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. 1989 Jun;8(6):1809–1817. doi: 10.1002/j.1460-2075.1989.tb03575.x

The DNA binding site of the Xenopus transcription factor IIIA has a non-B-form structure.

L Fairall 1, S Martin 1, D Rhodes 1
PMCID: PMC401027  PMID: 2767054

Abstract

On the basis of nuclease digestion studies we proposed that the DNA binding site of transcription factor IIIA (TFIIIA) may have an overall structure with A-type rather than B-type characteristics. This proposal was substantiated by the crystal structure of a part of the TFIIIA binding site. Recently, however, it has been reported that the binding site for TFIIIA is B-form in solution, thus implying that the conformation present in crystals is not the structure in solution. We have carried out a study using comparative circular dichroism (CD) spectroscopy of a number of double stranded deoxyoligonucleotides of different sequence, and known crystal structure. The correlation we have found between CD characteristics and certain structural parameters indicates that the solution and crystal structures of the TFIIIA binding site are closely related. This structure may be classed as an intermediate type, between A-form and B-form DNA.

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Selected References

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  1. Aboul-ela F., Varani G., Walker G. T., Tinoco I., Jr The TFIIIA recognition fragment d(GGATGGGAG).d(CTCCCATCC) is B-form in solution. Nucleic Acids Res. 1988 Apr 25;16(8):3559–3572. doi: 10.1093/nar/16.8.3559. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aggarwal A. K., Rodgers D. W., Drottar M., Ptashne M., Harrison S. C. Recognition of a DNA operator by the repressor of phage 434: a view at high resolution. Science. 1988 Nov 11;242(4880):899–907. doi: 10.1126/science.3187531. [DOI] [PubMed] [Google Scholar]
  3. Baase W. A., Johnson W. C., Jr Circular dichroism and DNA secondary structure. Nucleic Acids Res. 1979 Feb;6(2):797–814. doi: 10.1093/nar/6.2.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bram S. Polynucleotide polymorphism in solution. Nat New Biol. 1971 Oct 6;233(40):161–164. doi: 10.1038/newbio233161a0. [DOI] [PubMed] [Google Scholar]
  5. Brown D. D. How a simple animal gene works. Harvey Lect. 1980;76:27–44. [PubMed] [Google Scholar]
  6. Calladine C. R., Drew H. R. A base-centred explanation of the B-to-A transition in DNA. J Mol Biol. 1984 Sep 25;178(3):773–782. doi: 10.1016/0022-2836(84)90251-1. [DOI] [PubMed] [Google Scholar]
  7. Dickerson R. E., Goodsell D. S., Kopka M. L., Pjura P. E. The effect of crystal packing on oligonucleotide double helix structure. J Biomol Struct Dyn. 1987 Dec;5(3):557–579. doi: 10.1080/07391102.1987.10506413. [DOI] [PubMed] [Google Scholar]
  8. Diekmann S. Temperature and salt dependence of the gel migration anomaly of curved DNA fragments. Nucleic Acids Res. 1987 Jan 12;15(1):247–265. doi: 10.1093/nar/15.1.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Drew H. R., McCall M. J., Calladine C. R. Recent studies of DNA in the crystal. Annu Rev Cell Biol. 1988;4:1–20. doi: 10.1146/annurev.cb.04.110188.000245. [DOI] [PubMed] [Google Scholar]
  10. Drew H. R., Travers A. A. DNA structural variations in the E. coli tyrT promoter. Cell. 1984 Jun;37(2):491–502. doi: 10.1016/0092-8674(84)90379-9. [DOI] [PubMed] [Google Scholar]
  11. Drew H. R., Weeks J. R., Travers A. A. Negative supercoiling induces spontaneous unwinding of a bacterial promoter. EMBO J. 1985 Apr;4(4):1025–1032. doi: 10.1002/j.1460-2075.1985.tb03734.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Drew H. R., Wing R. M., Takano T., Broka C., Tanaka S., Itakura K., Dickerson R. E. Structure of a B-DNA dodecamer: conformation and dynamics. Proc Natl Acad Sci U S A. 1981 Apr;78(4):2179–2183. doi: 10.1073/pnas.78.4.2179. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Fairall L., Rhodes D., Klug A. Mapping of the sites of protection on a 5 S RNA gene by the Xenopus transcription factor IIIA. A model for the interaction. J Mol Biol. 1986 Dec 5;192(3):577–591. doi: 10.1016/0022-2836(86)90278-0. [DOI] [PubMed] [Google Scholar]
  14. Fratini A. V., Kopka M. L., Drew H. R., Dickerson R. E. Reversible bending and helix geometry in a B-DNA dodecamer: CGCGAATTBrCGCG. J Biol Chem. 1982 Dec 25;257(24):14686–14707. [PubMed] [Google Scholar]
  15. Frederick C. A., Grable J., Melia M., Samudzi C., Jen-Jacobson L., Wang B. C., Greene P., Boyer H. W., Rosenberg J. M. Kinked DNA in crystalline complex with EcoRI endonuclease. Nature. 1984 May 24;309(5966):327–331. doi: 10.1038/309327a0. [DOI] [PubMed] [Google Scholar]
  16. Gottesfeld J. M., Blanco J., Tennant L. L. The 5S gene internal control region is B-form both free in solution and in a complex with TFIIIA. Nature. 1987 Oct 1;329(6138):460–462. doi: 10.1038/329460a0. [DOI] [PubMed] [Google Scholar]
  17. Gottesfeld J. M. DNA sequence-directed nucleosome reconstitution on 5S RNA genes of Xenopus laevis. Mol Cell Biol. 1987 May;7(5):1612–1622. doi: 10.1128/mcb.7.5.1612. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gray D. M., Edmondson S. P., Lang D., Vaughan M. The circular dichroism and X-ray diffraction of DNA condensed from ethanolic solutions. Nucleic Acids Res. 1979;6(6):2089–2107. doi: 10.1093/nar/6.6.2089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hanas J. S., Hazuda D. J., Bogenhagen D. F., Wu F. Y., Wu C. W. Xenopus transcription factor A requires zinc for binding to the 5 S RNA gene. J Biol Chem. 1983 Dec 10;258(23):14120–14125. [PubMed] [Google Scholar]
  20. Heinemann U., Lauble H., Frank R., Blöcker H. Crystal structure analysis of an A-DNA fragment at 1.8 A resolution: d(GCCCGGGC). Nucleic Acids Res. 1987 Nov 25;15(22):9531–9550. doi: 10.1093/nar/15.22.9531. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hillen W., Wells R. D. Circular dichroism studies of the B goes to A conformational transition in seven small DNA restriction fragments containing the Escherichia coli lactose control region. Nucleic Acids Res. 1980 Nov 25;8(22):5427–5444. doi: 10.1093/nar/8.22.5427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hunter W. N., D'Estaintot B. L., Kennard O. Crystallization and preliminary analysis of the deoxyoligonucleotide d(CGTAGATCTACG). J Mol Biol. 1988 Aug 20;202(4):921–922. doi: 10.1016/0022-2836(88)90570-0. [DOI] [PubMed] [Google Scholar]
  23. Ivanov V. I., Minchenkova L. E., Schyolkina A. K., Poletayev A. I. Different conformations of double-stranded nucleic acid in solution as revealed by circular dichroism. Biopolymers. 1973;12(1):89–110. doi: 10.1002/bip.1973.360120109. [DOI] [PubMed] [Google Scholar]
  24. Jain S., Zon G., Sundaralingam M. The potentially Z-DNA-forming sequence d(GTGTACAC) crystallizes as A-DNA. J Mol Biol. 1987 Sep 5;197(1):141–145. doi: 10.1016/0022-2836(87)90616-4. [DOI] [PubMed] [Google Scholar]
  25. Johnson B. B., Dahl K. S., Tinoco I., Jr, Ivanov V. I., Zhurkin V. B. Correlations between deoxyribonucleic acid structural parameters and calculated circular dichroism spectra. Biochemistry. 1981 Jan 6;20(1):73–78. doi: 10.1021/bi00504a013. [DOI] [PubMed] [Google Scholar]
  26. Jordan S. R., Pabo C. O. Structure of the lambda complex at 2.5 A resolution: details of the repressor-operator interactions. Science. 1988 Nov 11;242(4880):893–899. doi: 10.1126/science.3187530. [DOI] [PubMed] [Google Scholar]
  27. Klug A., Jack A., Viswamitra M. A., Kennard O., Shakked Z., Steitz T. A. A hypothesis on a specific sequence-dependent conformation of DNA and its relation to the binding of the lac-repressor protein. J Mol Biol. 1979 Jul 15;131(4):669–680. doi: 10.1016/0022-2836(79)90196-7. [DOI] [PubMed] [Google Scholar]
  28. Lauble H., Frank R., Blöcker H., Heinemann U. Three-dimensional structure of d(GGGATCCC) in the crystalline state. Nucleic Acids Res. 1988 Aug 25;16(16):7799–7816. doi: 10.1093/nar/16.16.7799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Leslie A. G., Arnott S., Chandrasekaran R., Ratliff R. L. Polymorphism of DNA double helices. J Mol Biol. 1980 Oct 15;143(1):49–72. doi: 10.1016/0022-2836(80)90124-2. [DOI] [PubMed] [Google Scholar]
  30. Lomonossoff G. P., Butler P. J., Klug A. Sequence-dependent variation in the conformation of DNA. J Mol Biol. 1981 Jul 15;149(4):745–760. doi: 10.1016/0022-2836(81)90356-9. [DOI] [PubMed] [Google Scholar]
  31. McCall M., Brown T., Hunter W. N., Kennard O. The crystal structure of d(GGATGGGAG): an essential part of the binding site for transcription factor IIIA. Nature. 1986 Aug 14;322(6080):661–664. doi: 10.1038/322661a0. [DOI] [PubMed] [Google Scholar]
  32. McCall M., Brown T., Kennard O. The crystal structure of d(G-G-G-G-C-C-C-C). A model for poly(dG).poly(dC). J Mol Biol. 1985 Jun 5;183(3):385–396. doi: 10.1016/0022-2836(85)90009-9. [DOI] [PubMed] [Google Scholar]
  33. Miller J., McLachlan A. D., Klug A. Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 1985 Jun;4(6):1609–1614. doi: 10.1002/j.1460-2075.1985.tb03825.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Moore D. S., Wagner T. E. Origins of the differences between the circular dichroism of DNA and RNA: theoretical calculations. Biopolymers. 1973;12(1):201–221. doi: 10.1002/bip.1973.360120119. [DOI] [PubMed] [Google Scholar]
  35. 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]
  36. Nilsson L., Clore G. M., Gronenborn A. M., Brünger A. T., Karplus M. Structure refinement of oligonucleotides by molecular dynamics with nuclear Overhauser effect interproton distance restraints: application to 5' d(C-G-T-A-C-G)2. J Mol Biol. 1986 Apr 5;188(3):455–475. doi: 10.1016/0022-2836(86)90168-3. [DOI] [PubMed] [Google Scholar]
  37. Nishimura Y., Torigoe C., Tsuboi M. Salt induced B----A transition of poly(dG).poly(dC) and the stabilization of A form by its methylation. Nucleic Acids Res. 1986 Mar 25;14(6):2737–2748. doi: 10.1093/nar/14.6.2737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Otwinowski Z., Schevitz R. W., Zhang R. G., Lawson C. L., Joachimiak A., Marmorstein R. Q., Luisi B. F., Sigler P. B. Crystal structure of trp repressor/operator complex at atomic resolution. Nature. 1988 Sep 22;335(6188):321–329. doi: 10.1038/335321a0. [DOI] [PubMed] [Google Scholar]
  39. Peck L. J., Wang J. C. Sequence dependence of the helical repeat of DNA in solution. Nature. 1981 Jul 23;292(5821):375–378. doi: 10.1038/292375a0. [DOI] [PubMed] [Google Scholar]
  40. Picard B., Wegnez M. Isolation of a 7S particle from Xenopus laevis oocytes: a 5S RNA-protein complex. Proc Natl Acad Sci U S A. 1979 Jan;76(1):241–245. doi: 10.1073/pnas.76.1.241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Rhodes D., Klug A. An underlying repeat in some transcriptional control sequences corresponding to half a double helical turn of DNA. Cell. 1986 Jul 4;46(1):123–132. doi: 10.1016/0092-8674(86)90866-4. [DOI] [PubMed] [Google Scholar]
  42. Rhodes D., Klug A. Helical periodicity of DNA determined by enzyme digestion. Nature. 1980 Aug 7;286(5773):573–578. doi: 10.1038/286573a0. [DOI] [PubMed] [Google Scholar]
  43. Rhodes D., Klug A. Sequence-dependent helical periodicity of DNA. Nature. 1981 Jul 23;292(5821):378–380. doi: 10.1038/292378a0. [DOI] [PubMed] [Google Scholar]
  44. Rhodes D. Structural analysis of a triple complex between the histone octamer, a Xenopus gene for 5S RNA and transcription factor IIIA. EMBO J. 1985 Dec 16;4(13A):3473–3482. doi: 10.1002/j.1460-2075.1985.tb04106.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Shakked Z., Rabinovich D., Kennard O., Cruse W. B., Salisbury S. A., Viswamitra M. A. Sequence-dependent conformation of an A-DNA double helix. The crystal structure of the octamer d(G-G-T-A-T-A-C-C). J Mol Biol. 1983 May 15;166(2):183–201. doi: 10.1016/s0022-2836(83)80005-9. [DOI] [PubMed] [Google Scholar]
  46. Sprecher C. A., Baase W. A., Johnson W. C., Jr Conformation and circular dichroism of DNA. Biopolymers. 1979 Apr;18(4):1009–1019. doi: 10.1002/bip.1979.360180418. [DOI] [PubMed] [Google Scholar]
  47. Srinivasan A. R., Olson W. K. Nucleic acid model building: the multiple backbone solutions associated with a given base morphology. J Biomol Struct Dyn. 1987 Jun;4(6):895–938. doi: 10.1080/07391102.1987.10507690. [DOI] [PubMed] [Google Scholar]
  48. Tunis-Schneider M. J., Maestre M. F. Circular dichroism spectra of oriented and unoriented deoxyribonucleic acid films--a preliminary study. J Mol Biol. 1970 Sep 28;52(3):521–541. doi: 10.1016/0022-2836(70)90417-1. [DOI] [PubMed] [Google Scholar]
  49. Wang A. H., Fujii S., van Boom J. H., van der Marel G. A., van Boeckel S. A., Rich A. Molecular structure of r(GCG)d(TATACGC): a DNA--RNA hybrid helix joined to double helical DNA. Nature. 1982 Oct 14;299(5884):601–604. doi: 10.1038/299601a0. [DOI] [PubMed] [Google Scholar]
  50. Wells R. D., Larson J. E., Grant R. C., Shortle B. E., Cantor C. R. Physicochemical studies on polydeoxyribonucleotides containing defined repeating nucleotide sequences. J Mol Biol. 1970 Dec 28;54(3):465–497. doi: 10.1016/0022-2836(70)90121-x. [DOI] [PubMed] [Google Scholar]
  51. Yoon C., Privé G. G., Goodsell D. S., Dickerson R. E. Structure of an alternating-B DNA helix and its relationship to A-tract DNA. Proc Natl Acad Sci U S A. 1988 Sep;85(17):6332–6336. doi: 10.1073/pnas.85.17.6332. [DOI] [PMC free article] [PubMed] [Google Scholar]

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