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PMID: 8355673 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

An E box mediates activation and repression of the acetylcholine receptor delta-subunit gene during myogenesis.

Molecular and cellular biology ·Vol. 13 ·No. 9 ·1993-09-00 ·Pages 5133-40

Simon AM, Burden SJ

Abstract

The genes encoding the skeletal muscle acetylcholine receptor (AChR) are induced during muscle development and are regulated subsequently by innervation. Because both the initiation and the subsequent regulation of AChR expression are controlled by transcriptional mechanisms, an understanding of the steps that regulate AChR expression following innervation is likely to require knowledge of the pathway that activates AChR genes during myogenesis. Thus, we sought to identify the cis-acting sequences that regulate expression of the AChR delta-subunit gene during muscle differentiation. We transfected muscle and nonmuscle cell lines with gene fusions between 5'-flanking DNA from the AChR delta-subunit gene and the human growth hormone gene, and we show here that 148 bp of 5'-flanking DNA from the AChR delta-subunit gene contains two regulatory elements that control muscle-specific gene expression. One element is an E box, which is important both for activation of the delta-subunit gene in myotubes and for its repression in myoblasts and nonmuscle cells. Mutation of this E box, which prevents binding of MyoD-E2A and myogenin-E2A heterodimers, decreases expression in myotubes and increases expression in myoblasts and nonmuscle cells. An E-box binding activity, which does not contain MyoD, myogenin, or E2A proteins, is present in muscle and nonmuscle cells and may be responsible for repressing the delta-subunit gene in myoblasts and nonmuscle cells. An enhancer, which lacks E boxes, is also required for expression of the delta-subunit gene but does not confer muscle-specific expression.

MeSH Terms
Animals Base Sequence Cell Differentiation Cell Line DNA Mutational Analysis DNA-Binding Proteins/metabolism Enhancer Elements, Genetic Gene Expression Regulation In Vitro Techniques Mice Molecular Sequence Data Muscles/cytology,metabolism Nuclear Proteins/metabolism Receptors, Nicotinic/genetics Regulatory Sequences, Nucleic Acid Sequence Deletion Transfection
Chemicals
DNA-Binding Proteins Nuclear Proteins Receptors, Nicotinic
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Simon A M
Biology Department, Massachusetts Institute of Technology, Cambridge 02139.
Burden S J
References (46)
46 references, click to expand
  1. DNA-mediated transfer of the adenine phosphoribosyltransferase locus into mammalian cells.
    Proc Natl Acad Sci U S A. 1979 Mar;76(3):1373-6 PMID: 286319
  2. Electrical activity-dependent regulation of the acetylcholine receptor delta-subunit gene, MyoD, and myogenin in primary myotubes.
    Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):2040-4 PMID: 8383334
  3. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei.
    Nucleic Acids Res. 1983 Mar 11;11(5):1475-89 PMID: 6828386
  4. The rapid generation of oligonucleotide-directed mutations at high frequency using phosphorothioate-modified DNA.
    Nucleic Acids Res. 1985 Dec 20;13(24):8765-85 PMID: 3001650
  5. Transcriptional regulation of nicotinic acetylcholine receptor genes during muscle development.
    J Biol Chem. 1986 Sep 5;261(25):11452-5 PMID: 3745150
  6. Human growth hormone as a reporter gene in regulation studies employing transient gene expression.
    Mol Cell Biol. 1986 Sep;6(9):3173-9 PMID: 3023965
  7. Multiple protein-binding sites in the 5'-flanking region regulate c-fos expression.
    Mol Cell Biol. 1986 Dec;6(12):4305-16 PMID: 3025651
  8. Negative regulation by glucocorticoids through interference with a cAMP responsive enhancer.
    Science. 1988 Jul 15;241(4863):350-3 PMID: 2838908
  9. MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts.
    Science. 1988 Oct 21;242(4877):405-11 PMID: 3175662
  10. Isolation and characterization of the mouse acetylcholine receptor delta subunit gene: identification of a 148-bp cis-acting region that confers myotube-specific expression.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2271-9 PMID: 3198687
  11. Transcriptional inhibition by a glucocorticoid receptor-beta-galactosidase fusion protein.
    Cell. 1988 Dec 23;55(6):1109-14 PMID: 3144438
  12. Activation and repression of transcription by homoeodomain-containing proteins that bind a common site.
    Nature. 1988 Dec 22-29;336(6201):744-9 PMID: 2905023
  13. Skeletal muscle denervation activates acetylcholine receptor genes.
    J Cell Biol. 1989 Apr;108(4):1523-6 PMID: 2925794
  14. The "initiator" as a transcription control element.
    Cell. 1989 Apr 7;57(1):103-13 PMID: 2467742
  15. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence.
    Cell. 1989 Aug 11;58(3):537-44 PMID: 2503252
  16. Activity-dependent regulation of gene expression in muscle and neuronal cells.
    Mol Neurobiol. 1989 Spring-Summer;3(1-2):1-53 PMID: 2679765
  17. Multiple sequence elements of a single functional class are required for cyclic AMP responsiveness of the mouse c-fos promoter.
    Mol Cell Biol. 1989 Oct;9(10):4272-81 PMID: 2555687
  18. Neural regulation of gene expression by an acetylcholine receptor promoter in muscle of transgenic mice.
    Neuron. 1989 Apr;2(4):1295-300 PMID: 2627372
  19. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins.
    Cell. 1990 Apr 6;61(1):49-59 PMID: 2156629
  20. Binding site-dependent direct activation and repression of in vitro transcription by Drosophila homeodomain proteins.
    Cell. 1990 May 4;61(3):475-84 PMID: 1970761
  21. Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor alpha-subunit gene.
    Nature. 1990 May 24;345(6273):353-5 PMID: 2342565
  22. Myogenin resides in the nucleus and acquires high affinity for a conserved enhancer element on heterodimerization.
    Genes Dev. 1990 Apr;4(4):582-95 PMID: 2163343
  23. Muscle-specific expression of the cardiac alpha-actin gene requires MyoD1, CArG-box binding factor, and Sp1.
    Genes Dev. 1990 Oct;4(10):1811-22 PMID: 2123467
  24. Differences and similarities in DNA-binding preferences of MyoD and E2A protein complexes revealed by binding site selection.
    Science. 1990 Nov 23;250(4984):1104-10 PMID: 2174572
  25. Sequence-specific DNA binding by the c-Myc protein.
    Science. 1990 Nov 23;250(4984):1149-51 PMID: 2251503
  26. Muscle-specific expression of the troponin I gene requires interactions between helix-loop-helix muscle regulatory factors and ubiquitous transcription factors.
    Mol Cell Biol. 1991 Jan;11(1):267-80 PMID: 1846022
  27. Methylation-sensitive sequence-specific DNA binding by the c-Myc basic region.
    Science. 1991 Jan 11;251(4990):186-9 PMID: 1987636
  28. An inhibitory domain of E12 transcription factor prevents DNA binding in E12 homodimers but not in E12 heterodimers.
    Cell. 1991 Jan 25;64(2):459-70 PMID: 1846322
  29. Modulation of the IgH enhancer's cell type specificity through a genetic switch.
    Genes Dev. 1991 Jan;5(1):29-37 PMID: 1899229
  30. The myoD gene family: nodal point during specification of the muscle cell lineage.
    Science. 1991 Feb 15;251(4995):761-6 PMID: 1846704
  31. An acetylcholine receptor alpha-subunit promoter conferring preferential synaptic expression in muscle of transgenic mice.
    EMBO J. 1991 Mar;10(3):625-32 PMID: 1900467
  32. Cyclic amplification and selection of targets (CASTing) for the myogenin consensus binding site.
    Mol Cell Biol. 1991 Aug;11(8):4104-10 PMID: 1649388
  33. Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo.
    Cell. 1991 Jul 26;66(2):305-15 PMID: 1649701
  34. Different mechanisms regulate muscle-specific AChR gamma- and epsilon-subunit gene expression.
    EMBO J. 1991 Oct;10(10):2957-64 PMID: 1655408
  35. Multiple binding sites for myogenic regulatory factors are required for expression of the acetylcholine receptor gamma-subunit gene.
    J Biol Chem. 1991 Oct 25;266(30):19871-4 PMID: 1657903
  36. Cooperative interaction of an initiator-binding transcription initiation factor and the helix-loop-helix activator USF.
    Nature. 1991 Nov 21;354(6350):245-8 PMID: 1961251
  37. Max: functional domains and interaction with c-Myc.
    Genes Dev. 1992 Jan;6(1):81-92 PMID: 1730412
  38. Diversity and specificity in transcriptional regulation: the benefits of heterotypic dimerization.
    Trends Biochem Sci. 1991 Nov;16(11):417-22 PMID: 1776171
  39. HEB, a helix-loop-helix protein related to E2A and ITF2 that can modulate the DNA-binding ability of myogenic regulatory factors.
    Mol Cell Biol. 1992 Mar;12(3):1031-42 PMID: 1312219
  40. Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers.
    Development. 1991 Dec;113(4):1181-91 PMID: 1811935
  41. Spatial restriction of AChR gene expression to subsynaptic nuclei.
    Development. 1992 Mar;114(3):545-53 PMID: 1618127
  42. Overexpression of Id protein inhibits the muscle differentiation program: in vivo association of Id with E2A proteins.
    Genes Dev. 1992 Aug;6(8):1466-79 PMID: 1644289
  43. A 40-kilodalton protein binds specifically to an upstream sequence element essential for muscle-specific transcription of the human myoglobin promoter.
    Mol Cell Biol. 1992 Nov;12(11):5024-32 PMID: 1406677
  44. Synaptic basal lamina contains a signal for synapse-specific transcription.
    Development. 1992 Jul;115(3):673-80 PMID: 1425346
  45. Synapse-specific expression of acetylcholine receptor genes and their products at original synaptic sites in rat soleus muscle fibres regenerating in the absence of innervation.
    Development. 1992 Sep;116(1):41-53 PMID: 1282861
  46. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells.
    Mol Cell Biol. 1982 Sep;2(9):1044-51 PMID: 6960240
Article Info
Journal
Molecular and cellular biology
Abbr.
Mol Cell Biol
ISSN
0270-7306
Published
1993-09-00
Pages
5133-40
Language
English
Region
United States
NLM ID
8109087
PMCID
PMC360201
Subset
IM
Grants
NINDS NIH HHS · NS27963 · United States
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