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

Helen A. Grebneva (Donetsk Physical and Technical Institute, National Academy of Science of Ukraine, 03680 Kiev, Nauky av. 46, Ukraine,)

Article ID: 1584

DOI: https://doi.org/10.30564/jor.v1i2.1584

Abstract


Polymerase-tautomeric model for untargeted delayed base substitution mutations is proposed. Structural analysis of bases insertion showed that any canonical bases may be inserted opposite rare tautomeric forms of thymine T3*, adenines A2* and A4* so that between them hydrogen bonds are formed. Canonical adenine and cytosine can be incorporated opposite canonical thymine only. Canonical thymine and guanine can be incorporated opposite canonical adenine only. If in the synthesis of DNA containing rare tautomeric forms of thymine T3*, adenines A2* and A4*, involved DNA polymerases with relatively high fidelity of synthesis, mutations not appear. However, if further DNA synthesis will involve DNA polymerases having a low fidelity of synthesis, there may be base substitution mutations. It was shown that the conclusion made in the Tomasetti and Vogelstein cancer risk model that the formation of about 67% of all mutations was not caused by exposure to any mutagens is erroneous. 


Keywords


Radiation-induced genomic instability; Untargeted delayed base substitution mutations; UV-mutagenesis; Rare tautomeric forms of DNA bases; Thymine, adenine; Error-prone replication; SOS replication

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[1] Bernstein C., Prasad A.R., Nfonsam V., Bernstein H. DNA damage, DNA repair and cancer, new research directions in DNA repair. INTECH, Prof. Clark Chen (Ed.), 2013: 232. ISBN: 978-953-51-1114-6

[2] Berger M.F., Hodis E., Heffernan T.P. et al. Melanoma genome sequencing reveals frequent PREX2 mutations. Nature, 2012, 485(7399): 502–506.

[3]

[4] Little J.B. Genomic instability and bystander effects: a historical perspective. Oncogene, 2003, 22: 6978–6987.

[5] Ullrich R.L., Ponnaiya B. Radiation-induced instability and its relation to radiation carcinogenesis. Int. J. Radiat. Biol., 1998, 74(6): 747–754.

[6] Niwa O. Radiation induced dynamic mutations and transgenerational effects. J. Radiat. Res., 2006, 47: B25-B30.

[7] Maor-Shoshani A., Reuven N.B., Tomer G., Livneh Z. Highly mutagenic replication by polymerase V (UmuC) provides a mechanism for SOS untargeted mutagenesis. Proc. Natl. Acad. Sci. USA., 2000, 97: 565–570.

[8] Tang M., Pham P., Shen X., Taylor J.-S., O’Donnell M., Woodgate R., Goodman M. Roles of Escherichia coli DNA polymerase IV and V in lesion-targeted and untargeted SOS mutagenesis. Nature, 2000, 404: 1014-1018.

[9] Lawrence C.W., Christensen R.B. The mechanism of untargeted mutagenesis in UV-irradiated yeast. Mol. Gen. Genet., 1982, 186: 1-9.

[10] Wood R.D., Hutchinson F. Non-targeted mutagenesis induced by ultraviolet light in Escherichia coli. J. Mol. Biol., 1984, 173: 293–305.

[11] Kunz B.A., Glickman B.W. The role of pyrimidine dimers as premutagenic lesions: a study of targeted vs. untargeted mutagenesis in the lacI gene of Escherichia coli. Genetics, 1984, 106: 347–364.

[12] Brotcorne-Lanneye A., Maenhaul-Michel G. Role of RecA protein in untargeted UV mutagenesis of bacteriophage λ: evidence for requirement for the dinB gene. Proc. Natl. Acad. Sci. USA, 1986, 83: 3904–3908.

[13] Caillet-Fauquet P., Maenhaut-Michel G. Nature of the SOS mutator activity: genetic characterization of untargeted mutagenesis in Escherichia coli. Molecular and General Genetics, 1988, 213: 491-498.

[14] Kim S.R., Matsui K., Yamada M., Gruz P., Nohmi T. Roles of chromosomal and episomal dinB genes encoding DNA pol IV in targeted and untargeted mutagenesis in Escherichia coli. Mol. Genet. Genomics, 2001, 266: 207–215.

[15] Fijalkowska I.J., Dunn R.L., Schaaper R.M. Genetic requirements and mutational specificity of the Escherichia coli SOS mutator activity. J. Bacteriol., 1997, 179: 7435–7445.

[16] Nelson J.R., Lawrence C., Hinkle D.C. Thymine-thymine dimers bypass by yeast DNA polymerase ζ. Science, 1996, 272: 1646–1649.

[17] Watanabe-Akanuma M., Woodgate R., Ohta T. Enhanced generation of A:TT:A transitions in recA730 lexA51(Def) mutant of Escherichia coli. Mutat. Res., 1997, 373: 61–66.

[18] Whiteside J.R., Allinson S.L., Trevor J., McMillan T.J. Timeframes of UVA-induced bystander effects in human keratinocytes. Photochem. Photobiol., 2011, 87: 435-440.

[19] Morgan W.F., Sowa M.B. Non-targeted effects induced by ionizing radiation: Mechanisms and potential impact on radiation induced health effects. Cancer Lett., 2015, 356: 17-21.

[20] Kadhim M., Salomaa S., Wright E., Hildebrandt G., Belyakov O.V., Prise K.M., Little M.P. Non-targeted effects of ionising radiation—implications for low dose risk. Mutat. Res., 2013, 752: 84-98.

[21] Lyng F.M., Semour C.B., Mothersill C. Early events in the apoptotic cascade initiated in cells treated with medium from the progeny of irradiated cells. Radiat. Prot. Dosimetry, 2002, 99: 169-172.

[22] Tang M., Shen X., Frank E.G., O’Donnell M., Woodgate R., Goodman M.F. UmuD’(2)C is an error-prone DNA polymerase Escherichia coli pol V. Proc. Natl. Acad. Sci. USA, 1999, 96: 8919–8924.

[23] Ruiz-Rubio M., Bridges B.A. Mutagenic DNA repair in Escherichia coli 14. Influence of two DNA polymerase III mutator alleles on spontaneous and UV mutagenesis. Mol. Gen. Genet., 1987, 208: 542–548.

[24] Pham P., Bertram J.G., O’Donnell M., Woodgate R., Goodman M.F. A model for SOS-lesion-targeted mutations in Escherichia coli. Nature, 2001, 408: 366–370.

[25] 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. Mutat. Res., 2002, 510: 55–70.

[26] Rünger T.M., Kappes U.P. Mechanisms of mutation formation with long-wave ultraviolet light (UVA). Photoderm. Photoimmun. Photomed., 2008, 24: 2–10.

[27] Grebneva H.A. One of mechanisms of targeted substitution mutations formation at SOS-replication of double-stranded DNA containing cis-syn cyclobutane thymine dimers. Environ. Mol. Mutagen., 2006, 47: 733–745.

[28] Bebenek K., Pedersen L.C., Kunkel T.A. Replication infidelity via a mismatch with Watson-Crick geometry. Proc. Natl. Acad. Sci. USA, 2011, 108: 1862–1867.

[29] Wang W., Hellinga H.W., Beese L.S. Structural evidence for the rare tautomer hypothesis of spontaneous mutagenesis. Proc. Natl. Acad. Sci. USA, 2011, 108: 17644-17648.

[30] Xia S., Konigsberg W.H. Mispairs with Watson-Crick base-pair geometry observed in ternary complexes of an RB69 DNA polymerase variant. Protein Sci., 2014, 23: 508-513.

[31]

[32] Watson J. D., Crick F.H.C. The structure of DNA. Cold Spring Harbor Symp. Quant. Biol., 1953, 18: 123–131.

[33] 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. Int. J. Molec. Biol.: Open Access, 2016,1: 1-16.

[34] 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. Int. J. Molec. Biol.: Open Access, 2019, 4: 1-15.

[35] Grebneva H.A. Polymerase-tautomeric model for ultraviolet mutagenesis: targeted base substitution and frameshift mutations caused by cis-syn cyclobutane thymine dimers. Saarbrucken, Germany. LAP LAMBERT Academic Publishing, 2017: 134.

[36] Streisinger G., Okada J., Emerich J., Newrich J., Tsugita A., Terraghi E., Inouye M. Frameshift mutations and the genetic code. Cold Spring Harbor Symposia Quant. Biol., 1966. 31: 77-84.

[37] Strand M., Prolla T.A., Liskay R.M., Petes T.D. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature, 1993, 365: 274-276.

[38] Bzymek M., Saveson C.J., Feschenko V.V., Lovett S.T. Slipped misalignment mechanisms of deletion formation: in vivo susceptibility to nucleases. J. Bacteriol., 1999, 181: 477-482.

[39] Baase W.A., Jose D., Ponedel B.C., von Hippel P.H., Johnson N.P. DNA models of trinucleotide frameshift deletions: the formation of loops and bulges at the primer-template junction. Nucleic Acids Research, 2009, 37: 1682–1689.

[40] Grebneva H.A. Mechanisms targeted insertions formation under synthesis of DNA molecule containing cis-syn cyclobutane cytosine dimers. Dopovidi NAN Ukraine, 2014, (11): 156-164.

[41] Grebneva H.A. Mechanisms of targeted frameshift mutations – insertion formation under error-prone or SOS synthesis of DNA containing cis-syn cyclobutane thymine dimers. Mol. Biol. (Mosk), 2014, 48: 457-467.

[42] 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. J. Phot. Mat. Technology, 2015, 1: 19-26.

[43] Grebneva H.A. Mechanisms targeted deletions formation under synthesis of DNA molecule containing cis-syn cyclobutane thymine dimers. Dopovidi NAN Ukraine, 2015, (4): 124-132.

[44] Grebneva H.A. Mechanisms of targeted complex insertions formation under synthesis of DNA molecule containing cis-syn cyclobutane thymine dimers. Dopovidi NAN Ukraine, 2015, (5): 145-154.

[45] Campa A., Balduzzi M., Dini V., Esposito G., Tabocchini M.A. The complex interactions between radiation induced non-targeted effects and cancer. Cancer Lett., 2015, 356: 126-136.

[46] Morgan W.F. Is there a common mechanism underlying genomic instability, bystander effects and other nontargeted effects of exposure to ionizing radiation? Oncogene, 2003, 22: 7094–7099.

[47] Karotki A.V., Baverstock K. What mechanisms/processes underlie radiation-induced genomic instability? Cell Mol. Life Sci., 2012, 69: 3351-3360.

[48] Gorb L., Podolyan Y., Leszczynski J., Siebrand W., Fernández-Ramos A. A quantum-dynamics study of the prototropic tautomerism of guanine and its contribution to spontaneous point mutations in Escherichia coli. Biopolymers, 2002, 61(1): 77-83.

[49] Podolyan V., Gorb L., Leszczynski J. Ab initio study of the prototropic tautomerism of cytosine and guanine and their contribution to spontaneous point mutations. Int. J. Mol. Science, 2003, 4(7): 410-421.

[50] 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. Chem. Phys. Lett., 2005, 412(4-6): 285-293.

[51] Harris V.H., Smith C.L., Cummins J.W., Hamilton A.L., Adams H., et al. The effect of tautomeric constant on the specificity of nucleotide incorporation during DNA replication: support for the rare tautomer hypothesis of substitution mutagenesis. J. Mol. Biol., 2003, 326(5): 1389-1401.

[52] Srivastava R. The role of proton transfer on mutations. Front. Chem., 2019, https://doi.org/10.3389/fchem.2019.00536.

[53] Brovarets O., Timothy A. Oliynyk T.A., Hovorun D.M. Novel tautomerisation mechanisms of the biologically important conformers of the reverse Löwdin, Hoogsteen, and reverse Hoogsteen G*·C* DNA base pairs via proton transfer: a quantum-mechanical survey. Front. Chem., 2019.

[54] https://doi.org/10.3389/fchem.2019.00597.

[55] Grebneva H.A. The theory of thermal relaxation of the excitation energy of hydrogen bonds in a DNA molecule. Its contribution to ultraviolet mutagenesis. Saarbrucken, Germany. LAP LAMBERT Academic Publishing, 2019: 345. (In Russian).

[56] Grebneva H.A. Nature and mechanisms of hot and cold spots of ultraviolet mutagenesis formation. Dopovidi NAN Ukraine, 2012, (10): 181-187.

[57] Grebneva H.A. Targeted mutagenesis caused by cytosine dimers and mechanism substitution mutation formation under SOS-replication after irradiation double-stranded DNA by ultraviolet light. Dopovidi NAN Ukraine, 2001, (8): 183-189.

[58] Grebneva H.A. The molecular mechanisms derivation of mutation bases alteration after a post replication SOS-repair a DNA containing thymine dimers. Biopolymers Cell (Ukr), 2001, 17(6): 487-500.

[59] Grebneva H.A. The nature and possible mechanisms of potential mutations formation due to the appearance of thymine dimers after irradiating double-stranded DNA by ultra-violet light. Biopolymers Cell (Ukr), 2002, 18(1): 205-218.

[60] 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. J. Molec. Struct., 2003, 645: 133-143.

[61] Grebneva H.A., Ivanov M.O. The possible molecular mechanisms of untargeted type mutation under SOS replication of double-stranded DNA. Biopolymers Cell (Ukr), 2001, 17(5): 388 - 395.

[62] Grebneva H.A. Possible molecular mechanisms of untargeted mutagenesis upon a post-replication SOS repair after irradiating double-stranded DNA by ultraviolet light. Biopolymers Cell (Ukr), 2002, 18(5): 394-400.

[63] Grebneva H.A. Three sources of untargeted base-substitution mutations upon UV irradiation of DNA molecule. Dopovidi NAN Ukraine, 2013, 1: 143-150.

[64] 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. Int. J. Molec. Biol.: Open Access, 2017, 2: 1-14.

[65] Grebneva H.A. A polymerase-tautomeric model for radiation-induced bystander effects: a model for untargeted insertional mutagenesis during error-prone and SOS synthesis of double-stranded DNA containing thymine in the rare tautomeric form. Vestnik Luganskogo nationalnogo universiteta imeni Vladimira Dalya, 2017, 2(4): 157-161.

[66] Grebneva H.A. A polymerase-tautomeric model for radiation-induced genomic instability: targeted delayed substitution mutations under error-prone and SOS synthesis of double-stranded DNA containing cis-syn cyclobutane thymine dimers. Fizika and Tecknika visokih davleniy, 2017, 27(3): 131-148.

[67] Grebneva H.A. Polymerase-tautomeric model for mechanism of targeted delayed substitution mutations formation under synthesis of DNA containing cis-syn cyclobutane thymine dimers. Dopovidi NAN Ukraine, 2016, (5): 101-110.

[68] 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. Int. J. Molec. Biol.: Open Access, 2018, 3: 125-141.

[69] Grebneva H.A. A review of the polymerase-tautomeric models for targeted ultraviolet mutagenesis under error-prone and SOS synthesis of double-stranded DNA containing cis-syn cyclobutane thymine dimers. Fizika and Tecknika visokih davleniy, 2018, 28(3): 98-121.

[70] Grebneva H.A. Symptoms of crisis in mutagenesis and ways of its resolution. Vestnik Luganskogo nationalnogo universiteta imeni Vladimira Dalya, 2018, 5(11): 210-215.

[71] Grebneva H.A. Possible mechanism of formation of rare tautomeric forms of nucleotide bases on the example of UV-irradiation of DNA. Ukr. Phys. J., 1992, 37(11): 1636-1642.

[72]

[73] Grebneva H.A. The heat deexcitation as mechanism of double proton transitions in DNA. Dopovidi NAN Ukraine, 1994, (2): 73-75.

[74] Grebneva H.A. The irradiation of DNA by ultraviolet light: potential alterations and mutations. Mol. Biol. (Mosk.), 1994, 28(4): 527–532.

[75] Grebneva H.A. Mechanisms of formation of potential mutations under cytosine dimers formation in result irradiation double-stranded DNA by ultraviolet light. Dopovidi of NAN of Ukraine, 2001, (7): 165-169.

[76] Grebneva H.A. A polymerase-tautomeric model of UV mutagenesis: Formation of rare tautomeric forms of cytosine and guanine in double-stranded DNA. Vestnik Donetskogo Nationalnogo Univtrsiteta (Ukr), 2008, (2): 306-313.

[77]

[78] Gorb L., Podolyan Y., Leszczynski J., Siebrand W., Fernandez-Ramos A., Smedarchina Z. A quantum-dynamics study of the prototropic tautomerism of guanine and its contribution to spontaneous point mutations in Escherichia coli. Biopolymers (Nucleic Acids Sci.), 2002, 61: 77.

[79] Gorb L., Podolyan Y., Dziekonski P., Sokalski W.A., Leszczynski J. Double-proton transfer in adenine-thymine and guanine-cytosine base pairs. A post-Hartree-Fock ab initio study. J. Am. Chem. Soc., 2004, 126: 10119–10129.

[80] Clementi E., Corongiu G., Detrich J., Chin S., Domingo J. Parallelism in study in DNA pairs as an example. Int. J. Quant. Chem.: Quantum Chem. Symp., 1984, 18: 601–618.

[81] Clementi E., Corongiu G., Detrich J.H., Kahnmohammadbaigi H., Chin S., Domingo L., Laoksonen A., Nguyen N.L. Parallelism in computational chemistry:applications in quantum and statistical mechanics. Physica, 1985, BC 131: 74–102.

[82] Brovarets O.O., Hovorun D.M. Can tautomerization of the A-T Watson-Crick base pair via double proton transfer provoke point mutations during DNA replication? A comprehensive QM and QTAIM analysis. J. Biomol. Struct. Dyn., 2014, 32: 127–154.

[83] Raghunathan G., Kieber-Emmons T., Rein R., Alderfer J.L. Conformation features of DNA containing a cis-syn photodimer. J. Biopol. Struct. Dyn., 1990, 7: 899–913.

[84] Cooney M.G., Miller J.H. Calculated distortions of duplex DNA by a cis, syn cyclobutane thymine dimer are unaffected by a 3’ TpA step. Nucleic Acids Res., 1997, 25: 1432–1436.

[85] McAteer K., Jing Y., Kao J., Taylor J.-S., Kennedy M.A. Solution-state structure of a DNA dodecamer duplex containing a Cis-syn thymine cyclobutane dimer, the major UV photoproduct of DNA. J. Mol. Biol., 1998, 282: 1013–1032.

[86] Yamaguchi H., van Aalten D.M., Pinak M., Furukawa A., Osman R. Essential dynamics of DNA containing a cis.syn cyclobutane thymine dimer lesion. Nucleic Acids Res., 1998, 26: 1939-1946.

[87]

[88] Bdour H.M., Kao J.L., Taylor J.-S. Synthesis and characterization of a [3-15N]-labeled cis-syn thymine dimer-containing DNA duplex. J. Org. Chem., 2006, 71: 1640–1646.

[89] Grebneva H.A. A new semiempirical potential function for hydrogen bonds and its possible use in studying the DNA molecule. J. Mol. Struct., 1993, 296: 127-132.

[90] Tolpygo K.B., Grebneva H.A. Effect of the state of h-b-1 hydrogen bond of the character of some atom vibrations in guanine-cytosine pair of the DNA molecule. Int. J. Quant. Chem., 1996, 57: 219-227.

[91] Grebneva H.A., Tolpygo K.B. Crystalline and local vibrations of paired bases in poly (dG)-poly (dC) interacting with the h-b-1 hydrogen bond. Int. J. Quant. Chem., 1997, 62: 115-124.

[92] Grebneva H.A., Tolpygo K.B. The heat deexcitation of hydrogen bond protons in paired bases of DNA molecules. Studia Biophysica, 1990, 135: 115-125.

[93] Tolpygo K.B., Grebneva H.A. Stationary states of the proton excitation at the DNA site consisting of guanine-cytosine pairs with a single “defect”. Ukr. Phyz. J., 1993, 38: 855-861.

[94] Sargentini N.J., Smith K.C. Ionizing and ultraviolet radiation-induced reversion of sequenced frameshift mutations in Escherichia coli: a new role for umuDC suggested by delayed photoreactivation. Mutat. Res., 1987, 179(1): 55–63.

[95] Stamato T.D., Perez M.L. EMS and UV-light-induced colony sectoring and delayed mutation in Chinese hamster cells. Int. J. Radiat. Biol., 1998, 74(6): 739–745.

[96] Little J.B., Nagasawa H., Pfenning T., Vetrovs H. Radiation-induced genomic instability: delayed mutagenic and cytogenetic effects of X rays and alpha particles. Radiat. Res., 1997, 148(4): 299–307.

[97] Okazaki R., Ootsuyama A. P53-dependent delayed effects of radiation vary according to time of irradiation of p53+/- mice. J. Radiat. Res., 2014, 55: 25-37.

[98] Mothersill C., Moriarty M.J., Seymour C.B. Bystander and other delayed effects and multi-organ involvement and failure following high dose exposure to ionizing radiation. British. J. Radiology Supplement., 2005, 27: 128-131.

[99] Averbeck D. Non-targeted effects as a paradigm breaking evidence. Mutation Research, 2010, 687(1-2): 7-12.

[100] Widel M. Bystander effect induced by UV radiation; why should we be interested? Postepy Hig. Med. Dosw. (Online), 2012, 66: 828-837.

[101] Watanabe M. The first target of radiation carcinogenesis is not DNA. Int. Congress, 2007, 1299: 21-24.

[102] Irons S.L., Serra V., Bowler D., Chapman K., Militi S., Lyng F., Kadhim M. The effect of genetic background and dose on non-targeted effects of radiation. Int. J. Radiat. Biol., 2012, 88(10): 735-742.

[103] Schaaper R.M. Base selection, proofreading, and mismatch repair during DNA replication in Escherichia coli. J. Biol. Chem., 1993, 268: 23762-23765.

[104] 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.

[105] Patel M., Jiang Q.F., Woodgate R., Cox M.M., Goodman M.F. A new model for SOS-induced mutagenesis: how RecA protein activates DNA polymerase V. Crit. Rev. Biochem. Mol. Biol., 2010, 45: 171-184.

[106] Furukohri A., Goodman M.F., Maki H. Dynamic polymerase exchanges with Escherichia coli DNA polymerase IV replacing DNA polymerase III on the sliding clamp. J. Biol. Chem., 2008, 283: 11260-11269.

[107] Washington M.T., Prakash L., Prakash S. Mechanism of nucleotide incorporation opposite a thymine-thymine dimer by yeast DNA polymerase η. Proc. Natl. Acad. Sci. USA, 2003, 100: 12093-12098.

[108] Grebneva H.A. Proton potential for broad spectrum of hydrogen bond length in water dimer. Zhurnal Strukturnoy Khimii, 1997, 38(2): 422-430.

[109] Ostapenko N.I., Skryshevskii Yu.A., Kadashchuk A.K., Rubin Yu.V. Thermoluminescence of crystals of nuclein acids bases. Izvestia Acad Sci USSR, 1990, 54: 445-449.

[110] Banerjee S.K., A., Christensen R B., LeClerc J.E., Lawrence C.W. SOS-dependent replication past a single trans-syn T-T cyclobutane dimer gives a different mutation spectrum and increased error rate compared with replication past this lesion in induced cells. J. Bacteriology, 1990, 172(4): 2105-2112.

[111] Wang H., Hoffman P.D., Lawrence Ch., Hays J.B. Testing excision models for responses of mismatch-repair systems to UV photoproducts in DNA. Environ. Mol. Mutag., 2006, 47(4): 296-306.

[112] LeClerc J.E., Istock N.L. Specificity of UV-mutagenesis in the lac-promoter of M13 hybrid phage DNA. Nature, 1982, 297: 596-598.

[113] Kunz B.A., Straffon A.F.L., Vonarx E.J. DNA damage-induced mutation: tolerance via translesion synthesis. Mutat. Res., 2000, 451(1-2): 169-185.

[114] Leong-Morgenthaler P.-M., Duc R., Morgenthaler S. Comparison of the mutagenic responses of mismatch repair-proficient (TK6) and mismatch repair-deficient (MT1) human lymphoblast cells to the food-borne carcinogen PhlP. Environ. Mol. Mutagen., 2001, 38: 323-328.

[115] Doetsch P.W. Translesion synthesis by RNA polymerases: occurrence and biological implications for transcriptional mutagenesis. Mutat. Res., 2002, 510(1-2): 131-140.

[116] Choi J.-H., Besaratinia A., Lee D.-H. The role of DNA polymerase I in UV mutation spectra. Mutat. Res., 2006, 599: 58-65.

[117] Horsfall M.J., Lawrence C.W. Accuracy of replication past the (6-4) adduct. J. Mol. Biol., 1994, 235(2): 465-471.

[118] Tomasetti C., Vogelstein B. Variation in cancer risk among tissues can be explained by the number of stem cell divisions. Science, 2015, 347: 78–81.

[119] Boesen J.J., Stuivenberg S., Thyssens C.H., Panneman H., Darroudi F., Lohman P.H., Simons J.W. Stress response induced by DNA damage leads to specific, delayed and untargeted mutations. Mol. Gen. Genet., 1992, 234: 217–227.

[120] Khlifi R., Hamza-Chaffai A. Head and neck cancer due to heavy metal exposure via tobacco smoking and professional exposure: a review. Toxicol. Applied Pharmacol., 2010, 248: 71-88.


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