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. 1995 Mar 11;23(5):844–848. doi: 10.1093/nar/23.5.844

Determination of the number and location of the manganese binding sites of DNA quadruplexes in solution by EPR and NMR.

K Y Wang 1, L Gerena 1, S Swaminathan 1, P H Bolton 1
PMCID: PMC306768  PMID: 7708501

Abstract

The paramagnetic metal ion Mn2+ has been used to probe the electrostatic potentials of a DNA quadruplex that has two quartets with an overall fold of the chair type. A quadruplex with a basket type structure has also been examined. The binding of the paramagnetic ion manganese to these quadruplex DNAs has been investigated by solution state electron paramagnetic resonance (EPR) and nuclear magnetic resonance (NMR) spectroscopies. The EPR results indicate that the DNA aptamer, d(GGTTGGTGTGGTTGG), binds two manganese ions and that the binding constants for each of these sites is approximately 10(5) M-1. The NMR results indicate that the binding sites of the manganese are in the narrow grooves of this quadruplex DNA. The binding sites of the DNA quadruplex formed by dimers of d(GGGGTTTTGGGG) which forms a basket structure are also in the narrow groove. These results indicate that the close approach of phosphates in the narrow minor grooves of the quadruplex structures provide strong binding sites for the manganese ions and that EPR and NMR monitoring of manganese binding can be used to distinguish between the different types of quadruplex structures.

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Selected References

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

  1. Amano M., Kawakami M. Assignment of the magnetic resonances of the imino protons and methyl protons of Bombyx mori tRNA(GlyGCC) and the effect of ion binding on its structure. Eur J Biochem. 1992 Dec 15;210(3):671–681. doi: 10.1111/j.1432-1033.1992.tb17468.x. [DOI] [PubMed] [Google Scholar]
  2. Anwander E. H., Probst M. M., Rode B. M. The influence of Li+, Na+, Mg2+, Ca2+, and Zn2+ ions on the hydrogen bonds of the Watson-Crick base pairs. Biopolymers. 1990 Mar-Apr;29(4-5):757–769. doi: 10.1002/bip.360290410. [DOI] [PubMed] [Google Scholar]
  3. Ciesiołka J., Wrzesinski J., Górnicki P., Podkowiński J., Krzyzosiak W. J. Analysis of magnesium, europium and lead binding sites in methionine initiator and elongator tRNAs by specific metal-ion-induced cleavages. Eur J Biochem. 1989 Dec 8;186(1-2):71–77. doi: 10.1111/j.1432-1033.1989.tb15179.x. [DOI] [PubMed] [Google Scholar]
  4. Fenley M. O., Manning G. S., Olson W. K. Approach to the limit of counterion condensation. Biopolymers. 1990;30(13-14):1191–1203. doi: 10.1002/bip.360301305. [DOI] [PubMed] [Google Scholar]
  5. Granot J., Assa-Munt N., Kearns D. R. Interactions of DNA with divalent metal ions. IV. Competitive studies of Mn2+ binding to AT- and GC-rich DNAs. Biopolymers. 1982 May;21(5):873–883. doi: 10.1002/bip.360210502. [DOI] [PubMed] [Google Scholar]
  6. Granot J., Feigon J., Kearns D. R. Interactions of DNA with divalent metal ions. I. 31P-NMR studies. Biopolymers. 1982 Jan;21(1):181–201. doi: 10.1002/bip.360210115. [DOI] [PubMed] [Google Scholar]
  7. Hardin C. C., Watson T., Corregan M., Bailey C. Cation-dependent transition between the quadruplex and Watson-Crick hairpin forms of d(CGCG3GCG). Biochemistry. 1992 Jan 28;31(3):833–841. doi: 10.1021/bi00118a028. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Kennedy S. D., Bryant R. G. Manganese-deoxyribonucleic acid binding modes. Nuclear magnetic relaxation dispersion results. Biophys J. 1986 Oct;50(4):669–676. doi: 10.1016/S0006-3495(86)83507-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Manning G. S. The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Q Rev Biophys. 1978 May;11(2):179–246. doi: 10.1017/s0033583500002031. [DOI] [PubMed] [Google Scholar]
  12. Nagesh N., Bhargava P., Chatterji D. Terbium(III)-induced fluorescence of four-stranded G4-DNA. Biopolymers. 1992 Oct;32(10):1421–1424. doi: 10.1002/bip.360321015. [DOI] [PubMed] [Google Scholar]
  13. Olmsted M. C., Anderson C. F., Record M. T., Jr Monte Carlo description of oligoelectrolyte properties of DNA oligomers: range of the end effect and the approach of molecular and thermodynamic properties to the polyelectrolyte limits. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7766–7770. doi: 10.1073/pnas.86.20.7766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Ray J., Manning G. S. Theory of delocalized ionic binding to polynucleotides: structural and excluded-volume effects. Biopolymers. 1992 May;32(5):541–549. doi: 10.1002/bip.360320510. [DOI] [PubMed] [Google Scholar]
  15. Record M. T., Jr, Anderson C. F., Lohman T. M. Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening, and ion effects on water activity. Q Rev Biophys. 1978 May;11(2):103–178. doi: 10.1017/s003358350000202x. [DOI] [PubMed] [Google Scholar]
  16. Reid S. S., Cowan J. A. Biostructural chemistry of magnesium ion: characterization of the weak binding sites on tRNA(Phe)(yeast). Implications for conformational change and activity. Biochemistry. 1990 Jun 26;29(25):6025–6032. doi: 10.1021/bi00477a021. [DOI] [PubMed] [Google Scholar]
  17. Reuben J., Gabbay E. J. Binding of manganese(II) to DNA and the competitive effects of metal ions and organic cations. An electron paramagnetic resonance study. Biochemistry. 1975 Mar 25;14(6):1230–1235. doi: 10.1021/bi00677a022. [DOI] [PubMed] [Google Scholar]
  18. Schimmel P. R., Redfield A. G. Transfer RNA in solution: selected topics. Annu Rev Biophys Bioeng. 1980;9:181–221. doi: 10.1146/annurev.bb.09.060180.001145. [DOI] [PubMed] [Google Scholar]
  19. Smith F. W., Feigon J. Strand orientation in the DNA quadruplex formed from the Oxytricha telomere repeat oligonucleotide d(G4T4G4) in solution. Biochemistry. 1993 Aug 24;32(33):8682–8692. doi: 10.1021/bi00084a040. [DOI] [PubMed] [Google Scholar]
  20. Wang K. Y., Krawczyk S. H., Bischofberger N., Swaminathan S., Bolton P. H. The tertiary structure of a DNA aptamer which binds to and inhibits thrombin determines activity. Biochemistry. 1993 Oct 26;32(42):11285–11292. doi: 10.1021/bi00093a004. [DOI] [PubMed] [Google Scholar]
  21. Wang K. Y., McCurdy S., Shea R. G., Swaminathan S., Bolton P. H. A DNA aptamer which binds to and inhibits thrombin exhibits a new structural motif for DNA. Biochemistry. 1993 Mar 2;32(8):1899–1904. doi: 10.1021/bi00059a003. [DOI] [PubMed] [Google Scholar]
  22. Wang K. Y., Swaminathan S., Bolton P. H. Tertiary structure motif of Oxytricha telomere DNA. Biochemistry. 1994 Jun 21;33(24):7517–7527. doi: 10.1021/bi00190a004. [DOI] [PubMed] [Google Scholar]
  23. Wang Y., Patel D. J. Solution structure of the human telomeric repeat d[AG3(T2AG3)3] G-tetraplex. Structure. 1993 Dec 15;1(4):263–282. doi: 10.1016/0969-2126(93)90015-9. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Wyatt J. R., Puglisi J. D., Tinoco I., Jr RNA pseudoknots. Stability and loop size requirements. J Mol Biol. 1990 Jul 20;214(2):455–470. doi: 10.1016/0022-2836(90)90193-P. [DOI] [PubMed] [Google Scholar]
  26. Yue D., Kintanar A., Horowitz J. Nucleoside modifications stabilize Mg2+ binding in Escherichia coli tRNA(Val): an imino proton NMR investigation. Biochemistry. 1994 Aug 2;33(30):8905–8911. doi: 10.1021/bi00196a007. [DOI] [PubMed] [Google Scholar]

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