. 11:1997;3083-3095.
37. Haenlin M, Cubadda Y, Blondeau F, Heitzler P, Lutz Y, Simpson P, Ramain P Transcriptional activity of Pannier is regulated negatively by heterodimerization of the GATA DNA-binding domain with a cofactor encoded by the u-shaped gene of Drosophila. Genes Dev. 11:1997;3096-3108.
38. Saito T, Sawamoto K, Okano H, Anderson DJ, Mikoshiba K Mammalian BarH homologue is a potential regulator of neural bHLH genes. Dev Biol. 199:1998;216-225.
39. Gómez-Skarmeta JL, Glavic A, de la Calle-Mustienes E, Modolell J, Mayor R Xiro, a Xenopus homolog of the Drosophila Iroquois complex genes, controls development at the neural plate. EMBO J. 17:1998;181-190.
40. Bellefroid EJ, Kobbe A, Gruss P, Pieler T, Gurdon JB, Papalopulu N Xiro3 encodes a Xenopus homolog of the Drosophila Iroquois genes and functions in neural specification. EMBO J. 17:1998;191-203.
41. Bosse A, Zülch A, Becker M-B, Torres M, Gómez-Skarmeta J-L, Modolell J, Gruss P Identification of the vertebrate Iroquois homeobox gene family with overlapping expression during early development of the nervous system. Mech Dev. 69:1997;169-181.
42. Shibata K, Ishimura A, Maéno M GATA-1 inhibits the formation of notochord and neural tissue in Xenopus embryo. Biochem Biophys Res Commun. 252:1998;241-248.
43. Tevosian SG, Deconinck AE, Cantor AB, Rieff HI, Fujiwara Y, Corfas G, Orkin SH FOG-2: a novel GATA-family cofactor related to multitype zinc-finger proteins Friend of GATA-1 and U-shaped. Proc Natl Acad Sci USA. 96:1999;950-955.
44. Svensson EC, Tufts RL, Polk CE, Leiden JM Molecular cloning of FOG-2: a modulator of transcription factor GATA-4 in cardiomyocytes. Proc Natl Acad Sci USA. 96:1999;956-961.
45. Artavanis-Tsakonas S, Rand MD, Lake RJ Notch signaling: cell fate control and signal integration in development. Science. 284:1999;770-776.
46. Greenwald I LIN-12/Notch signaling: lessons from worms and flies. Genes Dev. 12:1998;1751-1762.
47. Kimble J, Simpson P The LIN-12/Notch signaling pathway and its regulation. Annu Rev Cell Dev Biol. 13:1997;333-361.
48. Lieber T, Kidd S, Alcamo E, Corbin V, Young MW Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes Dev. 7:1993;1949-1965.
49. Struhl G, Fitzgerald K, Greenwald I Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell. 74:1993;331-345.
50. 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.
51. Chan Y-M, Jan YN Presenilins, processing of β-amyloid precursor protein, and Notch signaling. Neuron. 23:1999;201-204.
52. Klueg KM, Parody TR, Muskavitch MAT Complex proteolytic processing acts on Delta, a transmembrane ligand for Notch, during Drosophila development. Mol Biol Cell. 9:1998;1709-1723.
53. Qi H, Rand MD, Wu X, Sestan N, Wang W, Rakic P, Xu T, Artavanis-Tsakonas S Processing of the Notch ligand Delta by the metalloprotease Kuzbanian. Science. 283:1999;91-94.
54. Torres M, Giráldez F The development of the vertebrate inner ear. Mech Dev. 71:1998;5-21.
55. Adam J, Myat A, Le Roux I, Eddison M, Henrique D, Ish-Horowicz D, Lewis J Cell fate choices and the expression of Notch, Delta and Serrate homologues in the chick inner ear: parallels with Drosophila sense-organ development. Development. 125:1998;4645-4654. Reports that the developing chick inner ear expresses Notch1 broadly throughout the otic epithelium, Serrate1 in prospective sensory patches, and Delta1 in prospective neurons and inner hair cells.
56. Stone JS, Rubel EW Delta1 expression during avian hair cell regeneration. Development. 126:1999;961-973. Reports that the regenerating chick ear expresses Serrate1 in prospective sensory patches. The authors also report that Delta1 and Notch1 are first expressed in dividing progenitor cells and inherited by both daughter cells; Delta1 is then quickly downregulated in prospective support cells.
57. •]) and that Jagged2 knockout mice have extra hair cells.
58. •]).
59. Haddon C, Jiang Y-J, Smithers L, Lewis J Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant. Development. 125:1998;4637-4644. Reports that Zebrafish mind bomb mutants appear to have a defect in Notch signaling, and that they exhibit extra hair cells and neurons and fewer support cells in the developing inner ear.
60. Weiss JB, Von Ohlen T, Mellerick DM, Dressler G, Doe CQ, Scott MP Dorsoventral patterning in the Drosophila central nervous system: the intermediate neuroblasts defective homeobox gene specifies intermediate column identity. Genes Dev. 12:1998;3591-3602. Reports that the newly identified ind gene is required for formation and identity of intermediate column neuroblasts. Expression of vnd, ind, and msh in the Drosophila neurogenic ectoderm is analogous to that of Nkx2.2, Gsh1, and Msx1 in the vertebrate neural tube.
61. McDonald JA, Holbrook S, Isshiki T, Weiss J, Doe CQ, Mellerick DM Dorsoventral patterning in the Drosophila central nervous system: the vnd homeobox gene specifies ventral column identity. Genes Dev. 12:1998;3603-3612.
62. Chu H, Parras C, White K, Jiménez F Formation and specification of ventral neuroblasts is controlled by vnd in Drosophila neurogenesis. Genes Dev. 12:1998;3613-3624.
63. Isshiki T, Takeichi M, Nose A The role of the msh homeobox gene during Drosophila neurogenesis: implication for the dorsoventral specification of the neuroectoderm. Development. 124:1997;3099-3109.
64. Sagasti A, Hobert O, Troemel E, Ruvkun G, Bargmann CI Alternative olfactory neuron fates are specified by the LIM homeobox gene lim-4. Genes Dev. 13:1999;1794-1806. Reports that in worms mutant for the LIM homeobox gene lim-4, the AWB olfactory neuron is transformed to the AWC fate, as determined by a number of criteria: expression of markers, morphology of dendrites and axons, ability to take up a lipophilic dye, and ability to mediate an attractive rather than a repulsive response to odorants. Ectopic expression of lim-4 in the AWC neuron causes it to adopt the AWB fate. lim-4, therefore, acts as a switch between the AWB and AWC fates.
65. Hobert O, Tessmar K, Ruvkun G The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons. Development. 126:1999;1547-1562.
66. Thor S, Andersson SGE, Tomlinson A, Thomas JB A LIM-homeodomain combinatorial code for motor-neuron pathway selection. Nature. 397:1999;76-80. lim-3 is expressed in a subset of neurons in the Drosophila central nervous system and is necessary and sufficient for neurons to send their axons along an inappropriate axonal pathway (ISNb) rather than the correct pathway (ISNd).
67. Sharma K, Sheng HZ, Lettieri K, Li H, Karavanov A, Potter S, Westphal H, Pfaff SL LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell. 95:1998;817-828. In Lhx3 and Lhx4 double-mutant mice, motor neurons that normally express Lhx3 migrate to a new position in the spinal cord and project their axons dorsally rather than ventrally. Ectopic expression of Lhx3 in chick causes neurons to project axons ventrally rather than dorsally.
68. Jan YN, Jan LY Functional gene cassettes in development. Proc Natl Acad Sci USA. 90:1993;8305-8307.
69. Gho M, Bellaïche Y, Schweisguth F Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development. 126:1999;3573-3584.