Nucleic acid polymerases use a general acid for nucleotidyl transfer (original) (raw)

References

  1. Steitz, T.A. A mechanism for all polymerases. Nature 391, 231–232 (1998).
    Article CAS Google Scholar
  2. Yang, W., Lee, J.Y. & Nowotny, M. Making and breaking nucleic acids: two-Mg2+-ion catalysis and substrate specificity. Mol. Cell 22, 5–13 (2006).
    Article CAS Google Scholar
  3. Fothergill, M., Goodman, M.F., Petruska, J. & Warshel, A. Structure-energy analysis of the role of metal ions in phosphodiester bond hydrolysis by DNA polymerase I. J. Am. Chem. Soc. 117, 11619–11627 (1995).
    Article CAS Google Scholar
  4. Castro, C. et al. Two proton transfers in the transition state for nucleotidyl transfer catalyzed by RNA- and DNA-dependent RNA and DNA polymerases. Proc. Natl. Acad. Sci. USA 104, 4267–4272 (2007).
    Article CAS Google Scholar
  5. Florian, J., Goodman, M.F. & Warshel, A. Computer simulation of the chemical catalysis of DNA polymerases: discriminating between alternative nucleotide insertion mechanisms for T7 DNA polymerase. J. Am. Chem. Soc. 125, 8163–8177 (2003).
    Article CAS Google Scholar
  6. Showalter, A.K. & Tsai, M.D. A reexamination of the nucleotide incorporation fidelity of DNA polymerases. Biochemistry 41, 10571–10576 (2002).
    Article CAS Google Scholar
  7. Florian, J., Goodman, M.F. & Warshel, A. Computer simulations of protein functions: searching for the molecular origin of the replication fidelity of DNA polymerases. Proc. Natl. Acad. Sci. USA 102, 6819–6824 (2005).
    Article CAS Google Scholar
  8. Sucato, C.A. et al. DNA polymerase β fidelity: halomethylene-modified leaving groups in pre-steady-state kinetic analysis reveal differences at the chemical transition state. Biochemistry 47, 870–879 (2008).
    Article CAS Google Scholar
  9. Anand, V.S. & Patel, S.S. Transient state kinetics of transcription elongation by T7 RNA polymerase. J. Biol. Chem. 281, 35677–35685 (2006).
    Article CAS Google Scholar
  10. Arnold, J.J. & Cameron, C.E. Poliovirus RNA-dependent RNA polymerase (3Dpol): pre-steady-state kinetic analysis of ribonucleotide incorporation in the presence of Mg2+. Biochemistry 43, 5126–5137 (2004).
    Article CAS Google Scholar
  11. Ferrer-Orta, C. et al. Sequential structures provide insights into the fidelity of RNA replication. Proc. Natl. Acad. Sci. USA 104, 9463–9468 (2007).
    Article CAS Google Scholar
  12. Franklin, M.C., Wang, J. & Steitz, T.A. Structure of the replicating complex of a Pol α family DNA polymerase. Cell 105, 657–667 (2001).
    Article CAS Google Scholar
  13. Gohara, D.W., Arnold, J.J. & Cameron, C.E. Poliovirus RNA-dependent RNA polymerase (3Dpol): kinetic, thermodynamic, and structural analysis of ribonucleotide selection. Biochemistry 43, 5149–5158 (2004).
    Article CAS Google Scholar
  14. Huang, H., Chopra, R., Verdine, G.L. & Harrison, S.C. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282, 1669–1675 (1998).
    Article CAS Google Scholar
  15. Pomerantz, R.T., Temiakov, D., Anikin, M., Vassylyev, D.G. & McAllister, W.T. A mechanism of nucleotide misincorporation during transcription due to template-strand misalignment. Mol. Cell 24, 245–255 (2006).
    Article CAS Google Scholar
  16. Sarafianos, S.G. et al. Structures of HIV-1 reverse transcriptase with pre- and post-translocation AZTMP-terminated DNA. EMBO J. 21, 6614–6624 (2002).
    Article CAS Google Scholar
  17. Spence, R.A., Kati, W.M., Anderson, K.S. & Johnson, K.A. Mechanism of inhibition of HIV-1 reverse transcriptase by nonnucleoside inhibitors. Science 267, 988–993 (1995).
    Article CAS Google Scholar
  18. Temiakov, D. et al. Structural basis for substrate selection by T7 RNA polymerase. Cell 116, 381–391 (2004).
    Article CAS Google Scholar
  19. Thompson, A.A. & Peersen, O.B. Structural basis for proteolysis-dependent activation of the poliovirus RNA-dependent RNA polymerase. EMBO J. 23, 3462–3471 (2004).
    Article CAS Google Scholar
  20. Yang, G., Franklin, M., Li, J., Lin, T.C. & Konigsberg, W. Correlation of the kinetics of finger domain mutants in RB69 DNA polymerase with its structure. Biochemistry 41, 2526–2534 (2002).
    Article CAS Google Scholar
  21. Yin, Y.W. & Steitz, T.A. The structural mechanism of translocation and helicase activity in T7 RNA polymerase. Cell 116, 393–404 (2004).
    Article CAS Google Scholar
  22. Zamyatkin, D.F. et al. Structural insights into mechanisms of catalysis and inhibition in Norwalk virus polymerase. J. Biol. Chem. 283, 7705–7712 (2008).
    Article CAS Google Scholar
  23. Canard, B., Chowdhury, K., Sarfati, R., Doublie, S. & Richardson, C.C. The motif D loop of human immunodeficiency virus type 1 reverse transcriptase is critical for nucleoside 5′-triphosphate selectivity. J. Biol. Chem. 274, 35768–35776 (1999).
    Article CAS Google Scholar
  24. Hizi, A., Tal, R., Shaharabany, M. & Loya, S. Catalytic properties of the reverse transcriptases of human immunodeficiency viruses type 1 and type 2. J. Biol. Chem. 266, 6230–6239 (1991).
    CAS PubMed Google Scholar
  25. Gillis, A.J., Schuller, A.P. & Skordalakes, E. Structure of the Tribolium castaneum telomerase catalytic subunit TERT. Nature 455, 633–637 (2008).
    Article CAS Google Scholar
  26. Ng, K.K., Arnold, J.J. & Cameron, C.E. Structure-function relationships among RNA-dependent RNA polymerases. Curr. Top. Microbiol. Immunol. 320, 137–156 (2008).
    CAS PubMed PubMed Central Google Scholar
  27. Rosta, E., Kamerlin, S.C. & Warshel, A. On the interpretation of the observed linear free energy relationship in phosphate hydrolysis: a thorough computational study of phosphate diester hydrolysis in solution. Biochemistry 47, 3725–3735 (2008).
    Article CAS Google Scholar
  28. Schowen, R.L. Mechanistic deductions from solvent isotope effects. Progr. Phys. Org. Chem. 9, 275–332 (1972).
    CAS Google Scholar
  29. Venkatasubban, K.S. & Schowen, R.L. The proton inventory technique. CRC Crit. Rev. Biochem. 17, 1–44 (1984).
    Article CAS Google Scholar
  30. Kraynov, V.S., Showalter, A.K., Liu, J., Zhong, X. & Tsai, M.D. DNA polymerase β: contributions of template-positioning and dNTP triphosphate-binding residues to catalysis and fidelity. Biochemistry 39, 16008–16015 (2000).
    Article CAS Google Scholar
  31. Wang, D., Bushnell, D.A., Westover, K.D., Kaplan, C.D. & Kornberg, R.D. Structural basis of transcription: role of the trigger loop in substrate specificity and catalysis. Cell 127, 941–954 (2006).
    Article CAS Google Scholar
  32. Xiang, Y., Oelschlaeger, P., Florian, J., Goodman, M.F. & Warshel, A. Simulating the effect of DNA polymerase mutations on transition-state energetics and fidelity: evaluating amino acid group contribution and allosteric coupling for ionized residues in human Pol β. Biochemistry 45, 7036–7048 (2006).
    Article CAS Google Scholar
  33. Yang, G., Lin, T., Karam, J. & Konigsberg, W.H. Steady-state kinetic characterization of RB69 DNA polymerase mutants that affect dNTP incorporation. Biochemistry 38, 8094–8101 (1999).
    Article CAS Google Scholar
  34. Kaplan, C.D., Larsson, K.M. & Kornberg, R.D. The RNA polymerase II trigger loop functions in substrate selection and is directly targeted by α-amanitin. Mol. Cell 30, 547–556 (2008).
    Article CAS Google Scholar
  35. Marchand, B. & Gotte, M. Site-specific footprinting reveals differences in the translocation status of HIV-1 reverse transcriptase. Implications for polymerase translocation and drug resistance. J. Biol. Chem. 278, 35362–35372 (2003).
    Article CAS Google Scholar
  36. Johnson, S.J., Taylor, J.S. & Beese, L.S. Processive DNA synthesis observed in a polymerase crystal suggests a mechanism for the prevention of frameshift mutations. Proc. Natl. Acad. Sci. USA 100, 3895–3900 (2003).
    Article CAS Google Scholar
  37. Erie, D.A., Yager, T.D. & von Hippel, P.H. The single-nucleotide addition cycle in transcription: a biophysical and biochemical perspective. Annu. Rev. Biophys. Biomol. Struct. 21, 379–415 (1992).
    Article CAS Google Scholar
  38. Rudd, M.D., Izban, M.G. & Luse, D.S. The active site of RNA polymerase II participates in transcript cleavage within arrested ternary complexes. Proc. Natl. Acad. Sci. USA 91, 8057–8061 (1994).
    Article CAS Google Scholar
  39. Wang, D. & Hawley, D.K. Identification of a 3′→5′ exonuclease activity associated with human RNA polymerase II. Proc. Natl. Acad. Sci. USA 90, 843–847 (1993).
    Article CAS Google Scholar
  40. Erie, D.A., Hajiseyedjavadi, O., Young, M.C. & von Hippel, P.H. Multiple RNA polymerase conformations and GreA: control of the fidelity of transcription. Science 262, 867–873 (1993).
    Article CAS Google Scholar
  41. Bebenek, A. et al. Dissecting the fidelity of bacteriophage RB69 DNA polymerase: site-specific modulation of fidelity by polymerase accessory proteins. Genetics 162, 1003–1018 (2002).
    CAS PubMed PubMed Central Google Scholar
  42. Carroll, S.S., Cowart, M. & Benkovic, S.J. A mutant of DNA polymerase I (Klenow fragment) with reduced fidelity. Biochemistry 30, 804–813 (1991).
    Article CAS Google Scholar
  43. Johnson, V.A. et al. Update of the drug resistance mutations in HIV-1: spring 2008. Top. HIV Med. 16, 62–68 (2008).
    PubMed Google Scholar
  44. Sousa, R. & Padilla, R. A mutant T7 RNA polymerase as a DNA polymerase. EMBO J. 14, 4609–4621 (1995).
    Article CAS Google Scholar
  45. Suzuki, M., Yoshida, S., Adman, E.T., Blank, A. & Loeb, L.A. Thermus aquaticus DNA polymerase I mutants with altered fidelity. Interacting mutations in the O-helix. J. Biol. Chem. 275, 32728–32735 (2000).
    Article CAS Google Scholar
  46. Zhang, H. et al. The L561A substitution in the nascent base-pair binding pocket of RB69 DNA polymerase reduces base discrimination. Biochemistry 45, 2211–2220 (2006).
    Article CAS Google Scholar
  47. Arnold, J.J., Vignuzzi, M., Stone, J.K., Andino, R. & Cameron, C.E. Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA polymerase. J. Biol. Chem. 280, 25706–25716 (2005).
    Article CAS Google Scholar
  48. Vignuzzi, M., Stone, J.K., Arnold, J.J., Cameron, C.E. & Andino, R. Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439, 344–348 (2006).
    Article CAS Google Scholar
  49. Vignuzzi, M., Wendt, E. & Andino, R. Engineering attenuated virus vaccines by controlling replication fidelity. Nat. Med. 14, 154–161 (2008).
    Article CAS Google Scholar
  50. Sawaya, M.R., Prasad, R., Wilson, S.H., Kraut, J. & Pelletier, H. Crystal structures of human DNA polymerase β complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry 36, 11205–11215 (1997).
    Article CAS Google Scholar

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