Dynamic basis for dG•dT misincorporation via tautomerization and ionization (original) (raw)

References

  1. Watson, J. D. & Crick, F. H. The structure of DNA. Cold Spring Harb. Symp. Quant. Biol. 18, 123–131 (1953)
    Article CAS PubMed Google Scholar
  2. Oertell, K. et al. Kinetic selection vs. free energy of DNA base pairing in control of polymerase fidelity. Proc. Natl Acad. Sci. USA 113, E2277–E2285 (2016)
    Article CAS PubMed PubMed Central Google Scholar
  3. Voorhees, R. M. & Ramakrishnan, V. Structural basis of the translational elongation cycle. Annu. Rev. Biochem. 82, 203–236 (2013)
    Article CAS PubMed Google Scholar
  4. Kool, E. T. Active site tightness and substrate fit in DNA replication. Annu. Rev. Biochem. 71, 191–219 (2002)
    Article CAS PubMed Google Scholar
  5. Demeshkina, N., Jenner, L., Westhof, E., Yusupov, M. & Yusupova, G. A new understanding of the decoding principle on the ribosome. Nature 484, 256–259 (2012)
    Article ADS CAS PubMed Google Scholar
  6. Wang, W., Hellinga, H. W. & Beese, L. S. Structural evidence for the rare tautomer hypothesis of spontaneous mutagenesis. Proc. Natl Acad. Sci. USA 108, 17644–17648 (2011)
    Article ADS CAS PubMed PubMed Central Google Scholar
  7. Bebenek, K., Pedersen, L. C. & Kunkel, T. A. Replication infidelity via a mismatch with Watson–Crick geometry. Proc. Natl Acad. Sci. USA 108, 1862–1867 (2011)
    Article ADS CAS PubMed PubMed Central Google Scholar
  8. Kimsey, I. J., Petzold, K., Sathyamoorthy, B., Stein, Z. W. & Al-Hashimi, H. M. Visualizing transient Watson–Crick-like mispairs in DNA and RNA duplexes. Nature 519, 315–320 (2015)
    Article ADS CAS PubMed PubMed Central Google Scholar
  9. Rozov, A., Demeshkina, N., Westhof, E., Yusupov, M. & Yusupova, G. Structural insights into the translational infidelity mechanism. Nat. Commun. 6, 7251 (2015)
    Article ADS CAS PubMed Google Scholar
  10. Topal, M. D. & Fresco, J. R. Base pairing and fidelity in codon–anticodon interaction. Nature 263, 289–293 (1976)
    Article ADS CAS PubMed Google Scholar
  11. Topal, M. D. & Fresco, J. R. Complementary base pairing and the origin of substitution mutations. Nature 263, 285–289 (1976)
    Article ADS CAS PubMed Google Scholar
  12. Loveland, A. B., Demo, G., Grigorieff, N. & Korostelev, A. A. Ensemble cryo-EM elucidates the mechanism of translation fidelity. Nature 546, 113–117 (2017)
    Article ADS CAS PubMed PubMed Central Google Scholar
  13. Singh, V., Fedeles, B. I. & Essigmann, J. M. Role of tautomerism in RNA biochemistry. RNA 21, 1–13 (2015)
    PubMed Google Scholar
  14. Yu, H., Eritja, R., Bloom, L. B. & Goodman, M. F. Ionization of bromouracil and fluorouracil stimulates base mispairing frequencies with guanine. J. Biol. Chem. 268, 15935–15943 (1993)
    CAS PubMed Google Scholar
  15. Koag, M. C., Nam, K. & Lee, S. The spontaneous replication error and the mismatch discrimination mechanisms of human DNA polymerase β. Nucleic Acids Res. 42, 11233–11245 (2014)
    Article CAS PubMed PubMed Central Google Scholar
  16. Rozov, A., Demeshkina, N., Westhof, E., Yusupov, M. & Yusupova, G. New structural insights into translational miscoding. Trends Biochem. Sci. 41, 798–814 (2016)
    Article CAS PubMed Google Scholar
  17. Tomasetti, C., Li, L. & Vogelstein, B. Stem cell divisions, somatic mutations, cancer etiology, and cancer prevention. Science 355, 1330–1334 (2017)
    Article ADS CAS PubMed PubMed Central Google Scholar
  18. Eckert, K. A. & Kunkel, T. A. Effect of reaction pH on the fidelity and processivity of exonuclease-deficient Klenow polymerase. J. Biol. Chem. 268, 13462–13471 (1993)
    CAS PubMed Google Scholar
  19. Warren, J. J., Forsberg, L. J. & Beese, L. S. The structural basis for the mutagenicity of _O_6-methyl-guanine lesions. Proc. Natl Acad. Sci. USA 103, 19701–19706 (2006)
    Article ADS CAS PubMed PubMed Central Google Scholar
  20. Dosanjh, M. K., Galeros, G., Goodman, M. F. & Singer, B. Kinetics of extension of _O_6-methylguanine paired with cytosine or thymine in defined oligonucleotide sequences. Biochemistry 30, 11595–11599 (1991)
    Article CAS PubMed Google Scholar
  21. Mendelman, L. V., Boosalis, M. S., Petruska, J. & Goodman, M. F. Nearest neighbor influences on DNA polymerase insertion fidelity. J. Biol. Chem. 264, 14415–14423 (1989)
    CAS PubMed Google Scholar
  22. Lee, H. R. & Johnson, K. A. Fidelity of the human mitochondrial DNA polymerase. J. Biol. Chem. 281, 36236–36240 (2006)
    Article CAS PubMed Google Scholar
  23. Xia, S. & Konigsberg, W. H. Mispairs with Watson–Crick base-pair geometry observed in ternary complexes of an RB69 DNA polymerase variant. Protein Sci. 23, 508–513 (2014)
    Article CAS PubMed PubMed Central Google Scholar
  24. Ogle, J. M., Murphy, F. V., Tarry, M. J. & Ramakrishnan, V. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111, 721–732 (2002)
    Article CAS PubMed Google Scholar
  25. Nomura, K. et al. DFT calculations on the effect of solvation on the tautomeric reactions for wobble gua–thy and canonical gua–cyt base-pairs. J. Mod. Phys. 4, 422–431 (2013)
    Article CAS Google Scholar
  26. Brovarets’, O. O. & Hovorun, D. M. The nature of the transition mismatches with Watson–Crick architecture: the G*•T or G•T* DNA base mispair or both? A QM/QTAIM perspective for the biological problem. J. Biomol. Struct. Dyn. 33, 925–945 (2015)
    Article PubMed CAS Google Scholar
  27. Trott, O., Abergel, D. & Palmer, A. G., III . An average-magnetization analysis of _R_1ρ relaxation outside of the fast exchange limit. Mol. Phys. 101, 753–763 (2003)
    Article ADS CAS Google Scholar
  28. Korzhnev, D. M., Orekhov, V. Y. & Kay, L. E. Off-resonance _R_1ρ NMR studies of exchange dynamics in proteins with low spin-lock fields: an application to a Fyn SH3 domain. J. Am. Chem. Soc. 127, 713–721 (2005)
    Article CAS PubMed Google Scholar
  29. Hansen, A. L., Nikolova, E. N., Casiano-Negroni, A. & Al-Hashimi, H. M. Extending the range of microsecond-to-millisecond chemical exchange detected in labeled and unlabeled nucleic acids by selective carbon _R_1ρ NMR spectroscopy. J. Am. Chem. Soc. 131, 3818–3819 (2009)
    Article CAS PubMed Google Scholar
  30. Mulder, F. A. A., Mittermaier, A., Hon, B., Dahlquist, F. W. & Kay, L. E. Studying excited states of proteins by NMR spectroscopy. Nat. Struct. Biol. 8, 932–935 (2001)
    Article CAS PubMed Google Scholar
  31. Szymanski, E. S., Kimsey, I. J. & Al-Hashimi, H. M. Direct NMR evidence that transient tautomeric and anionic states in dG•dT form Watson–Crick-like base pairs. J. Am. Chem. Soc. 139, 4326–4329 (2017)
    Article CAS PubMed PubMed Central Google Scholar
  32. Orozco, M., Hernández, B. & Luque, F. J. Tautomerism of 1-methyl derivatives of uracil, thymine, and 5-bromouracil. Is tautomerism the basis for the mutagenicity of 5-bromouridine? J. Phys. Chem. B 102, 5228–5233 (1998)
    Article CAS Google Scholar
  33. Ban, D. et al. Exceeding the limit of dynamics studies on biomolecules using high spin-lock field strengths with a cryogenically cooled probehead. J. Magn. Reson. 221, 1–4 (2012)
    Article ADS CAS PubMed Google Scholar
  34. Vallurupalli, P., Chakrabarti, N., Pomes, R. & Kay, L. Atomistic picture of conformational exchange in a T4 lysozyme cavity mutant: an experiment-guided molecular dynamics study. Chem. Sci. 7, 3602–3613 (2016)
    Article CAS PubMed PubMed Central Google Scholar
  35. Delaney, J. C. & Essigmann, J. M. Effect of sequence context on _O_6-methylguanine repair and replication in vivo. Biochemistry 40, 14968–14975 (2001)
    Article CAS PubMed Google Scholar
  36. Trott, O. & Palmer, A. G., III . Theoretical study of _R_1ρ rotating-frame and _R_2 free-precession relaxation in the presence of _n_-site chemical exchange. J. Magn. Reson. 170, 104–112 (2004)
    Article ADS CAS PubMed Google Scholar
  37. Sekhar, A. et al. Thermal fluctuations of immature SOD1 lead to separate folding and misfolding pathways. eLife 4, e07296 (2015)
    Article PubMed PubMed Central Google Scholar
  38. Kunkel, T. A. & Alexander, P. S. The base substitution fidelity of eukaryotic DNA polymerases. Mispairing frequencies, site preferences, insertion preferences, and base substitution by dislocation. J. Biol. Chem. 261, 160–166 (1986)
    CAS PubMed Google Scholar
  39. Zahurancik, W. J., Klein, S. J. & Suo, Z. Significant contribution of the 3′→5′ exonuclease activity to the high fidelity of nucleotide incorporation catalyzed by human DNA polymerase ε. Nucleic Acids Res. 42, 13853–13860 (2014)
    Article CAS PubMed PubMed Central Google Scholar
  40. Loeb, L. A. & Kunkel, T. A. Fidelity of DNA synthesis. Annu. Rev. Biochem. 51, 429–457 (1982)
    Article CAS PubMed Google Scholar
  41. Zhang, J., Ieong, K.-W., Johansson, M. & Ehrenberg, M. Accuracy of initial codon selection by aminoacyl-tRNAs on the mRNA-programmed bacterial ribosome. Proc. Natl Acad. Sci. USA 112, 9602–9607 (2015)
    Article ADS CAS PubMed PubMed Central Google Scholar
  42. Rothwell, P. J. & Waksman, G. Structure and mechanism of DNA polymerases. Adv. Protein Chem. 71, 401–440 (2005)
    Article CAS PubMed Google Scholar
  43. Tsai, Y. C. & Johnson, K. A. A new paradigm for DNA polymerase specificity. Biochemistry 45, 9675–9687 (2006)
    Article CAS PubMed Google Scholar
  44. Patel, S. S., Wong, I. & Johnson, K. A. Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant. Biochemistry 30, 511–525 (1991)
    Article CAS PubMed Google Scholar
  45. Zahurancik, W. J., Klein, S. J. & Suo, Z. Kinetic mechanism of DNA polymerization catalyzed by human DNA polymerase ε. Biochemistry 52, 7041–7049 (2013)
    Article CAS PubMed Google Scholar
  46. Balbo, P. B., Wang, E. C. & Tsai, M. D. Kinetic mechanism of active site assembly and chemical catalysis of DNA polymerase β. Biochemistry 50, 9865–9875 (2011)
    Article CAS PubMed Google Scholar
  47. Maximoff, S. N., Kamerlin, S. C. L. & Florián, J. DNA polymerase λ active site favors a mutagenic mispair between the enol form of deoxyguanosine triphosphate substrate and the keto form of thymidine template: a free energy perturbation study. J. Phys. Chem. B 121, 7813–7822 (2017)
    Article CAS PubMed Google Scholar
  48. Freudenthal, B. D., Beard, W. A., Shock, D. D. & Wilson, S. H. Observing a DNA polymerase choose right from wrong. Cell 154, 157–168 (2013)
    Article CAS PubMed PubMed Central Google Scholar
  49. Freudenthal, B. D., Beard, W. A., Cuneo, M. J., Dyrkheeva, N. S. & Wilson, S. H. Capturing snapshots of APE1 processing DNA damage. Nat. Struct. Mol. Biol. 22, 924–931 (2015)
    Article CAS PubMed PubMed Central Google Scholar
  50. Xue, Y. et al. Characterizing RNA excited states using NMR relaxation dispersion. Methods Enzymol. 558, 39–73 (2015)
    Article CAS PubMed PubMed Central Google Scholar
  51. Wagenmakers, E.-J. & Farrell, S. AIC model selection using Akaike weights. Psychon. Bull. Rev. 11, 192–196 (2004)
    Article PubMed Google Scholar
  52. Burnham, K. P. & Anderson, D. R. Multimodel inference. Understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304 (2004)
    Article MathSciNet Google Scholar

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