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. 1995 Jun 11;23(11):2065–2073. doi: 10.1093/nar/23.11.2065

Base-pair opening and spermine binding--B-DNA features displayed in the crystal structure of a gal operon fragment: implications for protein-DNA recognition.

L W Tari 1, A S Secco 1
PMCID: PMC306985  PMID: 7596838

Abstract

A sequence that is represented frequently in functionally important sites involving protein-DNA interactions is GTG/CAC, suggesting that the trimer may play a role in regulatory processes. The 2.5 A resolution structure of d(CGGTGG)/d(CCACCG), a part of the interior operator (OI, nucleotides +44 to +49) of the gal operon, co-crystallized with spermine, is described herein. The crystal packing arrangement in this structure is unprecedented in a crystal of B-DNA, revealing a close packing of columns of stacked DNA resembling a 5-stranded twisted wire cable. The final structure contains one hexamer duplex, 17 water molecules and 1.5 spermine molecules per crystallographic asymmetric unit. The hexamer exhibits base-pair opening and shearing at T.A resulting in a novel non-Watson-Crick hydrogen-bonding scheme between adenine and thymine in the GTG region. The ability of this sequence to adopt unusual conformations in its GTG region may be a critical factor conferring sequence selectivity on the binding of Gal repressor. In addition, this is the first conclusive example of a crystal structure of spermine with native B-DNA, providing insight into the mechanics of polyamine-DNA binding, as well as possible explanations for the biological action of spermine.

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Selected References

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

  1. Anin M. F., Leng M. Distortions induced in double-stranded oligonucleotides by the binding of cis- or trans-diammine-dichloroplatinum(II) to the d(GTG) sequence. Nucleic Acids Res. 1990 Aug 11;18(15):4395–4400. doi: 10.1093/nar/18.15.4395. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. Braunlin W. H., Strick T. J., Record M. T., Jr Equilibrium dialysis studies of polyamine binding to DNA. Biopolymers. 1982 Jul;21(7):1301–1314. doi: 10.1002/bip.360210704. [DOI] [PubMed] [Google Scholar]
  4. Brennan R. G., Roderick S. L., Takeda Y., Matthews B. W. Protein-DNA conformational changes in the crystal structure of a lambda Cro-operator complex. Proc Natl Acad Sci U S A. 1990 Oct;87(20):8165–8169. doi: 10.1073/pnas.87.20.8165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Briki F., Genest D. Molecular dynamics study of the base pair opening process in the self-complementary octanucleotide d(CTGATCAG). J Biomol Struct Dyn. 1993 Aug;11(1):43–56. doi: 10.1080/07391102.1993.10508708. [DOI] [PubMed] [Google Scholar]
  6. Dickerson R. E. DNA structure from A to Z. Methods Enzymol. 1992;211:67–111. doi: 10.1016/0076-6879(92)11007-6. [DOI] [PubMed] [Google Scholar]
  7. Dickerson R. E. Definitions and nomenclature of nucleic acid structure components. Nucleic Acids Res. 1989 Mar 11;17(5):1797–1803. doi: 10.1093/nar/17.5.1797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Donlan M. E., Lu P. Transcriptional enhancer related DNA sequences: anomalous 1H NMR NOE crosspeaks. Nucleic Acids Res. 1992 Feb 11;20(3):525–532. doi: 10.1093/nar/20.3.525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. 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]
  11. Feuerstein B. G., Pattabiraman N., Marton L. J. Spermine-DNA interactions: a theoretical study. Proc Natl Acad Sci U S A. 1986 Aug;83(16):5948–5952. doi: 10.1073/pnas.83.16.5948. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Feuerstein B. G., Williams L. D., Basu H. S., Marton L. J. Implications and concepts of polyamine-nucleic acid interactions. J Cell Biochem. 1991 May;46(1):37–47. doi: 10.1002/jcb.240460107. [DOI] [PubMed] [Google Scholar]
  13. Gralla J., Crothers D. M. Free energy of imperfect nucleic acid helices. 3. Small internal loops resulting from mismatches. J Mol Biol. 1973 Aug 5;78(2):301–319. doi: 10.1016/0022-2836(73)90118-6. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Hartmann B., Leng M., Ramstein J. Poly(dA-dT).poly(dA-dT) two-pathway proton exchange mechanism. Effect of general and specific base catalysis on deuteration rates. Biochemistry. 1986 Jun 3;25(11):3073–3077. doi: 10.1021/bi00359a001. [DOI] [PubMed] [Google Scholar]
  16. Igarashi K., Sakamoto I., Goto N., Kashiwagi K., Honma R., Hirose S. Interaction between polyamines and nucleic acids or phospholipids. Arch Biochem Biophys. 1982 Dec;219(2):438–443. doi: 10.1016/0003-9861(82)90175-8. [DOI] [PubMed] [Google Scholar]
  17. Irani M. H., Orosz L., Adhya S. A control element within a structural gene: the gal operon of Escherichia coli. Cell. 1983 Mar;32(3):783–788. doi: 10.1016/0092-8674(83)90064-8. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Kahn J. D., Yun E., Crothers D. M. Detection of localized DNA flexibility. Nature. 1994 Mar 10;368(6467):163–166. doi: 10.1038/368163a0. [DOI] [PubMed] [Google Scholar]
  20. Larsen T. A., Kopka M. L., Dickerson R. E. Crystal structure analysis of the B-DNA dodecamer CGTGAATTCACG. Biochemistry. 1991 May 7;30(18):4443–4449. doi: 10.1021/bi00232a010. [DOI] [PubMed] [Google Scholar]
  21. Lavery R., Sklenar H. Defining the structure of irregular nucleic acids: conventions and principles. J Biomol Struct Dyn. 1989 Feb;6(4):655–667. doi: 10.1080/07391102.1989.10507728. [DOI] [PubMed] [Google Scholar]
  22. Leijon M., Gräslund A. Effects of sequence and length on imino proton exchange and base pair opening kinetics in DNA oligonucleotide duplexes. Nucleic Acids Res. 1992 Oct 25;20(20):5339–5343. doi: 10.1093/nar/20.20.5339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Leroy J. L., Gao X. L., Guéron M., Patel D. J. Proton exchange and internal motions in two chromomycin dimer-DNA oligomer complexes. Biochemistry. 1991 Jun 11;30(23):5653–5661. doi: 10.1021/bi00237a003. [DOI] [PubMed] [Google Scholar]
  24. Leroy J. L., Kochoyan M., Huynh-Dinh T., Guéron M. Characterization of base-pair opening in deoxynucleotide duplexes using catalyzed exchange of the imino proton. J Mol Biol. 1988 Mar 20;200(2):223–238. doi: 10.1016/0022-2836(88)90236-7. [DOI] [PubMed] [Google Scholar]
  25. Lu P., Cheung S., Arndt K. Possible molecular detent in the DNA structure at regulatory sequences. J Biomol Struct Dyn. 1983 Oct;1(2):509–521. doi: 10.1080/07391102.1983.10507458. [DOI] [PubMed] [Google Scholar]
  26. Majumdar A., Adhya S. Effect of ethylation of operator-phosphates on Gal repressor binding. DNA contortion by repressor. J Mol Biol. 1989 Jul 20;208(2):217–223. doi: 10.1016/0022-2836(89)90383-5. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Marrot L., Leng M. Chemical probes of the conformation of DNA modified by cis-diamminedichloroplatinum(II). Biochemistry. 1989 Feb 21;28(4):1454–1461. doi: 10.1021/bi00430a005. [DOI] [PubMed] [Google Scholar]
  29. Matthews B. W. Protein-DNA interaction. No code for recognition. Nature. 1988 Sep 22;335(6188):294–295. doi: 10.1038/335294a0. [DOI] [PubMed] [Google Scholar]
  30. Meers P., Hong K., Bentz J., Papahadjopoulos D. Spermine as a modulator of membrane fusion: interactions with acidic phospholipids. Biochemistry. 1986 Jun 3;25(11):3109–3118. doi: 10.1021/bi00359a007. [DOI] [PubMed] [Google Scholar]
  31. Narayana N., Ginell S. L., Russu I. M., Berman H. M. Crystal and molecular structure of a DNA fragment: d(CGTGAATTCACG). Biochemistry. 1991 May 7;30(18):4449–4455. doi: 10.1021/bi00232a011. [DOI] [PubMed] [Google Scholar]
  32. Olson W. K. Computational studies of polynucleotide flexibility. Nucleic Acids Res. 1982 Feb 11;10(3):777–787. doi: 10.1093/nar/10.3.777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pabo C. O., Sauer R. T. Transcription factors: structural families and principles of DNA recognition. Annu Rev Biochem. 1992;61:1053–1095. doi: 10.1146/annurev.bi.61.070192.005201. [DOI] [PubMed] [Google Scholar]
  34. Pingoud A. Spermidine increases the accuracy of type II restriction endonucleases. Suppression of cleavage at degenerate, non-symmetrical sites. Eur J Biochem. 1985 Feb 15;147(1):105–109. doi: 10.1111/j.1432-1033.1985.tb08725.x. [DOI] [PubMed] [Google Scholar]
  35. Pingoud A., Urbanke C., Alves J., Ehbrecht H. J., Zabeau M., Gualerzi C. Effect of polyamines and basic proteins on cleavage of DNA by restriction endonucleases. Biochemistry. 1984 Nov 20;23(24):5697–5703. doi: 10.1021/bi00319a006. [DOI] [PubMed] [Google Scholar]
  36. Plaxco K. W., Goddard W. A., 3rd Contributions of the thymine methyl group to the specific recognition of poly- and mononucleotides: an analysis of the relative free energies of solvation of thymine and uracil. Biochemistry. 1994 Mar 15;33(10):3050–3054. doi: 10.1021/bi00176a038. [DOI] [PubMed] [Google Scholar]
  37. Pullman B. Electrostatics of Polymorphic DNA. J Biomol Struct Dyn. 1983 Dec;1(3):773–794. doi: 10.1080/07391102.1983.10507481. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Rastinejad F., Artz P., Lu P. Origin of the asymmetrical contact between lac repressor and lac operator DNA. J Mol Biol. 1993 Oct 5;233(3):389–399. doi: 10.1006/jmbi.1993.1519. [DOI] [PubMed] [Google Scholar]
  40. Sarai A., Takeda Y. Lambda repressor recognizes the approximately 2-fold symmetric half-operator sequences asymmetrically. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6513–6517. doi: 10.1073/pnas.86.17.6513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Schultz S. C., Shields G. C., Steitz T. A. Crystal structure of a CAP-DNA complex: the DNA is bent by 90 degrees. Science. 1991 Aug 30;253(5023):1001–1007. doi: 10.1126/science.1653449. [DOI] [PubMed] [Google Scholar]
  42. Tabor C. W., Tabor H. Polyamines. Annu Rev Biochem. 1984;53:749–790. doi: 10.1146/annurev.bi.53.070184.003533. [DOI] [PubMed] [Google Scholar]
  43. Thomas T. J., Bloomfield V. A. Ionic and structural effects on the thermal helix-coil transition of DNA complexed with natural and synthetic polyamines. Biopolymers. 1984 Jul;23(7):1295–1306. doi: 10.1002/bip.360230713. [DOI] [PubMed] [Google Scholar]
  44. Thomas T., Kiang D. T. A twenty-two-fold increase in the relative affinity of estrogen receptor to poly (dA-dC).poly (dG-dT) in the presence of polyamines. Nucleic Acids Res. 1988 May 25;16(10):4705–4720. doi: 10.1093/nar/16.10.4705. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Timsit Y., Westhof E., Fuchs R. P., Moras D. Unusual helical packing in crystals of DNA bearing a mutation hot spot. Nature. 1989 Oct 5;341(6241):459–462. doi: 10.1038/341459a0. [DOI] [PubMed] [Google Scholar]
  46. Wemmer D. E., Srivenugopal K. S., Reid B. R., Morris D. R. Nuclear magnetic resonance studies of polyamine binding to a defined DNA sequence. J Mol Biol. 1985 Sep 20;185(2):457–459. doi: 10.1016/0022-2836(85)90418-8. [DOI] [PubMed] [Google Scholar]
  47. Williams L. D., Frederick C. A., Ughetto G., Rich A. Ternary interactions of spermine with DNA: 4'-epiadriamycin and other DNA: anthracycline complexes. Nucleic Acids Res. 1990 Sep 25;18(18):5533–5541. doi: 10.1093/nar/18.18.5533. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Xiao L., Swank R. A., Matthews H. R. Photoaffinity polyamines: sequence-specific interactions with DNA. Nucleic Acids Res. 1991 Jul 11;19(13):3701–3708. doi: 10.1093/nar/19.13.3701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Zakrzewska K., Pullman B. Spermine-nucleic acid interactions: a theoretical study. Biopolymers. 1986 Mar;25(3):375–392. doi: 10.1002/bip.360250302. [DOI] [PubMed] [Google Scholar]
  50. Zwieb C., Kim J., Adhya S. DNA bending by negative regulatory proteins: Gal and Lac repressors. Genes Dev. 1989 May;3(5):606–611. doi: 10.1101/gad.3.5.606. [DOI] [PubMed] [Google Scholar]

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