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. 1997 Sep 1;25(17):3497–3502. doi: 10.1093/nar/25.17.3497

Effects of diaminopurine and inosine substitutions on A-tract induced DNA curvature. Importance of the 3'-A-tract junction.

N E Mollegaard 1, C Bailly 1, M J Waring 1, P E Nielsen 1
PMCID: PMC146927  PMID: 9254710

Abstract

Gel migration and uranyl photoprobing have been used to study the effects of inosine and 2,6-diaminopurine (2,6-DAP) substitution on adenine-tract (A-tract) induced DNA curvature. Using a 10mer repeated sequence including five inosines we show by uranyl photoprobing that a narrow minor groove varying in phase with the helix repeat is not the cause of DNA curvature. Further, we have systematically studied by gel migration the effects on A-tract induced curvature of either single or full substitution with inosine and/or 2,6-DAP in a 5'-AAAAAGCCGC-3'sequence. DNA curvature is shown to increase when inosines are substituted for the guanosines in the sequence between the A-tracts. By comparing the effects of each monosubstitution it can be seen that when the G closest to the 3'-end of the A-tract is substituted the effect on DNA curvature is much stronger than when substitution is made at any other position. By contrast, curvature is abolished when 2,6-DAP residues are substituted for all adenines, and monosubstitution reveals that the effect of substituting a single adenine is strongest at the 3'-end of the A-tract. These results favor a model in which the curvature induced by an A-tract in DNA molecules is primarily located at the junction with the 3'-end of the A-tract, and this peculiar junction is created because the A-tract has a preference to form a non-B-DNA structure which builds up from the 5'-end.

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Selected References

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

  1. Bailly C., Møllegaard N. E., Nielsen P. E., Waring M. J. The influence of the 2-amino group of guanine on DNA conformation. Uranyl and DNase I probing of inosine/diaminopurine substituted DNA. EMBO J. 1995 May 1;14(9):2121–2131. doi: 10.1002/j.1460-2075.1995.tb07204.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bailly C., Waring M. J. Transferring the purine 2-amino group from guanines to adenines in DNA changes the sequence-specific binding of antibiotics. Nucleic Acids Res. 1995 Mar 25;23(6):885–892. doi: 10.1093/nar/23.6.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bolshoy A., McNamara P., Harrington R. E., Trifonov E. N. Curved DNA without A-A: experimental estimation of all 16 DNA wedge angles. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2312–2316. doi: 10.1073/pnas.88.6.2312. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bone S., Small C. A. Dielectric studies of ion fluctuation and chain bending in native DNA. Biochim Biophys Acta. 1995 Jan 2;1260(1):85–93. doi: 10.1016/0167-4781(94)00181-2. [DOI] [PubMed] [Google Scholar]
  5. Chuprina V. P., Fedoroff OYu, Reid B. R. New insights into the structure of An tracts and B'-B' bends in DNA. Biochemistry. 1991 Jan 15;30(2):561–568. doi: 10.1021/bi00216a034. [DOI] [PubMed] [Google Scholar]
  6. Coll M., Frederick C. A., Wang A. H., Rich A. A bifurcated hydrogen-bonded conformation in the d(A.T) base pairs of the DNA dodecamer d(CGCAAATTTGCG) and its complex with distamycin. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8385–8389. doi: 10.1073/pnas.84.23.8385. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DeSantis P., Palleschi A., Savino M., Scipioni A. Theoretical prediction of the gel electrophoretic retardation changes due to point mutations in a tract of SV40 DNA. Biophys Chem. 1992 Feb;42(2):147–152. doi: 10.1016/0301-4622(92)85004-n. [DOI] [PubMed] [Google Scholar]
  8. Dickerson R. E., Goodsell D. S., Neidle S. "...the tyranny of the lattice...". Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3579–3583. doi: 10.1073/pnas.91.9.3579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Diekmann S., von Kitzing E., McLaughlin L., Ott J., Eckstein F. The influence of exocyclic substituents of purine bases on DNA curvature. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8257–8261. doi: 10.1073/pnas.84.23.8257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Goodsell D. S., Kopka M. L., Cascio D., Dickerson R. E. Crystal structure of CATGGCCATG and its implications for A-tract bending models. Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2930–2934. doi: 10.1073/pnas.90.7.2930. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grzeskowiak K., Goodsell D. S., Kaczor-Grzeskowiak M., Cascio D., Dickerson R. E. Crystallographic analysis of C-C-A-A-G-C-T-T-G-G and its implications for bending in B-DNA. Biochemistry. 1993 Aug 31;32(34):8923–8931. doi: 10.1021/bi00085a025. [DOI] [PubMed] [Google Scholar]
  13. Hagerman P. J. Sequence dependence of the curvature of DNA: a test of the phasing hypothesis. Biochemistry. 1985 Dec 3;24(25):7033–7037. doi: 10.1021/bi00346a001. [DOI] [PubMed] [Google Scholar]
  14. Hagerman P. J. Sequence-directed curvature of DNA. Nature. 1986 May 22;321(6068):449–450. doi: 10.1038/321449a0. [DOI] [PubMed] [Google Scholar]
  15. Hagerman P. J. Sequence-directed curvature of DNA. Annu Rev Biochem. 1990;59:755–781. doi: 10.1146/annurev.bi.59.070190.003543. [DOI] [PubMed] [Google Scholar]
  16. Haran T. E., Crothers D. M. Cooperativity in A-tract structure and bending properties of composite TnAn blocks. Biochemistry. 1989 Apr 4;28(7):2763–2767. doi: 10.1021/bi00433a003. [DOI] [PubMed] [Google Scholar]
  17. Haran T. E., Kahn J. D., Crothers D. M. Sequence elements responsible for DNA curvature. J Mol Biol. 1994 Nov 25;244(2):135–143. doi: 10.1006/jmbi.1994.1713. [DOI] [PubMed] [Google Scholar]
  18. Jeppesen C., Nielsen P. E. Uranyl mediated photofootprinting reveals strong E. coli RNA polymerase--DNA backbone contacts in the +10 region of the DeoP1 promoter open complex. Nucleic Acids Res. 1989 Jul 11;17(13):4947–4956. doi: 10.1093/nar/17.13.4947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Koo H. S., Crothers D. M. Chemical determinants of DNA bending at adenine-thymine tracts. Biochemistry. 1987 Jun 16;26(12):3745–3748. doi: 10.1021/bi00386a070. [DOI] [PubMed] [Google Scholar]
  20. Koo H. S., Wu H. M., Crothers D. M. DNA bending at adenine . thymine tracts. Nature. 1986 Apr 10;320(6062):501–506. doi: 10.1038/320501a0. [DOI] [PubMed] [Google Scholar]
  21. Leroy J. L., Charretier E., Kochoyan M., Guéron M. Evidence from base-pair kinetics for two types of adenine tract structures in solution: their relation to DNA curvature. Biochemistry. 1988 Dec 13;27(25):8894–8898. doi: 10.1021/bi00425a004. [DOI] [PubMed] [Google Scholar]
  22. Marini J. C., Levene S. D., Crothers D. M., Englund P. T. Bent helical structure in kinetoplast DNA. Proc Natl Acad Sci U S A. 1982 Dec;79(24):7664–7668. doi: 10.1073/pnas.79.24.7664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Møllegaard N. E., Rasmussen P. B., Valentin-Hansen P., Nielsen P. E. Characterization of promoter recognition complexes formed by CRP and CytR for repression and by CRP and RNA polymerase for activation of transcription on the Escherichia coli deoP2 promoter. J Biol Chem. 1993 Aug 15;268(23):17471–17477. [PubMed] [Google Scholar]
  24. Nagaich A. K., Bhattacharyya D., Brahmachari S. K., Bansal M. CA/TG sequence at the 5' end of oligo(A)-tracts strongly modulates DNA curvature. J Biol Chem. 1994 Mar 11;269(10):7824–7833. [PubMed] [Google Scholar]
  25. Nelson H. C., Finch J. T., Luisi B. F., Klug A. The structure of an oligo(dA).oligo(dT) tract and its biological implications. Nature. 1987 Nov 19;330(6145):221–226. doi: 10.1038/330221a0. [DOI] [PubMed] [Google Scholar]
  26. Nielsen P. E., Jeppesen C., Buchardt O. Uranyl salts as photochemical agents for cleavage of DNA and probing of protein-DNA contacts. FEBS Lett. 1988 Aug 1;235(1-2):122–124. doi: 10.1016/0014-5793(88)81245-6. [DOI] [PubMed] [Google Scholar]
  27. Nielsen P. E., Møllegaard N. E., Jeppesen C. DNA conformational analysis in solution by uranyl mediated photocleavage. Nucleic Acids Res. 1990 Jul 11;18(13):3847–3851. doi: 10.1093/nar/18.13.3847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shatzky-Schwartz M., Arbuckle N. D., Eisenstein M., Rabinovich D., Bareket-Samish A., Haran T. E., Luisi B. F., Shakked Z. X-ray and solution studies of DNA oligomers and implications for the structural basis of A-tract-dependent curvature. J Mol Biol. 1997 Apr 4;267(3):595–623. doi: 10.1006/jmbi.1996.0878. [DOI] [PubMed] [Google Scholar]
  29. Sönnichsen S. H., Nielsen P. E. Enhanced uranyl photocleavage across the minor groove of all (A/T)4 sequences indicates a similar narrow minor groove conformation. J Mol Recognit. 1996 May-Jun;9(3):219–227. doi: 10.1002/(sici)1099-1352(199605)9:3<219::aid-jmr242>3.0.co;2-s. [DOI] [PubMed] [Google Scholar]
  30. Trifonov E. N., Sussman J. L. The pitch of chromatin DNA is reflected in its nucleotide sequence. Proc Natl Acad Sci U S A. 1980 Jul;77(7):3816–3820. doi: 10.1073/pnas.77.7.3816. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Ulanovsky L. E., Trifonov E. N. Estimation of wedge components in curved DNA. Nature. 1987 Apr 16;326(6114):720–722. doi: 10.1038/326720a0. [DOI] [PubMed] [Google Scholar]
  32. Wu H. M., Crothers D. M. The locus of sequence-directed and protein-induced DNA bending. Nature. 1984 Apr 5;308(5959):509–513. doi: 10.1038/308509a0. [DOI] [PubMed] [Google Scholar]
  33. Xuan J. C., Weber I. T. Crystal structure of a B-DNA dodecamer containing inosine, d(CGCIAATTCGCG), at 2.4 A resolution and its comparison with other B-DNA dodecamers. Nucleic Acids Res. 1992 Oct 25;20(20):5457–5464. doi: 10.1093/nar/20.20.5457. [DOI] [PMC free article] [PubMed] [Google Scholar]

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