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PMID: 7638194 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

5-Methyl-2'-deoxycytidine in single-stranded DNA can act in cis to signal de novo DNA methylation.

Christman JK, Sheikhnejad G, Marasco CJ, Sufrin JR

Abstract

Methylation of cytosine residues in DNA plays an important role in regulating gene expression during vertebrate embryonic development. Conversely, disruption of normal patterns of methylation is common in tumors and occurs early in progression of some human cancers. In vertebrates, it appears that the same DNA methyltransferase maintains preexisting patterns of methylation during DNA replication and carries out de novo methylation to create new methylation patterns. There are several indications that inherent signals in DNA structure can act in vivo to initiate or block de novo methylation in adjacent DNA regions. To identify sequences capable of enhancing de novo methylation of DNA in vitro, we designed a series of oligodeoxyribonucleotide substrates with substrate cytosine residues in different sequence contexts. We obtained evidence that some 5-methylcytosine residues in these single-stranded DNAs can stimulate de novo methylation of adjacent sites by murine DNA 5-cytosine methyltransferase as effectively as 5-methylcytosine residues in double-stranded DNA stimulate maintenance methylation. This suggests that double-stranded DNA may not be the primary natural substrate for de novo methylation and that looped single-stranded structures formed during the normal course of DNA replication or repair serve as "nucleation" sites for de novo methylation of adjacent DNA regions.

MeSH Terms
Animals Base Sequence Binding Sites/genetics DNA, Single-Stranded/chemistry,genetics,metabolism DNA-Cytosine Methylases/metabolism Deoxycytidine/analogs & derivatives,metabolism Enzyme Activation Gene Expression Regulation Genetic Complementation Test Humans In Vitro Techniques Methylation Mice Models, Biological Molecular Sequence Data Oligodeoxyribonucleotides/chemistry,genetics,metabolism Signal Transduction Substrate Specificity
Chemicals
DNA, Single-Stranded Oligodeoxyribonucleotides Deoxycytidine 5-methyldeoxycytidine DNA-Cytosine Methylases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Christman J K
Molecular Oncology Program, Michigan Cancer Foundation, Detroit, USA.
Sheikhnejad G
Marasco C J
Sufrin J R
References (31)
31 references, click to expand
  1. Mechanism of human methyl-directed DNA methyltransferase and the fidelity of cytosine methylation.
    Proc Natl Acad Sci U S A. 1992 May 15;89(10):4744-8 PMID: 1584813
  2. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality.
    Cell. 1992 Jun 12;69(6):915-26 PMID: 1606615
  3. DNA looping.
    Annu Rev Biochem. 1992;61:199-223 PMID: 1497310
  4. A cis-acting element accounts for a conserved methylation pattern upstream of the mouse adenine phosphoribosyltransferase gene.
    J Biol Chem. 1993 Jan 5;268(1):552-8 PMID: 8416960
  5. DNA methylation and genomic imprinting in mammals.
    EXS. 1993;64:469-86 PMID: 8418956
  6. The cysteine conserved among DNA cytosine methylases is required for methyl transfer, but not for specific DNA binding.
    Nucleic Acids Res. 1993 Jan 25;21(2):295-301 PMID: 8441637
  7. Effects of DNA methylation on DNA-binding proteins and gene expression.
    Curr Opin Genet Dev. 1993 Apr;3(2):226-31 PMID: 8504247
  8. Eukaryotic DNA replication: anatomy of an origin.
    Annu Rev Biochem. 1993;62:29-63 PMID: 8352592
  9. HhaI methyltransferase flips its target base out of the DNA helix.
    Cell. 1994 Jan 28;76(2):357-69 PMID: 8293469
  10. Enhancement of reporter gene de novo methylation by DNA fragments from the alpha-fetoprotein control region.
    J Biol Chem. 1994 Jan 21;269(3):1821-6 PMID: 7507485
  11. Unusual DNA structures, chromatin and transcription.
    Bioessays. 1994 Jan;16(1):59-68 PMID: 8141807
  12. 5-Methylcytosine in eukaryotic DNA.
    Science. 1981 Jun 19;212(4501):1350-7 PMID: 6262918
  13. Inhibition of DNA methyltransferase and induction of Friend erythroleukemia cell differentiation by 5-azacytidine and 5-aza-2'-deoxycytidine.
    J Biol Chem. 1982 Feb 25;257(4):2041-8 PMID: 6173384
  14. Tissue-specific differences in DNA methylation in various mammals.
    Biochim Biophys Acta. 1983 Jun 24;740(2):212-9 PMID: 6860672
  15. Two DNA methyltransferases from murine erythroleukemia cells: purification, sequence specificity, and mode of interaction with DNA.
    Proc Natl Acad Sci U S A. 1983 Sep;80(18):5559-63 PMID: 6577443
  16. DNA methylation and gene activity.
    Annu Rev Biochem. 1983;52:93-124 PMID: 6311083
  17. Establishment of de novo DNA methylation patterns. Transcription factor binding and deoxycytidine methylation at CpG and non-CpG sequences in an integrated adenovirus promoter.
    J Mol Biol. 1990 Aug 5;214(3):673-83 PMID: 2143784
  18. Recognition of unusual DNA structures by human DNA (cytosine-5)methyltransferase.
    J Mol Biol. 1991 Jan 5;217(1):39-51 PMID: 1988679
  19. Direct identification of the active-site nucleophile in a DNA (cytosine-5)-methyltransferase.
    Biochemistry. 1991 Nov 19;30(46):11018-25 PMID: 1932026
  20. Recognition of foldback DNA by the human DNA (cytosine-5-)-methyltransferase.
    Biochemistry. 1992 Jan 28;31(3):850-4 PMID: 1731943
  21. Distinct hypermethylation patterns occur at altered chromosome loci in human lung and colon cancer.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1929-33 PMID: 1347428
  22. 5-methylcytosine, gene regulation, and cancer.
    Adv Cancer Res. 1983;40:1-30 PMID: 6197868
  23. DNA methylation in friend erythroleukemia cells: the effects of chemically induced differentiation and of treatment with inhibitors of DNA methylation.
    Curr Top Microbiol Immunol. 1984;108:49-78 PMID: 6201322
  24. Chromatin structure and de novo methylation of sperm DNA: implications for activation of the paternal genome.
    Science. 1985 May 31;228(4703):1061-8 PMID: 2986289
  25. Primary DNA sequence determines sites of maintenance and de novo methylation by mammalian DNA methyltransferases.
    Mol Cell Biol. 1986 Apr;6(4):1135-40 PMID: 3023872
  26. 5-Fluorocytosine in DNA is a mechanism-based inhibitor of HhaI methylase.
    Biochemistry. 1988 Jul 12;27(14):5204-10 PMID: 3167042
  27. Cloning and sequencing of a cDNA encoding DNA methyltransferase of mouse cells. The carboxyl-terminal domain of the mammalian enzymes is related to bacterial restriction methyltransferases.
    J Mol Biol. 1988 Oct 20;203(4):971-83 PMID: 3210246
  28. Mechanisms of X-chromosome regulation.
    Annu Rev Genet. 1988;22:199-233 PMID: 3071248
  29. Genomic sequencing reveals a 5-methylcytosine-free domain in active promoters and the spreading of preimposed methylation patterns.
    Proc Natl Acad Sci U S A. 1989 May;86(10):3728-32 PMID: 2524831
  30. Rapid appearance of hypomethylated DNA in livers of rats fed cancer-promoting, methyl-deficient diets.
    Cancer Res. 1989 Aug 1;49(15):4094-7 PMID: 2743304
  31. DNA methylation and development.
    Biochim Biophys Acta. 1990 May 24;1049(1):1-8 PMID: 1694091
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1995-08-01
Pages
7347-51
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC41336
Subset
IM
Grants
NCI NIH HHS · CA1303 · United States
NCI NIH HHS · CA16056 · United States
NCI NIH HHS · CA45028 · United States
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