Motif D of viral RNA-dependent RNA polymerases determines efficiency and fidelity of nucleotide addition

Structure

Volumn 20, Issue 9, 2012, Pages 1519-1527

  Yang, Xiaorong ^a   Smidansky, Eric D ^a   Maksimchuk, Kenneth R ^a   Lum, David ^a   Welch, Jesse L ^a   Arnold, Jamie J ^a   Cameron, Craig E ^a   Boehr, David D ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LYSINE; NUCLEOTIDE; RNA DIRECTED RNA POLYMERASE; VIRUS RNA;

ALPHA HELIX; ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; HYDROGEN BOND; MOTIF D; MUTATION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; PROTON TRANSPORT;

AMINO ACID MOTIFS; BASE PAIRING; BASE SEQUENCE; BIOCATALYSIS; CATALYTIC DOMAIN; HYDROGEN BONDING; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; NUCLEOTIDES; POLIOVIRUS; PROTEIN BINDING; RNA REPLICASE; VIRAL PROTEINS;

EID: 84865768433     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2012.06.012     Document Type: Article

References (55)

1. J.P. Anderson, R. Daifuku, and L.A. Loeb Viral error catastrophe by mutagenic nucleosides Annu. Rev. Microbiol. 58 2004 183 205
2. J.J. Arnold, and C.E. Cameron Poliovirus RNA-dependent RNA polymerase (3D(pol)). Assembly of stable, elongation-competent complexes by using a symmetrical primer-template substrate (sym/sub) J. Biol. Chem. 275 2000 5329 5336
3. J.J. Arnold, and C.E. Cameron Poliovirus RNA-dependent RNA polymerase (3Dpol): pre-steady-state kinetic analysis of ribonucleotide incorporation in the presence of Mg2+ Biochemistry 43 2004 5126 5137
4. J.J. Arnold, M. Vignuzzi, J.K. Stone, R. Andino, and C.E. Cameron Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA polymerase J. Biol. Chem. 280 2005 25706 25716
5. J.J. Arnold, A. Bernal, U. Uche, D.E. Sterner, T.R. Butt, C.E. Cameron, and M.R. Mattern Small ubiquitin-like modifying protein isopeptidase assay based on poliovirus RNA polymerase activity Anal. Biochem. 350 2006 214 221
6. W.A. Beard, and S.H. Wilson Structural insights into the origins of DNA polymerase fidelity Structure 11 2003 489 496
7. J.B. Bell, K.A. Eckert, C.M. Joyce, and T.A. Kunkel Base miscoding and strand misalignment errors by mutator Klenow polymerases with amino acid substitutions at tyrosine 766 in the O helix of the fingers subdomain J. Biol. Chem. 272 1997 7345 7351
8. B. Canard, K. Chowdhury, R. Sarfati, S. Doublié, and C.C. Richardson The motif D loop of human immunodeficiency virus type 1 reverse transcriptase is critical for nucleoside 5′-triphosphate selectivity J. Biol. Chem. 274 1999 35768 35776
9. C. Castro, E. Smidansky, K.R. Maksimchuk, J.J. Arnold, V.S. Korneeva, M. Götte, W. Konigsberg, and C.E. Cameron 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 2007 4267 4272
10. C. Castro, E.D. Smidansky, J.J. Arnold, K.R. Maksimchuk, I. Moustafa, A. Uchida, M. Götte, W. Konigsberg, and C.E. Cameron Nucleic acid polymerases use a general acid for nucleotidyl transfer Nat. Struct. Mol. Biol. 16 2009 212 218
11. J.R. Coleman, D. Papamichail, S. Skiena, B. Futcher, E. Wimmer, and S. Mueller Virus attenuation by genome-scale changes in codon pair bias Science 320 2008 1784 1787
12. S. Crotty, D. Maag, J.J. Arnold, W. Zhong, J.Y. Lau, Z. Hong, R. Andino, and C.E. Cameron The broad-spectrum antiviral ribonucleoside ribavirin is an RNA virus mutagen Nat. Med. 6 2000 1375 1379
13. C. Ferrer-Orta, A. Arias, R. Pérez-Luque, C. Escarmís, E. Domingo, and N. Verdaguer Sequential structures provide insights into the fidelity of RNA replication Proc. Natl. Acad. Sci. USA 104 2007 9463 9468
14. M.C. Franklin, J. Wang, and T.A. Steitz Structure of the replicating complex of a pol alpha family DNA polymerase Cell 105 2001 657 667
15. A.J. Gillis, A.P. Schuller, and E. Skordalakes Structure of the Tribolium castaneum telomerase catalytic subunit TERT Nature 455 2008 633 637
16. D.W. Gohara, C.S. Ha, S. Kumar, B. Ghosh, J.J. Arnold, T.J. Wisniewski, and C.E. Cameron Production of "authentic" poliovirus RNA-dependent RNA polymerase (3D(pol)) by ubiquitin-protease-mediated cleavage in Escherichia coli Protein Expr. Purif. 17 1999 128 138
17. P. Gong, and O.B. Peersen Structural basis for active site closure by the poliovirus RNA-dependent RNA polymerase Proc. Natl. Acad. Sci. USA 107 2010 22505 22510
18. J.L. Hansen, A.M. Long, and S.C. Schultz Structure of the RNA-dependent RNA polymerase of poliovirus Structure 5 1997 1109 1122
19. S.J. Johnson, and L.S. Beese Structures of mismatch replication errors observed in a DNA polymerase Cell 116 2004 803 816
20. S.J. Johnson, J.S. Taylor, and L.S. Beese Processive DNA synthesis observed in a polymerase crystal suggests a mechanism for the prevention of frameshift mutations Proc. Natl. Acad. Sci. USA 100 2003 3895 3900
21. C.M. Joyce, and T.A. Steitz Polymerase structures and function: variations on a theme? J. Bacteriol. 177 1995 6321 6329
22. W.M. Kati, K.A. Johnson, L.F. Jerva, and K.S. Anderson Mechanism and fidelity of HIV reverse transcriptase J. Biol. Chem. 267 1992 25988 25997
23. N. Kaushik, V.N. Pandey, and M.J. Modak Significance of the O-helix residues of Escherichia coli DNA polymerase I in DNA synthesis: dynamics of the dNTP binding pocket Biochemistry 35 1996 7256 7266
24. M.W. Kellinger, and K.A. Johnson Nucleotide-dependent conformational change governs specificity and analog discrimination by HIV reverse transcriptase Proc. Natl. Acad. Sci. USA 107 2010 7734 7739
25. J.R. Kiefer, C. Mao, J.C. Braman, and L.S. Beese Visualizing DNA replication in a catalytically active Bacillus DNA polymerase crystal Nature 391 1998 304 307
26. D.M. Knipe, P.M. Howley, D.E. Griffin, R.A. Lamb, M.A. Martin, B. Roizman, and S.E. Straus Field's Virology Fifth Edition 2007 Lippincott, Williams and Wilkins Philadelphia, PA
27. L.A. Kohlstaedt, J. Wang, J.M. Friedman, P.A. Rice, and T.A. Steitz Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor Science 256 1992 1783 1790
28. T.A. Kunkel, and K. Bebenek DNA replication fidelity Annu. Rev. Biochem. 69 2000 497 529
29. Y. Li, S. Korolev, and G. Waksman Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation EMBO J. 17 1998 7514 7525
30. S. Michielssens, S.L. Moors, M. Froeyen, P. Herdewijn, and A. Ceulemans Structural basis for the role of LYS220 as proton donor for nucleotidyl transfer in HIV-1 reverse transcriptase Biophys. Chem. 157 2011 1 6
31. I.M. Moustafa, H. Shen, B. Morton, C.M. Colina, and C.E. Cameron Molecular dynamics simulations of viral RNA polymerases link conserved and correlated motions of functional elements to fidelity J. Mol. Biol. 410 2011 159 181
32. K.K. Ng, J.J. Arnold, and C.E. Cameron Structure-function relationships among RNA-dependent RNA polymerases Curr. Top. Microbiol. Immunol. 320 2008 137 156
33. A. Nomoto, T. Omata, H. Toyoda, S. Kuge, H. Horie, Y. Kataoka, Y. Genba, Y. Nakano, and N. Imura Complete nucleotide sequence of the attenuated poliovirus Sabin 1 strain genome Proc. Natl. Acad. Sci. USA 79 1982 5793 5797
34. E.K. O'Reilly, and C.C. Kao Analysis of RNA-dependent RNA polymerase structure and function as guided by known polymerase structures and computer predictions of secondary structure Virology 252 1998 287 303
35. J.K. Pfeiffer, and K. Kirkegaard A single mutation in poliovirus RNA-dependent RNA polymerase confers resistance to mutagenic nucleotide analogs via increased fidelity Proc. Natl. Acad. Sci. USA 100 2003 7289 7294
36. J.K. Pfeiffer, and K. Kirkegaard Increased fidelity reduces poliovirus fitness and virulence under selective pressure in mice PLoS Pathog. 1 2005 e11
37. V.R. Racaniello One hundred years of poliovirus pathogenesis Virology 344 2006 9 16
38. Z. Ren, H. Wang, and R. Ghose Dynamics on multiple timescales in the RNA-directed RNA polymerase from the cystovirus phi6 Nucleic Acids Res. 38 2010 5105 5118
39. J.M. Seckler, K.J. Howard, M.D. Barkley, and P.L. Wintrode Solution structural dynamics of HIV-1 reverse transcriptase heterodimer Biochemistry 48 2009 7646 7655
40. K. Singh, and M.J. Modak A unified DNA- and dNTP-binding mode for DNA polymerases Trends Biochem. Sci. 23 1998 277 281
41. T.A. Steitz DNA polymerases: structural diversity and common mechanisms J. Biol. Chem. 274 1999 17395 17398
42. M. Suzuki, A.K. Avicola, L. Hood, and L.A. Loeb Low fidelity mutants in the O-helix of Thermus aquaticus DNA polymerase I J. Biol. Chem. 272 1997 11228 11235
43. M. Suzuki, S. Yoshida, E.T. Adman, A. Blank, and L.A. Loeb Thermus aquaticus DNA polymerase I mutants with altered fidelity. Interacting mutations in the O-helix J. Biol. Chem. 275 2000 32728 32735
44. T.H. Tahirov, D. Temiakov, M. Anikin, V. Patlan, W.T. McAllister, D.G. Vassylyev, and S. Yokoyama Structure of a T7 RNA polymerase elongation complex at 2.9 A resolution Nature 420 2002 43 50
45. D. Temiakov, V. Patlan, M. Anikin, W.T. McAllister, S. Yokoyama, and D.G. Vassylyev Structural basis for substrate selection by t7 RNA polymerase Cell 116 2004 381 391
46. Y.C. Tsai, and K.A. Johnson A new paradigm for DNA polymerase specificity Biochemistry 45 2006 9675 9687
47. M. Vignuzzi, J.K. Stone, J.J. Arnold, C.E. Cameron, and R. Andino Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population Nature 439 2006 344 348
48. M. Vignuzzi, E. Wendt, and R. Andino Engineering attenuated virus vaccines by controlling replication fidelity Nat. Med. 14 2008 154 161
49. D. Wang, D.A. Bushnell, K.D. Westover, C.D. Kaplan, and R.D. Kornberg Structural basis of transcription: role of the trigger loop in substrate specificity and catalysis Cell 127 2006 941 954
50. E.Y. Wu, and L.S. Beese The structure of a high fidelity DNA polymerase bound to a mismatched nucleotide reveals an "ajar" intermediate conformation in the nucleotide selection mechanism J. Biol. Chem. 286 2011 19758 19767
51. X. Yang, J.L. Welch, J.J. Arnold, and D.D. Boehr Long-range interaction networks in the function and fidelity of poliovirus RNA-dependent RNA polymerase studied by nuclear magnetic resonance Biochemistry 49 2010 9361 9371
52. Y.W. Yin, and T.A. Steitz Structural basis for the transition from initiation to elongation transcription in T7 RNA polymerase Science 298 2002 1387 1395
53. Y.W. Yin, and T.A. Steitz The structural mechanism of translocation and helicase activity in T7 RNA polymerase Cell 116 2004 393 404
54. D.F. Zamyatkin, F. Parra, J.M. Alonso, D.A. Harki, B.R. Peterson, P. Grochulski, and K.K. Ng Structural insights into mechanisms of catalysis and inhibition in Norwalk virus polymerase J. Biol. Chem. 283 2008 7705 7712
55. D.F. Zamyatkin, F. Parra, A. Machín, P. Grochulski, and K.K. Ng Binding of 2′-amino-2′-deoxycytidine-5′-triphosphate to norovirus polymerase induces rearrangement of the active site J. Mol. Biol. 390 2009 10 16