Home LiteratureArticle Details
PMID: 12351707 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Repressor element-1 silencing transcription/neuron-restrictive silencer factor is required for neural sodium channel expression during development of Xenopus.

Armisén R, Fuentes R, Olguín P, Cabrejos ME, Kukuljan M

Abstract

The ability of neurons to fire rapid action potential relies on the expression of voltage-gated sodium channels; the onset of the transcription of genes that encode these channels occurs during early neuronal development. The factors that direct and regulate the specific expression of ion channels are not well understood. Repressor element-1 silencing transcription/neuron-restrictive silencer factor (REST/NRSF) is a transcriptional regulator characterized as a repressor of the expression of NaV1.2, the gene encoding the voltage-gated sodium channel most abundantly expressed in the CNS, as well as of the expression of numerous other neuronal genes. In mammals, REST/NRSF is expressed mostly in non-neural cell types and immature neurons, and it is downregulated on neural maturation. To understand the mechanisms that govern sodium channel gene transcription and to explore the role of REST/NRSF in vivo, we inhibited REST/NRSF action in developing Xenopus laevis embryos by means of a dominant negative protein or antisense oligonucleotides. Contrary to what was expected, these maneuvers result in the decrease of the expression of the NaV1.2 gene, as well as of other neuronal genes in the primary spinal neurons and cranial ganglia, without overt perturbation of neurogenesis. These results, together with the demonstration of robust REST/NRSF expression in primary spinal neurons, suggest that REST/NRSF is required for the acquisition of the differentiated functional neuronal phenotype during early development. Furthermore, they suggest that REST/NRSF may be used to activate or repress transcription of neuronal genes in distinct cellular and developmental contexts.

MeSH Terms
Animals Cell Differentiation/physiology Cells, Cultured Electrophoretic Mobility Shift Assay Embryo, Nonmammalian Gene Silencing/physiology Genes, Dominant In Situ Hybridization NAV1.2 Voltage-Gated Sodium Channel Nerve Tissue Proteins/metabolism Neural Crest/cytology,embryology,metabolism Neurons/cytology,metabolism Oligonucleotides, Antisense/pharmacology Phenotype RNA, Messenger/antagonists & inhibitors,metabolism Repressor Proteins/antagonists & inhibitors,genetics,metabolism Sodium Channels/biosynthesis,metabolism Spinal Cord/cytology,embryology,metabolism Transcription Factors/antagonists & inhibitors,genetics,metabolism Xenopus laevis
Chemicals
NAV1.2 Voltage-Gated Sodium Channel Nerve Tissue Proteins Oligonucleotides, Antisense RE1-silencing transcription factor RNA, Messenger Repressor Proteins Sodium Channels Transcription Factors
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Armisén Ricardo
Programa de Fisiologia y Biofisica, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Independencia 1027, Santiago, Chile.
Fuentes Rómulo
Olguín Patricio
Cabrejos María E
Kukuljan Manuel
References (31)
31 references, click to expand
  1. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons.
    Cell. 1995 Mar 24;80(6):949-57 PMID: 7697725
  2. Regulation of neuronal traits by a novel transcriptional complex.
    Neuron. 2001 Aug 16;31(3):353-65 PMID: 11516394
  3. The neuron-restrictive silencer element-neuron-restrictive silencer factor system regulates basal and endothelin 1-inducible atrial natriuretic peptide gene expression in ventricular myocytes.
    Mol Cell Biol. 2001 Mar;21(6):2085-97 PMID: 11238943
  4. Silencing the type II sodium channel gene: a model for neural-specific gene regulation.
    Neuron. 1992 Jul;9(1):37-44 PMID: 1321645
  5. 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
  6. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes.
    Science. 1995 Mar 3;267(5202):1360-3 PMID: 7871435
  7. 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
  8. New functions for DNA binding domains.
    Sci STKE. 2001 May 08;2001(81):pe1 PMID: 11752650
  9. 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
  10. 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
  11. In vivo development of voltage-dependent ionic currents in embryonic Xenopus spinal neurons.
    J Neurosci. 1993 Jun;13(6):2575-81 PMID: 8501523
  12. Onset of electrical excitability during a period of circus plasma membrane movements in differentiating Xenopus neurons.
    J Neurosci. 1996 Aug 15;16(16):5117-29 PMID: 8756441
  13. The development of the action potential mechanism of amphibian neurons isolated in culture.
    Proc Natl Acad Sci U S A. 1976 May;73(5):1641-5 PMID: 1064036
  14. Early neurogenesis in Xenopus: the spatio-temporal pattern of proliferation and cell lineages in the embryonic spinal cord.
    Neuron. 1989 Oct;3(4):399-411 PMID: 2642003
  15. Xenopus spinal neurons express Kv2 potassium channel transcripts during embryonic development.
    J Neurosci. 1996 Feb 15;16(4):1412-21 PMID: 8778292
  16. The Xiro-repressed gene CoREST is expressed in Xenopus neural territories.
    Mech Dev. 2002 Jan;110(1-2):209-11 PMID: 11744385
  17. Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes.
    Nat Neurosci. 1999 Oct;2(10):867-72 PMID: 10491605
  18. Development of voltage-dependent calcium, sodium, and potassium currents in Xenopus spinal neurons.
    J Neurosci. 1988 Mar;8(3):792-805 PMID: 3346722
  19. Antisense suppression of potassium channel expression demonstrates its role in maturation of the action potential.
    J Neurosci. 2000 Aug 15;20(16):6087-94 PMID: 10934258
  20. 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
  21. The neural restrictive silencer element can act as both a repressor and enhancer of L1 cell adhesion molecule gene expression during postnatal development.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3233-8 PMID: 9501246
  22. Neuronal expression of zinc finger transcription factor REST/NRSF/XBR gene.
    J Neurosci. 1998 Feb 15;18(4):1280-96 PMID: 9454838
  23. Combinatorial roles of the nuclear receptor corepressor in transcription and development.
    Cell. 2000 Sep 15;102(6):753-63 PMID: 11030619
  24. A potassium channel gene is expressed at neural induction.
    Neuron. 1990 Nov;5(5):691-701 PMID: 2223094
  25. 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
  26. Neural restrictive silencer factor recruits mSin3 and histone deacetylase complex to repress neuron-specific target genes.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13691-6 PMID: 10570134
  27. Temporal regulation of Shaker- and Shab-like potassium channel gene expression in single embryonic spinal neurons during K+ current development.
    J Neurosci. 1996 May 15;16(10):3287-95 PMID: 8627366
  28. Repressor element silencing transcription factor/neuron-restrictive silencing factor (REST/NRSF) can act as an enhancer as well as a repressor of corticotropin-releasing hormone gene transcription.
    J Biol Chem. 2001 Apr 27;276(17):13917-23 PMID: 11278361
  29. The neuron-restrictive silencer element: a dual enhancer/silencer crucial for patterned expression of a nicotinic receptor gene in the brain.
    Proc Natl Acad Sci U S A. 1997 May 27;94(11):5906-11 PMID: 9159173
  30. A zinc finger protein that represses transcription of the human MHC class II gene, DPA.
    J Immunol. 1996 Feb 15;156(4):1448-57 PMID: 8568247
  31. A critical period of transcription required for differentiation of the action potential of spinal neurons.
    Neuron. 1989 Jan;2(1):1055-62 PMID: 2483107
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2002-10-01
Pages
8347-51
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6757790
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]