Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1997 Sep;73(3):1553–1561. doi: 10.1016/S0006-3495(97)78187-6

Crystal structure of d(GCGCGCG) with 5'-overhang G residues.

B Pan 1, C Ban 1, M C Wahl 1, M Sundaralingam 1
PMCID: PMC1181054  PMID: 9284322

Abstract

The crystal structure of the DNA heptamer d(GCGCGCG) has been solved at 1.65 A resolution by the molecular replacement method and refined to an R-value of 0.184 for 3598 reflections. The heptamer forms a Z-DNA d(CGCGCG)2 with 5'-overhang G residues instead of an A-DNA d(GCGCGC)2 with 3'-overhang G residues. The overhang G residues from parallel strands of two adjacent duplexes form a trans reverse Hoogsteen G x G basepair that stacks on the six Z-DNA basepairs to produce a pseudocontinuous helix. The reverse Hoogsteen G x G basepair is unusual in that the displacement of one G base relative to the other allows them to participate in a bifurcated (G1)N2 . . . N7(G8) and an enhanced (G8)C8-H . . . O6(G1) hydrogen bond, in addition to the two usual hydrogen bonds. The 5'-overhang G residues are anti and C2'-endo while the 3'-terminal G residues are syn and C2'-endo. The conformations of both G residues are different from the syn/C3'-endo for the guanosine in a standard Z-DNA. The two cobalt hexammine ions bind to the phosphate groups in both GpC and CpG steps in Z(I) and Z(II) conformations. The water structure motif is similar to the other Z-DNA structures.

Full text

PDF
1554

Selected References

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

  1. Ban C., Ramakrishnan B., Sundaralingam M. Crystal structure of the self-complementary 5'-purine start decamer d(GCGCGCGCGC) in the Z-DNA conformation. I. Biophys J. 1996 Sep;71(3):1215–1221. doi: 10.1016/S0006-3495(96)79350-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Behe M., Felsenfeld G. Effects of methylation on a synthetic polynucleotide: the B--Z transition in poly(dG-m5dC).poly(dG-m5dC). Proc Natl Acad Sci U S A. 1981 Mar;78(3):1619–1623. doi: 10.1073/pnas.78.3.1619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berman H. M., Olson W. K., Beveridge D. L., Westbrook J., Gelbin A., Demeny T., Hsieh S. H., Srinivasan A. R., Schneider B. The nucleic acid database. A comprehensive relational database of three-dimensional structures of nucleic acids. Biophys J. 1992 Sep;63(3):751–759. doi: 10.1016/S0006-3495(92)81649-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bingman C., Jain S., Zon G., Sundaralingam M. Crystal and molecular structure of the alternating dodecamer d(GCGTACGTACGC) in the A-DNA form: comparison with the isomorphous non-alternating dodecamer d(CCGTACGTACGG). Nucleic Acids Res. 1992 Dec 25;20(24):6637–6647. doi: 10.1093/nar/20.24.6637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Brennan R. G., Westhof E., Sundaralingam M. Structure of a Z-DNA with two different backbone chain conformations. Stabilization of the decadeoxyoligonucleotide d(CGTACGTACG) by [Co(NH3)6]3+ binding to the guanine. J Biomol Struct Dyn. 1986 Feb;3(4):649–665. doi: 10.1080/07391102.1986.10508453. [DOI] [PubMed] [Google Scholar]
  6. Brown T., Kneale G., Hunter W. N., Kennard O. Structural characterisation of the bromouracil.guanine base pair mismatch in a Z-DNA fragment. Nucleic Acids Res. 1986 Feb 25;14(4):1801–1809. doi: 10.1093/nar/14.4.1801. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chen X., Ramakrishnan B., Rao S. T., Sundaralingam M. Binding of two distamycin A molecules in the minor groove of an alternating B-DNA duplex. Nat Struct Biol. 1994 Mar;1(3):169–175. doi: 10.1038/nsb0394-169. [DOI] [PubMed] [Google Scholar]
  8. Cruse W. B., Salisbury S. A., Brown T., Cosstick R., Eckstein F., Kennard O. Chiral phosphorothioate analogues of B-DNA. The crystal structure of Rp-d[Gp(S)CpGp(S)CpGp(S)C]. J Mol Biol. 1986 Dec 20;192(4):891–905. doi: 10.1016/0022-2836(86)90035-5. [DOI] [PubMed] [Google Scholar]
  9. Egli M., Gessner R. V., Williams L. D., Quigley G. J., van der Marel G. A., van Boom J. H., Rich A., Frederick C. A. Atomic-resolution structure of the cellulose synthase regulator cyclic diguanylic acid. Proc Natl Acad Sci U S A. 1990 Apr;87(8):3235–3239. doi: 10.1073/pnas.87.8.3235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fujii S., Wang A. H., Quigley G. J., Westerink H., Van der Marel G., Van Boom J. H., Rich A. The octamers d(CGCGCGCG) and d(CGCATGCG) both crystallize as Z-DNA in the same hexagonal lattice. Biopolymers. 1985 Jan;24(1):243–250. doi: 10.1002/bip.360240118. [DOI] [PubMed] [Google Scholar]
  11. Fujii S., Wang A. H., van der Marel G., van Boom J. H., Rich A. Molecular structure of (m5 dC-dG)3: the role of the methyl group on 5-methyl cytosine in stabilizing Z-DNA. Nucleic Acids Res. 1982 Dec 11;10(23):7879–7892. doi: 10.1093/nar/10.23.7879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gessner R. V., Quigley G. J., Egli M. Comparative studies of high resolution Z-DNA crystal structures. Part 1: Common hydration patterns of alternating dC-dG. J Mol Biol. 1994 Mar 4;236(4):1154–1168. doi: 10.1016/0022-2836(94)90018-3. [DOI] [PubMed] [Google Scholar]
  13. Gessner R. V., Quigley G. J., Wang A. H., van der Marel G. A., van Boom J. H., Rich A. Structural basis for stabilization of Z-DNA by cobalt hexaammine and magnesium cations. Biochemistry. 1985 Jan 15;24(2):237–240. doi: 10.1021/bi00323a001. [DOI] [PubMed] [Google Scholar]
  14. Gruskin E. A., Rich A. B-DNA to Z-DNA structural transitions in the SV40 enhancer: stabilization of Z-DNA in negatively supercoiled DNA minicircles. Biochemistry. 1993 Mar 9;32(9):2167–2176. doi: 10.1021/bi00060a007. [DOI] [PubMed] [Google Scholar]
  15. Ho P. S., Frederick C. A., Quigley G. J., van der Marel G. A., van Boom J. H., Wang A. H., Rich A. G.T wobble base-pairing in Z-DNA at 1.0 A atomic resolution: the crystal structure of d(CGCGTG). EMBO J. 1985 Dec 16;4(13A):3617–3623. doi: 10.1002/j.1460-2075.1985.tb04125.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jain S., Zon G., Sundaralingam M. The potentially Z-DNA-forming sequence d(GTGTACAC) crystallizes as A-DNA. J Mol Biol. 1987 Sep 5;197(1):141–145. doi: 10.1016/0022-2836(87)90616-4. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Kumar V. D., Harrison R. W., Andrews L. C., Weber I. T. Crystal structure at 1.5-A resolution of d(CGCICICG), an octanucleotide containing inosine, and its comparison with d(CGCG) and d(CGCGCG) structures. Biochemistry. 1992 Feb 11;31(5):1541–1550. doi: 10.1021/bi00120a035. [DOI] [PubMed] [Google Scholar]
  19. Laughlan G., Murchie A. I., Norman D. G., Moore M. H., Moody P. C., Lilley D. M., Luisi B. The high-resolution crystal structure of a parallel-stranded guanine tetraplex. Science. 1994 Jul 22;265(5171):520–524. doi: 10.1126/science.8036494. [DOI] [PubMed] [Google Scholar]
  20. Lukomski S., Wells R. D. Left-handed Z-DNA and in vivo supercoil density in the Escherichia coli chromosome. Proc Natl Acad Sci U S A. 1994 Oct 11;91(21):9980–9984. doi: 10.1073/pnas.91.21.9980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Malinina L., Urpí L., Salas X., Huynh-Dinh T., Subirana J. A. Recombination-like structure of d(CCGCGG). J Mol Biol. 1994 Oct 28;243(3):484–493. doi: 10.1006/jmbi.1994.1674. [DOI] [PubMed] [Google Scholar]
  22. Mooers B. H., Schroth G. P., Baxter W. W., Ho P. S. Alternating and non-alternating dG-dC hexanucleotides crystallize as canonical A-DNA. J Mol Biol. 1995 Jun 16;249(4):772–784. doi: 10.1006/jmbi.1995.0336. [DOI] [PubMed] [Google Scholar]
  23. Pietrasanta L. I., Schaper A., Jovin T. M. Probing specific molecular conformations with the scanning force microscope. Complexes of plasmid DNA and anti-Z-DNA antibodies. Nucleic Acids Res. 1994 Aug 25;22(16):3288–3292. doi: 10.1093/nar/22.16.3288. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pohl F. M., Jovin T. M. Salt-induced co-operative conformational change of a synthetic DNA: equilibrium and kinetic studies with poly (dG-dC). J Mol Biol. 1972 Jun 28;67(3):375–396. doi: 10.1016/0022-2836(72)90457-3. [DOI] [PubMed] [Google Scholar]
  25. Quadrifoglio F., Manzini G., Yathindra N. Short oligodeoxynucleotides with d(G-C)n sequence do not assume left-handed conformation in high salt conditions. J Mol Biol. 1984 May 25;175(3):419–423. doi: 10.1016/0022-2836(84)90358-9. [DOI] [PubMed] [Google Scholar]
  26. Ramakrishnan B., Sundaralingam M. High resolution crystal structure of the A-DNA decamer d(CCCGGCCGGG). Novel intermolecular base-paired G*(G.C) triplets. J Mol Biol. 1993 May 20;231(2):431–444. doi: 10.1006/jmbi.1993.1292. [DOI] [PubMed] [Google Scholar]
  27. Senior M., Jones R. A., Breslauer K. J. Influence of dangling thymidine residues on the stability and structure of two DNA duplexes. Biochemistry. 1988 May 17;27(10):3879–3885. doi: 10.1021/bi00410a053. [DOI] [PubMed] [Google Scholar]
  28. Skelly J. V., Edwards K. J., Jenkins T. C., Neidle S. Crystal structure of an oligonucleotide duplex containing G.G base pairs: influence of mispairing on DNA backbone conformation. Proc Natl Acad Sci U S A. 1993 Feb 1;90(3):804–808. doi: 10.1073/pnas.90.3.804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Teng M. K., Liaw Y. C., van der Marel G. A., van Boom J. H., Wang A. H. Effects of the O2' hydroxyl group on Z-DNA conformation: structure of Z-RNA and (araC)-[Z-DNA]. Biochemistry. 1989 Jun 13;28(12):4923–4928. doi: 10.1021/bi00438a001. [DOI] [PubMed] [Google Scholar]
  30. Van Meervelt L., Vlieghe D., Dautant A., Gallois B., Précigoux G., Kennard O. High-resolution structure of a DNA helix forming (C.G)*G base triplets. Nature. 1995 Apr 20;374(6524):742–744. doi: 10.1038/374742a0. [DOI] [PubMed] [Google Scholar]
  31. Vlieghe D., Van Meervelt L., Dautant A., Gallois B., Précigoux G., Kennard O. Parallel and antiparallel (G.GC)2 triple helix fragments in a crystal structure. Science. 1996 Sep 20;273(5282):1702–1705. doi: 10.1126/science.273.5282.1702. [DOI] [PubMed] [Google Scholar]
  32. Wahl M. C., Rao S. T., Sundaralingam M. The structure of r(UUCGCG) has a 5'-UU-overhang exhibiting Hoogsteen-like trans U.U base pairs. Nat Struct Biol. 1996 Jan;3(1):24–31. doi: 10.1038/nsb0196-24. [DOI] [PubMed] [Google Scholar]
  33. Wang A. H., Hakoshima T., van der Marel G., van Boom J. H., Rich A. AT base pairs are less stable than GC base pairs in Z-DNA: the crystal structure of d(m5CGTAm5CG). Cell. 1984 May;37(1):321–331. doi: 10.1016/0092-8674(84)90328-3. [DOI] [PubMed] [Google Scholar]
  34. 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]
  35. Yoon C., Privé G. G., Goodsell D. S., Dickerson R. E. Structure of an alternating-B DNA helix and its relationship to A-tract DNA. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6332–6336. doi: 10.1073/pnas.85.17.6332. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Zhang S., Lockshin C., Herbert A., Winter E., Rich A. Zuotin, a putative Z-DNA binding protein in Saccharomyces cerevisiae. EMBO J. 1992 Oct;11(10):3787–3796. doi: 10.1002/j.1460-2075.1992.tb05464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES