Home LiteratureArticle Details
PMID: 15908587 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Formation and properties of hairpin and tetraplex structures of guanine-rich regulatory sequences of muscle-specific genes.

Nucleic acids research ·Vol. 33 ·No. 9 ·2005-00-00 ·Pages 2887-900

Yafe A, Etzioni S, Weisman-Shomer P, Fry M

Abstract

Clustered guanine residues in DNA readily generate hairpin or a variety of tetrahelical structures. The myogenic determination protein MyoD was reported to bind to a tetrahelical structure of guanine-rich enhancer sequence of muscle creatine kinase (MCK) more tightly than to its target E-box motif [K. Walsh and A. Gualberto (1992) J. Biol. Chem., 267, 13714-13718], suggesting that tetraplex structures of regulatory sequences of muscle-specific genes could contribute to transcriptional regulation. In the current study we show that promoter or enhancer sequences of various muscle-specific genes display a disproportionately high incidence of guanine clusters. The sequences derived from the guanine-rich promoter or enhancer regions of three muscle-specific genes, human sarcomeric mitochondrial creatine kinase (sMtCK), mouse MCK and alpha7 integrin formed diverse secondary structures. The sMtCK sequence folded into a hairpin structure; the alpha7 integrin oligonucleotide generated a unimolecular tetraplex; and sequences from all three genes associated to generate bimolecular tetraplexes. Furthermore, two neighboring non-contiguous guanine-rich tracts in the alpha7 integrin promoter region also paired to form a tetraplex structure. We also show that homodimeric MyoD bound bimolecular tetraplex structures of muscle-specific regulatory sequences more efficiently than its target E-box motif. These results are consistent with a role of tetrahelical structures of DNA in the regulation of muscle-specific gene expression.

MeSH Terms
Antigens, CD/genetics Base Sequence Creatine Kinase/genetics Creatine Kinase, MM Form Creatine Kinase, Mitochondrial Form DNA/chemistry E-Box Elements Enhancer Elements, Genetic G-Quadruplexes Guanine/analysis Integrin alpha Chains/genetics Isoenzymes/genetics Molecular Sequence Data Muscles/metabolism MyoD Protein/metabolism Nucleic Acid Conformation Porphyrins/chemistry Promoter Regions, Genetic Temperature
Chemicals
Antigens, CD Integrin alpha Chains Isoenzymes MyoD Protein Porphyrins integrin alpha7 Guanine DNA Creatine Kinase Creatine Kinase, MM Form Creatine Kinase, Mitochondrial Form
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Yafe Anat
Department of Biochemistry, Rappaport Faculty of Medicine, Technion-Israel Institute of Technology PO Box 9649 Bat Galim, Haifa 31096, Israel.
Etzioni Shulamit
Weisman-Shomer Pnina
Fry Michael
References (63)
63 references, click to expand
  1. The cationic porphyrin TMPyP4 down-regulates c-MYC and human telomerase reverse transcriptase expression and inhibits tumor growth in vivo.
    Mol Cancer Ther. 2002 Jun;1(8):565-73 PMID: 12479216
  2. Did quadruplex DNA play a role in the evolution of the eukaryotic linear chromosome?
    Mini Rev Med Chem. 2003 Feb;3(1):1-9 PMID: 12570850
  3. The cationic porphyrin TMPyP4 destabilizes the tetraplex form of the fragile X syndrome expanded sequence d(CGG)n.
    Nucleic Acids Res. 2003 Jul 15;31(14):3963-70 PMID: 12853612
  4. Intracellular transcription of G-rich DNAs induces formation of G-loops, novel structures containing G4 DNA.
    Genes Dev. 2004 Jul 1;18(13):1618-29 PMID: 15231739
  5. Propeller-type parallel-stranded G-quadruplexes in the human c-myc promoter.
    J Am Chem Soc. 2004 Jul 21;126(28):8710-6 PMID: 15250723
  6. Detection of quadruplex DNA structures in human telomeres by a fluorescent carbazole derivative.
    Anal Chem. 2004 Aug 1;76(15):4490-4 PMID: 15283592
  7. Destabilization of tetraplex structures of the fragile X repeat sequence (CGG)n is mediated by homolog-conserved domains in three members of the hnRNP family.
    Nucleic Acids Res. 2004;32(14):4145-54 PMID: 15302914
  8. Unusual DNA structure of the diabetes susceptibility locus IDDM2 and its effect on transcription by the insulin promoter factor Pur-1/MAZ.
    Proc Natl Acad Sci U S A. 2000 Nov 7;97(23):12508-12 PMID: 11070077
  9. Cationic porphyrins promote the formation of i-motif DNA and bind peripherally by a nonintercalative mechanism.
    Biochemistry. 2000 Dec 12;39(49):15083-90 PMID: 11106486
  10. Functional and dysfunctional roles of quadruplex DNA in cells.
    Chem Biol. 2001 Mar;8(3):221-30 PMID: 11306347
  11. G-quadruplex DNA structures--variations on a theme.
    Biol Chem. 2001 Apr;382(4):621-8 PMID: 11405224
  12. In vitro generated antibodies specific for telomeric guanine-quadruplex DNA react with Stylonychia lemnae macronuclei.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8572-7 PMID: 11438689
  13. Selective interactions of cationic porphyrins with G-quadruplex structures.
    J Am Chem Soc. 2001 Sep 19;123(37):8902-13 PMID: 11552797
  14. A human nuclease specific for G4 DNA.
    Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12444-9 PMID: 11675489
  15. Binding and partial denaturing of G-quartet DNA by Cdc13p of Saccharomyces cerevisiae.
    J Biol Chem. 2001 Dec 14;276(50):47671-4 PMID: 11585819
  16. Biological aspects of DNA/RNA quadruplexes.
    Biopolymers. 2000-2001;56(3):209-27 PMID: 11745112
  17. Quadruplex-interactive agents as telomerase inhibitors: synthesis of porphyrins and structure-activity relationship for the inhibition of telomerase.
    J Med Chem. 2001 Dec 20;44(26):4509-23 PMID: 11741471
  18. Promoter-specific regulation of MyoD binding and signal transduction cooperate to pattern gene expression.
    Mol Cell. 2002 Mar;9(3):587-600 PMID: 11931766
  19. Crystal structure of parallel quadruplexes from human telomeric DNA.
    Nature. 2002 Jun 20;417(6891):876-80 PMID: 12050675
  20. Direct evidence for a G-quadruplex in a promoter region and its targeting with a small molecule to repress c-MYC transcription.
    Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11593-8 PMID: 12195017
  21. G4 DNA unwinding by BLM and Sgs1p: substrate specificity and substrate-specific inhibition.
    Nucleic Acids Res. 2002 Sep 15;30(18):3954-61 PMID: 12235379
  22. Unfolding of quadruplex structure in the G-rich strand of the minisatellite repeat by the binding protein UP1.
    Proc Natl Acad Sci U S A. 2002 Oct 1;99(20):12685-90 PMID: 12235355
  23. Porphyrin binding to quadrupled T4G4.
    Biochemistry. 1998 Mar 3;37(9):2709-14 PMID: 9537740
  24. Fluorescent dyes specific for quadruplex DNA.
    Nucleic Acids Res. 1998 Aug 15;26(16):3724-8 PMID: 9685488
  25. The Bloom's syndrome helicase unwinds G4 DNA.
    J Biol Chem. 1998 Oct 16;273(42):27587-92 PMID: 9765292
  26. The Saccharomyces cerevisiae Sgs1 helicase efficiently unwinds G-G paired DNAs.
    Nucleic Acids Res. 1999 May 1;27(9):1978-84 PMID: 10198430
  27. Human werner syndrome DNA helicase unwinds tetrahelical structures of the fragile X syndrome repeat sequence d(CGG)n.
    J Biol Chem. 1999 Apr 30;274(18):12797-802 PMID: 10212265
  28. Stabilization of the c-myc gene promoter quadruplex by specific ligands' inhibitors of telomerase.
    Biochem Biophys Res Commun. 2004 Oct 22;323(3):802-8 PMID: 15381071
  29. Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis.
    Nature. 1988 Jul 28;334(6180):364-6 PMID: 3393228
  30. Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops.
    Nature. 1989 Dec 14;342(6251):825-9 PMID: 2601741
  31. Inhibition of telomerase by G-quartet DNA structures.
    Nature. 1991 Apr 25;350(6320):718-20 PMID: 2023635
  32. Structural characterization and tissue-specific expression of the mRNAs encoding isoenzymes from two rat mitochondrial creatine kinase genes.
    Biochim Biophys Acta. 1991 Jul 23;1089(3):352-61 PMID: 1859839
  33. Regulatory element analysis and structural characterization of the human sarcomeric mitochondrial creatine kinase gene.
    J Biol Chem. 1991 Sep 25;266(27):18058-65 PMID: 1917943
  34. The human insulin gene linked polymorphic region exhibits an altered DNA structure.
    Nucleic Acids Res. 1992 Jan 25;20(2):231-6 PMID: 1741248
  35. Laminin-binding integrin alpha 7 beta 1: functional characterization and expression in normal and malignant melanocytes.
    Cell Regul. 1991 Oct;2(10):805-17 PMID: 1839357
  36. Integrins: versatility, modulation, and signaling in cell adhesion.
    Cell. 1992 Apr 3;69(1):11-25 PMID: 1555235
  37. Sr2+ facilitates intermolecular G-quadruplex formation of telomeric sequences.
    Biochemistry. 1992 Apr 21;31(15):3769-76 PMID: 1567831
  38. MyoD binds to the guanine tetrad nucleic acid structure.
    J Biol Chem. 1992 Jul 5;267(19):13714-8 PMID: 1320026
  39. Thermodynamics of G-tetraplex formation by telomeric DNAs.
    Biochemistry. 1993 Jan 19;32(2):598-601 PMID: 8422371
  40. QUAD, a protein from hepatocyte chromatin that binds selectively to guanine-rich quadruplex DNA.
    J Biol Chem. 1993 Feb 15;268(5):3306-12 PMID: 8429007
  41. Identification and characterization of a nuclease activity specific for G4 tetrastranded DNA.
    Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3157-61 PMID: 8475054
  42. The beta subunit of Oxytricha telomere-binding protein promotes G-quartet formation by telomeric DNA.
    Cell. 1993 Sep 10;74(5):875-85 PMID: 8374954
  43. Characterization of a G-quartet formation reaction promoted by the beta-subunit of the Oxytricha telomere-binding protein.
    Biochemistry. 1993 Nov 2;32(43):11646-57 PMID: 8218232
  44. A protein from Tetrahymena thermophila that specifically binds parallel-stranded G4-DNA.
    Biochemistry. 1994 Mar 1;33(8):2240-6 PMID: 7509637
  45. The yeast telomere-binding protein RAP1 binds to and promotes the formation of DNA quadruplexes in telomeric DNA.
    EMBO J. 1994 May 15;13(10):2411-20 PMID: 8194531
  46. The fragile X syndrome d(CGG)n nucleotide repeats form a stable tetrahelical structure.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):4950-4 PMID: 8197163
  47. The yeast KEM1 gene encodes a nuclease specific for G4 tetraplex DNA: implication of in vivo functions for this novel DNA structure.
    Cell. 1994 Jul 1;77(7):1083-92 PMID: 8020096
  48. Promotion of parallel DNA quadruplexes by a yeast telomere binding protein: a circular dichroism study.
    Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7658-62 PMID: 8052638
  49. Developmental expression of sarcomeric and ubiquitous mitochondrial creatine kinase is tissue-specific.
    Biochim Biophys Acta. 1994 Sep 13;1219(1):33-8 PMID: 8086475
  50. A novel K(+)-dependent DNA synthesis arrest site in a commonly occurring sequence motif in eukaryotes.
    J Biol Chem. 1994 Oct 28;269(43):27029-35 PMID: 7929444
  51. Tissue-specific gene activation by MyoD: determination of specificity by cis-acting repression elements.
    Genes Dev. 1994 Sep 15;8(18):2203-11 PMID: 7958889
  52. Expression of the mitochondrial creatine kinase genes.
    Mol Cell Biochem. 1994 Apr-May;133-134:235-43 PMID: 7808456
  53. A yeast gene product, G4p2, with a specific affinity for quadruplex nucleic acids.
    J Biol Chem. 1995 Apr 21;270(16):9413-9 PMID: 7721866
  54. CGG repeats associated with DNA instability and chromosome fragility form structures that block DNA synthesis in vitro.
    Nucleic Acids Res. 1995 Oct 25;23(20):4202-9 PMID: 7479085
  55. The fragile X syndrome single strand d(CGG)n nucleotide repeats readily fold back to form unimolecular hairpin structures.
    J Biol Chem. 1995 Dec 1;270(48):28970-7 PMID: 7499428
  56. The chicken beta-globin gene promoter forms a novel "cinched" tetrahelical structure.
    J Biol Chem. 1996 Mar 1;271(9):5208-14 PMID: 8617804
  57. Identification and characterization of the cell type-specific and developmentally regulated alpha7 integrin gene promoter.
    J Biol Chem. 1996 Sep 13;271(37):22915-22 PMID: 8798472
  58. Purification and characterization of qTBP42, a new single-stranded and quadruplex telomeric DNA-binding protein from rat hepatocytes.
    J Biol Chem. 1997 Feb 14;272(7):4474-82 PMID: 9020172
  59. A mouse cytoplasmic exoribonuclease (mXRN1p) with preference for G4 tetraplex substrates.
    J Cell Biol. 1997 Feb 24;136(4):761-73 PMID: 9049243
  60. Purification, characterization and molecular cloning of TGP1, a novel G-DNA binding protein from Tetrahymena thermophila.
    Nucleic Acids Res. 1998 Apr 1;26(7):1613-20 PMID: 9512530
  61. Tetrahelical forms of the fragile X syndrome expanded sequence d(CGG)(n) are destabilized by two heterogeneous nuclear ribonucleoprotein-related telomeric DNA-binding proteins.
    J Biol Chem. 2000 Jan 21;275(3):2231-8 PMID: 10636930
  62. Yeast meiosis-specific protein Hop1 binds to G4 DNA and promotes its formation.
    Mol Cell Biol. 2000 Feb;20(4):1361-9 PMID: 10648621
  63. Human Ku antigen tightly binds and stabilizes a tetrahelical form of the Fragile X syndrome d(CGG)n expanded sequence.
    J Biol Chem. 2000 Oct 20;275(42):33134-41 PMID: 10924524
Article Info
Journal
Nucleic acids research
Abbr.
Nucleic Acids Res
ISSN
1362-4962
Published
2005-00-00
Epub
2005-00-20
Pages
2887-900
Language
English
Region
England
NLM ID
0411011
PMCID
PMC1133794
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