Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1996 Aug 1;24(15):2911–2918. doi: 10.1093/nar/24.15.2911

Minor groove hydration of DNA in aqueous solution: sequence-dependent next neighbor effect of the hydration lifetimes in d(TTAA)2 segments measured by NMR spectroscopy.

A Jacobson 1, W Leupin 1, E Liepinsh 1, F Otting 1
PMCID: PMC146052  PMID: 8760873

Abstract

The hydration in the minor groove of double stranded DNA fragments containing the sequences 5'-dTTAAT, 5'-dTTAAC, 5'-dTTAAA and 5'-dTTAAG was investigated by studying the decanucleotide duplex d(GCATTAATGC)2 and the singly cross-linked decameric duplexes 5'-d(GCATTAACGC)-3'-linker-5'-d(GCGTTAATGC)-3' and 5'-d(GCCTTAAAGC)-3'-linker-5'-d(GCTTTAAGGC)-3' by NMR spectroscopy. The linker employed consisted of six ethyleneglycol units. The hydration water was detected by NOEs between water and DNA protons in NOESY and ROESY spectra. NOE-NOESY and ROE-NOESY experiments were used to filter out intense exchange cross-peaks and to observe water-DNA NOEs with sugar 1' protons. Positive NOESY cross-peaks corresponding to residence times longer than approximately 0.5 ns were observed for 2H resonances of the central adenine residues in the duplex containing the sequences 5'-dTTAAT and 5'-dTTAAC, but not in the duplex containing the sequences 5'-dTTAAA and 5'-dTTAAG. In all nucleotide sequences studied here, the hydration water in the minor groove is significantly more mobile at both ends of the AT-rich inner segments, as indicated by very weak or negative water-A 2H NOESY cross-peaks. No positive NOESY cross-peaks were detected with the G 1'H and C 1'H resonances, indicating that the minor groove hydration water near GC base pairs is kinetically less restrained than for AT-rich DNA segments. Kinetically stabilized minor groove hydration water was manifested by positive NOESY cross-peaks with both A 2H and 1'H signals of the 5'-dTTAA segment in d(GCATTAATGC)2. More rigid hydration water was detected near T4 in d(GCATTAATGC)2 as compared with 5'-d(GCATTAACGC)-3'-linker-5'-d(GCGTTAATGC)-3', although the sequences differ only in a single base pair. This illustrates the high sensitivity of water-DNA NOEs towards small conformational differences.

Full Text

The Full Text of this article is available as a PDF (107.6 KB).

Selected References

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

  1. Altmann S., Labhardt A. M., Bur D., Lehmann C., Bannwarth W., Billeter M., Wüthrich K., Leupin W. NMR studies of DNA duplexes singly cross-linked by different synthetic linkers. Nucleic Acids Res. 1995 Dec 11;23(23):4827–4835. doi: 10.1093/nar/23.23.4827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Denisov V. P., Halle B. Hydrogen exchange and protein hydration: the deuteron spin relaxation dispersions of bovine pancreatic trypsin inhibitor and ubiquitin. J Mol Biol. 1995 Feb 3;245(5):698–709. doi: 10.1006/jmbi.1994.0056. [DOI] [PubMed] [Google Scholar]
  3. Denisov V. P., Halle B., Peters J., Hörlein H. D. Residence times of the buried water molecules in bovine pancreatic trypsin inhibitor and its G36S mutant. Biochemistry. 1995 Jul 18;34(28):9046–9051. doi: 10.1021/bi00028a013. [DOI] [PubMed] [Google Scholar]
  4. Denisov V. P., Halle B. Protein hydration dynamics in aqueous solution: a comparison of bovine pancreatic trypsin inhibitor and ubiquitin by oxygen-17 spin relaxation dispersion. J Mol Biol. 1995 Feb 3;245(5):682–697. doi: 10.1006/jmbi.1994.0055. [DOI] [PubMed] [Google Scholar]
  5. Drew H. R., Dickerson R. E. Structure of a B-DNA dodecamer. III. Geometry of hydration. J Mol Biol. 1981 Sep 25;151(3):535–556. doi: 10.1016/0022-2836(81)90009-7. [DOI] [PubMed] [Google Scholar]
  6. Eisenstein M., Shakked Z. Hydration patterns and intermolecular interactions in A-DNA crystal structures. Implications for DNA recognition. J Mol Biol. 1995 May 5;248(3):662–678. doi: 10.1006/jmbi.1995.0250. [DOI] [PubMed] [Google Scholar]
  7. Fawthrop S. A., Yang J. C., Fisher J. Structural and dynamic studies of a non-self-complementary dodecamer DNA duplex. Nucleic Acids Res. 1993 Oct 25;21(21):4860–4866. doi: 10.1093/nar/21.21.4860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Goodsell D. S., Kaczor-Grzeskowiak M., Dickerson R. E. The crystal structure of C-C-A-T-T-A-A-T-G-G. Implications for bending of B-DNA at T-A steps. J Mol Biol. 1994 May 27;239(1):79–96. doi: 10.1006/jmbi.1994.1352. [DOI] [PubMed] [Google Scholar]
  9. Guéron M., Kochoyan M., Leroy J. L. A single mode of DNA base-pair opening drives imino proton exchange. Nature. 1987 Jul 2;328(6125):89–92. doi: 10.1038/328089a0. [DOI] [PubMed] [Google Scholar]
  10. Kochoyan M., Leroy J. L. Hydration and solution structure of nucleic acids. Curr Opin Struct Biol. 1995 Jun;5(3):329–333. doi: 10.1016/0959-440x(95)80094-8. [DOI] [PubMed] [Google Scholar]
  11. Leijon M., Zdunek J., Fritzsche H., Sklenar H., Gräslund A. NMR studies and restrained-molecular-dynamics calculations of a long A+T-rich stretch in DNA. Effects of phosphate charge and solvent approximations. Eur J Biochem. 1995 Dec 15;234(3):832–842. doi: 10.1111/j.1432-1033.1995.832_a.x. [DOI] [PubMed] [Google Scholar]
  12. Leroy J. L., Broseta D., Guéron M. Proton exchange and base-pair kinetics of poly(rA).poly(rU) and poly(rI).poly(rC). J Mol Biol. 1985 Jul 5;184(1):165–178. doi: 10.1016/0022-2836(85)90050-6. [DOI] [PubMed] [Google Scholar]
  13. Liepinsh E., Leupin W., Otting G. Hydration of DNA in aqueous solution: NMR evidence for a kinetic destabilization of the minor groove hydration of d-(TTAA)2 versus d-(AATT)2 segments. Nucleic Acids Res. 1994 Jun 25;22(12):2249–2254. doi: 10.1093/nar/22.12.2249. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Liepinsh E., Otting G. Proton exchange rates from amino acid side chains--implications for image contrast. Magn Reson Med. 1996 Jan;35(1):30–42. doi: 10.1002/mrm.1910350106. [DOI] [PubMed] [Google Scholar]
  15. Liepinsh E., Otting G., Wüthrich K. NMR observation of individual molecules of hydration water bound to DNA duplexes: direct evidence for a spine of hydration water present in aqueous solution. Nucleic Acids Res. 1992 Dec 25;20(24):6549–6553. doi: 10.1093/nar/20.24.6549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Maltseva T. V., Agback P., Chattopadhyaya J. How much hydration is necessary for the stabilisation of DNA-duplex? Nucleic Acids Res. 1993 Sep 11;21(18):4246–4252. doi: 10.1093/nar/21.18.4246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Otting G., Liepinsh E., Farmer B. T., 2nd, Wüthrich K. Protein hydration studied with homonuclear 3D 1H NMR experiments. J Biomol NMR. 1991 Jul;1(2):209–215. doi: 10.1007/BF01877232. [DOI] [PubMed] [Google Scholar]
  18. Otting G., Liepinsh E., Wüthrich K. Protein hydration in aqueous solution. Science. 1991 Nov 15;254(5034):974–980. doi: 10.1126/science.1948083. [DOI] [PubMed] [Google Scholar]
  19. Quintana J. R., Grzeskowiak K., Yanagi K., Dickerson R. E. Structure of a B-DNA decamer with a central T-A step: C-G-A-T-T-A-A-T-C-G. J Mol Biol. 1992 May 20;225(2):379–395. doi: 10.1016/0022-2836(92)90928-d. [DOI] [PubMed] [Google Scholar]
  20. Umrania Y., Nikjoo H., Goodfellow J. M. A knowledge-based model of DNA hydration. Int J Radiat Biol. 1995 Feb;67(2):145–152. doi: 10.1080/09553009514550181. [DOI] [PubMed] [Google Scholar]
  21. Westhof E. Water: an integral part of nucleic acid structure. Annu Rev Biophys Biophys Chem. 1988;17:125–144. doi: 10.1146/annurev.bb.17.060188.001013. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES