Europe PMC

This website requires cookies, and the limited processing of your personal data in order to function. By using the site you are agreeing to this as outlined in our privacy notice and cookie policy.

Xiro, a Xenopus homolog of the Drosophila Iroquois complex genes, controls development at the neural plate.

Author information

Affiliations

  • 1. Laboratorio de Biología del Desarrollo, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile.
      Authors
    • Gómez-Skarmeta JL 1
    (1 author)

ORCIDs linked to this article

The EMBO Journal, 01 Jan 1998, 17(1):181-190
https://doi.org/10.1093/emboj/17.1.181 PMID: 9427752 PMCID: PMC1170369

Free full text in Europe PMC

Abstract 

The Drosophila homeoproteins Ara and Caup are members of a combination of factors (prepattern) that control the highly localized expression of the proneural genes achaete and scute. We have identified two Xenopus homologs of ara and caup, Xiro1 and Xiro2. Similarly to their Drosophila counterparts, they control the expression of proneural genes and, probably as a consequence, the size of the neural plate. Moreover, Xiro1 and Xiro2 are themselves controlled by noggin and retinoic acid and, similarly to ara and caup, they are overexpressed by expression in Xenopus embryos of the Drosophila cubitus interruptus gene. These and other findings suggest the conservation of at least part of the genetic cascade that regulates proneural genes, and the existence in vertebrates of a prepattern of factors important to control the differentiation of the neural plate.

Free full text 

Logo of embojLink to Publisher's site
EMBO J. 1998 Jan 2; 17(1): 181–190.
PMCID: PMC1170369
PMID: 9427752

Xiro, a Xenopus homolog of the Drosophila Iroquois complex genes, controls development at the neural plate.

J L Gómez-Skarmeta, A Glavic, E de la Calle-Mustienes, J Modolell, and R Mayor
Author information Copyright and License information Disclaimer

Abstract

The Drosophila homeoproteins Ara and Caup are members of a combination of factors (prepattern) that control the highly localized expression of the proneural genes achaete and scute. We have identified two Xenopus homologs of ara and caup, Xiro1 and Xiro2. Similarly to their Drosophila counterparts, they control the expression of proneural genes and, probably as a consequence, the size of the neural plate. Moreover, Xiro1 and Xiro2 are themselves controlled by noggin and retinoic acid and, similarly to ara and caup, they are overexpressed by expression in Xenopus embryos of the Drosophila cubitus interruptus gene. These and other findings suggest the conservation of at least part of the genetic cascade that regulates proneural genes, and the existence in vertebrates of a prepattern of factors important to control the differentiation of the neural plate.

Full Text

The Full Text of this article is available as a PDF (588K).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Alexandre C, Jacinto A, Ingham PW. Transcriptional activation of hedgehog target genes in Drosophila is mediated directly by the cubitus interruptus protein, a member of the GLI family of zinc finger DNA-binding proteins. Genes Dev. 1996 Aug 15;10(16):2003–2013. [Abstract] [Google Scholar]
  • Bang AG, Papalopulu N, Kintner C, Goulding MD. Expression of Pax-3 is initiated in the early neural plate by posteriorizing signals produced by the organizer and by posterior non-axial mesoderm. Development. 1997 May;124(10):2075–2085. [Abstract] [Google Scholar]
  • Blitz IL, Cho KW. Anterior neurectoderm is progressively induced during gastrulation: the role of the Xenopus homeobox gene orthodenticle. Development. 1995 Apr;121(4):993–1004. [Abstract] [Google Scholar]
  • Blumberg B, Bolado J, Jr, Moreno TA, Kintner C, Evans RM, Papalopulu N. An essential role for retinoid signaling in anteroposterior neural patterning. Development. 1997 Jan;124(2):373–379. [Abstract] [Google Scholar]
  • Bradley LC, Snape A, Bhatt S, Wilkinson DG. The structure and expression of the Xenopus Krox-20 gene: conserved and divergent patterns of expression in rhombomeres and neural crest. Mech Dev. 1993 Jan;40(1-2):73–84. [Abstract] [Google Scholar]
  • Campuzano S, Modolell J. Patterning of the Drosophila nervous system: the achaete-scute gene complex. Trends Genet. 1992 Jun;8(6):202–208. [Abstract] [Google Scholar]
  • Chitnis A, Kintner C. Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurons in Xenopus embryos. Development. 1996 Jul;122(7):2295–2301. [Abstract] [Google Scholar]
  • Cho KW, Blumberg B, Steinbeisser H, De Robertis EM. Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell. 1991 Dec 20;67(6):1111–1120. [Abstract] [Google Scholar]
  • Coffman CR, Skoglund P, Harris WA, Kintner CR. Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell. 1993 May 21;73(4):659–671. [Abstract] [Google Scholar]
  • Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. [Europe PMC free article] [Abstract] [Google Scholar]
  • Dickinson ME, Selleck MA, McMahon AP, Bronner-Fraser M. Dorsalization of the neural tube by the non-neural ectoderm. Development. 1995 Jul;121(7):2099–2106. [Abstract] [Google Scholar]
  • Dixon JE, Kintner CR. Cellular contacts required for neural induction in Xenopus embryos: evidence for two signals. Development. 1989 Aug;106(4):749–757. [Abstract] [Google Scholar]
  • Domínguez M, Brunner M, Hafen E, Basler K. Sending and receiving the hedgehog signal: control by the Drosophila Gli protein Cubitus interruptus. Science. 1996 Jun 14;272(5268):1621–1625. [Abstract] [Google Scholar]
  • Doniach T. Planar and vertical induction of anteroposterior pattern during the development of the amphibian central nervous system. J Neurobiol. 1993 Oct;24(10):1256–1275. [Abstract] [Google Scholar]
  • Ekker SC, McGrew LL, Lai CJ, Lee JJ, von Kessler DP, Moon RT, Beachy PA. Distinct expression and shared activities of members of the hedgehog gene family of Xenopus laevis. Development. 1995 Aug;121(8):2337–2347. [Abstract] [Google Scholar]
  • Ferreiro B, Kintner C, Zimmerman K, Anderson D, Harris WA. XASH genes promote neurogenesis in Xenopus embryos. Development. 1994 Dec;120(12):3649–3655. [Abstract] [Google Scholar]
  • Ghysen A, Dambly-Chaudière C. From DNA to form: the achaete-scute complex. Genes Dev. 1988 May;2(5):495–501. [Abstract] [Google Scholar]
  • Ghysen A, Dambly-Chaudiere C. Genesis of the Drosophila peripheral nervous system. Trends Genet. 1989 Aug;5(8):251–255. [Abstract] [Google Scholar]
  • Gómez-Skarmeta JL, Modolell J. araucan and caupolican provide a link between compartment subdivisions and patterning of sensory organs and veins in the Drosophila wing. Genes Dev. 1996 Nov 15;10(22):2935–2945. [Abstract] [Google Scholar]
  • Gómez-Skarmeta JL, Rodríguez I, Martínez C, Culí J, Ferrés-Marcó D, Beamonte D, Modolell J. Cis-regulation of achaete and scute: shared enhancer-like elements drive their coexpression in proneural clusters of the imaginal discs. Genes Dev. 1995 Aug 1;9(15):1869–1882. [Abstract] [Google Scholar]
  • Gomez-Skarmeta JL, Diez del Corral R, de la Calle-Mustienes E, Ferré-Marcó D, Modolell J. Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell. 1996 Apr 5;85(1):95–105. [Abstract] [Google Scholar]
  • Graf JD, Kobel HR. Genetics of Xenopus laevis. Methods Cell Biol. 1991;36:19–34. [Abstract] [Google Scholar]
  • Graff JM, Thies RS, Song JJ, Celeste AJ, Melton DA. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell. 1994 Oct 7;79(1):169–179. [Abstract] [Google Scholar]
  • Hammerschmidt M, Brook A, McMahon AP. The world according to hedgehog. Trends Genet. 1997 Jan;13(1):14–21. [Abstract] [Google Scholar]
  • Harland RM. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 1991;36:685–695. [Abstract] [Google Scholar]
  • Harland R, Weintraub H. Translation of mRNA injected into Xenopus oocytes is specifically inhibited by antisense RNA. J Cell Biol. 1985 Sep;101(3):1094–1099. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hawley SH, Wünnenberg-Stapleton K, Hashimoto C, Laurent MN, Watabe T, Blumberg BW, Cho KW. Disruption of BMP signals in embryonic Xenopus ectoderm leads to direct neural induction. Genes Dev. 1995 Dec 1;9(23):2923–2935. [Abstract] [Google Scholar]
  • Hemmati-Brivanlou A, Melton DA. Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell. 1994 Apr 22;77(2):273–281. [Abstract] [Google Scholar]
  • Hemmati-Brivanlou A, de la Torre JR, Holt C, Harland RM. Cephalic expression and molecular characterization of Xenopus En-2. Development. 1991 Mar;111(3):715–724. [Abstract] [Google Scholar]
  • Hemmati-Brivanlou A, Kelly OG, Melton DA. Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell. 1994 Apr 22;77(2):283–295. [Abstract] [Google Scholar]
  • Hepker J, Wang QT, Motzny CK, Holmgren R, Orenic TV. Drosophila cubitus interruptus forms a negative feedback loop with patched and regulates expression of Hedgehog target genes. Development. 1997 Jan;124(2):549–558. [Abstract] [Google Scholar]
  • Hui CC, Slusarski D, Platt KA, Holmgren R, Joyner AL. Expression of three mouse homologs of the Drosophila segment polarity gene cubitus interruptus, Gli, Gli-2, and Gli-3, in ectoderm- and mesoderm-derived tissues suggests multiple roles during postimplantation development. Dev Biol. 1994 Apr;162(2):402–413. [Abstract] [Google Scholar]
  • Johnson RL, Grenier JK, Scott MP. patched overexpression alters wing disc size and pattern: transcriptional and post-transcriptional effects on hedgehog targets. Development. 1995 Dec;121(12):4161–4170. [Abstract] [Google Scholar]
  • Kintner CR, Melton DA. Expression of Xenopus N-CAM RNA in ectoderm is an early response to neural induction. Development. 1987 Mar;99(3):311–325. [Abstract] [Google Scholar]
  • Lamb TM, Harland RM. Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior neural pattern. Development. 1995 Nov;121(11):3627–3636. [Abstract] [Google Scholar]
  • Lamb TM, Knecht AK, Smith WC, Stachel SE, Economides AN, Stahl N, Yancopolous GD, Harland RM. Neural induction by the secreted polypeptide noggin. Science. 1993 Oct 29;262(5134):713–718. [Abstract] [Google Scholar]
  • Lecuit T, Brook WJ, Ng M, Calleja M, Sun H, Cohen SM. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature. 1996 May 30;381(6581):387–393. [Abstract] [Google Scholar]
  • Leyns L, Gómez-Skarmeta JL, Dambly-Chaudière C. iroquois: a prepattern gene that controls the formation of bristles on the thorax of Drosophila. Mech Dev. 1996 Sep;59(1):63–72. [Abstract] [Google Scholar]
  • Liem KF, Jr, Tremml G, Roelink H, Jessell TM. Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell. 1995 Sep 22;82(6):969–979. [Abstract] [Google Scholar]
  • Ma Q, Kintner C, Anderson DJ. Identification of neurogenin, a vertebrate neuronal determination gene. Cell. 1996 Oct 4;87(1):43–52. [Abstract] [Google Scholar]
  • Mancilla A, Mayor R. Neural crest formation in Xenopus laevis: mechanisms of Xslug induction. Dev Biol. 1996 Aug 1;177(2):580–589. [Abstract] [Google Scholar]
  • Mayor R, Essex LJ, Bennett MF, Sargent MG. Distinct elements of the xsna promoter are required for mesodermal and ectodermal expression. Development. 1993 Nov;119(3):661–671. [Abstract] [Google Scholar]
  • Mayor R, Morgan R, Sargent MG. Induction of the prospective neural crest of Xenopus. Development. 1995 Mar;121(3):767–777. [Abstract] [Google Scholar]
  • McNeill H, Yang CH, Brodsky M, Ungos J, Simon MA. mirror encodes a novel PBX-class homeoprotein that functions in the definition of the dorsal-ventral border in the Drosophila eye. Genes Dev. 1997 Apr 15;11(8):1073–1082. [Abstract] [Google Scholar]
  • Mo R, Freer AM, Zinyk DL, Crackower MA, Michaud J, Heng HH, Chik KW, Shi XM, Tsui LC, Cheng SH, et al. Specific and redundant functions of Gli2 and Gli3 zinc finger genes in skeletal patterning and development. Development. 1997 Jan;124(1):113–123. [Abstract] [Google Scholar]
  • Motzny CK, Holmgren R. The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech Dev. 1995 Jul;52(1):137–150. [Abstract] [Google Scholar]
  • Moury JD, Jacobson AG. The origins of neural crest cells in the axolotl. Dev Biol. 1990 Oct;141(2):243–253. [Abstract] [Google Scholar]
  • Nellen D, Burke R, Struhl G, Basler K. Direct and long-range action of a DPP morphogen gradient. Cell. 1996 May 3;85(3):357–368. [Abstract] [Google Scholar]
  • Pannese M, Polo C, Andreazzoli M, Vignali R, Kablar B, Barsacchi G, Boncinelli E. The Xenopus homologue of Otx2 is a maternal homeobox gene that demarcates and specifies anterior body regions. Development. 1995 Mar;121(3):707–720. [Abstract] [Google Scholar]
  • Papalopulu N, Kintner C. A posteriorising factor, retinoic acid, reveals that anteroposterior patterning controls the timing of neuronal differentiation in Xenopus neuroectoderm. Development. 1996 Nov;122(11):3409–3418. [Abstract] [Google Scholar]
  • Piccolo S, Sasai Y, Lu B, De Robertis EM. Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell. 1996 Aug 23;86(4):589–598. [Abstract] [Google Scholar]
  • Ruiz i Altaba A. Induction and axial patterning of the neural plate: planar and vertical signals. J Neurobiol. 1993 Oct;24(10):1276–1304. [Abstract] [Google Scholar]
  • Sánchez-Herrero E, Couso JP, Capdevila J, Guerrero I. The fu gene discriminates between pathways to control dpp expression in Drosophila imaginal discs. Mech Dev. 1996 Apr;55(2):159–170. [Abstract] [Google Scholar]
  • Sasai Y, De Robertis EM. Ectodermal patterning in vertebrate embryos. Dev Biol. 1997 Feb 1;182(1):5–20. [Abstract] [Google Scholar]
  • Sasai Y, Lu B, Steinbeisser H, Geissert D, Gont LK, De Robertis EM. Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell. 1994 Dec 2;79(5):779–790. [Abstract] [Google Scholar]
  • Sasai Y, Lu B, Steinbeisser H, De Robertis EM. Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus. Nature. 1995 Jul 27;376(6538):333–336. [Abstract] [Google Scholar]
  • Schmidt JE, Suzuki A, Ueno N, Kimelman D. Localized BMP-4 mediates dorsal/ventral patterning in the early Xenopus embryo. Dev Biol. 1995 May;169(1):37–50. [Abstract] [Google Scholar]
  • Sharpe CR, Goldstone K. Retinoid receptors promote primary neurogenesis in Xenopus. Development. 1997 Jan;124(2):515–523. [Abstract] [Google Scholar]
  • Slack JM. Regional biosynthetic markers in the early amphibian embryo. J Embryol Exp Morphol. 1984 Apr;80:289–319. [Abstract] [Google Scholar]
  • Slusarski DC, Motzny CK, Holmgren R. Mutations that alter the timing and pattern of cubitus interruptus gene expression in Drosophila melanogaster. Genetics. 1995 Jan;139(1):229–240. [Europe PMC free article] [Abstract] [Google Scholar]
  • Smith WC, Harland RM. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell. 1992 Sep 4;70(5):829–840. [Abstract] [Google Scholar]
  • Smith WC, Knecht AK, Wu M, Harland RM. Secreted noggin protein mimics the Spemann organizer in dorsalizing Xenopus mesoderm. Nature. 1993 Feb 11;361(6412):547–549. [Abstract] [Google Scholar]
  • Oda S, Nishimatsu S, Murakami K, Ueno N. Molecular cloning and functional analysis of a new activin beta subunit: a dorsal mesoderm-inducing activity in Xenopus. Biochem Biophys Res Commun. 1995 May 16;210(2):581–588. [Abstract] [Google Scholar]
  • Takebayashi K, Takahashi S, Yokota C, Tsuda H, Nakanishi S, Asashima M, Kageyama R. 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. 1997 Jan 15;16(2):384–395. [Europe PMC free article] [Abstract] [Google Scholar]
  • Turner DL, Weintraub H. Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 1994 Jun 15;8(12):1434–1447. [Abstract] [Google Scholar]
  • Wilson PA, Hemmati-Brivanlou A. Vertebrate neural induction: inducers, inhibitors, and a new synthesis. Neuron. 1997 May;18(5):699–710. [Abstract] [Google Scholar]
  • Zimmerman K, Shih J, Bars J, Collazo A, Anderson DJ. 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. 1993 Sep;119(1):221–232. [Abstract] [Google Scholar]
  • Zimmerman LB, De Jesús-Escobar JM, Harland RM. The Spemann organizer signal noggin binds and inactivates bone morphogenetic protein 4. Cell. 1996 Aug 23;86(4):599–606. [Abstract] [Google Scholar]
  • 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. 1998 Jan 2;17(1):191–203. [Europe PMC free article] [Abstract] [Google Scholar]
Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

Full text links 

Read article at publisher's site: https://doi.org/10.1093/emboj/17.1.181

Read article for free, from open access legal sources, via Unpaywall: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1170369Unpaywall

Citations & impact 

Impact metrics

94
Citations
Jump to Citations
9
Data citations
Jump to Data

Citations of article over time

Smart citations by scite.ai
Smart citations by scite.ai include citation statements extracted from the full text of the citing article. The number of the statements may be higher than the number of citations provided by EuropePMC if one paper cites another multiple times or lower if scite has not yet processed some of the citing articles.
Explore citation contexts and check if this article has been supported or disputed.
https://scite.ai/reports/10.1093/emboj/17.1.181

Supporting
Mentioning
Contrasting
3
114
0

Article citations

Go to all (94) article citations

Data 

Data behind the article

This data has been text mined from the article, or deposited into data resources.

BioStudies: supplemental material and supporting data

Similar Articles 

To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.