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JOURNAL ARTICLES
Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurons in Xenopus embryos
A. Chitnis, C. Kintner
Development 1996 122: 2295-2301;

Summary

We have compared the roles of XASH-3 and NeuroD, two basic helix-loop-helix transcription factors, in the formation of primary neurons in early Xenopus embryos. When ectopically expressed in Xenopus embryos, XASH-3 and NeuroD induce ectopic primary neurons in very different spatial patterns. We show that the pattern of primary neurons induced by XASH-3 and NeuroD can be accounted for by a difference in their sensitivity to inhibitory interactions mediated by the neurogenic genes, X-Delta-1 and X-Notch-1. Both NeuroD and XASH-3 promote the expression of the inhibitory ligand, X-Delta-1. However, XASH-3 appears to be sensitive to the inhibitory effects of X-Delta-1 while NeuroD is much less so. Consequently only a subset of cells that ectopically express XASH-3 eventually form neurons, giving a scattered pattern, while the ectopic expression of NeuroD leads to a relatively dense pattern of ectopic neurons. We propose that differences in the sensitivity of XASH-3 and NeuroD to lateral inhibition play an important role during their respective roles in neuronal determination and differentiation.

Reference

    1. Cabrera C. V.,
    2. Alonso M. C.,
    3. Huikeshoven H.
    (1994) Regulation of scute function by extramacrochaete in vitro and in vivo. Development 120, 3595–3603
    OpenUrlAbstract
    1. Campos-Ortega J. A.
    (1994) Genetic mechanisms of early neurogenesis in Drosophilamelanogaster. J. Physiol. Paris 88, 111–122
    OpenUrlCrossRefPubMed
    1. Chitnis A.,
    2. Henrique D.,
    3. Lewis J.,
    4. Ish-Horowicz D.,
    5. Kintner C.
    (1995) Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature 375, 761–766
    OpenUrlCrossRefPubMedWeb of Science
    1. Coffman C. R.,
    2. Skoglund P.,
    3. Harris W. A.,
    4. Kintner C. R.
    (1993) Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell 73, 659–671
    OpenUrlCrossRefPubMedWeb of Science
    1. Ferreiro B.,
    2. Kintner C.,
    3. Zimmerman K.,
    4. Anderson D.,
    5. Harris W. A.
    (1994) XASH genes promote neurogenesis in Xenopusembryos. Development 120, 3649–3655
    OpenUrlAbstract
    1. Ferreiro B.,
    2. Skoglund P.,
    3. Bailey A.,
    4. Dorsky R.,
    5. Harris W. A.
    (1993) XASH1, a Xenopus homolog of achaete-scute: a proneural gene in anterior regions of the vertebrate CNS. Mech. Dev 40, 25–36
    OpenUrlCrossRefPubMedWeb of Science
    1. Garrell J.,
    2. Modolell J.
    (1990) The Drosophila extramacrochaete locus, an antagonist of proneural genes that, like these genes, encodes a helix-loop-helix protein. Cell 61, 39–48
    OpenUrlCrossRefPubMedWeb of Science
    1. Ghysen A.,
    2. Dambly C. C.,
    3. Jan L. Y.,
    4. Jan Y. N.
    (1993) Cell interactions and gene interactions in peripheral neurogenesis. Genes Dev 7, 723–733
    OpenUrlFREE Full Text
    1. Guillemot F.,
    2. Lo L. C.,
    3. Johnson J. E.,
    4. Auerbach A.,
    5. Anderson D. J.,
    6. Joyner A. L.
    (1993) Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463–476
    OpenUrlCrossRefPubMedWeb of Science
    1. Haenlin M.,
    2. Kunisch M.,
    3. Kramatschek B.,
    4. Campos-Ortega J. A.
    (1994) Genomic regions regulating early embryonic expression of the Drosophila neurogenic gene Delta. Mech. Dev 47, 99–110
    OpenUrlCrossRefPubMed
    1. Harland R. M.
    (1991) In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol 36, 685–695
    OpenUrlCrossRefPubMedWeb of Science
    1. Heitzler P.,
    2. Bourouis M.,
    3. Ruel L.,
    4. Carteret C.,
    5. Simpson P.
    (1996) Genes of the Enhancerofsplit and achaete-scute complexes are required for a regulatory loop between Notch and Delta during lateral inhibition in Drosophila. Development 122, 161–171
    OpenUrlAbstract
    1. Heitzler P.,
    2. Simpson P.
    (1991) The choice of cell fate in the epidermis of Drosophila. Cell 64, 1083–1092
    OpenUrlCrossRefPubMedWeb of Science
    1. Hinz U.,
    2. Giebel B.,
    3. Campos-Ortega J. A.
    (1994) The basic-helix-loop-helix domain of Drosophila lethal of scute protein is sufficient for proneural function and activates neurogenic genes. Cell 76, 77–87
    OpenUrlCrossRefPubMedWeb of Science
    1. Jennings B.,
    2. deCelis J.,
    3. Delidakis C.,
    4. Preiss A.,
    5. Bray S.
    (1995) Role of Notch and achaete-scute complex in the expression of Enhancer of Split bHLH proteins. Development 121, 3745–3752
    OpenUrlAbstract
    1. Johnson J. E.,
    2. Birren S. J.,
    3. Anderson D. J.
    (1990) Two rat homologues of Drosophila achaete-scute specifically expressed in neuronal precursors. Nature 346, 858–861
    OpenUrlCrossRefPubMedWeb of Science
    1. Kintner C. R.,
    2. Melton D. A.
    (1987) Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. Development 99, 311–325
    OpenUrlAbstract
    1. Kopan R.,
    2. Nye J. S.,
    3. Weintraub H.
    (1994) The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basi helix-loop-helix region of MyoD. Development 120, 2385–2396
    OpenUrlAbstract/FREE Full Text
    1. Krieg P. A.,
    2. Melton D. A.
    (1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res 12, 7057–7070
    OpenUrlAbstract/FREE Full Text
    1. Krieg P. A.,
    2. Varnum S. M.,
    3. Wormington W. M.,
    4. Melton D. A.
    (1989) The mRNA encoding elongation factor 1-alpha (EF-1 alpha) is a major transcript at the midblastula transition in Xenopus. Dev. Biol 133, 93–100
    OpenUrlCrossRefPubMedWeb of Science
    1. Kunisch M.,
    2. Haenlin M.,
    3. Campos-Ortega J. A.
    (1994) Lateral inhibition mediated by the Drosophila neurogenic gene Delta is enhanced by proneural genes. Proc. Natl. Acad. Sci.USA 91, 10139–10143
    OpenUrlAbstract/FREE Full Text
    1. Lamb T. M.,
    2. Knecht A. K.,
    3. Smith W. C.,
    4. Stachel S. E.,
    5. Economides A. N.,
    6. Stahl N.,
    7. Yancopolous G. D.,
    8. Harland R. M.
    (1993) Neural induction by the secreted polypeptide noggin. Science 262, 713–718
    OpenUrlAbstract/FREE Full Text
    1. Lee J. E.,
    2. Hollenberg S. M.,
    3. Snider L.,
    4. Turner D. L.,
    5. Lipnick N.,
    6. Weintraub H.
    (1995) Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268, 836–44
    OpenUrlAbstract/FREE Full Text
    1. Martinez C.,
    2. Modolell J.
    (1991) Cross-regulatory interactions between proneural achaete and scute genes of Drosophila. Science 251, 1485–1487
    OpenUrlAbstract/FREE Full Text
    1. Muskavitch M. A.
    (1994) Delta-Notch signaling and Drosophila cell fate choice. Dev. Biol 166, 415–430
    OpenUrlCrossRefPubMedWeb of Science
    1. Oschwald R.,
    2. Richter K.,
    3. Grunz H.
    (1991) Localization of a nervous system-specific class II beta-tubulin gene in Xenopuslaevis embryos by whole-mount insitu hybridization. Int. J. Dev. Biol 35, 399–405
    OpenUrlPubMed
    1. Richter K.,
    2. Grunz H.,
    3. Dawid I. B.
    (1988) Gene expression in the embryonic nervous system of Xenopus laevis. Proc. Natl. Acad. Sci. USA 85, 8086–8090
    OpenUrlAbstract/FREE Full Text
    1. Roehl H.,
    2. Kimble J.
    (1993) Control of cell fate in C. elegans by a Glp-1 peptide consisting primarily of ankyrin repeats. Nature 264, 632–635
    OpenUrl
    1. Skeath J. B.,
    2. Carroll S. B.
    (1991) Regulation of achaete-scute gene expression and sensory organ pattern formation in the Drosophila wing. Gen. Dev 5, 984–995
    OpenUrlAbstract/FREE Full Text
    1. Skeath J. B.,
    2. Carroll S. B.
    (1994) The achaete-scute complex: generation of cellular pattern and fate within the Drosophila nervous system. Faseb J 8, 714–721
    OpenUrlAbstract
    1. Struhl G.,
    2. Fitzgerald K.,
    3. Greenwald I.
    (1993) Intrinsic activity of the Lin-12 and Notch intracellular domains in vivo. Cell 74, 331–345
    OpenUrlCrossRefPubMedWeb of Science
    1. Turner D. L.,
    2. Weintraub H.
    (1994) Expression of acheate-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev 8, 1434–1447
    OpenUrlAbstract/FREE Full Text
    1. Van Doren M.,
    2. Ellis H. M.,
    3. Posakony J. W.
    (1991) The Drosophila extramacrochaete protein anatagonizes sequence-specific DNA binding by daughterless/achaete-scute protein complexes. Development 113, 244–255
    OpenUrl
    1. Weintraub H.
    (1993) The MyoD family and myogenesis: redundancy, networks, and thresholds. Cell 75, 1241–1244
    OpenUrlCrossRefPubMedWeb of Science
    1. Zimmerman K.,
    2. Shih J.,
    3. Bars J.,
    4. Collazo A.,
    5. Anderson D. J.
    (1993) XASH-3, a novel Xenopus achaete-scute homolog, provides an early marker of planar neural induction and position along the mediolateral axis of the neural plate. Development 119, 221–232
    OpenUrlAbstract
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JOURNAL ARTICLES
Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurons in Xenopus embryos
A. Chitnis, C. Kintner
Development 1996 122: 2295-2301;
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