Home LiteratureArticle Details
PMID: 19736322 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The posteriorizing gene Gbx2 is a direct target of Wnt signalling and the earliest factor in neural crest induction.

Development (Cambridge, England) ·Vol. 136 ·No. 19 ·2009-10-00 ·Pages 3267-78

Li B, Kuriyama S, Moreno M, Mayor R

Abstract

Wnt signalling is required for neural crest (NC) induction; however, the direct targets of the Wnt pathway during NC induction remain unknown. We show here that the homeobox gene Gbx2 is essential in this process and is directly activated by Wnt/beta-catenin signalling. By ChIP and transgenesis analysis we show that the Gbx2 regulatory elements that drive expression in the NC respond directly to Wnt/beta-catenin signalling. Gbx2 has previously been implicated in posteriorization of the neural plate. Here we unveil a new role for this gene in neural fold patterning. Loss-of-function experiments using antisense morpholinos against Gbx2 inhibit NC and expand the preplacodal domain, whereas Gbx2 overexpression leads to transformation of the preplacodal domain into NC cells. We show that the NC specifier activity of Gbx2 is dependent on the interaction with Zic1 and the inhibition of preplacodal genes such as Six1. In addition, we demonstrate that Gbx2 is upstream of the neural fold specifiers Pax3 and Msx1. Our results place Gbx2 as the earliest factor in the NC genetic cascade being directly regulated by the inductive molecules, and support the notion that posteriorization of the neural folds is an essential step in NC specification. We propose a new genetic cascade that operates in the distinction between anterior placodal and NC territories.

MeSH Terms
Animals Animals, Genetically Modified Base Sequence Binding Sites/genetics Body Patterning DNA Primers/genetics Enhancer Elements, Genetic Genes, Homeobox Homeodomain Proteins/genetics,metabolism Models, Biological Molecular Sequence Data Neural Crest/embryology,metabolism RNA, Messenger/genetics,metabolism Signal Transduction Transcription Factors/genetics,metabolism Wnt Proteins/metabolism Xenopus/embryology,genetics,metabolism Xenopus Proteins/genetics,metabolism beta Catenin/metabolism
Chemicals
CTNNB1 protein, Xenopus DNA Primers Gbx2 protein, Xenopus Homeodomain Proteins RNA, Messenger Transcription Factors Wnt Proteins Xenopus Proteins Zic1 protein, Xenopus beta Catenin
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Li Bo
Department of Cell and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK.
Kuriyama Sei
Moreno Mauricio
Mayor Roberto
References (82)
82 references, click to expand
  1. In situ hybridization: an improved whole-mount method for Xenopus embryos.
    Methods Cell Biol. 1991;36:685-95 PMID: 1811161
  2. Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach.
    Dev Biol. 2000 Jun 1;222(1):124-34 PMID: 10885751
  3. Otx2, Gbx2 and Fgf8 interact to position and maintain a mid-hindbrain organizer.
    Curr Opin Cell Biol. 2000 Dec;12(6):736-41 PMID: 11063941
  4. Differential requirements of BMP and Wnt signalling during gastrulation and neurulation define two steps in neural crest induction.
    Development. 2009 Mar;136(5):771-9 PMID: 19176585
  5. Requirement of Sox2-mediated signaling for differentiation of early Xenopus neuroectoderm.
    Development. 2000 Feb;127(4):791-800 PMID: 10648237
  6. Tissues and signals involved in the induction of placodal Six1 expression in Xenopus laevis.
    Dev Biol. 2005 Dec 1;288(1):40-59 PMID: 16271713
  7. Vertebrate anteroposterior patterning: the Xenopus neurectoderm as a paradigm.
    Bioessays. 2000 Nov;22(11):976-86 PMID: 11056474
  8. A balance between the anti-apoptotic activity of Slug and the apoptotic activity of msx1 is required for the proper development of the neural crest.
    Dev Biol. 2004 Nov 15;275(2):325-42 PMID: 15501222
  9. A posteriorising factor, retinoic acid, reveals that anteroposterior patterning controls the timing of neuronal differentiation in Xenopus neuroectoderm.
    Development. 1996 Nov;122(11):3409-18 PMID: 8951057
  10. Chromatin immunoprecipitation for studying transcriptional regulation in Xenopus oocytes and tadpoles.
    Methods Mol Biol. 2006;322:165-81 PMID: 16739723
  11. Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirl pathway of genes.
    Dev Biol. 1998 Jul 1;199(1):93-110 PMID: 9676195
  12. Neural crest induction by the canonical Wnt pathway can be dissociated from anterior-posterior neural patterning in Xenopus.
    Dev Biol. 2005 Mar 1;279(1):220-32 PMID: 15708570
  13. Zebrafish zic1 expression in brain and somites is affected by BMP and hedgehog signalling.
    Mech Dev. 1999 Jul;85(1-2):147-59 PMID: 10415355
  14. Early induction of neural crest cells: lessons learned from frog, fish and chick.
    Curr Opin Genet Dev. 2002 Aug;12(4):452-8 PMID: 12100892
  15. Direct regulation of the Xenopus engrailed-2 promoter by the Wnt signaling pathway, and a molecular screen for Wnt-responsive genes, confirm a role for Wnt signaling during neural patterning in Xenopus.
    Mech Dev. 1999 Sep;87(1-2):21-32 PMID: 10495268
  16. Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction.
    Dev Cell. 2005 Feb;8(2):167-78 PMID: 15691759
  17. Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction.
    Development. 1998 Feb;125(4):579-87 PMID: 9435279
  18. A developmentally regulated, nervous system-specific gene in Xenopus encodes a putative RNA-binding protein.
    New Biol. 1990 Jun;2(6):556-65 PMID: 1708282
  19. Transcriptional regulation of a Xenopus embryonic epidermal keratin gene.
    Development. 1989 Jun;106(2):399-405 PMID: 2480217
  20. Essential role of non-canonical Wnt signalling in neural crest migration.
    Development. 2005 Jun;132(11):2587-97 PMID: 15857909
  21. A gene regulatory network orchestrates neural crest formation.
    Nat Rev Mol Cell Biol. 2008 Jul;9(7):557-68 PMID: 18523435
  22. Positioning the isthmic organizer where Otx2 and Gbx2meet.
    Trends Genet. 2000 Jun;16(6):237-40 PMID: 10827447
  23. Posteriorization by FGF, Wnt, and retinoic acid is required for neural crest induction.
    Dev Biol. 2002 Jan 15;241(2):289-301 PMID: 11784112
  24. A role for Gbx2 in repression of Otx2 and positioning the mid/hindbrain organizer.
    Nature. 1999 Sep 9;401(6749):161-4 PMID: 10490024
  25. The homeoprotein Xiro1 is required for midbrain-hindbrain boundary formation.
    Development. 2002 Apr;129(7):1609-21 PMID: 11923198
  26. Control of cell behavior during vertebrate development by Slug, a zinc finger gene.
    Science. 1994 May 6;264(5160):835-9 PMID: 7513443
  27. Analysis of Dishevelled signalling pathways during Xenopus development.
    Curr Biol. 1996 Nov 1;6(11):1456-67 PMID: 8939601
  28. xDnmt1 regulates transcriptional silencing in pre-MBT Xenopus embryos independently of its catalytic function.
    Development. 2008 Apr;135(7):1295-302 PMID: 18305009
  29. Requirement of FoxD3-class signaling for neural crest determination in Xenopus.
    Development. 2001 Jul;128(13):2525-36 PMID: 11493569
  30. Snail precedes slug in the genetic cascade required for the specification and migration of the Xenopus neural crest.
    Development. 2003 Feb;130(3):483-94 PMID: 12490555
  31. Early development of the cranial sensory nervous system: from a common field to individual placodes.
    Dev Biol. 2004 Dec 1;276(1):1-15 PMID: 15531360
  32. 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):2075-85 PMID: 9169853
  33. Molecular cloning and embryonic expression of Xenopus Six homeobox genes.
    Mech Dev. 2001 Mar;101(1-2):271-7 PMID: 11231090
  34. Loss of Gbx2 results in neural crest cell patterning and pharyngeal arch artery defects in the mouse embryo.
    Dev Biol. 2005 Aug 1;284(1):233-45 PMID: 15996652
  35. Xiro, a Xenopus homolog of the Drosophila Iroquois complex genes, controls development at the neural plate.
    EMBO J. 1998 Jan 2;17(1):181-90 PMID: 9427752
  36. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo.
    Cell. 1994 Oct 7;79(1):169-79 PMID: 7522972
  37. Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus.
    Development. 1998 Aug;125(15):2867-82 PMID: 9655809
  38. Xenopus Six1 gene is expressed in neurogenic cranial placodes and maintained in the differentiating lateral lines.
    Mech Dev. 2000 Sep;96(2):253-7 PMID: 10960794
  39. The genesis of avian neural crest cells: a classic embryonic induction.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9352-7 PMID: 8790333
  40. Translation of mRNA injected into Xenopus oocytes is specifically inhibited by antisense RNA.
    J Cell Biol. 1985 Sep;101(3):1094-9 PMID: 2411734
  41. Induction of the prospective neural crest of Xenopus.
    Development. 1995 Mar;121(3):767-77 PMID: 7720581
  42. The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient.
    Dev Biol. 1998 Jun 15;198(2):319-29 PMID: 9659936
  43. Tol2: a versatile gene transfer vector in vertebrates.
    Genome Biol. 2007;8 Suppl 1:S7 PMID: 18047699
  44. Comparative analysis of Otx2, Gbx2, Pax2, Fgf8 and Wnt1 gene expressions during the formation of the chick midbrain/hindbrain domain.
    Mech Dev. 1999 Mar;81(1-2):175-8 PMID: 10330495
  45. Gene-regulatory interactions in neural crest evolution and development.
    Dev Cell. 2004 Sep;7(3):291-9 PMID: 15363405
  46. Regulation of Msx genes by a Bmp gradient is essential for neural crest specification.
    Development. 2003 Dec;130(26):6441-52 PMID: 14627721
  47. Cephalic expression and molecular characterization of Xenopus En-2.
    Development. 1991 Mar;111(3):715-24 PMID: 1679005
  48. The activity of Pax3 and Zic1 regulates three distinct cell fates at the neural plate border.
    Mol Biol Cell. 2007 Jun;18(6):2192-202 PMID: 17409353
  49. Xenopus Zic family and its role in neural and neural crest development.
    Mech Dev. 1998 Jul;75(1-2):43-51 PMID: 9739105
  50. Neuroepithelial co-expression of Gbx2 and Otx2 precedes Fgf8 expression in the isthmic organizer.
    Mech Dev. 2001 Mar;101(1-2):111-8 PMID: 11231064
  51. Anterior neurectoderm is progressively induced during gastrulation: the role of the Xenopus homeobox gene orthodenticle.
    Development. 1995 Apr;121(4):993-1004 PMID: 7743941
  52. Epidermal keratin gene expressed in embryos of Xenopus laevis.
    Proc Natl Acad Sci U S A. 1985 Aug;82(16):5413-7 PMID: 2410923
  53. A balance of FGF, BMP and WNT signalling positions the future placode territory in the head.
    Development. 2005 Sep;132(18):4051-62 PMID: 16093325
  54. Ectodermal Wnt function as a neural crest inducer.
    Science. 2002 Aug 2;297(5582):848-51 PMID: 12161657
  55. Paraxial-fated mesoderm is required for neural crest induction in Xenopus embryos.
    Dev Biol. 1998 Jan 15;193(2):156-68 PMID: 9473321
  56. Development of neural crest in Xenopus.
    Curr Top Dev Biol. 1999;43:85-113 PMID: 9891884
  57. Molecular mechanisms of neural crest induction.
    Birth Defects Res C Embryo Today. 2004 Jun;72(2):109-23 PMID: 15269886
  58. The Xenopus laevis homeobox gene Xgbx-2 is an early marker of anteroposterior patterning in the ectoderm.
    Mech Dev. 1996 Feb;54(2):149-60 PMID: 8652408
  59. 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 PMID: 8443108
  60. Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor.
    Development. 2004 Dec;131(23):5871-81 PMID: 15525662
  61. Identification of a BMP inhibitor-responsive promoter module required for expression of the early neural gene zic1.
    Dev Biol. 2006 Jan 15;289(2):517-29 PMID: 16307736
  62. Genetic network during neural crest induction: from cell specification to cell survival.
    Semin Cell Dev Biol. 2005 Dec;16(6):647-54 PMID: 16084743
  63. The Wnt/beta-catenin pathway posteriorizes neural tissue in Xenopus by an indirect mechanism requiring FGF signalling.
    Dev Biol. 2001 Nov 1;239(1):148-60 PMID: 11784025
  64. Induction and specification of cranial placodes.
    Dev Biol. 2006 Jun 15;294(2):303-51 PMID: 16677629
  65. Lrig3 regulates neural crest formation in Xenopus by modulating Fgf and Wnt signaling pathways.
    Development. 2008 Apr;135(7):1283-93 PMID: 18287203
  66. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway.
    Development. 2000 May;127(10):2227-38 PMID: 10769246
  67. Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm.
    Development. 2005 May;132(10):2355-63 PMID: 15843410
  68. Neural crest induction by paraxial mesoderm in Xenopus embryos requires FGF signals.
    Development. 2003 Jul;130(14):3111-24 PMID: 12783784
  69. Neural crest formation in Xenopus laevis: mechanisms of Xslug induction.
    Dev Biol. 1996 Aug 1;177(2):580-9 PMID: 8806833
  70. Gene expression in the embryonic nervous system of Xenopus laevis.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8086-90 PMID: 3186710
  71. Establishment and maintenance of the border of the neural plate in the chick: involvement of FGF and BMP activity.
    Mech Dev. 1999 Apr;82(1-2):51-66 PMID: 10354471
  72. Formation of morphogen gradients in the Drosophila wing.
    Semin Cell Dev Biol. 1999 Jun;10(3):335-44 PMID: 10441548
  73. Induction and development of neural crest in Xenopus laevis.
    Cell Tissue Res. 2001 Aug;305(2):203-9 PMID: 11545257
  74. Regulation of dorsal fate in the neuraxis by Wnt-1 and Wnt-3a.
    Proc Natl Acad Sci U S A. 1997 Dec 9;94(25):13713-8 PMID: 9391091
  75. Regulation of LEF-1/TCF transcription factors by Wnt and other signals.
    Curr Opin Cell Biol. 1999 Apr;11(2):233-40 PMID: 10209158
  76. Neural crest induction in Xenopus: evidence for a two-signal model.
    Development. 1998 Jul;125(13):2403-14 PMID: 9609823
  77. Cloning and characterization of three Xenopus slug promoters reveal direct regulation by Lef/beta-catenin signaling.
    J Biol Chem. 2001 Aug 10;276(32):30350-8 PMID: 11402039
  78. Neural crests are actively precluded from the anterior neural fold by a novel inhibitory mechanism dependent on Dickkopf1 secreted by the prechordal mesoderm.
    Dev Biol. 2007 Sep 15;309(2):208-21 PMID: 17669393
  79. Conserved expression control and shared activity between cognate T-box genes Tbx2 and Tbx3 in connection with Sonic hedgehog signaling during Xenopus eye development.
    Dev Growth Differ. 2002 Aug;44(4):257-71 PMID: 12175361
  80. Xenopus msx1 mediates epidermal induction and neural inhibition by BMP4.
    Development. 1997 Aug;124(16):3037-44 PMID: 9272945
  81. Caudalization of neural fate by tissue recombination and bFGF.
    Development. 1995 Dec;121(12):4349-58 PMID: 8575335
  82. Neural plate patterning: upstream and downstream of the isthmic organizer.
    Nat Rev Neurosci. 2001 Feb;2(2):99-108 PMID: 11253000
Article Info
Journal
Development (Cambridge, England)
Abbr.
Development
ISSN
1477-9129
Published
2009-10-00
Pages
3267-78
Language
English
Region
England
NLM ID
8701744
PMCID
PMC2808295
Subset
IM
Grants
Medical Research Council · G0801145 · United Kingdom
Biotechnology and Biological Sciences Research Council · United Kingdom
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]