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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 5225-30 (2015)
Related entries: 4rpx, 4rpy, 4rpz, 4rq0, 4rq1, 4rq2, 4rq3, 4rq4, 4rq6, 4rq7, 4rq8

Cited: 34 times
EuropePMC logo PMID: 25825995

Abstract

One common oxidative DNA lesion, 8-oxo-7,8-dihydro-2'-deoxyguanine (8-oxoG), is highly mutagenic in vivo due to its anti-conformation forming a Watson-Crick base pair with correct deoxycytidine 5'-triphosphate (dCTP) and its syn-conformation forming a Hoogsteen base pair with incorrect deoxyadenosine 5'-triphosphate (dATP). Here, we utilized time-resolved X-ray crystallography to follow 8-oxoG bypass by human DNA polymerase β (hPolβ). In the 12 solved structures, both Watson-Crick (anti-8-oxoG:anti-dCTP) and Hoogsteen (syn-8-oxoG:anti-dATP) base pairing were clearly visible and were maintained throughout the chemical reaction. Additionally, a third Mg(2+) appeared during the process of phosphodiester bond formation and was located between the reacting α- and β-phosphates of the dNTP, suggesting its role in stabilizing reaction intermediates. After phosphodiester bond formation, hPolβ reopened its conformation, pyrophosphate was released, and the newly incorporated primer 3'-terminal nucleotide stacked, rather than base paired, with 8-oxoG. These structures provide the first real-time pictures, to our knowledge, of how a polymerase correctly and incorrectly bypasses a DNA lesion.

Reviews - 4rq5 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 - 4rq5 mentioned but not cited (1)

  1. 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)


Reviews citing this publication (6)

  1. Structure and function relationships in mammalian DNA polymerases. Hoitsma NM, Whitaker AM, Schaich MA, Smith MR, Fairlamb MS, Freudenthal BD. Cell Mol Life Sci 77 35-59 (2020)
  2. Two-Metal-Ion Catalysis: Inhibition of DNA Polymerase Activity by a Third Divalent Metal Ion. Wang J, Konigsberg WH. Front Mol Biosci 9 824794 (2022)
  3. Catalytic mechanism of DNA polymerases-Two metal ions or three? Tsai MD. Protein Sci 28 288-291 (2019)
  4. Structural and Molecular Kinetic Features of Activities of DNA Polymerases. Kuznetsova AA, Fedorova OS, Kuznetsov NA. Int J Mol Sci 23 6373 (2022)
  5. The Role of Natural Polymorphic Variants of DNA Polymerase β in DNA Repair. Kladova OA, Fedorova OS, Kuznetsov NA. Int J Mol Sci 23 2390 (2022)
  6. Watching the bacterial RNA polymerase transcription reaction by time-dependent soak-trigger-freeze X-ray crystallography. Shin Y, Murakami KS. Enzymes 49 305-314 (2021)

Articles citing this publication (26)

  1. Capture of a third Mg²⁺ is essential for catalyzing DNA synthesis. Gao Y, Yang W. Science 352 1334-1337 (2016)
  2. Time-lapse crystallography snapshots of a double-strand break repair polymerase in action. Jamsen JA, Beard WA, Pedersen LC, Shock DD, Moon AF, Krahn JM, Bebenek K, Kunkel TA, Wilson SH. Nat Commun 8 253 (2017)
  3. Requirement for transient metal ions revealed through computational analysis for DNA polymerase going in reverse. Perera L, Freudenthal BD, Beard WA, Shock DD, Pedersen LG, Wilson SH. Proc Natl Acad Sci U S A 112 E5228-36 (2015)
  4. Exploring the Role of the Third Active Site Metal Ion in DNA Polymerase η with QM/MM Free Energy Simulations. Stevens DR, Hammes-Schiffer S. J Am Chem Soc 140 8965-8969 (2018)
  5. 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)
  6. 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)
  7. Crystal structures of ternary complexes of archaeal B-family DNA polymerases. Kropp HM, Betz K, Wirth J, Diederichs K, Marx A. PLoS One 12 e0188005 (2017)
  8. Modulating the DNA polymerase β reaction equilibrium to dissect the reverse reaction. Shock DD, Freudenthal BD, Beard WA, Wilson SH. Nat Chem Biol 13 1074-1080 (2017)
  9. Reactive Oxygen Species Play an Important Role in the Bactericidal Activity of Quinolone Antibiotics. Kottur J, Nair DT. Angew Chem Int Ed Engl 55 2397-2400 (2016)
  10. Simulating the fidelity and the three Mg mechanism of pol η and clarifying the validity of transition state theory in enzyme catalysis. Yoon H, Warshel A. Proteins 85 1446-1453 (2017)
  11. Calcium-driven DNA synthesis by a high-fidelity DNA polymerase. Ralec C, Henry E, Lemor M, Killelea T, Henneke G. Nucleic Acids Res 45 12425-12440 (2017)
  12. Structural Insights into the Post-Chemistry Steps of Nucleotide Incorporation Catalyzed by a DNA Polymerase. Reed AJ, Vyas R, Raper AT, Suo Z. J Am Chem Soc 139 465-471 (2017)
  13. Multiple deprotonation paths of the nucleophile 3'-OH in the DNA synthesis reaction. Gregory MT, Gao Y, Cui Q, Yang W. Proc Natl Acad Sci U S A 118 e2103990118 (2021)
  14. Watching a double strand break repair polymerase insert a pro-mutagenic oxidized nucleotide. Jamsen JA, Sassa A, Shock DD, Beard WA, Wilson SH. Nat Commun 12 2059 (2021)
  15. 2.0 Å resolution crystal structure of human polκ reveals a new catalytic function of N-clasp in DNA replication. Jha V, Ling H. Sci Rep 8 15125 (2018)
  16. In crystallo observation of three metal ion promoted DNA polymerase misincorporation. Chang C, Lee Luo C, Gao Y. Nat Commun 13 2346 (2022)
  17. Intrinsic Cleavage of RNA Polymerase II Adopts a Nucleobase-independent Mechanism Assisted by Transcript Phosphate. Ka Man Tse C, Xu J, Xu L, Sheong FK, Wang S, Chow HY, Gao X, Li X, Cheung PP, Wang D, Zhang Y, Huang X. Nat Energy 2 228-235 (2019)
  18. Structural basis for the D-stereoselectivity of human DNA polymerase β. Vyas R, Reed AJ, Raper AT, Zahurancik WJ, Wallenmeyer PC, Suo Z. Nucleic Acids Res 45 6228-6237 (2017)
  19. Interlocking activities of DNA polymerase β in the base excision repair pathway. Kumar A, Reed AJ, Zahurancik WJ, Daskalova SM, Hecht SM, Suo Z. Proc Natl Acad Sci U S A 119 e2118940119 (2022)
  20. Visualization of mutagenic nucleotide processing by Escherichia coli MutT, a Nudix hydrolase. Nakamura T, Yamagata Y. Proc Natl Acad Sci U S A 119 e2203118119 (2022)
  21. Watching right and wrong nucleotide insertion captures hidden polymerase fidelity checkpoints. Jamsen JA, Shock DD, Wilson SH. Nat Commun 13 3193 (2022)
  22. HIV Reverse Transcriptase Pre-Steady-State Kinetic Analysis of Chain Terminators and Translocation Inhibitors Reveals Interactions between Magnesium and Nucleotide 3'-OH. Dilmore CR, DeStefano JJ. ACS Omega 6 14621-14628 (2021)
  23. Advances in Structural and Single-Molecule Methods for Investigating DNA Lesion Bypass and Repair Polymerases. Raper AT, Reed AJ, Gadkari VV, Suo Z. Chem Res Toxicol 30 260-269 (2017)
  24. In crystallo observation of active site dynamics and transient metal ion binding within DNA polymerases. Chang C, Zhou G, Gao Y. Struct Dyn 10 034702 (2023)
  25. On the Role of Molecular Conformation of the 8-Oxoguanine Lesion in Damaged DNA Processing by Polymerases. Geronimo I, Vidossich P, De Vivo M. J Chem Inf Model 63 1521-1528 (2023)
  26. Visualizing the three-metal-ion-dependent cleavage of a mutagenic nucleotide. Samara NL. Proc Natl Acad Sci U S A 119 e2207180119 (2022)


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