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. 1996 Oct 15;319(Pt 2):607–611. doi: 10.1042/bj3190607

Nucleosome core particles inhibit DNA triple helix formation.

P M Brown 1, K R Fox 1
PMCID: PMC1217810  PMID: 8912701

Abstract

We have used DNase I footprinting to examine the formation of DNA triple helices at target sites on DNA fragments that have been reconstituted with nucleosome core particles. We show that a 12 bp homopurine target site, located 45 bp from the end of the 160 bp tyrT(46A) fragment, cannot be targeted with either parallel (CT-containing) or antiparallel (GT-containing) triplex-forming oligonucleotides when reconstituted on to nucleosome core particles. Binding is not facilitated by the presence of a triplex-binding ligand. However, both parallel and antiparallel triplexes could be formed on a truncated DNA fragment in which the target site was located closer to the end of the DNA fragment. We suggest that intermolecular DNA triplexes can only be formed on those DNA regions that are less tightly associated with the protein core.

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Selected References

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

  1. Arnott S., Selsing E. Structures for the polynucleotide complexes poly(dA) with poly (dT) and poly(dT) with poly(dA) with poly (dT). J Mol Biol. 1974 Sep 15;88(2):509–521. doi: 10.1016/0022-2836(74)90498-7. [DOI] [PubMed] [Google Scholar]
  2. Beal P. A., Dervan P. B. Second structural motif for recognition of DNA by oligonucleotide-directed triple-helix formation. Science. 1991 Mar 15;251(4999):1360–1363. doi: 10.1126/science.2003222. [DOI] [PubMed] [Google Scholar]
  3. Brown P. M., Drabble A., Fox K. R. Effect of a triplex-binding ligand on triple helix formation at a site within a natural DNA fragment. Biochem J. 1996 Mar 1;314(Pt 2):427–432. doi: 10.1042/bj3140427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cassidy S. A., Strekowski L., Wilson W. D., Fox K. R. Effect of a triplex-binding ligand on parallel and antiparallel DNA triple helices using short unmodified and acridine-linked oligonucleotides. Biochemistry. 1994 Dec 27;33(51):15338–15347. doi: 10.1021/bi00255a015. [DOI] [PubMed] [Google Scholar]
  5. Chandler S. P., Strekowski L., Wilson W. D., Fox K. R. Footprinting studies on ligands which stabilize DNA triplexes: effects on stringency within a parallel triple helix. Biochemistry. 1995 May 30;34(21):7234–7242. doi: 10.1021/bi00021a039. [DOI] [PubMed] [Google Scholar]
  6. Chen F. M. Intramolecular triplex formation of the purine.purine.pyrimidine type. Biochemistry. 1991 May 7;30(18):4472–4479. doi: 10.1021/bi00232a014. [DOI] [PubMed] [Google Scholar]
  7. Drew H. R., Calladine C. R. Sequence-specific positioning of core histones on an 860 base-pair DNA. Experiment and theory. J Mol Biol. 1987 May 5;195(1):143–173. doi: 10.1016/0022-2836(87)90333-0. [DOI] [PubMed] [Google Scholar]
  8. Drew H. R., Travers A. A. DNA bending and its relation to nucleosome positioning. J Mol Biol. 1985 Dec 20;186(4):773–790. doi: 10.1016/0022-2836(85)90396-1. [DOI] [PubMed] [Google Scholar]
  9. FELSENFELD G., RICH A. Studies on the formation of two- and three-stranded polyribonucleotides. Biochim Biophys Acta. 1957 Dec;26(3):457–468. doi: 10.1016/0006-3002(57)90091-4. [DOI] [PubMed] [Google Scholar]
  10. Felsenfeld G. Chromatin as an essential part of the transcriptional mechanism. Nature. 1992 Jan 16;355(6357):219–224. doi: 10.1038/355219a0. [DOI] [PubMed] [Google Scholar]
  11. Finch J. T., Lutter L. C., Rhodes D., Brown R. S., Rushton B., Levitt M., Klug A. Structure of nucleosome core particles of chromatin. Nature. 1977 Sep 1;269(5623):29–36. doi: 10.1038/269029a0. [DOI] [PubMed] [Google Scholar]
  12. Fox K. R., Waring M. J. DNA structural variations produced by actinomycin and distamycin as revealed by DNAase I footprinting. Nucleic Acids Res. 1984 Dec 21;12(24):9271–9285. doi: 10.1093/nar/12.24.9271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hayes J. J., Tullius T. D., Wolffe A. P. The structure of DNA in a nucleosome. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7405–7409. doi: 10.1073/pnas.87.19.7405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Howard F. B., Miles H. T., Liu K., Frazier J., Raghunathan G., Sasisekharan V. Structure of d(T)n.d(A)n.d(T)n: the DNA triple helix has B-form geometry with C2'-endo sugar pucker. Biochemistry. 1992 Nov 10;31(44):10671–10677. doi: 10.1021/bi00159a005. [DOI] [PubMed] [Google Scholar]
  15. Kunkel G. R., Martinson H. G. Nucleosomes will not form on double-stranded RNa or over poly(dA).poly(dT) tracts in recombinant DNA. Nucleic Acids Res. 1981 Dec 21;9(24):6869–6888. doi: 10.1093/nar/9.24.6869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Le Doan T., Perrouault L., Praseuth D., Habhoub N., Decout J. L., Thuong N. T., Lhomme J., Hélène C. Sequence-specific recognition, photocrosslinking and cleavage of the DNA double helix by an oligo-[alpha]-thymidylate covalently linked to an azidoproflavine derivative. Nucleic Acids Res. 1987 Oct 12;15(19):7749–7760. doi: 10.1093/nar/15.19.7749. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Low C. M., Drew H. R., Waring M. J. Echinomycin and distamycin induce rotation of nucleosome core DNA. Nucleic Acids Res. 1986 Sep 11;14(17):6785–6801. doi: 10.1093/nar/14.17.6785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Low C. M., Drew H. R., Waring M. J. Sequence-specific binding of echinomycin to DNA: evidence for conformational changes affecting flanking sequences. Nucleic Acids Res. 1984 Jun 25;12(12):4865–4879. doi: 10.1093/nar/12.12.4865. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Malkov V. A., Voloshin O. N., Soyfer V. N., Frank-Kamenetskii M. D. Cation and sequence effects on stability of intermolecular pyrimidine-purine-purine triplex. Nucleic Acids Res. 1993 Feb 11;21(3):585–591. doi: 10.1093/nar/21.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Moser H. E., Dervan P. B. Sequence-specific cleavage of double helical DNA by triple helix formation. Science. 1987 Oct 30;238(4827):645–650. doi: 10.1126/science.3118463. [DOI] [PubMed] [Google Scholar]
  21. Pennings S., Muyldermans S., Meersseman G., Wyns L. Formation, stability and core histone positioning of nucleosomes reassembled on bent and other nucleosome-derived DNA. J Mol Biol. 1989 May 5;207(1):183–192. doi: 10.1016/0022-2836(89)90449-x. [DOI] [PubMed] [Google Scholar]
  22. Pilch D. S., Levenson C., Shafer R. H. Structure, stability, and thermodynamics of a short intermolecular purine-purine-pyrimidine triple helix. Biochemistry. 1991 Jun 25;30(25):6081–6088. doi: 10.1021/bi00239a001. [DOI] [PubMed] [Google Scholar]
  23. Portugal J., Waring M. J. Antibiotics which can alter the rotational orientation of nucleosome core DNA. Nucleic Acids Res. 1986 Nov 25;14(22):8735–8754. doi: 10.1093/nar/14.22.8735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Ramsay N. Deletion analysis of a DNA sequence that positions itself precisely on the nucleosome core. J Mol Biol. 1986 May 5;189(1):179–188. doi: 10.1016/0022-2836(86)90389-x. [DOI] [PubMed] [Google Scholar]
  25. Richmond T. J., Finch J. T., Rushton B., Rhodes D., Klug A. Structure of the nucleosome core particle at 7 A resolution. Nature. 1984 Oct 11;311(5986):532–537. doi: 10.1038/311532a0. [DOI] [PubMed] [Google Scholar]
  26. Satchwell S. C., Drew H. R., Travers A. A. Sequence periodicities in chicken nucleosome core DNA. J Mol Biol. 1986 Oct 20;191(4):659–675. doi: 10.1016/0022-2836(86)90452-3. [DOI] [PubMed] [Google Scholar]
  27. Shrader T. E., Crothers D. M. Artificial nucleosome positioning sequences. Proc Natl Acad Sci U S A. 1989 Oct;86(19):7418–7422. doi: 10.1073/pnas.86.19.7418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Travers A. A. DNA conformation and protein binding. Annu Rev Biochem. 1989;58:427–452. doi: 10.1146/annurev.bi.58.070189.002235. [DOI] [PubMed] [Google Scholar]
  29. Washbrook E., Fox K. R. Comparison of antiparallel A.AT and T.AT triplets within an alternate strand DNA triple helix. Nucleic Acids Res. 1994 Sep 25;22(19):3977–3982. doi: 10.1093/nar/22.19.3977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Westin L., Blomquist P., Milligan J. F., Wrange O. Triple helix DNA alters nucleosomal histone-DNA interactions and acts as a nucleosome barrier. Nucleic Acids Res. 1995 Jun 25;23(12):2184–2191. doi: 10.1093/nar/23.12.2184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wilson W. D., Tanious F. A., Mizan S., Yao S., Kiselyov A. S., Zon G., Strekowski L. DNA triple-helix specific intercalators as antigene enhancers: unfused aromatic cations. Biochemistry. 1993 Oct 12;32(40):10614–10621. doi: 10.1021/bi00091a011. [DOI] [PubMed] [Google Scholar]
  32. Wolffe A. P. Nucleosome positioning and modification: chromatin structures that potentiate transcription. Trends Biochem Sci. 1994 Jun;19(6):240–244. doi: 10.1016/0968-0004(94)90148-1. [DOI] [PubMed] [Google Scholar]
  33. de los Santos C., Rosen M., Patel D. NMR studies of DNA (R+)n.(Y-)n.(Y+)n triple helices in solution: imino and amino proton markers of T.A.T and C.G.C+ base-triple formation. Biochemistry. 1989 Sep 5;28(18):7282–7289. doi: 10.1021/bi00444a021. [DOI] [PubMed] [Google Scholar]

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