Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1997 Jul;73(1):76–87. doi: 10.1016/S0006-3495(97)78049-4

Base-base and deoxyribose-base stacking interactions in B-DNA and Z-DNA: a quantum-chemical study.

J Sponer 1, H A Gabb 1, J Leszczynski 1, P Hobza 1
PMCID: PMC1180910  PMID: 9199773

Abstract

Base-stacking interactions in canonical and crystal B-DNA and in Z-DNA steps are studied using the ab initio quantum-chemical method with inclusion of electron correlation. The stacking energies in canonical B-DNA base-pair steps vary from -9.5 kcal/mol (GG) to -13.2 kcal/mol (GC). The many-body nonadditivity term, although rather small in absolute value, influences the sequence dependence of stacking energy. The base-stacking energies calculated for CGC and a hypothetical TAT sequence in Z-configuration are similar to those in B-DNA. Comparison with older quantum-chemical studies shows that they do not provide even a qualitatively correct description of base stacking. We also evaluate the base-(deoxy)ribose stacking geometry that occurs in Z-DNA and in nucleotides linked by 2',5'-phosphodiester bonds. Although the molecular orbital analysis does not rule out the charge-transfer n-pi* interaction of the sugar 04' with the aromatic base, the base-sugar contact is stabilized by dispersion energy similar to that of stacked bases. The stabilization amounts to almost 4 kcal/mol and is thus comparable to that afforded by normal base-base stacking. This enhancement of the total stacking interaction could contribute to the propensity of short d(CG)n sequences to adopt the Z-conformation.

Full text

PDF
80

Images in this article

79FIGURE 2
on p.79
83FIGURE 4
on p.83

Selected References

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

  1. Aida M. An ab initio molecular orbital study on the sequence-dependency of DNA conformation: an evaluation of intra- and inter-strand stacking interaction energy. J Theor Biol. 1988 Feb 7;130(3):327–335. doi: 10.1016/s0022-5193(88)80032-8. [DOI] [PubMed] [Google Scholar]
  2. Arnott S., Chandrasekaran R., Birdsall D. L., Leslie A. G., Ratliff R. L. Left-handed DNA helices. Nature. 1980 Feb 21;283(5749):743–745. doi: 10.1038/283743a0. [DOI] [PubMed] [Google Scholar]
  3. Berger I., Egli M., Rich A. Inter-strand C-H...O hydrogen bonds stabilizing four-stranded intercalated molecules: stereoelectronic effects of O4' in cytosine-rich DNA. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12116–12121. doi: 10.1073/pnas.93.22.12116. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berger I., Kang C., Fredian A., Ratliff R., Moyzis R., Rich A. Extension of the four-stranded intercalated cytosine motif by adenine.adenine base pairing in the crystal structure of d(CCCAAT). Nat Struct Biol. 1995 May;2(5):416–425. doi: 10.1038/nsb0595-416. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Calladine C. R., Drew H. R. Principles of sequence-dependent flexure of DNA. J Mol Biol. 1986 Dec 20;192(4):907–918. doi: 10.1016/0022-2836(86)90036-7. [DOI] [PubMed] [Google Scholar]
  7. DEVOE H., TINOCO I., Jr The stability of helical polynucleotides: base contributions. J Mol Biol. 1962 Jun;4:500–517. doi: 10.1016/s0022-2836(62)80105-3. [DOI] [PubMed] [Google Scholar]
  8. Dang L. X., Pearlman D. A., Kollman P. A. Why do A.T base pairs inhibit Z-DNA formation? Proc Natl Acad Sci U S A. 1990 Jun;87(12):4630–4634. doi: 10.1073/pnas.87.12.4630. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Egli M., Gessner R. V. Stereoelectronic effects of deoxyribose O4' on DNA conformation. Proc Natl Acad Sci U S A. 1995 Jan 3;92(1):180–184. doi: 10.1073/pnas.92.1.180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Florián J., Leszczyński J. Theoretical investigation of the molecular structure of the pi kappa DNA base pair. J Biomol Struct Dyn. 1995 Apr;12(5):1055–1062. doi: 10.1080/07391102.1995.10508797. [DOI] [PubMed] [Google Scholar]
  11. Friedman R. A., Honig B. The electrostatic contribution to DNA base-stacking interactions. Biopolymers. 1992 Feb;32(2):145–159. doi: 10.1002/bip.360320205. [DOI] [PubMed] [Google Scholar]
  12. Gabb H. A., Sanghani S. R., Robert C. H., Prévost C. Finding and visualizing nucleic acid base stacking. J Mol Graph. 1996 Feb;14(1):6-11, 23-4. doi: 10.1016/0263-7855(95)00086-0. [DOI] [PubMed] [Google Scholar]
  13. Gessner R. V., Frederick C. A., Quigley G. J., Rich A., Wang A. H. The molecular structure of the left-handed Z-DNA double helix at 1.0-A atomic resolution. Geometry, conformation, and ionic interactions of d(CGCGCG). J Biol Chem. 1989 May 15;264(14):7921–7935. doi: 10.2210/pdb1dcg/pdb. [DOI] [PubMed] [Google Scholar]
  14. Gorin A. A., Zhurkin V. B., Olson W. K. B-DNA twisting correlates with base-pair morphology. J Mol Biol. 1995 Mar 17;247(1):34–48. doi: 10.1006/jmbi.1994.0120. [DOI] [PubMed] [Google Scholar]
  15. Halgren T. A. Potential energy functions. Curr Opin Struct Biol. 1995 Apr;5(2):205–210. doi: 10.1016/0959-440x(95)80077-8. [DOI] [PubMed] [Google Scholar]
  16. Harvey S. C. DNA structural dynamics: longitudinal breathing as a possible mechanism for the B in equilibrium Z transition. Nucleic Acids Res. 1983 Jul 25;11(14):4867–4878. doi: 10.1093/nar/11.14.4867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Heinemann U., Alings C. Crystallographic study of one turn of G/C-rich B-DNA. J Mol Biol. 1989 Nov 20;210(2):369–381. doi: 10.1016/0022-2836(89)90337-9. [DOI] [PubMed] [Google Scholar]
  18. Herbert A. G., Spitzner J. R., Lowenhaupt K., Rich A. Z-DNA binding protein from chicken blood nuclei. Proc Natl Acad Sci U S A. 1993 Apr 15;90(8):3339–3342. doi: 10.1073/pnas.90.8.3339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hunter C. A. Sequence-dependent DNA structure. The role of base stacking interactions. J Mol Biol. 1993 Apr 5;230(3):1025–1054. doi: 10.1006/jmbi.1993.1217. [DOI] [PubMed] [Google Scholar]
  20. Jaworski A., Hsieh W. T., Blaho J. A., Larson J. E., Wells R. D. Left-handed DNA in vivo. Science. 1987 Nov 6;238(4828):773–777. doi: 10.1126/science.3313728. [DOI] [PubMed] [Google Scholar]
  21. Kagawa T. F., Stoddard D., Zhou G. W., Ho P. S. Quantitative analysis of DNA secondary structure from solvent-accessible surfaces: the B- to Z-DNA transition as a model. Biochemistry. 1989 Aug 8;28(16):6642–6651. doi: 10.1021/bi00442a017. [DOI] [PubMed] [Google Scholar]
  22. Kang C. H., Berger I., Lockshin C., Ratliff R., Moyzis R., Rich A. Crystal structure of intercalated four-stranded d(C3T) at 1.4 A resolution. Proc Natl Acad Sci U S A. 1994 Nov 22;91(24):11636–11640. doi: 10.1073/pnas.91.24.11636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kerr I. M., Brown R. E. pppA2'p5'A2'p5'A: an inhibitor of protein synthesis synthesized with an enzyme fraction from interferon-treated cells. Proc Natl Acad Sci U S A. 1978 Jan;75(1):256–260. doi: 10.1073/pnas.75.1.256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Krishnan R., Seshadri T. P. Stereochemistry of 2'-5' linked nucleic acids: crystal and molecular structure of ammonium adenylyl-2',5'-adenosine tetrahydrate: a core fragment of 2'-5' oligo A's produced by interferon induced adenylate synthetase. J Biomol Struct Dyn. 1993 Feb;10(4):727–745. doi: 10.1080/07391102.1993.10508003. [DOI] [PubMed] [Google Scholar]
  25. Kudritskaya Z. G., Danilov V. I. Quantum mechanical study of bases interactions in various associates in atomic dipole approximation. J Theor Biol. 1976 Jul 7;59(2):303–318. doi: 10.1016/0022-5193(76)90172-7. [DOI] [PubMed] [Google Scholar]
  26. Lavery R., Hartmann B. Modelling DNA conformational mechanics. Biophys Chem. 1994 May;50(1-2):33–45. doi: 10.1016/0301-4622(94)85018-6. [DOI] [PubMed] [Google Scholar]
  27. Lavery R., Sklenar H. The definition of generalized helicoidal parameters and of axis curvature for irregular nucleic acids. J Biomol Struct Dyn. 1988 Aug;6(1):63–91. doi: 10.1080/07391102.1988.10506483. [DOI] [PubMed] [Google Scholar]
  28. Lavery R., Sklenar H., Zakrzewska K., Pullman B. The flexibility of the nucleic acids: (II). The calculation of internal energy and applications to mononucleotide repeat DNA. J Biomol Struct Dyn. 1986 Apr;3(5):989–1014. doi: 10.1080/07391102.1986.10508478. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. 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]
  31. Müller V., Takeya M., Brendel S., Wittig B., Rich A. Z-DNA-forming sites within the human beta-globin gene cluster. Proc Natl Acad Sci U S A. 1996 Jan 23;93(2):780–784. doi: 10.1073/pnas.93.2.780. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Olson W. K., Srinivasan A. R., Marky N. L., Balaji V. N. Theoretical probes of DNA conformation examining the B leads to Z conformational transition. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 1):229–241. doi: 10.1101/sqb.1983.047.01.028. [DOI] [PubMed] [Google Scholar]
  33. Pearlman D. A., Kollman P. A. The calculated free energy effects of 5-methyl cytosine on the B to Z transition in DNA. 1990 Jul-Aug 5Biopolymers. 29(8-9):1193–1209. doi: 10.1002/bip.360290810. [DOI] [PubMed] [Google Scholar]
  34. Privé G. G., Yanagi K., Dickerson R. E. Structure of the B-DNA decamer C-C-A-A-C-G-T-T-G-G and comparison with isomorphous decamers C-C-A-A-G-A-T-T-G-G and C-C-A-G-G-C-C-T-G-G. J Mol Biol. 1991 Jan 5;217(1):177–199. doi: 10.1016/0022-2836(91)90619-h. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Rahmouni A. R., Wells R. D. Stabilization of Z DNA in vivo by localized supercoiling. Science. 1989 Oct 20;246(4928):358–363. doi: 10.1126/science.2678475. [DOI] [PubMed] [Google Scholar]
  37. Rich A. Speculation on the biological roles of left-handed Z-DNA. Ann N Y Acad Sci. 1994 Jul 29;726:1–17. doi: 10.1111/j.1749-6632.1994.tb52792.x. [DOI] [PubMed] [Google Scholar]
  38. Saenger W., Heinemann U. Raison d'être and structural model for the B-Z transition of poly d(G-C).poly d(G-C). FEBS Lett. 1989 Nov 6;257(2):223–227. doi: 10.1016/0014-5793(89)81539-x. [DOI] [PubMed] [Google Scholar]
  39. Sponer J., Hobza P. G.C base pair in parallel-stranded DNA--a novel type of base pairing: an ab initio quantum chemical study. J Biomol Struct Dyn. 1994 Dec;12(3):671–680. doi: 10.1080/07391102.1994.10508766. [DOI] [PubMed] [Google Scholar]
  40. Sponer J., Kypr J. Base pair buckling can eliminate the interstrand purine clash at the CpG steps in B-DNA caused by the base pair propeller twisting. J Biomol Struct Dyn. 1990 Jun;7(6):1211–1220. doi: 10.1080/07391102.1990.10508560. [DOI] [PubMed] [Google Scholar]
  41. Sponer J., Kypr J. Different intrastrand and interstrand contributions to stacking account for roll variations at the alternating purine-pyrimidine sequences in A-DNA and A-RNA. J Mol Biol. 1991 Oct 5;221(3):761–764. doi: 10.1016/0022-2836(91)80172-q. [DOI] [PubMed] [Google Scholar]
  42. Sponer J., Kypr J. Relationships among rise, cup, roll and stagger in DNA suggested by empirical potential studies of base stacking. J Biomol Struct Dyn. 1993 Aug;11(1):27–41. doi: 10.1080/07391102.1993.10508707. [DOI] [PubMed] [Google Scholar]
  43. Sponer J., Kypr J. Theoretical analysis of the base stacking in DNA: choice of the force field and a comparison with the oligonucleotide crystal structures. J Biomol Struct Dyn. 1993 Oct;11(2):277–292. doi: 10.1080/07391102.1993.10508726. [DOI] [PubMed] [Google Scholar]
  44. 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]
  45. Wang S., Kool E. T. Origins of the large differences in stability of DNA and RNA helices: C-5 methyl and 2'-hydroxyl effects. Biochemistry. 1995 Mar 28;34(12):4125–4132. doi: 10.1021/bi00012a031. [DOI] [PubMed] [Google Scholar]
  46. Wölfl S., Martinez C., Rich A., Majzoub J. A. Transcription of the human corticotropin-releasing hormone gene in NPLC cells is correlated with Z-DNA formation. Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3664–3668. doi: 10.1073/pnas.93.8.3664. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES