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
Volume 1, Issue 2, September 2015, Pages: 19-26
Received: Jul. 8, 2015; Accepted: Jul. 16, 2015; Published: Jul. 17, 2015
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Author
Helen A. Grebneva, Dept. of dynamical properties of complex systems, Galkin Institute for Physics & Engineering NAN Ukraine, Donetsk, Ukraine
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Abstract
Now it is still unclear how frameshift mutations arise at cyclobutane pyrimidine dimers. The author develops polymerase – tautomeric model of ultraviolet mutagenesis. The model is described that is based on the formation of rare tautomeric bases in cis-syn cyclobutane thymine dimers. A mechanism was proposed for targeted deletions caused by cis-syn cyclobutane thymine dimers. Targeted deletions are frameshift mutations when one or several nucleotides are dropped out in a DNA site opposite to a lesion capable of stopping DNA synthesis. Ultraviolet irradiation may result in changes of tautomer states of DNA bases. Thymine molecule may form 5 rare tautomer forms. They are stable if these bases are part of cyclobutane dimers. Structural analysis indicates that opposite one type of cis-syn cyclobutane thymine dimers containing a single tautomeric base (TT2*, with the ‘*’ indicating a rare tautomeric base and the subscript referring to the particular conformation) it is impossible to insert any canonical DNA bases with the template bases with hydrogen bonds formation. Therefore it is proposed that under synthesis DNA containing cis-syn cyclobutane thymine dimers TT2* specialize or modified DNA polymerases will leave one nucleotide gaps opposite these cis-syn cyclobutane thymine dimers. Daughter DNA strand opposite cis-syn cyclobutane thymine dimers TT2* may fall out. If in opposite DNA strand the loop is formed, daughter strand becomes shorter. Some DNA nucleotides are lost. Targeted deletion is formed. According to the polymerase-tautomeric model of ultraviolet mutagenesis cis-syn cyclobutane thymine dimers wherein a thymine is in the canonical tautomeric forms do not result in mutations. Cis-syn cyclobutane thymine dimers wherein a thymine is in the rare tautomeric forms T1*, T4*, or T5* were shown to cause only targeted base substitution mutations. Cis-syn cyclobutane thymine dimers wherein a thymine is in the rare tautomeric form T2* may result in targeted frameshift mutations (targeted insertions and targeted deletions).
Keywords
UV-mutagenesis, Rare Tautomeric Forms, Targeted Frameshift Mutations, Targeted Deletion,cis-syn Thymine Cyclobutane Dimers, Error-prone Replication, SOS-replication
To cite this article
Helen A. Grebneva, 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. Vol. 1, No. 2, 2015, pp. 19-26. doi: 10.11648/j.jmpt.20150102.11
References
[1]
C.W. Lawrence, R.B. Christensen and J.R. Christensen, “Identity of the photoproduct that cause lacI mutations in UV-irradiated Escherichia coli”, J. Bacter., vol. 161, pp. 767–768, 1985.
[2]
D. Chandrasekhar and B.V. Houten, “In vivo formation and repair of cyclobutane pyrimidine dimers and 6-4 photoproducts measured at the gene and nucleotide level in Escherichia coli”, Mutat. Res., vol. 450, pp. 19-40, 2000.
[3]
J. Yao, K. Dixon and M.P. Carty, “A single (6-4) photoproduct inhibits plasmid DNA replication in xeroderma pigmentosum variant cell extracts”, Environ. Mol. Mutagen., vol. 38, pp. 19-29, 2001.
[4]
H.M. Bdour, J.L. Kao and J.S. Taylor, “Synthesis and characterization of a [3-15N]-labeled cis-syn thymine dimer-containing DNA duplex”, J. Org. Chem., vol. 71, pp. 1640–1646, 2006.
[5]
A. Besaratinia, J.I. Yoon, C. Schroeder, S.E. Bradforth, M. Cockburn and G.P. Pfeifer. “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”, FASEB. J., vol. 25, pp. 3079–3091, 2011.
[6]
A. Banyasz, I. Vayá, P. Changenet-Barret, T. Gustavsson, T. Douki and D. Markovitsi. “Base pairing enhances fluorescence and favors cyclobutane dimer formation induced upon absorption of UVA radiation by DNA”, J. Am. Chem. Soc., vol. 133, pp. 5163–5165, 2011.
[7]
W. Saenger, Principles of Nucleic Acid Structure. New York: Springer-Verlag New York Inc. 1984.
[8]
J.E. LeClerc and N.L. Istock. “Specificity of UV-mutagenesis in the lac-promoter of M13 hybrid phage DNA”, Nature, vol. 297, pp. 596-598, 1982.
[9]
C.W. Lawrence, S.K. Banerjee, A. Borden and J.E. LeClerc, “T-T cyclobutane dimers are misinstructive, rather than non-instructive, mutagenic lesions”, Mol. Gen. Genet., vol. 222, pp. 166-169, 1990.
[10]
J.E. LeClerc, A. Borden and C.W. Lawrence, “The thymine-thymine pyrimidine-pyrimidine (6-4) ultraviolet light photoproduct is highly mutagenic and specifically induces 3' thymine-to-cytosine transitions in Escherichia coli”, Proc. Natl. Acad. Sci. USA, vol. 88, pp.9685-9689, 1991.
[11]
C.I. Wang and J.S. Taylor, “In vitro evidence that UV-induced frameshift and substitution mutations at T tracts are the result of misalignment-mediated replication past a specific thymine dimer”, Biochemistry, vol. 31, pp.3671–3681, 1992.
[12]
C.W. Lawrence, P.E.M. Gibbs, A. Borden, M.J. Horsfall and B.Y. Kilbey, “Mutagenesis induced by single UV photoproducts in E. coli and yeast”, Mutat. Res., vol. 299, pp. 157–163, 1993.
[13]
C.W. Lawrence, “Accuracy of replication past the T-C (6-4) adduct”, J. Mol. Biol., vol. 235, pp. 465-471, 1994.
[14]
P.E.M. Gibbs, A. Borden and C.W. Lawrence, “The T-T pyrimidine (6-4) pyrimidone UV photoproduct is much less mutagenic in yeast than in Escherichia coli”, Nucleic Acids Res., vol. 23, pp. 1919-1922, 1995.
[15]
J.E. LeClerc, W.L. Payne and T.A. Cebula, “High mutation frequencies among Escherichia coli and Salmonella pathogens”, Science, vol. 274, pp. 1208–1211, 1996.
[16]
D.J. Moshinsky and G.N. Wogan, “UV-induced mutagenesis of human p53: analysis using a double-selection method in yeast”, Environ. Mol. Mutagen., vol. 35, pp. 31-38, 2000.
[17]
X. Veaute, G. Mari-Giglia, C.W. Lawrence and A. Sarasin, “UV lesions located on the leading strand inhibit DNA replication but do not inhibit SV40 T-antigen helicase activity”, Mutat. Res., vol. 459, pp. 19-28, 2000.
[18]
Y.-H. You, D.H. Lee, J.-H. Yoon, S. Nakajima, A. Yasui and G.P. Pfeifer, “Cyclobutane pyrimidine dimers are responsible for the vast majority of mutations induced by UVB irradiation in mammalian cells”, J. Biol. Chem., vol. 276, pp. 44688–44694, 2001.
[19]
J.E. Trosko, “From bacteria to humans: lessons learned from a reductionist’s view of ultraviolet light-induced DNA lesions”, Environ. Mol. Mutagen., vol. 38, pp. 118-121, 2001.
[20]
A.L. Abdulovic and S. Jinks-Robertson, “The in vivo characterization of translesion synthesis across UV-induced lesions in Saccharomyces cerevisiae: insights into Pol ζ- and Pol η-dependent frameshift mutagenesis”, Genetics, vol. 172, pp. 1487-1498, 2006.
[21]
P. Iengar, “An analysis of substitution, deletion and insertion mutations in cancer genes”, Nucleic. Acids. Res., vol. 40, pp. 6401-6413, 2012.
[22]
J.G. Levine, R.M. Schaaper and D.M. DeMarini, “Complex frameshift mutations mediated by plasmid pKM101: mutational mechanisms deduced from 4-aminobiphenyl-induced mutation spectra in Salmonella”, Genetics, vol. 136, pp. 731–746, 1994.
[23]
S. Shibutani, M. Takeshita and A.P. Grollman, “Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxoG”, Nature, vol. 349, pp. 431–434, 1991.
[24]
J.M. Cuevas, S. Duffy and R. Sanjuán, “Point mutation rate of bacteriophage {Phi}X174”, Genetics, vol. 183, pp. 747-749, 2009.
[25]
S. Kobayashi, M.R. Valentine, P. Pham, M. O'Donnell and M.F. Goodman, “Fidelity of Escherichia coli DNA polymerase IV. Preferential generation of small deletion mutations by dNTP-stabilized misalignment”, J. Biol. Chem., vol. 277, pp. 34198–34207, 2002.
[26]
S.R. Kim, K. Matsui, P. Yamada, P. Gruz and T. Nohm, “Roles of chromosomal and episomal dinB genes encoding Pol IV in targeted and untargeted mutagenesis in Escherichia coli”, Mol. Genet. Genomics, vol. 266, pp. 207-215, 2001.
[27]
G. Streisinger and J. Owen, “Mechanisms of spontaneous and induced frameshift mutation in bacteriophage T4”, Genetics, vol. 109, pp. 633-659, 1985.
[28]
H. Chung, C.G. Lopez, J. Holmstrom, D.J. Young, J.F. Lai, D. Ream-Robinson and J.M. Carethers, “Both microsatellite length and sequence context determine frameshift mutation rates in defective DNA mismatch repair”, Hum. Mol. Genet., vol. 19, pp. 2638-2647, 2010.
[29]
A.M. Skinner, C. Dan and M.S. Turker, “The frequency of CC to TT tandem mutations in mismatch repair-deficient cells is increased in a cytosine run”, Mutagenesis, vol. 23, pp. 87-91, 2008.
[30]
J.M. Gore, F.A. Ran and L.N. Ornston, “Deletion mutations caused by DNA strand slippage in Acinetobacter baylyi”, Appl. Environ. Microbiol., vol. 72, pp. 5239-5245, 2006.
[31]
Y. Wu, R.C. Wilson and J.D. Pata, “The Y-family DNA polymerase Dpo4 uses a template slippage mechanism to create single-base deletions”, J. Bacteriol., vol. 193, pp. 2630-2636, 2011.
[32]
H. Gragg, B.D. Harfe and S. Jinks-Robertson, “Base composition of mononucleotide runs affects DNA polymerase slippage and removal of frameshift intermediates by mismatch repair in Saccharomyces cerevisiae”, Mol. Cell Biol., vol. 22, pp. 8756-8762, 2002.
[33]
Campregher, T. Scharl, M. Nemeth, C. Honeder, T. Jascur, R.B. Boland and C. Gasche, “The nucleotide composition of microsatellites impacts both replication fidelity and mismatch repair in human colorectal cells”, Hum. Mol. Genet., vol. 19, pp. 2648-2657, 2010.
[34]
J.M. Fortune, C.M. Stith, G.E. Kissling, P.M.J. Burgers and T. Kunkel, “RPA and PCNA suppress formation of large deletion errors by yeast DNA polymerase {delta}”, Nucleic Acids Res., vol. 34, pp. 4335-4341, 2006.
[35]
J.J. Foti, A.M. DeLucia, C.M. Joyce and G.C. Walker, “UmuD2 inhibits a non-covalent step during DinB-mediated template slippage on homopolymeric nucleotide runs”, J. Biol. Chem., vol. 285, pp. 23086-23095, 2010.
[36]
J.J. Foti and G.C. Walker, “Efficient extension of slipped DNA intermediates by DinB is required to escape primer template realignment by DnaQ”, J. Bacteriol., vol. 193, pp. 2637-2641, 2011.
[37]
D.M. Lyons and P.J. O'Brien, “Human base excision repair creates a bias toward -1 frameshift mutations”, J. Biol. Chem., vol. 285, pp. 25203-25212, 2010.
[38]
H. Zhang, J.W. Beckman and F.P. Guengerich, “Frameshift deletion by Sulfolobus solfataricus P2 DNA polymerase Dpo4 T239W is selective for purines and involves normal conformational change followed by slow phosphodiester bond formation”, J. Biol. Chem., vol. 284, pp. 35144-35153, 2009.
[39]
P. Mukherjee, I. Lahiri and J.D. Pata, “Human polymerase kappa uses a template-slippage deletion mechanism, but can realign the slipped strands to favour base substitution mutations over deletions”, Nucleic Acids Res., vol. 41, pp. 5024-5035, 2013.
[40]
W.-D. Chen, J.R. Eshleman, M.R. Aminoshariae, A.-H. Ma, N. Veloso, S.D. Markowitz, W.D. Sedwick and M.L. Veig, “Cytotoxicity and mutagenicity of frameshift-inducing agent ICR191 in mismatch repair-deficient colon cancer cells”, J. Natl. Cancer. Inst., vol. 92, pp. 480-485, 2000.
[41]
G. Streisinger, J. Okada, J. Emerich, J. Newrich, A. Tsugita, E. Terraghi, M. Inouye, “Frameshift mutations and the genetic code”, Cold Spring Harbor Symp. Quant. Biol., vol. 31, pp. 77–84, 1966.
[42]
M. Strand, T.A. Prolla, R.M. Liskay and T.D. Petes, “Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair”, Nature, vol. 365, pp. 274-276, 1993.
[43]
M. Bzymek, C.J. Saveson, V.V. Feschenko and S.T. Lovett, “Slipped misalignment mechanisms of deletion formation: in vivo susceptibility to nucleases”, J. Bacteriol., vol. 181, pp. 477-482, 1999.
[44]
W.A. Baase, D. Jose, B.C. Ponedel, P.H. von Hippel and N.P. Johnson, “DNA models of trinucleotide frameshift deletions: the formation of loops and bulges at the primer-template junction”, Nucleic Acids Res., vol. 37, pp. 1682–1689, 2009.
[45]
T.A. Kunkel and A. Soni, “Mutagenesis by transient misalignment”, J. Biol. Chem., vol. 263, pp. 14784-14789, 1988.
[46]
K. Bebenek and T.A. Kunkel, “Mutagenesis by transient misalignment”, Proc. Natl. Acad. Sci. USA, vol. 87, pp. 4946-4950, 1990.
[47]
K. Bebenek and T.A. Kunkel, “Streisinger revisited: DNA synthesis errors mediated by substrate misalignments”, Cold Spring Harb. Symp. Quant. Biol., vol. 65, pp. 81-92, 2000.
[48]
P.T. Pham, M.W. Olson, C.S. McHenry and R.M. Schaaper, “The base substitution and frameshift fidelity of Escherichia coli DNA polymerase III holoenzyme in vitro”, J. Biol. Chem., vol. 273, pp. 23575-23584, 1998.
[49]
J. Bauer, G. Xing, H. Yagi, J.M. Sayer, D.M. Jerina and H. Ling, “A structural gap in Dpo4 supports mutagenic bypass of a major benzo[a]pyrene dG adduct in DNA through template misalignment”, Proc. Natl. Acad. Sci. USA, vol. 104, pp. 14905-14910, 2007.
[50]
M. Bzymek and S.T. Lovett, “Evidence for two mechanisms of palindrome-stimulated deletion in Escherichia coli: single-strand annealing and replication slipped mispairing”, Genetics, vol. 158, pp. 527-540, 2001.
[51]
M. Bzymek, S.T. Lovett, “Instability of repetitive DNA sequences: The role of replication in multiple mechanisms”, Proc. Natl. Acad. Sci. USA, vol. 98, pp. 8319-8325, 2001.
[52]
H.A. Grebneva, “Possible mechanism of formation of rare tautomeric forms of nucleotide bases on the example of UV-irradiation of DNA”, Ukr. Phys. J., vol. 37, pp. 1636-1639, 1992.
[53]
H.A. Grebneva, “The role of hydrogen bonds in the formation of genetic mutations”, Chem. Phys. (Mosk.), vol. 12, pp. 1027-1031, 1993.
[54]
H.A. Grebneva, “The heat deexcitation as mechanism of double proton transitions in DNA”, Dopovidi NAN Ukraine, vol. 2, pp. 73-75, 1994.
[55]
H.A. Grebneva, “The irradiation of DNA by ultraviolet light: potential alterations and mutations”, Mol. Biol. (Mosk.), vol. 28, pp. 805-812, 1994.
[56]
H.A. Grebneva, “Proton potential for broad spectrum of hydrogen bond length in water dimer”, Zh. Struckt. Khim., vol. 38, pp. 422-430, 1997.
[57]
H.A. Grebneva, “The molecular mechanisms derivation of mutation bases alteration after a post replication SOS-repair a DNA containing thymine dimers”, Biopolymers Cell (Ukr.), vol. 17, pp. 487-500, 2001.
[58]
H.A. Grebneva, “Mechanisms of formation of potential mutations under cytosine dimers formation in result irradiation double-stranded DNA by ultraviolet light”, Dopovidi NAN Ukraine, vol. 7, pp. 165-169, 2001.
[59]
H.A. Grebneva, “Targeted mutagenesis caused by cytosine dimers and mechanism substitution mutation formation under SOS-replication after airradiation double-stranded DNA by ultraviolet light”, Dopovidi NAN Ukraine, vol. 8, pp. 183-189, 2001.
[60]
H.A. Grebneva, Ivanov M.O. 2001. “The possible molecular mechanisms of untargeted type mutation under SOS replication of double-stranded DNA”, Biopolymers Cell (Ukr.), vol. 17, pp. 388-395 2001.
[61]
H.A. Grebneva, “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.), vol. 18, pp. 205-218, 2002.
[62]
H.A. Grebneva, “Possible molecular mechanisms of untargeted mutagenesis upon a post-replication SOS-reparation after irradiating double-stranded DNA by ultraviolet light”, Biopolymers Cell (Ukr.), vol. 18, pp. 394-400, 2002.
[63]
H.A. Grebneva, “Nature and possible mechanisms formation of potential mutations arising at emerging of thymine dimers after irradiation of double-stranded DNA by ultraviolet light”, J. Mol. Struct., vol. 645, pp. 133-143, 2003.
[64]
H.A. Grebneva, “One of mechanisms of targeted substitution mutations formation at SOS-replication of double-stranded DNA containing cis-syn cyclobutane thymine dimers”, Environ. Mol. Mutagen., vol. 47, pp. 733-745, 2006.
[65]
H.A. Grebneva, 2008. “A polymerase-tautomeric model of UV mutagenesis: Formation of rare tautomeric forms of cytosine and guanine in double-stranded DNA”, Vestn. Donetsk Univ. (Ukr.), vol. 2, pp. 306-313, 2008.
[66]
H.A. Grebneva, “Targeted base-substitution mutations during the synthesis of double-stranded DNA containing cis-syn cyclobutane pyrimidine dimers”, Vestn. Donetsk Univ. (Ukr.), vol. 1, pp. 323-330, 2009.
[67]
H.A. Grebneva, “Mechanism of untargeted substitution mutations formation during error-prone and SOS-synthesis of double-stranded DNA containing cis-syn cyclobutane cytosine dimers in both DNA strands”, Vestn. Donetsk Univ. (Ukr.), vol. 2, pp. 132-138, 2011.
[68]
H.A. Grebneva, “The nature and formation mechanisms of hot and cold spots for UV mutagenesis”, Dopovidi NAN Ukraine, vol. 10, pp. 181-187, 2012.
[69]
H.A. Grebneva, “Three sources of untargeted base-substitution mutations upon UV irradiation of DNA molecule”, Dopovidi NAN Ukraine, vol. 1, pp. 143-150, 2013.
[70]
H.A. Grebneva, “Mechanisms of targeted frameshift mutations: insertions arising during error-prone or SOS synthesis of DNA containing cis-syn cyclobutane thymine dimers”, Mol. Biol. (Mosk.), vol. 48, pp. 457–467, 2014.
[71]
H.A. Grebneva, “Mechanisms targeted insertions formation under synthesis of DNA molecule containing cis-syn cyclobutane cytosine dimers”, Dopovidi NAN Ukraine, vol. 11, pp. 156-164, 2014.
[72]
H.A. Grebneva, “Mechanisms targeted deletions formation under synthesis of DNA molecule containing cis-syn cyclobutane thymine dimers”, Dopovidi NAN Ukraine, vol. 4, pp. 124-132, 2015.
[73]
H.A. Grebneva, “Mechanisms of targeted complex insertions formation under synthesis of DNA molecule containing cis-syn cyclobutane thymine dimers”, Dopovidi NAN Ukraine, vol. 5, pp. 145-154, 2015.
[74]
J.D. Watson and F.H.C. Crick. “The structure of DNA”, Cold Spring Harbor Symp. Quant. Biol., vol. 18, pp. 123-131, 1953.
[75]
K. Bebenek, L.C. Pedersen and T. Kunkel. “Replication infidelity via a mismatch with Watson–Crick geometry”, Proc. Natl. Acad. Sci. USA, vol. 108, pp. 1862-1867, 2011.
[76]
W. Wang, H.W. Hellinga and L.S. Beese. “Structural evidence for the rare tautomer hypothesis of spontaneous mutagenesis”, Proc. Natl. Acad. Sci. USA, vol. 108, pp. 17644-17648, 2011.
[77]
C.S. Peng, C.R. Baiz and A. Tokmakoff. “Direct observation of ground-state lactam-lactim tautomerization using temperature-jump transient 2D IR spectroscopy”, Proc. Natl. Acad. Sci. USA, vol. 110, pp. 9243-9248, 2013.
[78]
D. Li, B.I. Fedeles, V. Singh, C.S. Peng, K.J. Silvestre, A.K. Simi, J.H. Simpson, A. Tokmakoff and J.M. Essigmann. “Tautomerism provides a molecular explanation for the mutagenic properties of the anti-HIV nucleoside 5-aza-5,6-dihydro-2'-deoxycytidine”, Proc. Natl. Acad. Sci. USA, vol. 11, pp. E3252-E3259, 2014.
[79]
S. Xia and W.H. Konigsberg. “Mispairs with Watson-Crick base-pair geometry observed in ternary complexes of an RB69 DNA polymerase variant”, Protein Sci., vol. 23, pp. 508-513, 2014.
[80]
V. Singh, B.I. Fedeles and J.M. Essigmann. “Role of tautomerism in RNA biochemistry”, RNA, vol. 21, pp. 1-13, 2015.
[81]
S.K. Banerjee, A. Borden, R.B. Christensen, J.E. LeClerc and C.W. Lawrence. “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. Bacteriol., vol. 172, pp. 2105-2112, 1990.
[82]
B.A. Kunz, A.F.L. Straffon and E.J. Vonarx. “DNA damage-induced mutation: tolerance via translesion synthesis”, Mutat. Res., vol. 45, pp. 169-185, 2000.
[83]
P.-M. Leong-Morgenthaler, R. Duc and S. Morgenthaler. “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., vol. 38, pp. 323-328, 2001.
[84]
P.W. Doetsch. “Translesion synthesis by RNA polymerases: occurrence and biological implications for transcriptional mutagenesis”, Mutat. Res., vol. 510, pp. 131-140, 2002.
[85]
A. Furukohri, M.F. Goodman and H.A. Maki. “Dynamic polymerase exchange with Escherichia coli DNA polymerase IV replacing DNA polymerase III on the sliding clamp”, J. Biol. Chem., vol. 283, pp. 11260–11269, 2008.
[86]
J.R. Nelson, C.W. Lawrence and D.C. Hinkle. “Deoxycytidyl transferase activities of years REV 1 protein”, Nature, vol. 382, pp. 729–731, 1996.
[87]
M. Tang, X. Shen, E.G. Frank, M. O’Donnell, R. Woodgate and M.F. Goodman. “UmuD’(2)C is an error-prone DNA polymerase. Escherichia coli pol V”, Proc. Natl. Acad. Sci. USA, vol. 96, pp. 8919-8924, 1999.
[88]
M. Tang, P. Pham, X. Shen, J.-S. Taylor, M. O’Donnell, R. Woodgate and M. Goodman. “Roles of Escherichia coli DNA polymerase IV and V in lesion-targeted and untargeted SOS mutagenesis”, Nature, vol. 404, pp.1014-1018, 2000.
[89]
M.T. Washington, R.E. Johnson, S. Prakash and L. Prakash. “Accuracy of thymine-thymine dimer bypasses by Saccharomyces cerevisiae DNA polymerase eta”, Proc. Natl. Acad. Sci. USA, vol. 97, pp. 3094–3099, 2000.
[90]
R.E. Johnson, L. Haracska, S. Prakash and L. Prakash. “Role of DNA polymerase zeta in the bypass of a (6-4) TT photoproduct”, Mol. Cell. Biol., vol. 21, pp. 3558-3563, 2001.
[91]
C.W. Lawrence, “Cellular roles DNA polymerase zeta and Rev1 protein”, DNA repair, vol. 1, pp. 425-435, 2002.
[92]
M.T. Washington, L. Prakash and S. Prakash, “Mechanism of nucleotide incorporation opposite a thymine-thymine dimer by yeast DNA polymerase η”, Proc. Natl. Acad. Sci. USA, vol. 100, pp. 12093–12098, 2003.
[93]
G.S. Kozmin, Y.I. Pavlov, T.A. Kunkel, E. Sage. “Roles of Saccharomyces cerevisiae DNA polymerases Pol{eta} and Pol{zeta} in response to irradiation by simulated sunlight”, Nucleic Acids Res., vol. 31, pp. 4541-4552, 2003.
[94]
P.E.M. Gibbs, J. McDonald, R. Woodgate and C.W. Lawrence, “The relative roles in vivo of Saccharomyces cerevisiae Pol η, Pol ζ, Rev1 protein and Pol32 in the bypass and mutation induction of an abasic site, T-T (6-4) photoadduct and T-T cis-syn cyclobutane dimer”, Genetics, vol. 169, pp. 575–582, 2005.
[95]
Y. Wang, R. Woodgate, T.P. McManus, S. Mead, J.J. McCormick and V.M. Maher, “Evidence that in xeroderma pigmentosum variant cells, which lack DNA polymerase η, DNA polymerase ι causes the very high frequency and unique spectrum of UV-induced mutations”, Cancer Research, vol. 67, pp. 3018–3026, 2007.
[96]
S. Shachar, O. Ziv, S. Avkin, S. Adar, J. Wittschieben, T. Reißner, S. Chaney, E.S. Friedberg, Z. Wang, T. Carell, N. Geacintov and Z. Livneh, “Two-polymerase mechanisms dictate error-free and error-prone translesion DNA synthesis in mammals”, EMBO J., vol. 28, pp. 383–393, 2009.
[97]
R. Kasiviswanathan, M.A. Gustafson, W.C. Copeland and J.N. Meyer, “Human mitochondrial DNA polymerase γ exhibits potential for bypass and mutagenesis at UV-induced cyclobutane thymine dimers”, J. Biol. Chem., vol. 287, pp. 9222-9229, 2012.
[98]
G. Raghunathan, T. Kieber-Emmons, R. Rein and I.L. Alderfer, “Conformation features of DNA containing a cis-syn photodimer”, J. Biomol. Struct. Dyn., vol. 7, pp. 899-913, 1990.
[99]
M.G. Cooney and J.H. Miller, “Calculated distortions of duplex DNA by a cis, syn cyclobutane thymine dimer are unaffected by a 3' TpA step”, Nucleic Acids Res., vol. 25, pp. 1432–1436, 1997.
[100]
K. McAteer, Y. Jing, J. Kao, J.-S. Taylor and M.A. Kennedy. “Solution-state structure of a DNA dodecamer duplex containing a Cis-syn thymine cyclobutane dimer, the major UV photoproduct of DNA”, J. Mol. Biol., vol. 282, pp. 1013–1032.
[101]
H. Yamaguchi, D.M. van Aalten, M. Pinak, A. Furukawa, R. Osman, “Essential dynamics of DNA containing a cis.syn cyclobutane thymine dimer lesion”, Nucleic Acids Res., vol. 26, pp. 1939-1946, 1998.
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