Home LiteratureArticle Details
PMID: 8036150 Published · ppublish English Journal Article

MyoD1 promoter autoregulation is mediated by two proximal E-boxes.

Nucleic acids research ·Vol. 22 ·No. 12 ·1994-06-25 ·Pages 2234-41

Zingg JM, Pedraza-Alva G, Jost JP

Abstract

We show that in mouse myoblasts the MyoD1 promoter is highly stimulated by MyoD1 expression, suggesting that it is controlled by a positive feedback loop. Using deletion and mutation analyses, we identified the targets for MyoD1 promoter autoregulation as the two proximal E-boxes located close to the MyoD1 core promoter. Gel mobility shift competition assays with MyoD1 antibodies as competitor suggest that the MyoD1 protein is binding directly to these E-boxes. Autoregulation did not occur in fibroblasts cotransfected with the expression vector of MyoD1. It is assumed that autoregulation is controlled by the stoichiometry between the MyoD1 protein and negatively regulatory proteins like Id, which is known to be highly expressed in fibroblasts. When the MyoD1 promoter was methylated, autoregulation only occurred when the density of methylated sites was low. The density of DNA methylation, therefore, can determine the accessibility of the MyoD1 promoter to transcription factors and interfere with the auto- and crossregulatory loop. The MyoD1 promoter in vivo was found to be only partially methylated in all tissues tested except in skeletal muscle where it was demethylated. We propose that high level expression of the MyoD1 gene is a result of release from constraints such as negative regulatory factors and/or DNA methylation interfering with MyoD1 autoregulation.

MeSH Terms
Animals Base Sequence Cell Line DNA Enhancer Elements, Genetic Feedback Fibroblasts/cytology Gene Expression Regulation Methylation Mice Mice, Inbred C3H Molecular Sequence Data Muscles/cytology MyoD Protein/genetics,metabolism Promoter Regions, Genetic Protein Binding Trans-Activators/genetics,metabolism
Chemicals
MyoD Protein MyoD1 myogenic differentiation protein Trans-Activators DNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Zingg J M
Friedrich Miescher Institut, Basel, Switzerland.
Pedraza-Alva G
Jost J P
References (63)
63 references, click to expand
  1. MyoD binds cooperatively to two sites in a target enhancer sequence: occupancy of two sites is required for activation.
    Proc Natl Acad Sci U S A. 1990 Aug;87(15):5623-7 PMID: 2377600
  2. AP-1 binds to a putative cAMP response element of the MyoD1 promoter and negatively modulates MyoD1 expression in dividing myoblasts.
    J Biol Chem. 1994 Mar 4;269(9):6978-85 PMID: 8120060
  3. MyoD family: a paradigm for development?
    Genes Dev. 1990 Sep;4(9):1454-61 PMID: 2253873
  4. The myoD gene family: nodal point during specification of the muscle cell lineage.
    Science. 1991 Feb 15;251(4995):761-6 PMID: 1846704
  5. Potentiation of MyoD1 activity by 5-aza-2'-deoxycytidine.
    Cell Growth Differ. 1990 Aug;1(8):383-92 PMID: 1703777
  6. Paired MyoD-binding sites regulate myosin light chain gene expression.
    Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1242-6 PMID: 1847512
  7. An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene.
    Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1815-9 PMID: 2000388
  8. Myogenesis and developmental control genes.
    Curr Opin Cell Biol. 1990 Dec;2(6):1065-75 PMID: 2099799
  9. The interaction of transcription factors with nucleosomal DNA.
    Bioessays. 1992 Sep;14(9):597-603 PMID: 1365915
  10. 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
  11. Mitogenic repression of myogenin autoregulation.
    J Biol Chem. 1991 Nov 15;266(32):21343-6 PMID: 1718977
  12. Characterisation of a genomic clone covering the structural mouse MyoD1 gene and its promoter region.
    Nucleic Acids Res. 1991 Dec 11;19(23):6433-9 PMID: 1754380
  13. Repression of genes by DNA methylation depends on CpG density and promoter strength: evidence for involvement of a methyl-CpG binding protein.
    EMBO J. 1992 Jan;11(1):327-33 PMID: 1310933
  14. Methylation of an alpha-foetoprotein gene intragenic site modulates gene activity.
    Nucleic Acids Res. 1992 Jan 25;20(2):171-8 PMID: 1371343
  15. Regulation of muscle cell growth and differentiation by the MyoD family of helix-loop-helix proteins.
    Adv Cancer Res. 1992;58:95-119 PMID: 1312291
  16. Fos and Jun repress transcriptional activation by myogenin and MyoD: the amino terminus of Jun can mediate repression.
    Genes Dev. 1992 Apr;6(4):676-89 PMID: 1313772
  17. Direct homeodomain-DNA interaction in the autoregulation of the fushi tarazu gene.
    Nature. 1992 Apr 30;356(6372):804-7 PMID: 1574120
  18. Differential trans-activation of muscle-specific regulatory elements including the mysosin light chain box by chicken MyoD, myogenin, and MRF4.
    J Biol Chem. 1992 May 15;267(14):10031-8 PMID: 1374396
  19. Purification, sequence, and cellular localization of a novel chromosomal protein that binds to methylated DNA.
    Cell. 1992 Jun 12;69(6):905-14 PMID: 1606614
  20. The essentials of DNA methylation.
    Cell. 1992 Jul 10;70(1):5-8 PMID: 1377983
  21. Making muscle in mammals.
    Trends Genet. 1992 Apr;8(4):144-8 PMID: 1321521
  22. Genomic sequencing.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991-5 PMID: 6326095
  23. Induction of alpha-fetoprotein synthesis in differentiating F9 teratocarcinoma cells is accompanied by a genome-wide loss of DNA methylation.
    Mol Cell Biol. 1984 May;4(5):898-907 PMID: 6203029
  24. Differentiation of two mouse cell lines is associated with hypomethylation of their genomes.
    Mol Cell Biol. 1984 Sep;4(9):1800-6 PMID: 6092940
  25. Muscle-specific activation of a methylated chimeric actin gene.
    Cell. 1986 Aug 1;46(3):409-16 PMID: 3731275
  26. Firefly luciferase gene: structure and expression in mammalian cells.
    Mol Cell Biol. 1987 Feb;7(2):725-37 PMID: 3821727
  27. Positive and negative regulation of transcription in vitro: enhancer-binding protein AP-2 is inhibited by SV40 T antigen.
    Cell. 1987 Sep 11;50(6):847-61 PMID: 3040262
  28. Expression of a single transfected cDNA converts fibroblasts to myoblasts.
    Cell. 1987 Dec 24;51(6):987-1000 PMID: 3690668
  29. MyoD1: a nuclear phosphoprotein requiring a Myc homology region to convert fibroblasts to myoblasts.
    Science. 1988 Oct 21;242(4877):405-11 PMID: 3175662
  30. Gene structure and transcription in mouse cells with extensively demethylated DNA.
    Mol Cell Biol. 1989 Mar;9(3):885-92 PMID: 2471061
  31. A partial methylation profile for a CpG site is stably maintained in mammalian tissues and cultured cell lines.
    J Biol Chem. 1989 Jul 15;264(20):11632-6 PMID: 2545677
  32. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD.
    Proc Natl Acad Sci U S A. 1989 Jul;86(14):5434-8 PMID: 2748593
  33. Positive autoregulation of the myogenic determination gene MyoD1.
    Cell. 1989 Jul 28;58(2):241-8 PMID: 2546677
  34. Autoregulation--a common property of eukaryotic transcription factors?
    Trends Genet. 1989 May;5(5):131-3 PMID: 2569243
  35. 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
  36. How fixed is the differentiated state? Lessons from heterokaryons.
    Trends Genet. 1989 Aug;5(8):268-72 PMID: 2686116
  37. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins.
    Cell. 1990 Apr 6;61(1):49-59 PMID: 2156629
  38. Effect of cell history on response to helix-loop-helix family of myogenic regulators.
    Nature. 1990 Mar 29;344(6265):454-8 PMID: 2157160
  39. Determination genes.
    Curr Opin Cell Biol. 1989 Dec;1(6):1075-80 PMID: 2561452
  40. Transcription control and differentiation: the HLH family, c-myc and C/EBP.
    Curr Opin Cell Biol. 1989 Dec;1(6):1081-7 PMID: 2561453
  41. Muscle cell differentiation.
    Curr Opin Cell Biol. 1989 Dec;1(6):1094-101 PMID: 2699798
  42. Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor alpha-subunit gene.
    Nature. 1990 May 24;345(6273):353-5 PMID: 2342565
  43. Differential trans activation associated with the muscle regulatory factors MyoD1, myogenin, and MRF4.
    Mol Cell Biol. 1990 Aug;10(8):3934-44 PMID: 1695319
  44. Autoregulation of pit-1 gene expression mediated by two cis-active promoter elements.
    Nature. 1990 Aug 9;346(6284):583-6 PMID: 2142999
  45. Differentiation requires continuous active control.
    Annu Rev Biochem. 1992;61:1213-30 PMID: 1497309
  46. Chromatin structure and gene expression.
    Curr Opin Cell Biol. 1992 Jun;4(3):436-43 PMID: 1497914
  47. Hemimethylation and hypersensitivity are early events in transcriptional reactivation of human inactive X-linked genes in a hamster x human somatic cell hybrid.
    Mol Cell Biol. 1992 Sep;12(9):3819-26 PMID: 1380647
  48. Characterization of MeCP2, a vertebrate DNA binding protein with affinity for methylated DNA.
    Nucleic Acids Res. 1992 Oct 11;20(19):5085-92 PMID: 1408825
  49. The repressor MDBP-2 is a member of the histone H1 family that binds preferentially in vitro and in vivo to methylated nonspecific DNA sequences.
    Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9499-503 PMID: 1409659
  50. Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death.
    Cell. 1992 Oct 30;71(3):369-82 PMID: 1423602
  51. Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development.
    Cell. 1992 Oct 30;71(3):383-90 PMID: 1330322
  52. Interplay between proliferation and differentiation within the myogenic lineage.
    Dev Biol. 1992 Dec;154(2):261-72 PMID: 1330787
  53. Myogenic cell lineages.
    Dev Biol. 1992 Dec;154(2):284-98 PMID: 1426639
  54. MHox: a mesodermally restricted homeodomain protein that binds an essential site in the muscle creatine kinase enhancer.
    Development. 1992 Aug;115(4):1087-101 PMID: 1360403
  55. FGF inactivates myogenic helix-loop-helix proteins through phosphorylation of a conserved protein kinase C site in their DNA-binding domains.
    Cell. 1992 Dec 24;71(7):1181-94 PMID: 1335366
  56. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation.
    Cell. 1993 Feb 12;72(3):309-24 PMID: 8381715
  57. Regulation of the mouse desmin gene: transactivated by MyoD, myogenin, MRF4 and Myf5.
    Nucleic Acids Res. 1993 Jan 25;21(2):335-43 PMID: 8382796
  58. Transcriptional regulation of multigene loci: multilevel control.
    Trends Genet. 1993 Apr;9(4):134-7 PMID: 8516848
  59. Role of gene order in developmental control of human gamma- and beta-globin gene expression.
    Mol Cell Biol. 1993 Aug;13(8):4836-43 PMID: 8336720
  60. An E box mediates activation and repression of the acetylcholine receptor delta-subunit gene during myogenesis.
    Mol Cell Biol. 1993 Sep;13(9):5133-40 PMID: 8355673
  61. HLH forced dimers: tethering MyoD to E47 generates a dominant positive myogenic factor insulated from negative regulation by Id.
    Cell. 1993 Sep 24;74(6):1033-42 PMID: 7691411
  62. Role for DNA methylation in genomic imprinting.
    Nature. 1993 Nov 25;366(6453):362-5 PMID: 8247133
  63. Hypomethylation of the interphotoreceptor retinoid-binding protein (IRBP) promotor and first exon is linked to expression of the gene.
    Nucleic Acids Res. 1990 Sep 11;18(17):5181-7 PMID: 2402443
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
0305-1048
Published
1994-06-25
Pages
2234-41
Language
English
Region
England
NLM ID
0411011
PMCID
PMC523679
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: product@genelibs.com