Home LiteratureArticle Details
PMID: 16525062 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

RE-1 silencer of transcription/neural restrictive silencer factor modulates ectodermal patterning during Xenopus development.

Olguín P, Oteíza P, Gamboa E, Gómez-Skármeta JL, Kukuljan M

Abstract

RE-1 silencer of transcription/neural restrictive silencer factor (REST/NRSF), a transcriptional repressor, binds to the RE-1 element present in many vertebrate genes. In vitro studies indicate that REST/NRSF plays important roles in several stages of neural development. However, a full understanding of its physiological function requires in vivo approaches. We find that impairment of REST/NRSF function in Xenopus embryos leads to the perturbation of neural tube, cranial ganglia, and eye development. The origin of these defects is the abnormal patterning of the ectoderm during gastrulation. Interference of REST/NRSF function during the late blastula stage leads to an expansion of the neural plate, concomitant with a decrease of the expression of epidermal keratin and neural crest markers. Furthermore, neurogenesis proceeds abnormally, with loss of the expression of proneural, neurogenic, and neuronal genes. The interference of REST/NRSF mimics several features associated with a decreased bone morphogenetic protein (BMP) function and counteracts some effects of BMP4 misexpression. Our results indicate that REST/NRSF function is required in vivo for the acquisition of specific ectodermal cell fates.

MeSH Terms
Animals Body Patterning/drug effects,physiology Ectoderm/metabolism Embryo, Nonmammalian Gene Expression Regulation, Developmental/drug effects,physiology Immunohistochemistry/methods In Situ Hybridization/methods Microinjections/methods Molecular Biology/methods Morphogenesis Neurons/physiology RNA, Messenger/metabolism Repressor Proteins/genetics,metabolism Reverse Transcriptase Polymerase Chain Reaction/methods Transcription Factors/genetics,metabolism Transcription, Genetic/drug effects,physiology Xenopus
Chemicals
RE1-silencing transcription factor RNA, Messenger Repressor Proteins Transcription Factors
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Olguín Patricio
Centro de Neurociencias Integradas, Iniciativa Científica Milenio, Programa de Fisiología y Biofísica, Instituto de Ciencias Biomedicas, Facultad de Medicina, Universidad de Chile, 838-0453 Independencia, Chile. [email protected]
Oteíza Pablo
Gamboa Eduardo
Gómez-Skármeta José Luis
Kukuljan Manuel
References (52)
52 references, click to expand
  1. CoREST: a functional corepressor required for regulation of neural-specific gene expression.
    Proc Natl Acad Sci U S A. 1999 Aug 17;96(17):9873-8 PMID: 10449787
  2. Protein kinase A regulates cholinergic gene expression in PC12 cells: REST4 silences the silencing activity of neuron-restrictive silencer factor/REST.
    Mol Cell Biol. 1999 Oct;19(10):6788-95 PMID: 10490617
  3. Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes.
    Nat Neurosci. 1999 Oct;2(10):867-72 PMID: 10491605
  4. The co-repressor mSin3A is a functional component of the REST-CoREST repressor complex.
    J Biol Chem. 2000 Mar 31;275(13):9461-7 PMID: 10734093
  5. A splice variant of the neuron-restrictive silencer factor repressor is expressed in small cell lung cancer: a potential role in derepression of neuroendocrine genes and a useful clinical marker.
    Cancer Res. 2000 Apr 1;60(7):1840-4 PMID: 10766169
  6. Constitutive expression of the neuron-restrictive silencer factor (NRSF)/REST in differentiating neurons disrupts neuronal gene expression and causes axon pathfinding errors in vivo.
    Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12318-23 PMID: 11050251
  7. The Wnt-activated Xiro1 gene encodes a repressor that is essential for neural development and downregulates Bmp4.
    Development. 2001 Feb;128(4):551-60 PMID: 11171338
  8. Regulation of neuronal traits by a novel transcriptional complex.
    Neuron. 2001 Aug 16;31(3):353-65 PMID: 11516394
  9. The Xiro-repressed gene CoREST is expressed in Xenopus neural territories.
    Mech Dev. 2002 Jan;110(1-2):209-11 PMID: 11744385
  10. A transcriptional response to Wnt protein in human embryonic carcinoma cells.
    BMC Dev Biol. 2002 Jul 02;2:8 PMID: 12095419
  11. REST repression of neuronal genes requires components of the hSWI.SNF complex.
    J Biol Chem. 2002 Oct 25;277(43):41038-45 PMID: 12192000
  12. Repressor element-1 silencing transcription/neuron-restrictive silencer factor is required for neural sodium channel expression during development of Xenopus.
    J Neurosci. 2002 Oct 1;22(19):8347-51 PMID: 12351707
  13. Corepressor-dependent silencing of chromosomal regions encoding neuronal genes.
    Science. 2002 Nov 29;298(5599):1747-52 PMID: 12399542
  14. Silencing the type II sodium channel gene: a model for neural-specific gene regulation.
    Neuron. 1992 Jul;9(1):37-44 PMID: 1321645
  15. A common silencer element in the SCG10 and type II Na+ channel genes binds a factor present in nonneuronal cells but not in neuronal cells.
    Neuron. 1992 Jul;9(1):45-54 PMID: 1321646
  16. Regulation of Msx genes by a Bmp gradient is essential for neural crest specification.
    Development. 2003 Dec;130(26):6441-52 PMID: 14627721
  17. NRSF regulates the fetal cardiac gene program and maintains normal cardiac structure and function.
    EMBO J. 2003 Dec 1;22(23):6310-21 PMID: 14633990
  18. A small modulatory dsRNA specifies the fate of adult neural stem cells.
    Cell. 2004 Mar 19;116(6):779-93 PMID: 15035981
  19. Localized domains of G9a-mediated histone methylation are required for silencing of neuronal genes.
    Mol Cell. 2004 Jun 18;14(6):727-38 PMID: 15200951
  20. Genome-wide analysis of repressor element 1 silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) target genes.
    Proc Natl Acad Sci U S A. 2004 Jul 13;101(28):10458-63 PMID: 15240883
  21. Dorsal-ventral patterning and neural induction in Xenopus embryos.
    Annu Rev Cell Dev Biol. 2004;20:285-308 PMID: 15473842
  22. Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists.
    Development. 2004 Nov;131(22):5671-81 PMID: 15509767
  23. The SWI/SNF chromatin remodeling protein Brg1 is required for vertebrate neurogenesis and mediates transactivation of Ngn and NeuroD.
    Development. 2005 Jan;132(1):105-15 PMID: 15576411
  24. Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition.
    Development. 2005 Jan;132(2):299-310 PMID: 15590738
  25. Conditional BMP inhibition in Xenopus reveals stage-specific roles for BMPs in neural and neural crest induction.
    Dev Biol. 2005 Jan 15;277(2):425-42 PMID: 15617685
  26. Small CTD phosphatases function in silencing neuronal gene expression.
    Science. 2005 Jan 28;307(5709):596-600 PMID: 15681389
  27. Default neural induction: neuralization of dissociated Xenopus cells is mediated by Ras/MAPK activation.
    Genes Dev. 2005 May 1;19(9):1022-7 PMID: 15879552
  28. REST and its corepressors mediate plasticity of neuronal gene chromatin throughout neurogenesis.
    Cell. 2005 May 20;121(4):645-657 PMID: 15907476
  29. A genetic screen for candidate tumor suppressors identifies REST.
    Cell. 2005 Jun 17;121(6):837-48 PMID: 15960972
  30. Distinct profiles of REST interactions with its target genes at different stages of neuronal development.
    Mol Biol Cell. 2005 Dec;16(12):5630-8 PMID: 16195345
  31. Activation of muscle genes without myogenesis by ectopic expression of MyoD in frog embryo cells.
    Nature. 1990 Sep 13;347(6289):197-200 PMID: 1697650
  32. In situ hybridization: an improved whole-mount method for Xenopus embryos.
    Methods Cell Biol. 1991;36:685-95 PMID: 1811161
  33. Epidermal keratin gene expressed in embryos of Xenopus laevis.
    Proc Natl Acad Sci U S A. 1985 Aug;82(16):5413-7 PMID: 2410923
  34. Efficient hormone-inducible protein function in Xenopus laevis.
    Dev Biol. 1995 Sep;171(1):267-72 PMID: 7556904
  35. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta.
    Nature. 1995 Jun 29;375(6534):761-6 PMID: 7596407
  36. Induction of epidermis and inhibition of neural fate by Bmp-4.
    Nature. 1995 Jul 27;376(6538):331-3 PMID: 7630398
  37. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons.
    Cell. 1995 Mar 24;80(6):949-57 PMID: 7697725
  38. Induction of the prospective neural crest of Xenopus.
    Development. 1995 Mar;121(3):767-77 PMID: 7720581
  39. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes.
    Science. 1995 Mar 3;267(5202):1360-3 PMID: 7871435
  40. Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate.
    Genes Dev. 1994 Jun 15;8(12):1434-47 PMID: 7926743
  41. Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes.
    Cell. 1994 Dec 2;79(5):779-90 PMID: 8001117
  42. Antagonizing the Spemann organizer: role of the homeobox gene Xvent-1.
    EMBO J. 1995 Dec 15;14(24):6268-79 PMID: 8557046
  43. Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurons in Xenopus embryos.
    Development. 1996 Jul;122(7):2295-301 PMID: 8681809
  44. Identification of potential target genes for the neuron-restrictive silencer factor.
    Proc Natl Acad Sci U S A. 1996 Sep 3;93(18):9881-6 PMID: 8790425
  45. Identification of neurogenin, a vertebrate neuronal determination gene.
    Cell. 1996 Oct 4;87(1):43-52 PMID: 8858147
  46. Xenopus msx1 mediates epidermal induction and neural inhibition by BMP4.
    Development. 1997 Aug;124(16):3037-44 PMID: 9272945
  47. 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
  48. Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene.
    J Neurosci. 1998 Feb 15;18(4):1280-96 PMID: 9454838
  49. Neural crest induction in Xenopus: evidence for a two-signal model.
    Development. 1998 Jul;125(13):2403-14 PMID: 9609823
  50. Gli/Zic factors pattern the neural plate by defining domains of cell differentiation.
    Nature. 1998 Jun 11;393(6685):579-83 PMID: 9634234
  51. SoxD: an essential mediator of induction of anterior neural tissues in Xenopus embryos.
    Neuron. 1998 Jul;21(1):77-85 PMID: 9697853
  52. NRSF/REST is required in vivo for repression of multiple neuronal target genes during embryogenesis.
    Nat Genet. 1998 Oct;20(2):136-42 PMID: 9771705
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2006-03-08
Pages
2820-9
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6675167
Subset
IM
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]