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. 1979 Aug;76(8):3870–3874. doi: 10.1073/pnas.76.8.3870

Torsional stress and local denaturation in supercoiled DNA.

C J Benham
PMCID: PMC383937  PMID: 226985

Abstract

It is shown that local denaturation can be a natural consequence of supercoiling, even in environments where base pairing of linear DNA is energetically favored. Any change in the molecular total twist from its unstressed value is partitioned between local denaturation and smooth twisting in both the native and coil regions so as to minimize the total conformational free energy involved. Threshold degrees of torsional deformation are found for the existence of stable, locally melted conformations. As these thresholds are surpassed, the number of denatured bases increase smoothly from zero. Existing experimental evidence regarding denaturation in supercoiled DNA is in good agreement with the predictions of this theory. In addition, from existing data one can estimate the partitioning of superhelicity between twisting and writhing. Possible consequences of stress-induced strand separation on the accessibility of the DNA to enzyme attack are discussed. Control of local melting by DNA topoisomerases and DNA gyrases could regulate diverse events involved in transcription, replication, recombination, and repair.

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Selected References

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

  1. Anderson P., Bauer W. Supercoiling in closed circular DNA: dependence upon ion type and concentration. Biochemistry. 1978 Feb 21;17(4):594–601. doi: 10.1021/bi00597a006. [DOI] [PubMed] [Google Scholar]
  2. Beard P., Morrow J. F., Berg P. Cleavage of circular, superhelical simian virus 40 DNA to a linear duplex by S1 nuclease. J Virol. 1973 Dec;12(6):1303–1313. doi: 10.1128/jvi.12.6.1303-1313.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Beerman T. A., Lebowitz J. Further analysis of the altered secondary structure of superhelical DNA. Sensitivity to methylmercuric hydroxide a chemical probe for unpaired bases. J Mol Biol. 1973 Sep 25;79(3):451–470. doi: 10.1016/0022-2836(73)90398-7. [DOI] [PubMed] [Google Scholar]
  4. Benham C. J. An elastic model of the large-scale structure of duplex DNA. Biopolymers. 1979 Mar;18(3):609–623. doi: 10.1002/bip.1979.360180310. [DOI] [PubMed] [Google Scholar]
  5. Botchan P., Wang J. C., Echols H. Effect of circularity and superhelicity on transcription from bacteriophagelambda DNA. Proc Natl Acad Sci U S A. 1973 Nov;70(11):3077–3081. doi: 10.1073/pnas.70.11.3077. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brack C., Bickle T. A., Yuan R. The relation of single-stranded regions in bacteriophage PM2 supercoiled DNA to the early melting sequences. J Mol Biol. 1975 Aug 25;96(4):693–702. doi: 10.1016/0022-2836(75)90146-1. [DOI] [PubMed] [Google Scholar]
  7. CROTHERS D. M., ZIMM B. H. THEORY OF THE MELTING TRANSITION OF SYNTHETIC POLYNUCLEOTIDES: EVALUATION OF THE STACKING FREE ENERGY. J Mol Biol. 1964 Jul;9:1–9. doi: 10.1016/s0022-2836(64)80086-3. [DOI] [PubMed] [Google Scholar]
  8. Dean W. W., Lebowitz J. Partial alteration of secondary structure in native superhelical DNA. Nat New Biol. 1971 May 5;231(18):5–8. [PubMed] [Google Scholar]
  9. Delius H., Mantell N. J., Alberts B. Characterization by electron microscopy of the complex formed between T4 bacteriophage gene 32-protein and DNA. J Mol Biol. 1972 Jun 28;67(3):341–350. doi: 10.1016/0022-2836(72)90454-8. [DOI] [PubMed] [Google Scholar]
  10. Eisenberg S., Scott J. F., Kornberg A. An enzyme system for replication of duplex circular DNA: the replicative form of phage phi X174. Proc Natl Acad Sci U S A. 1976 May;73(5):1594–1597. doi: 10.1073/pnas.73.5.1594. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Eisenberg S., Scott J. F., Kornberg A. Enzymatic replication of viral and complementary strands of duplex DNA of phage phiX174 proceeds by seprate mechanisms. Proc Natl Acad Sci U S A. 1976 Sep;73(9):3151–3155. doi: 10.1073/pnas.73.9.3151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Falco S. C., Zivin R., Rothman-Denes L. B. Novel template requirements of N4 virion RNA polymerase. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3220–3224. doi: 10.1073/pnas.75.7.3220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Grosschedl R., Hobom G. DNA sequences and structural homologies of the replication origins of lambdoid bacteriophages. Nature. 1979 Feb 22;277(5698):621–627. doi: 10.1038/277621a0. [DOI] [PubMed] [Google Scholar]
  14. Hays J. B., Boehmer S. Antagonists of DNA gyrase inhibit repair and recombination of UV-irradiated phage lambda. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4125–4129. doi: 10.1073/pnas.75.9.4125. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Holloman W. K., Wiegand R., Hoessli C., Radding C. M. Uptake of homologous single-stranded fragments by superhelical DNA: a possible mechanism for initiation of genetic recombination. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2394–2398. doi: 10.1073/pnas.72.6.2394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hsieh T. S., Wang J. C. Thermodynamic properties of superhelical DNAs. Biochemistry. 1975 Feb 11;14(3):527–535. doi: 10.1021/bi00674a011. [DOI] [PubMed] [Google Scholar]
  17. INMAN R. B., BALDWIN R. L. Formation of hybrid molecules from two alternating DNA copolymers. J Mol Biol. 1962 Aug;5:185–200. doi: 10.1016/s0022-2836(62)80083-7. [DOI] [PubMed] [Google Scholar]
  18. Johnson P. H., Laskowski M., Sr Mung bean nuclease I. II. Resistance of double stranded deoxyribonucleic acid and susceptibility of regions rich in adenosine and thymidine to enzymatic hydrolysis. J Biol Chem. 1970 Feb 25;245(4):891–898. [PubMed] [Google Scholar]
  19. Landy A., Ross W. Viral integration and excision: structure of the lambda att sites. Science. 1977 Sep 16;197(4309):1147–1160. doi: 10.1126/science.331474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lau P. P., Gray H. B., Jr Extracellular nucleases of Alteromonas espejiana BAL 31.IV. The single strand-specific deoxyriboendonuclease activity as a probe for regions of altered secondary structure in negatively and positively supercoiled closed circular DNA. Nucleic Acids Res. 1979 Jan;6(1):331–357. doi: 10.1093/nar/6.1.331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. LeBon J. M., Kado C. I., Rosenthal L. J., Chirikjian J. G. DNA modifying enzymes of Agrobacterium tumefaciens: effect of DNA topoisomerase, restriction endonuclease, and unique DNA endonuclease on plasmid and plant DNA. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4097–4101. doi: 10.1073/pnas.75.9.4097. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Levitt M. How many base-pairs per turn does DNA have in solution and in chromatin? Some theoretical calculations. Proc Natl Acad Sci U S A. 1978 Feb;75(2):640–644. doi: 10.1073/pnas.75.2.640. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Marians K. J., Ikeda J. E., Schlagman S., Hurwitz J. Role of DNA gyrase in phiX replicative-form replication in vitro. Proc Natl Acad Sci U S A. 1977 May;74(5):1965–1968. doi: 10.1073/pnas.74.5.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mizuuchi K., Gellert M., Nash H. A. Involement of supertwisted DNA in integrative recombination of bacteriophage lambda. J Mol Biol. 1978 May 25;121(3):375–392. doi: 10.1016/0022-2836(78)90370-4. [DOI] [PubMed] [Google Scholar]
  25. Mizuuchi K., Nash H. A. Restriction assay for integrative recombination of bacteriophage lambda DNA in vitro: requirement for closed circular DNA substrate. Proc Natl Acad Sci U S A. 1976 Oct;73(10):3524–3528. doi: 10.1073/pnas.73.10.3524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Morrow J. F., Berg P. Cleavage of Simian virus 40 DNA at a unique site by a bacterial restriction enzyme. Proc Natl Acad Sci U S A. 1972 Nov;69(11):3365–3369. doi: 10.1073/pnas.69.11.3365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Spatz H. C., Crothers D. M. The rate of DNA unwinding. J Mol Biol. 1969 Jun 14;42(2):191–219. doi: 10.1016/0022-2836(69)90038-2. [DOI] [PubMed] [Google Scholar]
  28. Sumida-Yasumoto C., Hurwitz J. Synthesis of phiX174 viral DNA in vitro depends on phiX replicative form DNA. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4195–4199. doi: 10.1073/pnas.74.10.4195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Vinograd J., Lebowitz J., Watson R. Early and late helix-coil transitions in closed circular DNA. The number of superhelical turns in polyoma DNA. J Mol Biol. 1968 Apr 14;33(1):173–197. doi: 10.1016/0022-2836(68)90287-8. [DOI] [PubMed] [Google Scholar]
  30. Wang J. C. Interactions between twisted DNAs and enzymes: the effects of superhelical turns. J Mol Biol. 1974 Aug 25;87(4):797–816. doi: 10.1016/0022-2836(74)90085-0. [DOI] [PubMed] [Google Scholar]
  31. Woodworth-Gutai M., Lebowitz J. Introduction of interrupted secondary structure in supercoiled DNA as a function of superhelix density: consideration of hairpin structures in superhelical DNA. J Virol. 1976 Apr;18(1):195–204. doi: 10.1128/jvi.18.1.195-204.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]

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