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. 1982 Jun;79(11):3584–3588. doi: 10.1073/pnas.79.11.3584

Tissue specificity and clustering of methylated cystosines in bovine satellite I DNA.

H Sano, R Sager
PMCID: PMC346466  PMID: 6954504

Abstract

The positions of all 5-methylcytosine (mC) residues in bovine satellite I DNA were determined by sequence analysis of native purified satellite I DNAs from three bovine tissues as well as from cloned DNA. The EcoRI cleavage units from thymus and liver were found to contain 1,402 residues; that from brain contained 1,401 residues. Satellite I DNA from thymus contained a total of 5.0% mC, whereas that from liver and brain contained 4.4% and 2.6% mC, respectively. Thus, the extent of methylation of this DNA is tissue-specific. So is the location. In each tissue, the location of mCs is nonrandom, consisting of three clusters of heavily methylated regions, each of about 200 bases. However, the extent of methylation within each cluster is tissue-specific. The mCs are located entirely in C-G doublets and primarily in palindromic sequences, C-C-G-G sequences (10 methylatable sites) are almost completely methylated in all tissues examined, but T-G-G-A sequences (16 methylated in all tissues examined, but T-G-G-A sequences (16 metylatable sites) are methylated to different extents in each tissue. Neither the tissue specificity of methylation nor the clustering pattern is detectable by examining only G-C-G-G sites, leading us to emphasize the importance of total sequence determination for genomic DNAs in studies of methylation. The clustering pattern, which is preserved despite a 2-fold difference in mC content between brain and thymus, may indicate a role for DNA methylation in chromatin structure.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bird A., Taggart M., Macleod D. Loss of rDNA methylation accompanies the onset of ribosomal gene activity in early development of X. laevis. Cell. 1981 Nov;26(3 Pt 1):381–390. doi: 10.1016/0092-8674(81)90207-5. [DOI] [PubMed] [Google Scholar]
  2. Challberg M. D., Englund P. T. Specific labeling of 3' termini with T4 DNA polymerase. Methods Enzymol. 1980;65(1):39–43. doi: 10.1016/s0076-6879(80)65008-3. [DOI] [PubMed] [Google Scholar]
  3. Compere S. J., Palmiter R. D. DNA methylation controls the inducibility of the mouse metallothionein-I gene lymphoid cells. Cell. 1981 Jul;25(1):233–240. doi: 10.1016/0092-8674(81)90248-8. [DOI] [PubMed] [Google Scholar]
  4. Ehrlich M., Wang R. Y. 5-Methylcytosine in eukaryotic DNA. Science. 1981 Jun 19;212(4501):1350–1357. doi: 10.1126/science.6262918. [DOI] [PubMed] [Google Scholar]
  5. Felsenfeld G. Chromatin. Nature. 1978 Jan 12;271(5641):115–122. doi: 10.1038/271115a0. [DOI] [PubMed] [Google Scholar]
  6. Friedland P., Kedes L., Brutlag D., Iwasaki Y., Bach R. GENESIS, a knowledge-based genetic engineering simulation system for representation of genetic data and experiment planning. Nucleic Acids Res. 1982 Jan 11;10(1):323–340. doi: 10.1093/nar/10.1.323. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gaillard C., Doly J., Cortadas J., Bernardi G. The primary structure of bovine satellite 1.715. Nucleic Acids Res. 1981 Nov 25;9(22):6069–6082. doi: 10.1093/nar/9.22.6069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Groudine M., Eisenman R., Weintraub H. Chromatin structure of endogenous retroviral genes and activation by an inhibitor of DNA methylation. Nature. 1981 Jul 23;292(5821):311–317. doi: 10.1038/292311a0. [DOI] [PubMed] [Google Scholar]
  9. Holland M. J., Holland J. P., Jackson K. A. Cloning of yeast genes coding for glycolytic enzymes. Methods Enzymol. 1979;68:408–419. doi: 10.1016/0076-6879(79)68030-8. [DOI] [PubMed] [Google Scholar]
  10. Katz L., Kingsbury D. T., Helinski D. R. Stimulation by cyclic adenosine monophosphate of plasmid deoxyribonucleic acid replication and catabolite repression of the plasmid deoxyribonucleic acid-protein relaxation complex. J Bacteriol. 1973 May;114(2):577–591. doi: 10.1128/jb.114.2.577-591.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lipchitz L., Axel R. Restriction endonuclease cleavage of satellite DNA in intact bovine nuclei. Cell. 1976 Oct;9(2):355–364. doi: 10.1016/0092-8674(76)90125-2. [DOI] [PubMed] [Google Scholar]
  12. Mandel J. L., Chambon P. DNA methylation: organ specific variations in the methylation pattern within and around ovalbumin and other chicken genes. Nucleic Acids Res. 1979 Dec 20;7(8):2081–2103. doi: 10.1093/nar/7.8.2081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  14. McGhee J. D., Felsenfeld G. Nucleosome structure. Annu Rev Biochem. 1980;49:1115–1156. doi: 10.1146/annurev.bi.49.070180.005343. [DOI] [PubMed] [Google Scholar]
  15. McGhee J. D., Ginder G. D. Specific DNA methylation sites in the vicinity of the chicken beta-globin genes. Nature. 1979 Aug 2;280(5721):419–420. doi: 10.1038/280419a0. [DOI] [PubMed] [Google Scholar]
  16. McGhee J. D., Wood W. I., Dolan M., Engel J. D., Felsenfeld G. A 200 base pair region at the 5' end of the chicken adult beta-globin gene is accessible to nuclease digestion. Cell. 1981 Nov;27(1 Pt 2):45–55. doi: 10.1016/0092-8674(81)90359-7. [DOI] [PubMed] [Google Scholar]
  17. Mohandas T., Sparkes R. S., Shapiro L. J. Reactivation of an inactive human X chromosome: evidence for X inactivation by DNA methylation. Science. 1981 Jan 23;211(4480):393–396. doi: 10.1126/science.6164095. [DOI] [PubMed] [Google Scholar]
  18. Naveh-Many T., Cedar H. Active gene sequences are undermethylated. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4246–4250. doi: 10.1073/pnas.78.7.4246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ohmori H., Tomizawa J. I., Maxam A. M. Detection of 5-methylcytosine in DNA sequences. Nucleic Acids Res. 1978 May;5(5):1479–1485. doi: 10.1093/nar/5.5.1479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Pellicer A., Robins D., Wold B., Sweet R., Jackson J., Lowy I., Roberts J. M., Sim G. K., Silverstein S., Axel R. Altering genotype and phenotype by DNA-mediated gene transfer. Science. 1980 Sep 19;209(4463):1414–1422. doi: 10.1126/science.7414320. [DOI] [PubMed] [Google Scholar]
  21. Razin A., Cedar H. Distribution of 5-methylcytosine in chromatin. Proc Natl Acad Sci U S A. 1977 Jul;74(7):2725–2728. doi: 10.1073/pnas.74.7.2725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Razin A., Riggs A. D. DNA methylation and gene function. Science. 1980 Nov 7;210(4470):604–610. doi: 10.1126/science.6254144. [DOI] [PubMed] [Google Scholar]
  23. Roychoudhury R., Wu R. Terminal transferase-catalyzed addition of nucleotides to the 3' termini of DNA. Methods Enzymol. 1980;65(1):43–62. doi: 10.1016/s0076-6879(80)65009-5. [DOI] [PubMed] [Google Scholar]
  24. Sager R., Grabowy C., Sano H. The mat-1 gene in Chlamydomonas regulates DNA methylation during gametogenesis. Cell. 1981 Apr;24(1):41–47. doi: 10.1016/0092-8674(81)90499-2. [DOI] [PubMed] [Google Scholar]
  25. Sager R., Kitchin R. Selective silencing of eukaryotic DNA. Science. 1975 Aug 8;189(4201):426–433. [PubMed] [Google Scholar]
  26. Sano H., Royer H. D., Sager R. Identification of 5-methylcytosine in DNA fragments immobilized on nitrocellulose paper. Proc Natl Acad Sci U S A. 1980 Jun;77(6):3581–3585. doi: 10.1073/pnas.77.6.3581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shen C. K., Maniatis T. Tissue-specific DNA methylation in a cluster of rabbit beta-like globin genes. Proc Natl Acad Sci U S A. 1980 Nov;77(11):6634–6638. doi: 10.1073/pnas.77.11.6634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Singer J., Roberts-Ems J., Luthardt F. W., Riggs A. D. Methylation of DNA in mouse early embryos, teratocarcinoma cells and adult tissues of mouse and rabbit. Nucleic Acids Res. 1979 Dec 20;7(8):2369–2385. doi: 10.1093/nar/7.8.2369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Solage A., Cedar H. Organization of 5-methylcytosine in chromosomal DNA. Biochemistry. 1978 Jul 11;17(14):2934–2938. doi: 10.1021/bi00607a036. [DOI] [PubMed] [Google Scholar]
  30. Weintraub H., Larsen A., Groudine M. Alpha-Globin-gene switching during the development of chicken embryos: expression and chromosome structure. Cell. 1981 May;24(2):333–344. doi: 10.1016/0092-8674(81)90323-8. [DOI] [PubMed] [Google Scholar]
  31. Yagi M., Koshland M. E. Expression of the J chain gene during B cell differentiation is inversely correlated with DNA methylation. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4907–4911. doi: 10.1073/pnas.78.8.4907. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. van der Ploeg L. H., Flavell R. A. DNA methylation in the human gamma delta beta-globin locus in erythroid and nonerythroid tissues. Cell. 1980 Apr;19(4):947–958. doi: 10.1016/0092-8674(80)90086-0. [DOI] [PubMed] [Google Scholar]

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