INTERPRETATION OF HOT SPOTS OF ULTRAVOLETIC MUTAGENESIS FORMED ON A LAGGING STRAND OF DOUBLE-STRANDED DNA OF THE SUPF GENE
Abstract and keywords
Abstract (English):
At present, the mechanism of formation of hot and cold spots of ultraviolet mutagenesis is not clear. I developed a polymerase-tautomeric model of the mechanism of formation of hot and cold spots of ultraviolet mutagenesis and showed that the probability of mutation formation depends on the processes of propagation of excitation energy along the DNA molecule. In my proposed polymerase-tautomeric model of ultraviolet mutagenesis, it was shown that mutations are formed opposite only those cis-syn cyclobutane pyrimidine dimers, one or both of which are in rare tautomeric forms. In the polymerase-tautomeric model of the mechanism of formation of hot and cold spots of ultraviolet mutagenesis, I have shown that the hot spots of ultraviolet mutagenesis are those cis-syn cyclobutane pyrimidine dimers to which the most excitation energy is transferred. In a number of works, I calculated the relative probabilities of mutations formed opposite the DNA bases that are part of the cis-syn cyclobutane pyrimidine dimers that appeared upon irradiation of double-stranded DNA of the supF gene. In this article, based on the results of previous calculations, I interpret experimental data in which hot spots of ultraviolet mutagenesis are DNA regions consisting of three or more pyrimidine DNA bases arranged in a row.

Keywords:
UV mutagenesis, rare tautomeric forms of DNA bases, cis-syn cyclobutane pyrimidine dimers, hot and cold spots of ultraviolet mutagenesis, excitation energy transfer along the DNA molecule, singlet levels of DNA bases, triplet levels of DNA bases
Text
Publication text (PDF): Read Download
References

1. Banyasz A., Vayá I., Changenet-Barret P., Gustavsson T., Douki T., Markovitsi D. Base pairing enhances fluorescence and favors cyclobutane dimer formation induced upon absorption of UVA radiation by DNA. Journal of the American Chemical Society, 2011, vol. 133, no. 14, pp. 5163-5165.

2. Besaratinia A., Yoon J.I., Schroeder C., Bradforth S.E., Cockburn M., Pfeifer G.P. Wavelength dependence of ultraviolet radiation-induced DNA damage as determined by laser irradiation suggests that cyclobutane pyrimidine dimers are the principal DNA lesions produced by terrestrial sunlight. The Federation of American Societies for Experimental Biology Journal, 2011, vol. 25, no. 9, pp. 3079-3091.

3. Hendel A., Ziv O., Gueranger Q., Geacintov N., Livneh Z. Reduced efficiency and increased mutagenicity of translesion DNA synthesis across a TT cyclobutane pyrimidine dimer, but not a TT 6-4 photoproduct, in human cells lacking DNA polymerase η. DNA Repair, 2008, vol. 7, no. 10, pp. 1636-1646.

4. Vasquez-Del C.R., Silverstein T.D., Lone S., Johnson R.E., Prakash L., Prakash S., Aggarwal A.K. Role of human DNA polymerase κ in extension opposite from a cis-syn thymine dimer. Journal of Molecular Biology, 2011, vol. 408, no. 2, pp. 252-261.

5. Lawrence C.W., Banerjee S.K., Borden A., LeClerc J.E. T-T cyclobutane dimers are misinstructive, rather than non-instructive, mutagenic lesions. Molecular and General Genetics, 1990, vol. 222, no. 1, pp. 166-169.

6. Santiago M.J., Alejandre-Durán A., Ruiz-Rubio M. Analysis of UV-induced mutation spectra in Escherichia coli by DNA polymerase η from Arabidopsis thaliana. Mutation Research, 2006, vol. 601, no. 1-2, pp. 51-60.

7. Parris C.N., Levy D.D., Jessee J., Seidman M.M. Proximal and distal effects of sequence context on ultraviolet mutational hotspots in a shuttle vector replicated in xeroderma cells. Journal of Molecular Biology, 1994, vol. 236, no. 2, pp. 491-502.

8. Canella K.A., Seidman M.M. Mutation spectra in supF: approaches to elucidating sequence context effects. Mutation Research, 2000, vol. 450, no. 1-2, pp. 61-73.

9. Taylor J.-S. New structural and mechanistic insight into the A-rule and the instructional and non-instructional behavior of DNA photoproducts and other lesions. Mutation Research, 2002, vol. 510, no. 1, pp. 55-70.

10. Bebenek K., Pedersen L.C., Kunkel T.A. Replication infidelity via a mismatch with Watson-Crick geometry. Proceedings of the National Academy of Sciences of the United States of America, 2011, vol. 108, no. 5, pp. 1862-1867.

11. Wang W., Hellinga H.W., Beese L.S. Structural evidence for the rare tautomer hypothesis of spontaneous mutagenesis. Proceedings of the National Academy of Sciences of the United States of America, 2011, vol. 108, no. 43, pp. 17644-17648.

12. Danilov V.I., Mikhaleva O.V., Slyusarchuk O.N., Stewart J.J., Alderfer J.L. On a new mechanism of mutations induced by UV light. Theoretical study of two-proton phototautomerization in model DNA base pairs. Biopolymers and Kletka, vol. 13, no. 4, pp. 261-268 (In Russ.).

13. Podolyan Y., Gorb L., Leszczynski J. Ab initio study of the prototropic tautomerism of cytosine and guanine and their contribution to spontaneous point mutations. International Journal of Molecular Sciences, 2003, vol. 4, no. 7, pp. 410-421.

14. Danilov V.I., Anisimov V.M., Kurita N., Hovorun D.M. MP2 and DFT studies of the DNA rare base pairs: the molecular mechanism of spontaneous substitution mutations conditioned by tautomerism of bases. Chemical Physics Letters, 2005, vol. 412, no. 4-6, pp. 285-293.

15. Grebneva H.A. Nature and possible mechanisms formation of potential mutations arising at emerging of thymine dimers after irradiation of double-stranded DNA by ultraviolet light. Journal of Molecule Structure, 2003, vol. 645, pp. 133-143.

16. Grebneva H.A. A model for targeted substitution mutagenesis during SOS replication of double-stranded DNA containing cis-syn cyclobutane thymine dimers. Environmental and Molecular Mutagenesis, 2006, vol. 47, no. 9, pp. 733-745.

17. Grebneva E.A. Three sources of potential untargeted ultraviolet mutations. Proceedings of the VI All-Ukrainian Scientific and Technical Conference. Topical issues of theoretical and applied biophysics, physics and chemistry. Ukraine, Sevastopol, April 26-30, 2010, pp. 15-18 (In Russ.).

18. Grebneva E.A. Nature and mechanisms of formation of hot and cold spots of ultraviolet mutagenesis. Dopovidi NAN Ukraine, 2012, no. 10, p. 181-187. (In Russ.).

19. Grebneva E.A. The mechanism of deletion formation during the synthesis of DNA containing cis-syn cyclobutane cytosine dimers. Proceedings of the VIII International Scientific and Technical Conference “Actual Issues of Biological Physics and Chemistry”, Sevastopol, April 23-27, 2012, pp. 88-90 (In Russ.).

20. Grebneva E.A. Mechanisms of formation of hot and cold spots of ultraviolet targeted base substitution mutations. Proceedings of the IX International Scientific and Technical Conference "Actual Issues of Biological Physics and Chemistry", Sevastopol, April 23-27, 2013, pp. 18-20 (In Russ.).

21. Grebneva H.A. Mechanisms of targeted frameshift mutations – insertion formation under error-prone or SOS synthesis of DNA containing cis-syn cyclobutane thymine dimers. Molecular Biology (Moscow), 2014, vol. 48, no. 4, pp. 457-467 (In Russ.).

22. Grebneva H.A. A polymerase – tautomeric model for targeted frameshift mutations: deletions formation during error-prone or SOS replication of double-stranded DNA containing cis-syn cyclobutane thymine dimers. Journal of Photonic Materials and Technology, 2015, vol. 1, no. 2, pp. 19-26.

23. Grebneva E.A. Mechanisms for the formation of targeted complex insertions during the synthesis of a DNA molecule containing cis-syn cyclobutane thymine dimers. Dopovidi NAN Ukraine, 2015, no. 5, pp. 145-154 (In Russ.).

24. Grebneva E.A. Mechanisms of formation of targeted insertions during error-prone or SOS synthesis of DNA containing cis-syn cyclobutane thymine dimers. Proceedings of the X International Scientific and Technical Conference “Actual Issues of Biological Physics and Chemistry. Sevastopol August 17-21, 2015, pp. 70-74 (In Russ.).

25. Grebneva E.A. Polymerase-tautomeric model of the mechanism of formation of targeted complex insertions during the synthesis of DNA containing cis-syn cyclobutane thymine dimers. Proceedings of the XI International Scientific and Technical Conference "Actual Issues of Biological Physics and Chemistry" in 2 volumes, Sevastopol State University, vol. 1, 298 p., Sevastopol, April 25-29, 2016, pp. 156-160 (In Russ.).

26. Grebneva H.A. A polymerase-tautomeric model for radiation-induced bystander effects: a model for untargeted substitution mutagenesis during error-prone and SOS replication of double-stranded DNA containing thymine and adenine in rare tautomeric forms. International Journal of Molecular Biology: Open Access, 2017, vol. 2, no. 2, pp. 1-14.

27. Grebneva H.A. A Polymerase-tautomeric model for targeted substitution mutations formation during error-prone and SOS replication of double-stranded DNA, containing cis-syn cyclobutane cytosine dimers. International Journal of Molecular Biology: Open Access, 2016, vol. I, no. 1, pp. 1-16.

28. Grebneva H.A. Polymerase-tautomeric model for ultraviolet mutagenesis: targeted base substitution and frameshift mutations caused by cis-syn cyclobutane thymine dimers. Germany, LAP LAMBERT Academic Publishing, 2017, 132 p.

29. Grebneva H.A. A polymerase-tautomeric model for radiation-induced genomic instability: targeted delayed substitution mutations during error-prone and SOS replication of double-stranded DNA, containing cis-syn cyclobutane cytosine dimers. International Journal of Molecular Biology: Open Access, 2018, vol. 3, pp. 125-141.

30. Grebneva H.A. Paradigm change in mutagenesis: polymerase-tautomeric models for targeted, delayed and untargeted ultraviolet mutagenesis during error-prone and SOS replication of double-stranded DNA, containing cis-syn cyclobutane thymine dimers. International Journal of Molecular Biology: Open Access, 2019, vol. 4, no. 1, pp. 1-15.

31. Grebneva E.A. Theory of thermal relaxation of the excitation energy of hydrogen bonds in DNA. Its contribution to ultraviolet mutagenesis. Saarbrucken, Germany. LAP LAMBERT Academic Publishing, 2019, 345 p. (In Russ.).

32. Grebneva H.A. Polymerase-tautomeric model for untargeted delayed base substitution mutations formation during error-prone and SOS replication of double-stranded DNA containing thymine and adenine in some rare tautomeric forms. Journal of Oncology Research, 2019, vol. 1, no. 2, pp. 24-37.

33. Grebneva H.A. Polymerase-tautomeric models for A-rule during error-prone and SOS synthesis of DNA containing cis-syn cyclobutane thymine dimers or thymines and adenines in some rare tautomeric forms. Trends in Cell & Molecular Biology, 2019, vol. 14, pp. 51-68.

34. Grebneva H.A. 2020. Polymerase-tautomeric cancer risk model: the formation of 100% mutations is due to exposure to mutagens. Trends in Cell & Molecular Biology, 2020, vol. 15, pp. 13-28.

35. Grebneva H.A. Method for calculating the relative probabilities of the formation of cis-syn cyclobutane pyrimidine dimers and rare tautomeric forms of DNA bases at any sites of double-stranded DNA. Fizika and Tecknika Visokih Davleniy, 2021, vol. 31, no. 3, pp. 88-103 (In Russ.).

36. Grebneva E.A. The percentage of mutations that are formed under the influence of mutagens. Fizika and Tecknika Visokih Davleniy, 2022, vol. 32, no. 1, pp. 101-113 (In Russ.).

37. Grebneva E.A. Polymerase-tautomeric model of the risk of malignant tumor formation. Fizika and Tecknika Visokih Davleniy, 2022, vol. 32, no. 4, pp. 99-104 (In Russ.).

38. Grebneva E.A. A model for the formation of hot and cold spots of ultraviolet mutagenesis in the double-stranded DNA region of the supF gene. Fizika and Tecknika Visokih Davleniy, 2023, vol. 33, no. 2, pp. 101-111 (In Russ.).

39. Watson J.D., Grick F.H.C. The structure of DNA. Cold Spring Harbor Symposia on Quantitative Biology, 1953, vol. 18, pp. 123-131.

40. Hauswirth W., Daniels M. Excited states of the nucleic acids: polymeric forms. Photochemistry and Photobiology of Nucleic Acids, 1976, vol. 1, pp. 109-167.

41. Galley W.C. On the triplet states of polynucleotide-acridine complexes. I. triplet energy delocalization in the 9-aminiacridine-DNA complex. Biopolymers, 1968, vol. 6, pp. 1279-1296.

42. Rahn R., Shulman R., Longworth J. Phosphorescence and electron-spin resonance studies of the UV-excited triplet state of DNA. The Journal of Chemical Physics, 1966, vol. 45, pp. 2955-2965.

43. Vekshin N.L. Photonics of biological structures. Pushchino: Institute of Biological Physics of the Academy of Sciences of the USSR, 1988, 51 p. (In Russ.).

44. Vekshin N.L. Transfer of excitation in macromolecules. Results of science and technology. Series Radiation Chemistry. Photochemistry, vol. 7. M.: VINITI, 1989, 164 p. (In Russ.).

45. Lamola A.A., Gamane T. Sensitized photodimerization of thymine in DNA. Proceedings of the National Academy of Sciences of the United States of America, 1967, vol. 58, no. 2, pp. 443-446.

46. Novak M.J., Lapinski L., Kwiatkowski J.S., Leszczynski J. Molecular structure and infrared spectra of the DNA bases and their derivatives: theory and experiment. Computational chemistry: reviews of current trends. J. Leszczynski Ed., Wold Scientific Publishing Co. Pte. Ltd, River Edge, NJ, 1997, vol. 2, pp. 140-182.

47. Friedberg E.C., Walker G.C., Siede W. DNA repair and mutagenesis. Washington: ASM Press, DC 1995.

48. Friedberg E.C., Walker G.C., Siede W., Wood R.D., Schultz R.A., Ellenberger T. DNA repair and mutagenesis. part 3. ASM Press, 2006.

49. Lockshin R.A., Zakeri Z. (eds.). When cells die II: A comprehensive evaluation of apoptosis and programmed cell death. John Wiley & Sons, 2004, 572 p.


Login or Create
* Forgot password?