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. 1992 Oct;11(10):3777–3786. doi: 10.1002/j.1460-2075.1992.tb05463.x

Alternating d(G-A) sequences form a parallel-stranded DNA homoduplex.

K Rippe 1, V Fritsch 1, E Westhof 1, T M Jovin 1
PMCID: PMC556838  PMID: 1396571

Abstract

The oligonucleotides d[(G-A)7G] and d[(G-A)12G] self-associate under physiological conditions (10 mM MgCl2, neutral pH) into a stable double-helical structure (psRR-DNA) in which the two polypurine strands are in a parallel orientation in contrast to the antiparallel disposition of conventional B-DNA. We have characterized psRR-DNA by gel electrophoresis, UV absorption, vacuum UV circular dichroism, monomer-excimer fluorescence of oligonucleotides end-labelled with pyrene, and chemical probing with diethyl pyrocarbonate and dimethyl sulfate. The duplex is stable at pH 4-9, suggesting that the structure is compatible with, but does not require, protonation of the A residues. The data support a model derived from force-field analysis in which the parallel-stranded d(G-A)n helix is right-handed and constituted of alternating, symmetrical Gsyn.Gsyn and Aanti.Aanti base pairs with N1H...O6 and N6H...N7 hydrogen bonds, respectively. This dinucleotide structure may be the source of a negative peak observed at 190 nm in the vacuum UV CD spectrum, a feature previously reported only for left-handed Z-DNA. The related sequence d[(GAAGGA)4G] also forms a parallel-stranded duplex but one that is less stable and probably involves a slightly different secondary structure. We discuss the potential intervention of psRR-DNA in recombination, gene expression and the stabilization of genomic structure.

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Selected References

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  1. Antao V. P., Gray D. M., Ratliff R. L. CD of six different conformational rearrangements of poly[d(A-G).d(C-T)] induced by low pH. Nucleic Acids Res. 1988 Jan 25;16(2):719–738. doi: 10.1093/nar/16.2.719. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BOLLUM F. J., GROENIGER E., YONEDA M. POLYDEOXYADENYLIC ACID. Proc Natl Acad Sci U S A. 1964 May;51:853–859. doi: 10.1073/pnas.51.5.853. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bernués J., Beltrán R., Casasnovas J. M., Azorín F. Structural polymorphism of homopurine--homopyrimidine sequences: the secondary DNA structure adopted by a d(GA.CT)22 sequence in the presence of zinc ions. EMBO J. 1989 Jul;8(7):2087–2094. doi: 10.1002/j.1460-2075.1989.tb03617.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Collier D. A., Griffin J. A., Wells R. D. Non-B right-handed DNA conformations of homopurine.homopyrimidine sequences in the murine immunoglobulin C alpha switch region. J Biol Chem. 1988 May 25;263(15):7397–7405. [PubMed] [Google Scholar]
  5. Hakoshima T., Fukui T., Ikehara M., Tomita K. Molecular structure of a double helix that has non-Watson-Crick type base pairing formed by 2-substituted poly(A) and poly(U). Proc Natl Acad Sci U S A. 1981 Dec;78(12):7309–7313. doi: 10.1073/pnas.78.12.7309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Htun H., Dahlberg J. E. Single strands, triple strands, and kinks in H-DNA. Science. 1988 Sep 30;241(4874):1791–1796. doi: 10.1126/science.3175620. [DOI] [PubMed] [Google Scholar]
  7. Kang C., Zhang X., Ratliff R., Moyzis R., Rich A. Crystal structure of four-stranded Oxytricha telomeric DNA. Nature. 1992 Mar 12;356(6365):126–131. doi: 10.1038/356126a0. [DOI] [PubMed] [Google Scholar]
  8. Klysik J., Rippe K., Jovin T. M. Reactivity of parallel-stranded DNA to chemical modification reagents. Biochemistry. 1990 Oct 23;29(42):9831–9839. doi: 10.1021/bi00494a012. [DOI] [PubMed] [Google Scholar]
  9. Kung H. J., Hu S., Bender W., Bailey J. M., Davidson N., Nicolson M. O., McAllister R. M. RD-114, baboon, and woolly monkey viral RNA's compared in size and structure. Cell. 1976 Apr;7(4):609–620. doi: 10.1016/0092-8674(76)90211-7. [DOI] [PubMed] [Google Scholar]
  10. Lee J. S., Evans D. H., Morgan A. R. Polypurine DNAs and RNAs form secondary structures which may be tetra-stranded. Nucleic Acids Res. 1980 Sep 25;8(18):4305–4320. doi: 10.1093/nar/8.18.4305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lee J. S., Johnson D. A., Morgan A. R. Complexes formed by (pyrimidine)n . (purine)n DNAs on lowering the pH are three-stranded. Nucleic Acids Res. 1979 Jul 11;6(9):3073–3091. doi: 10.1093/nar/6.9.3073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Lee J. S. The stability of polypurine tetraplexes in the presence of mono- and divalent cations. Nucleic Acids Res. 1990 Oct 25;18(20):6057–6060. doi: 10.1093/nar/18.20.6057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lyamichev V. I., Mirkin S. M., Frank-Kamenetskii M. D. Structures of homopurine-homopyrimidine tract in superhelical DNA. J Biomol Struct Dyn. 1986 Feb;3(4):667–669. doi: 10.1080/07391102.1986.10508454. [DOI] [PubMed] [Google Scholar]
  14. Lyamichev V. I., Voloshin O. N., Frank-Kamenetskii M. D., Soyfer V. N. Photofootprinting of DNA triplexes. Nucleic Acids Res. 1991 Apr 11;19(7):1633–1638. doi: 10.1093/nar/19.7.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Manor H., Rao B. S., Martin R. G. Abundance and degree of dispersion of genomic d(GA)n.d(TC)n sequences. J Mol Evol. 1988;27(2):96–101. doi: 10.1007/BF02138367. [DOI] [PubMed] [Google Scholar]
  16. Palecek E. Local supercoil-stabilized DNA structures. Crit Rev Biochem Mol Biol. 1991;26(2):151–226. doi: 10.3109/10409239109081126. [DOI] [PubMed] [Google Scholar]
  17. Parniewski P., Galazka G., Wilk A., Klysik J. Complex structural behavior of oligopurine-oligopyrimidine sequence cloned within the supercoiled plasmid. Nucleic Acids Res. 1989 Jan 25;17(2):617–629. doi: 10.1093/nar/17.2.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. RICH A., DAVIES D. R., CRICK F. H., WATSON J. D. The molecular structure of polyadenylic acid. J Mol Biol. 1961 Feb;3:71–86. doi: 10.1016/s0022-2836(61)80009-0. [DOI] [PubMed] [Google Scholar]
  20. Ramsing N. B., Jovin T. M. Parallel stranded duplex DNA. Nucleic Acids Res. 1988 Jul 25;16(14A):6659–6676. doi: 10.1093/nar/16.14.6659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ramsing N. B., Rippe K., Jovin T. M. Helix-coil transition of parallel-stranded DNA. Thermodynamics of hairpin and linear duplex oligonucleotides. Biochemistry. 1989 Nov 28;28(24):9528–9535. doi: 10.1021/bi00450a042. [DOI] [PubMed] [Google Scholar]
  22. Reaban M. E., Griffin J. A. Induction of RNA-stabilized DNA conformers by transcription of an immunoglobulin switch region. Nature. 1990 Nov 22;348(6299):342–344. doi: 10.1038/348342a0. [DOI] [PubMed] [Google Scholar]
  23. Riazance J. H., Johnson W. C., Jr, McIntosh L. P., Jovin T. M. Vacuum UV circular dichroism is diagnostic for the left-handed Z form of poly [d(A-C).d(G-T)] and other polydeoxynucleotides. Nucleic Acids Res. 1987 Sep 25;15(18):7627–7636. doi: 10.1093/nar/15.18.7627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rippe K., Jovin T. M. Parallel-stranded duplex DNA. Methods Enzymol. 1992;211:199–220. doi: 10.1016/0076-6879(92)11013-9. [DOI] [PubMed] [Google Scholar]
  25. Rippe K., Ramsing N. B., Jovin T. M. Spectroscopic properties and helical stabilities of 25-nt parallel-stranded linear DNA duplexes. Biochemistry. 1989 Nov 28;28(24):9536–9541. doi: 10.1021/bi00450a043. [DOI] [PubMed] [Google Scholar]
  26. Rippe K., Ramsing N. B., Klement R., Jovin T. M. A parallel stranded linear DNA duplex incorporating dG.dC base pairs. J Biomol Struct Dyn. 1990 Jun;7(6):1199–1209. doi: 10.1080/07391102.1990.10508559. [DOI] [PubMed] [Google Scholar]
  27. Sarma M. H., Gupta G., Sarma R. H. A cytosine . cytosine base paired parallel DNA double helix with thymine . thymine bulges. FEBS Lett. 1986 Sep 15;205(2):223–229. doi: 10.1016/0014-5793(86)80902-4. [DOI] [PubMed] [Google Scholar]
  28. Sen D., Gilbert W. Formation of parallel four-stranded complexes by guanine-rich motifs in DNA and its implications for meiosis. Nature. 1988 Jul 28;334(6180):364–366. doi: 10.1038/334364a0. [DOI] [PubMed] [Google Scholar]
  29. Shimizu M., Hanvey J. C., Wells R. D. Intramolecular DNA triplexes in supercoiled plasmids. I. Effect of loop size on formation and stability. J Biol Chem. 1989 Apr 5;264(10):5944–5949. [PubMed] [Google Scholar]
  30. Smith F. W., Feigon J. Quadruplex structure of Oxytricha telomeric DNA oligonucleotides. Nature. 1992 Mar 12;356(6365):164–168. doi: 10.1038/356164a0. [DOI] [PubMed] [Google Scholar]
  31. Son T. D., Guschlbauer W., Guéron M. Flexibility and conformations of guanosine monophosphates by the Overhauser effect. J Am Chem Soc. 1972 Nov 1;94(22):7903–7911. doi: 10.1021/ja00777a038. [DOI] [PubMed] [Google Scholar]
  32. Sprecher C. A., Johnson W. C., Jr Circular dichroism of the nucleic acid monomers. Biopolymers. 1977 Oct;16(10):2243–2264. doi: 10.1002/bip.1977.360161012. [DOI] [PubMed] [Google Scholar]
  33. Stavnezer J. Triple helix stabilization? Nature. 1991 Jun 6;351(6326):447–448. doi: 10.1038/351447b0. [DOI] [PubMed] [Google Scholar]
  34. Sundquist W. I., Klug A. Telomeric DNA dimerizes by formation of guanine tetrads between hairpin loops. Nature. 1989 Dec 14;342(6251):825–829. doi: 10.1038/342825a0. [DOI] [PubMed] [Google Scholar]
  35. Tavale S. S., Sobell H. M. Crystal and molecular structure of 8-bromoguanosine and 8-bromoadenosine, two purine nucleosides in the syn conformation. J Mol Biol. 1970 Feb 28;48(1):109–123. doi: 10.1016/0022-2836(70)90222-6. [DOI] [PubMed] [Google Scholar]
  36. Tripathi J., Brahmachari S. K. Distribution of simple repetitive (TG/CA)n and (CT/AG)n sequences in human and rodent genomes. J Biomol Struct Dyn. 1991 Oct;9(2):387–397. doi: 10.1080/07391102.1991.10507919. [DOI] [PubMed] [Google Scholar]
  37. Wang A. H., Quigley G. J., Kolpak F. J., Crawford J. L., van Boom J. H., van der Marel G., Rich A. Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature. 1979 Dec 13;282(5740):680–686. doi: 10.1038/282680a0. [DOI] [PubMed] [Google Scholar]
  38. Wells R. D., Collier D. A., Hanvey J. C., Shimizu M., Wohlrab F. The chemistry and biology of unusual DNA structures adopted by oligopurine.oligopyrimidine sequences. FASEB J. 1988 Nov;2(14):2939–2949. [PubMed] [Google Scholar]
  39. Westhof E., Dumas P., Moras D. Crystallographic refinement of yeast aspartic acid transfer RNA. J Mol Biol. 1985 Jul 5;184(1):119–145. doi: 10.1016/0022-2836(85)90048-8. [DOI] [PubMed] [Google Scholar]
  40. Westhof E., Rao S. T., Sundaralingam M. Crystallographic studies of drug-nucleic acid interactions: proflavine intercalation between the non-complementary base-pairs of cytidilyl-3',5'-adenosine. J Mol Biol. 1980 Sep 25;142(3):331–361. doi: 10.1016/0022-2836(80)90276-4. [DOI] [PubMed] [Google Scholar]
  41. Williamson J. R., Raghuraman M. K., Cech T. R. Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell. 1989 Dec 1;59(5):871–880. doi: 10.1016/0092-8674(89)90610-7. [DOI] [PubMed] [Google Scholar]
  42. Yagil G. Paranemic structures of DNA and their role in DNA unwinding. Crit Rev Biochem Mol Biol. 1991;26(5-6):475–559. doi: 10.3109/10409239109086791. [DOI] [PubMed] [Google Scholar]
  43. Yee H. A., Wong A. K., van de Sande J. H., Rattner J. B. Identification of novel single-stranded d(TC)n binding proteins in several mammalian species. Nucleic Acids Res. 1991 Feb 25;19(4):949–953. doi: 10.1093/nar/19.4.949. [DOI] [PMC free article] [PubMed] [Google Scholar]

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