Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 1997 Sep;73(3):1539–1552. doi: 10.1016/S0006-3495(97)78186-4

Conformational transitions of the phosphodiester backbone in native DNA: two-dimensional magic-angle-spinning 31P-NMR of DNA fibers.

Z Song 1, O N Antzutkin 1, Y K Lee 1, S C Shekar 1, A Rupprecht 1, M H Levitt 1
PMCID: PMC1181053  PMID: 9284321

Abstract

Solid-state 31P-NMR is used to investigate the orientation of the phosphodiester backbone in NaDNA-, LiDNA-, MgDNA-, and NaDNA-netropsin fibers. The results for A- and B-DNA agree with previous interpretations. We verify that the binding of netropsin to NaDNA stabilizes the B form, and find that in NaDNA, most of the phosphate groups adopt a conformation typical of the A form, although there are minor components with phosphate orientations close to the B form. For LiDNA and MgDNA samples, on the other hand, we find phosphate conformations that are in variance with previous models. These samples display x-ray diffraction patterns that correspond to C-DNA. However, we find two distinct phosphate orientations in these samples, one resembling that in B-DNA, and one displaying a twist of the PO4 groups about the O3-P-O4 bisectors. The latter conformation is not in accordance with previous models of C-DNA structure.

Full text

PDF
1546

Images in this article

Selected References

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

  1. Arnott S., Hukins D. W. Optimised parameters for A-DNA and B-DNA. Biochem Biophys Res Commun. 1972 Jun 28;47(6):1504–1509. doi: 10.1016/0006-291x(72)90243-4. [DOI] [PubMed] [Google Scholar]
  2. Arnott S., Hukins D. W. Refinement of the structure of B-DNA and implications for the analysis of x-ray diffraction data from fibers of biopolymers. J Mol Biol. 1973 Dec 5;81(2):93–105. doi: 10.1016/0022-2836(73)90182-4. [DOI] [PubMed] [Google Scholar]
  3. Arnott S., Selsing E. The conformation of C-DNA. J Mol Biol. 1975 Oct 15;98(1):265–269. doi: 10.1016/s0022-2836(75)80115-x. [DOI] [PubMed] [Google Scholar]
  4. Balendiran K., Rao S. T., Sekharudu C. Y., Zon G., Sundaralingam M. X-ray structures of the B-DNA dodecamer d(CGCGTTAACGCG) with an inverted central tetranucleotide and its netropsin complex. Acta Crystallogr D Biol Crystallogr. 1995 Mar 1;51(Pt 2):190–198. doi: 10.1107/S0907444994010759. [DOI] [PubMed] [Google Scholar]
  5. Brahms J., Pilet J., Phuong Lan T. T., Hill L. R. Direct evidence of the C-like form of sodium deoxyribonucleate. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3352–3355. doi: 10.1073/pnas.70.12.3352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brandes R., Vold R. R., Kearns D. R., Rupprecht A. A 2H-NMR study of the A-DNA conformation in films of oriented Na-DNA: evidence of a disordered B-DNA contribution. Biopolymers. 1988 Jul;27(7):1159–1170. doi: 10.1002/bip.360270709. [DOI] [PubMed] [Google Scholar]
  7. Brandes R., Vold R. R., Kearns D. R., Rupprecht A. Static disorder and librational motions of the purine bases in films of oriented Li-DNA. J Mol Biol. 1988 Jul 20;202(2):321–332. doi: 10.1016/0022-2836(88)90461-5. [DOI] [PubMed] [Google Scholar]
  8. Chandrasekaran R., Arnott S. The structure of B-DNA in oriented fibers. J Biomol Struct Dyn. 1996 Jun;13(6):1015–1027. doi: 10.1080/07391102.1996.10508916. [DOI] [PubMed] [Google Scholar]
  9. Chandrasekaran R., Wang M., He R. G., Puigjaner L. C., Byler M. A., Millane R. P., Arnott S. A re-examination of the crystal structure of A-DNA using fiber diffraction data. J Biomol Struct Dyn. 1989 Jun;6(6):1189–1202. doi: 10.1080/07391102.1989.10506544. [DOI] [PubMed] [Google Scholar]
  10. Coll M., Aymami J., van der Marel G. A., van Boom J. H., Rich A., Wang A. H. Molecular structure of the netropsin-d(CGCGATATCGCG) complex: DNA conformation in an alternating AT segment. Biochemistry. 1989 Jan 10;28(1):310–320. doi: 10.1021/bi00427a042. [DOI] [PubMed] [Google Scholar]
  11. FULLER W., WILKINS M. H., WILSON H. R., HAMILTON L. D. THE MOLECULAR CONFIGURATION OF DEOXYRIBONUCLEIC ACID. IV. X-RAY DIFFRACTION STUDY OF THE A FORM. J Mol Biol. 1965 May;12:60–76. doi: 10.1016/s0022-2836(65)80282-0. [DOI] [PubMed] [Google Scholar]
  12. Flanagan M. E., Rollins S. B., Williams R. M. Netropsin and spermine conjugates of a water-soluble quinocarcin analog: analysis of sequence-specific DNA interactions. Chem Biol. 1995 Mar;2(3):147–156. doi: 10.1016/1074-5521(95)90069-1. [DOI] [PubMed] [Google Scholar]
  13. Fritzsche H., Brandes R., Rupprecht A., Song Z., Weidlich T., Kearns D. R. The formation of A-DNA in NaDNA films is suppressed by netropsin. Nucleic Acids Res. 1992 Mar 25;20(6):1223–1228. doi: 10.1093/nar/20.6.1223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fritzsche H. Infrared linear dichroism studies of DNA-drug complexes: quantitative determination of the drug-induced restriction of the B-A transition. Nucleic Acids Res. 1994 Mar 11;22(5):787–791. doi: 10.1093/nar/22.5.787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fritzsche H., Rupprecht A., Richter M. Infrared linear dichroism of oriented DNA-ligand complexes prepared with the wet-spinning method. Nucleic Acids Res. 1984 Dec 11;12(23):9165–9177. doi: 10.1093/nar/12.23.9165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fujiwara T., Shindo H. Phosphorus-31 nuclear magnetic resonance of highly oriented DNA fibers. 2. Molecular motions in hydrated DNA. Biochemistry. 1985 Feb 12;24(4):896–902. doi: 10.1021/bi00325a013. [DOI] [PubMed] [Google Scholar]
  17. Gabriëlse W., van Well H. F., Veeman W. S. Determination of the 13C magnetic shielding tensor in partially oriented polymer systems. Solid State Nucl Magn Reson. 1996 Jun;6(3):231–240. doi: 10.1016/0926-2040(95)01217-6. [DOI] [PubMed] [Google Scholar]
  18. Goodsell D. S., Kopka M. L., Dickerson R. E. Refinement of netropsin bound to DNA: bias and feedback in electron density map interpretation. Biochemistry. 1995 Apr 18;34(15):4983–4993. doi: 10.1021/bi00015a009. [DOI] [PubMed] [Google Scholar]
  19. Heinemann U., Alings C., Hahn M. Crystallographic studies of DNA helix structure. Biophys Chem. 1994 May;50(1-2):157–167. doi: 10.1016/0301-4622(94)85028-3. [DOI] [PubMed] [Google Scholar]
  20. Herzfeld J., Griffin R. G., Haberkorn R. A. Phosphorus-31 chemical-shift tensors in barium diethyl phosphate and urea-phosphoric acid: model compounds for phospholipid head-group studies. Biochemistry. 1978 Jul 11;17(14):2711–2718. doi: 10.1021/bi00607a003. [DOI] [PubMed] [Google Scholar]
  21. Juang C. L., Tang P., Harbison G. S. Solid-state NMR of DNA. Methods Enzymol. 1995;261:256–270. doi: 10.1016/s0076-6879(95)61013-8. [DOI] [PubMed] [Google Scholar]
  22. Kopka M. L., Yoon C., Goodsell D., Pjura P., Dickerson R. E. Binding of an antitumor drug to DNA, Netropsin and C-G-C-G-A-A-T-T-BrC-G-C-G. J Mol Biol. 1985 Jun 25;183(4):553–563. doi: 10.1016/0022-2836(85)90171-8. [DOI] [PubMed] [Google Scholar]
  23. Kopka M. L., Yoon C., Goodsell D., Pjura P., Dickerson R. E. The molecular origin of DNA-drug specificity in netropsin and distamycin. Proc Natl Acad Sci U S A. 1985 Mar;82(5):1376–1380. doi: 10.1073/pnas.82.5.1376. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. MARVIN D. A., SPENCER M., WILKINS M. H., HAMILTON L. D. The molecular configuration of deoxyribonucleic acid. III. X-ray diffraction study of the C form of the lithium salt. J Mol Biol. 1961 Oct;3:547–565. doi: 10.1016/s0022-2836(61)80021-1. [DOI] [PubMed] [Google Scholar]
  25. Nall B. T., Rothwell W. P., Waugh J. S., Rupprecht A. Structural studies of A-form sodium deoxyribonucleic acid: phosphorus-31 nuclear magnetic resonance of oriented fibers. Biochemistry. 1981 Mar 31;20(7):1881–1887. doi: 10.1021/bi00510a025. [DOI] [PubMed] [Google Scholar]
  26. Patel D. J., Shapiro L. Molecular recognition in noncovalent antitumor agent-DNA complexes: NMR studies of the base and sequence dependent recognition of the DNA minor groove by netropsin. Biochimie. 1985 Jul-Aug;67(7-8):887–915. doi: 10.1016/s0300-9084(85)80181-4. [DOI] [PubMed] [Google Scholar]
  27. Pilet J., Brahms J. Dependence of B-A conformational change in DNA on base composition. Nat New Biol. 1972 Mar 29;236(65):99–100. doi: 10.1038/newbio236099a0. [DOI] [PubMed] [Google Scholar]
  28. Pohle W., Zhurkin V. B., Fritzsche H. The DNA phosphate orientation. Infrared data and energetically favorable structures. Biopolymers. 1984 Nov;23(11 Pt 2):2603–2622. doi: 10.1002/bip.360231131. [DOI] [PubMed] [Google Scholar]
  29. Premilat S., Albiser G. Conformations of A-DNA and B-DNA in agreement with fiber X-ray and infrared dichroism. Nucleic Acids Res. 1983 Mar 25;11(6):1897–1908. doi: 10.1093/nar/11.6.1897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rupprecht A. A wet spinning apparatus and auxiliary equipment suitable for preparing samples of oriented DNA. Biotechnol Bioeng. 1970 Jan;12(1):93–121. doi: 10.1002/bit.260120109. [DOI] [PubMed] [Google Scholar]
  31. Rupprecht A., Forslind B. Variation of electrolyte content in wet-spun lithium- and sodium-DNA. Biochim Biophys Acta. 1970 Apr 15;204(2):304–316. doi: 10.1016/0005-2787(70)90148-6. [DOI] [PubMed] [Google Scholar]
  32. Rupprecht A. Preparation of oriented DNA by wet spinning. Acta Chem Scand. 1966;20(2):494–504. doi: 10.3891/acta.chem.scand.20-0494. [DOI] [PubMed] [Google Scholar]
  33. Schultz J., Rupprecht A., Song Z., Piskur J., Nordenskiöld L., Lahajnar G. A mechanochemical study of MgDNA fibers in ethanol-water solutions. Biophys J. 1994 Mar;66(3 Pt 1):810–819. doi: 10.1016/s0006-3495(94)80857-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shindo H., Fujiwara T., Akutsu H., Matsumoto U., Kyogoku Y. Phosphorus-31 nuclear magnetic resonance of highly oriented DNA fibers. 1. Static geometry of DNA double helices. Biochemistry. 1985 Feb 12;24(4):887–895. doi: 10.1021/bi00325a012. [DOI] [PubMed] [Google Scholar]
  35. Tabernero L., Verdaguer N., Coll M., Fita I., van der Marel G. A., van Boom J. H., Rich A., Aymamí J. Molecular structure of the A-tract DNA dodecamer d(CGCAAATTTGCG) complexed with the minor groove binding drug netropsin. Biochemistry. 1993 Aug 24;32(33):8403–8410. doi: 10.1021/bi00084a004. [DOI] [PubMed] [Google Scholar]
  36. Tang P., Juang C. L., Harbison G. S. Intercalation complex of proflavine with DNA: structure and dynamics by solid-state NMR. Science. 1990 Jul 6;249(4964):70–72. doi: 10.1126/science.2367853. [DOI] [PubMed] [Google Scholar]
  37. Wahl M. C., Sundaralingam M. New crystal structures of nucleic acids and their complexes. Curr Opin Struct Biol. 1995 Jun;5(3):282–295. doi: 10.1016/0959-440x(95)80089-1. [DOI] [PubMed] [Google Scholar]
  38. Wartell R. M., Larson J. E., Wells R. D. Netropsin. A specific probe for A-T regions of duplex deoxyribonucleic acid. J Biol Chem. 1974 Nov 10;249(21):6719–6731. [PubMed] [Google Scholar]

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

RESOURCES