3rjk › Citations

Binary complex crystal structure of DNA polymerase β reveals multiple conformations of the templating 8-oxoguanine lesion.

Batra VK, Shock DD, Beard WA, McKenna CE, Wilson SH
Proc Natl Acad Sci U S A 109 113-8 (2012)
Related entries: 3rje, 3rjf, 3rjg, 3rjh, 3rji, 3rjj

Cited: 58 times
EuropePMC logo PMID: 22178760

Abstract

Oxidation of genomic DNA forms the guanine lesion 7,8-dihydro-8-oxoguanine (8-oxoG). When in the template base position during DNA synthesis the 8-oxoG lesion has dual coding potential by virtue of its anti- and syn-conformations, base pairing with cytosine and adenine, respectively. This impacts mutagenesis, because insertion of adenine opposite template 8-oxoG can result in a G to T transversion. DNA polymerases vary by orders of magnitude in their preferences for mutagenic vs. error-free 8-oxoG lesion bypass. Yet, the structural basis for lesion bypass specificity is not well understood. The DNA base excision repair enzyme DNA polymerase (pol) β is presented with gap-filling synthesis opposite 8-oxoG during repair and has similar insertion efficiencies for dCTP and dATP. We report the structure of pol β in binary complex with template 8-oxoG in a base excision repair substrate. The structure reveals both the syn- and anti-conformations of template 8-oxoG in the confines of the polymerase active site, consistent with the dual coding observed kinetically for this enzyme. A ternary complex structure of pol β with the syn-8-oxoG:anti-A Hoogsteen base pair in the closed fully assembled preinsertion active site is also reported. The syn-conformation of 8-oxoG is stabilized by minor groove hydrogen bonding between the side chain of Arg283 and O8 of 8-oxoG. An adjustment in the position of the phosphodiester backbone 5'-phosphate enables 8-oxoG to adopt the syn-conformation.

Reviews - 3rjk mentioned but not cited (1)

  1. Structural Insights into the Specificity of 8-Oxo-7,8-dihydro-2'-deoxyguanosine Bypass by Family X DNA Polymerases. Kaminski AM, Kunkel TA, Pedersen LC, Bebenek K. Genes (Basel) 13 15 (2021)

Articles - 3rjk mentioned but not cited (3)

  1. Binary complex crystal structure of DNA polymerase β reveals multiple conformations of the templating 8-oxoguanine lesion. Batra VK, Shock DD, Beard WA, McKenna CE, Wilson SH. Proc Natl Acad Sci U S A 109 113-118 (2012)
  2. Structure of New Delhi metallo-β-lactamase 1 (NDM-1). Green VL, Verma A, Owens RJ, Phillips SE, Carr SB. Acta Crystallogr Sect F Struct Biol Cryst Commun 67 1160-1164 (2011)
  3. The dipeptidyl peptidase IV inhibitors vildagliptin and K-579 inhibit a phospholipase C: a case of promiscuous scaffolds in proteins. Chakraborty S, Rendón-Ramírez A, Ásgeirsson B, Dutta M, Ghosh AS, Oda M, Venkatramani R, Rao BJ, Dandekar AM, Goñi FM. F1000Res 2 286 (2013)


Reviews citing this publication (7)

  1. Translesion DNA synthesis and mutagenesis in eukaryotes. Sale JE. Cold Spring Harb Perspect Biol 5 a012708 (2013)
  2. Base excision repair of oxidative DNA damage: from mechanism to disease. Whitaker AM, Schaich MA, Smith MR, Flynn TS, Freudenthal BD. Front Biosci (Landmark Ed) 22 1493-1522 (2017)
  3. Close encounters: Moving along bumps, breaks, and bubbles on expanded trinucleotide tracts. Polyzos AA, McMurray CT. DNA Repair (Amst) 56 144-155 (2017)
  4. Oxidant and environmental toxicant-induced effects compromise DNA ligation during base excision DNA repair. Çağlayan M, Wilson SH. DNA Repair (Amst) 35 85-89 (2015)
  5. History of DNA polymerase β X-ray crystallography. Whitaker AM, Freudenthal BD. DNA Repair (Amst) 93 102928 (2020)
  6. Reprint of "Oxidant and environmental toxicant-induced effects compromise DNA ligation during base excision DNA repair". Çağlayan M, Wilson SH. DNA Repair (Amst) 36 86-90 (2015)
  7. DNA polymerase mu: An inflexible scaffold for substrate flexibility. Kaminski AM, Bebenek K, Pedersen LC, Kunkel TA. DNA Repair (Amst) 93 102932 (2020)

Articles citing this publication (47)

  1. Structure and mechanism of DNA polymerase β. Beard WA, Wilson SH. Biochemistry 53 2768-2780 (2014)
  2. Effects of Matrix Stiffness on the Morphology, Adhesion, Proliferation and Osteogenic Differentiation of Mesenchymal Stem Cells. Sun M, Chi G, Li P, Lv S, Xu J, Xu Z, Xia Y, Tan Y, Xu J, Li L, Li Y. Int J Med Sci 15 257-268 (2018)
  3. Structures of dNTP intermediate states during DNA polymerase active site assembly. Freudenthal BD, Beard WA, Wilson SH. Structure 20 1829-1837 (2012)
  4. A switch between DNA polymerases δ and λ promotes error-free bypass of 8-oxo-G lesions. Markkanen E, Castrec B, Villani G, Hübscher U. Proc Natl Acad Sci U S A 109 20401-20406 (2012)
  5. Intrinsic mutagenic properties of 5-chlorocytosine: A mechanistic connection between chronic inflammation and cancer. Fedeles BI, Freudenthal BD, Yau E, Singh V, Chang SC, Li D, Delaney JC, Wilson SH, Essigmann JM. Proc Natl Acad Sci U S A 112 E4571-80 (2015)
  6. Viewing Human DNA Polymerase β Faithfully and Unfaithfully Bypass an Oxidative Lesion by Time-Dependent Crystallography. Vyas R, Reed AJ, Tokarsky EJ, Suo Z. J Am Chem Soc 137 5225-5230 (2015)
  7. DNA polymerase minor groove interactions modulate mutagenic bypass of a templating 8-oxoguanine lesion. Freudenthal BD, Beard WA, Wilson SH. Nucleic Acids Res 41 1848-1858 (2013)
  8. Oxidized nucleotide insertion by pol β confounds ligation during base excision repair. Çağlayan M, Horton JK, Dai DP, Stefanick DF, Wilson SH. Nat Commun 8 14045 (2017)
  9. Impact of ribonucleotide incorporation by DNA polymerases β and λ on oxidative base excision repair. Crespan E, Furrer A, Rösinger M, Bertoletti F, Mentegari E, Chiapparini G, Imhof R, Ziegler N, Sturla SJ, Hübscher U, van Loon B, Maga G. Nat Commun 7 10805 (2016)
  10. Formation and Repair of Mismatches Containing Ribonucleotides and Oxidized Bases at Repeated DNA Sequences. Cilli P, Minoprio A, Bossa C, Bignami M, Mazzei F. J Biol Chem 290 26259-26269 (2015)
  11. Structural and Kinetic Studies of the Effect of Guanine N7 Alkylation and Metal Cofactors on DNA Replication. Kou Y, Koag MC, Lee S. Biochemistry 57 5105-5116 (2018)
  12. Structures of DNA Polymerase Mispaired DNA Termini Transitioning to Pre-catalytic Complexes Support an Induced-Fit Fidelity Mechanism. Batra VK, Beard WA, Pedersen LC, Wilson SH. Structure 24 1863-1875 (2016)
  13. Transition state in DNA polymerase β catalysis: rate-limiting chemistry altered by base-pair configuration. Oertell K, Chamberlain BT, Wu Y, Ferri E, Kashemirov BA, Beard WA, Wilson SH, McKenna CE, Goodman MF. Biochemistry 53 1842-1848 (2014)
  14. Crystal structure of DNA polymerase β with DNA containing the base lesion spiroiminodihydantoin in a templating position. Eckenroth BE, Fleming AM, Sweasy JB, Burrows CJ, Doublié S. Biochemistry 53 2075-2077 (2014)
  15. Rapid inactivation and proteasome-mediated degradation of OGG1 contribute to the synergistic effect of hyperthermia on genotoxic treatments. Fantini D, Moritz E, Auvré F, Amouroux R, Campalans A, Epe B, Bravard A, Radicella JP. DNA Repair (Amst) 12 227-237 (2013)
  16. A fidelity mechanism in DNA polymerase lambda promotes error-free bypass of 8-oxo-dG. Burak MJ, Guja KE, Hambardjieva E, Derkunt B, Garcia-Diaz M. EMBO J 35 2045-2059 (2016)
  17. Capturing a mammalian DNA polymerase extending from an oxidized nucleotide. Whitaker AM, Smith MR, Schaich MA, Freudenthal BD. Nucleic Acids Res 45 6934-6944 (2017)
  18. Metal-dependent conformational activation explains highly promutagenic replication across O6-methylguanine by human DNA polymerase β. Koag MC, Lee S. J Am Chem Soc 136 5709-5721 (2014)
  19. Insights into the base-pairing preferences of 8-oxoguanosine on the ribosome. Thomas EN, Simms CL, Keedy HE, Zaher HS. Nucleic Acids Res 47 9857-9870 (2019)
  20. Mutagenesis mechanism of the major oxidative adenine lesion 7,8-dihydro-8-oxoadenine. Koag MC, Jung H, Lee S. Nucleic Acids Res 48 5119-5134 (2020)
  21. Mutagenic Replication of the Major Oxidative Adenine Lesion 7,8-Dihydro-8-oxoadenine by Human DNA Polymerases. Koag MC, Jung H, Lee S. J Am Chem Soc 141 4584-4596 (2019)
  22. Promutagenicity of 8-Chloroguanine, A Major Inflammation-Induced Halogenated DNA Lesion. Kou Y, Koag MC, Lee S. Molecules 24 E3507 (2019)
  23. hOGG1-Cys326 variant cells are hypersensitive to DNA repair inhibition by nitric oxide. Moritz E, Pauly K, Bravard A, Hall J, Radicella JP, Epe B. Carcinogenesis 35 1426-1433 (2014)
  24. The distribution of DNA damage is defined by region-specific susceptibility to DNA damage formation rather than repair differences. Strand JM, Scheffler K, Bjørås M, Eide L. DNA Repair (Amst) 18 44-51 (2014)
  25. Probing DNA Base-Dependent Leaving Group Kinetic Effects on the DNA Polymerase Transition State. Oertell K, Kashemirov BA, Negahbani A, Minard C, Haratipour P, Alnajjar KS, Sweasy JB, Batra VK, Beard WA, Wilson SH, McKenna CE, Goodman MF. Biochemistry 57 3925-3933 (2018)
  26. Unexpected behavior of DNA polymerase Mu opposite template 8-oxo-7,8-dihydro-2'-guanosine. Kaminski AM, Chiruvella KK, Ramsden DA, Kunkel TA, Bebenek K, Pedersen LC. Nucleic Acids Res 47 9410-9422 (2019)
  27. A guardian residue hinders insertion of a Fapy•dGTP analog by modulating the open-closed DNA polymerase transition. Smith MR, Shock DD, Beard WA, Greenberg MM, Freudenthal BD, Wilson SH. Nucleic Acids Res 47 3197-3207 (2019)
  28. Conformational stabilities of iminoallantoin and its base pairs in DNA: implications for mutagenicity. Jena NR, Bansal M, Mishra PC. Phys Chem Chem Phys 18 12774-12783 (2016)
  29. Insertion of oxidized nucleotide triggers rapid DNA polymerase opening. Kim T, Freudenthal BD, Beard WA, Wilson SH, Schlick T. Nucleic Acids Res 44 4409-4424 (2016)
  30. Insights into the effect of minor groove interactions and metal cofactors on mutagenic replication by human DNA polymerase β. Koag MC, Lee S. Biochem J 475 571-585 (2018)
  31. Is FapyG mutagenic?: Evidence from the DFT study. Jena NR, Mishra PC. Chemphyschem 14 3263-3270 (2013)
  32. Klenow Fragment Discriminates against the Incorporation of the Hyperoxidized dGTP Lesion Spiroiminodihydantoin into DNA. Huang J, Yennie CJ, Delaney S. Chem Res Toxicol 28 2325-2333 (2015)
  33. Molecular basis for the faithful replication of 5-methylcytosine and its oxidized forms by DNA polymerase β. Howard MJ, Foley KG, Shock DD, Batra VK, Wilson SH. J Biol Chem 294 7194-7201 (2019)
  34. Structural basis of DNA synthesis opposite 8-oxoguanine by human PrimPol primase-polymerase. Rechkoblit O, Johnson RE, Gupta YK, Prakash L, Prakash S, Aggarwal AK. Nat Commun 12 4020 (2021)
  35. How DNA polymerase X preferentially accommodates incoming dATP opposite 8-oxoguanine on the template. Sampoli Benítez B, Barbati ZR, Arora K, Bogdanovic J, Schlick T. Biophys J 105 2559-2568 (2013)
  36. The anti/syn conformation of 8-oxo-7,8-dihydro-2'-deoxyguanosine is modulated by Bacillus subtilis PolX active site residues His255 and Asn263. Efficient processing of damaged 3'-ends. Zafra O, Pérez de Ayala L, de Vega M. DNA Repair (Amst) 52 59-69 (2017)
  37. Oxidative Damage Induces a Vacancy G-Quadruplex That Binds Guanine Metabolites: Solution Structure of a cGMP Fill-in Vacancy G-Quadruplex in the Oxidized BLM Gene Promoter. Wang KB, Liu Y, Li Y, Dickerhoff J, Li J, Yang MH, Yang D, Kong LY. J Am Chem Soc 144 6361-6372 (2022)
  38. Promutagenic bypass of 7,8-dihydro-8-oxoadenine by translesion synthesis DNA polymerase Dpo4. Jung H, Lee S. Biochem J 477 2859-2871 (2020)
  39. Structural basis for promutagenicity of 8-halogenated guanine. Koag MC, Min K, Lee S. J Biol Chem 289 6289-6298 (2014)
  40. Structural Determinants Responsible for the Preferential Insertion of Ribonucleotides by Bacterial NHEJ PolDom. Sánchez-Salvador A, de Vega M. Biomolecules 10 E203 (2020)
  41. 7,8-Dihydro-8-oxo-1,N6-ethenoadenine: an exclusively Hoogsteen-paired thymine mimic in DNA that induces A→T transversions in Escherichia coli. Aralov AV, Gubina N, Cabrero C, Tsvetkov VB, Turaev AV, Fedeles BI, Croy RG, Isaakova EA, Melnik D, Dukova S, Ryazantsev DY, Khrulev AA, Varizhuk AM, González C, Zatsepin TS, Essigmann JM. Nucleic Acids Res 50 3056-3069 (2022)
  42. Dynamic basis for dA•dGTP and dA•d8OGTP misincorporation via Hoogsteen base pairs. Gu S, Szymanski ES, Rangadurai AK, Shi H, Liu B, Manghrani A, Al-Hashimi HM. Nat Chem Biol 19 900-910 (2023)
  43. Structural Dynamics of a Common Mutagenic Oxidative DNA Lesion in Duplex DNA and during DNA Replication. Ryan BJ, Yang H, Bacurio JHT, Smith MR, Basu AK, Greenberg MM, Freudenthal BD. J Am Chem Soc 144 8054-8065 (2022)
  44. Structural insights into the promutagenic bypass of the major cisplatin-induced DNA lesion. Ouzon-Shubeita H, Vilas CK, Lee S. Biochem J 477 937-951 (2020)
  45. Structure of a DNA polymerase abortive complex with the 8OG:dA base pair at the primer terminus. Batra VK, Wilson SH. Commun Biol 3 348 (2020)
  46. Dual coding potential of a 2',5'-branched ribonucleotide in DNA. Döring J, Hurek T. RNA 25 105-120 (2019)
  47. Processing oxidatively damaged bases at DNA strand breaks by APE1. Whitaker AM, Stark WJ, Freudenthal BD. Nucleic Acids Res 50 9521-9533 (2022)


Quick links