Highly similar structural frames link the template tunnel and NTP entry tunnel to the exterior surface in RNA-dependent RNA polymerases

Nucleic Acids Research

Volumn 41, Issue 3, 2013, Pages 1464-1482

  Lang, Dorothy M ^a   Zemla, A T ^a   Ecale Zhou, C L ^a  

^a LAWRENCE LIVERMORE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOSIDE TRIPHOSPHATE; RNA DIRECTED RNA POLYMERASE;

AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ACTIVITY; ENZYME STRUCTURE; GENETIC ALGORITHM; GENETIC DIFFERENCE; GENETIC VARIABILITY; PRIORITY JOURNAL; PROCESS DEVELOPMENT; PROTEIN DETERMINATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SEQUENCE ANALYSIS; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEOTIDES; RNA REPLICASE; SEQUENCE ALIGNMENT; STRUCTURAL HOMOLOGY, PROTEIN; TEMPLATES, GENETIC; VIRUSES;

EID: 84873669740     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks1251     Document Type: Article

References (56)

1. Zemla,A.T., Lang,D.M., Kostova,T., Andino,R. and Ecale Zhou,C.L. (2011) StralSV: Assessment of sequence variability within similar 3D structures and application to polio RNA-dependent RNA polymerase. BMC Bioinformatics, 12, e226.
2. Ferrer-Orta,C., Arias,A., Perez-Luque,E., Escarmi,C., Domingo,E. and Verdaguer,N. (2004) Structure of Foot-and-Mouth Disease Virus RNA-dependent RNA polymerase and its complex with a template-primer RNA. J. Biol. Chem., 279, 47212-47221.
3. Thompson,A.A. and Peersen,O.B. (2004) Structural basis for proteolysis-dependent activation of the poliovirus RNA-dependent RNA polymerase. EMBO J., 23, 3462-3471.
4. Poch,O., Sauvaget,I., Delarue,M. and Tordo,N. (1989) Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J., 8, 3867-3874.
5. Pan,J., Vakharia,V.N. and Tao,Y.J. (2007) The structure of a birnavirus polymerase reveals a distinct active site topology. Proc. Natl Acad. Sci. USA, 104, 7385-7390.
6. Koonin,E.V., Wolf,Y.I., Nagasaki,K. and Dolja,V.V. (2008) The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat. Rev. Microbiol., 6, 925-939.
7. Edgar,R.C. (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
8. Berman,H.M., Battistuz,T., Bhat,T.N., Bluhm,W.F., Bourne,P.E., Burkhardt,K., Feng,Z., Gilliland,G.L., Iype,L., Jain,S. et al. (2002) The Protein Data Bank. Acta Crystallogr., D: Biol. Crystallogr., 58, 899-907.
9. Gong,P. and Peersen,O.B. (2010) Structural basis for active site closure by the poliovirus RNA-dependent RNA polymerase. Proc. Natl Acad. Sci. USA, 107, 22505-22510.
10. Wang,Y., Geer,L.Y., Chappey,C., Kans,J.A. and Bryant,S.H. (2000) Cn3D: Sequence and structure views for Entrez. Trends Biochem. Sci., 25, 300-302.
11. Campognola,G., Weygandt,M.H., Scoggin,K.E. and Peersen,O.B. (2008) Crystal structure of coxsackievirus B3 3Dpol highlights the functional importance of residue 5 in picornavirus polymerases. J. Virol., 82, 9458-9464.
12. Love,R.A., Maegley,K.A., Yu,X., Ferre,R.A., Lingardo,L.K., Diehl,W., Parge,H.E., Dragovich,P.S. and Fuhrman,S.A. (2004) The crystal structure of the RNA-dependent RNA polymerase from human rhinovirus: A dual function target for common cold antiviral therapy. Structure, 12, 1533-1544.
13. Ng,K.K., Pendas-Franco,N., Rojo,J., Boga,J.A., Machin,A., Alonso,J.M. and Parra,F. (2004) Crystal structure of Norwalk virus polymerase reveals the carboxyl terminus in the active site cleft. J. Biol. Chem., 279, 16638-16645.
14. Ng,K.K., Cherney,M.M., Vazquez,A.L., Machin,A., Alonso,J.M., Parra,F. and James,M.N. (2002) Crystal structures of active and inactive conformations of a caliciviral RNA-dependent RNA polymerase. J. Biol. Chem., 277, 1381-1387.
15. Fullerton,S.W.B., Blaschke,M., Coutard,B., Gebhardt,J., Gorbalenya,A., Canard,B., Tucker,P.A. and Rohayem,J. (2007) The 2.3 A resolution structure of the sapporo virus RNA dependant RNA polymerase. J. Virol., 81, 1858-1871.
16. O'Farrell,D., Trowbridge,R., Rowlands,D. and Jager,J. (2003) Substrate complexes of hepatitis C virus RNA polymerase (HC-J4): Structural evidence for nucleotide import and De-novo initiation. J. Mol. Biol., 326, 1025-1035.
17. Choi,K.H., Groarke,J.M., Young,D.C., Kuhn,R.J., Smith,J.L., Pevear,D.C. and Rossmann,M.G. (2004) The structure of the RNA-dependent RNA polymerase from bovine viral diarrhea virus establishes the role of GTP in de novo initiation. Proc. Natl Acad. Sci. USA, 101, 4425-4430.
18. Malet,H., Egloff,M.P., Selisko,B., Butcher,R.E., Wright,P.H., Roberts,M., Gruez,A., Sulzenbacher,G., Vonrhein,C., Bricogne,G. et al. (2007) Crystal structure of the RNA polymerase domain of the West Nile virus non-structural protein 5. J. Biol. Chem., 282, 10678-10698.
19. Yap,T.L., Xu,T., Chen,Y.L., Malet,H., Egloff,M.P., Canard,B., Vasudevan,S.G. and Lescar,J. (2007) Crystal structure of the Dengue virus RNA-dependent RNA polymerase catalytic domain at 1.85-angstrom resolution. J. Virol., 81, 4753-4765.
20. Butcher,S.J., Grimes,J.M., Makeyev,E.V., Bamford,D.H. and Stuart,D.I. (2001) A mechanism for initiating RNA-dependent RNA polymerization. Nature, 410, 235-240.
21. Tao,Y., Farsetta,D.L., Nibert,M.L. and Harrison,S.C. (2002) RNA synthesis in a cage-structural studies of reovirus polymerase lambda3. Cell, 111, 733-745.
22. Lu,X., McDonald,S.M., Tortorici,M.A., Tao,Y.J., Vasquez-Del Carpio,R., Nibert,M.L., Patton,J.T. and Harrison,T.C. (2008) Mechanism for coordinated RNA packaging and genome replication by rotavirus polymerase VP1. Structure, 16, 1678-1688.
23. Graham,R.L., Sarin,L.P., Bahar,M.W., Myers,R.A., Stuart,D.H. and Grimes,J.M. (2011) The N-terminus of the RNA polymerase from infectious pancreatic necrosis virus is the determinant of genome attachment. PLoS Pathog., 7, e1002085.
24. Hopkins,A.L., Ren,J., Esnouf,R.M., Willcox,B.E., Jones,E.Y., Ross,C., Miyasaka,T., Walker,R.T., Tanaka,H., Stammers,D.K. et al. (1996) Complexes of HIV-1 reverse transcriptase with inhibitors of the HEPT series reveal conformational changes relevant to the design of potent non-nucleoside inhibitors. J. Med. Chem., 39, 1589-1600.
25. Huang,H., Chopra,R., Verdine,G.L. and Harrison,S.C. (1998) Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: Implications for drug resistance. Science, 282, 1669-1675.
26. Ding,J., Das,K., Hsiou,Y., Sarafianos,S.G., Clark,A.D. Jr, Jacobo-Molina,A., Tantillo,C., Hughes,S.H. and Arnold,E. (1998) Structure and functional Implications of the polymerase active site region in a complex of HIV-1 RT with a double-stranded DNA template-primer and an antibody Fab fragment at 2.8 A ̊ resolution. J. Mol. Biol., 284, 1095-1111.
27. Gillis,A.J., Schuller,A.P. and Skordalakes,E. (2008) Structure of the Tribolium castaneum telomerase catalytic subunit TERT. Nature, 455, 633-637.
28. Yin,Y.W. and Steitz,T.A. (2001) The structural mechanism of translocation and helicase activity in T7 RNA polymerase. Cell, 116, 393-404.
29. Brieba,L. and Ellenberger,T. (2005) Structure of replicative DNA polymerase provides insights into the mechanisms for processivity, frameshifting and editing, doi: 10.2210/pdb2ajq/pdb
30. Yin,Y.W. and Steitz,T.A. (2002) Structural basis for the transition from initiation to elongation transcription in T7 RNA Polymerase. Science, 298, 1387-1395.
31. Gleghorn,M.L., Davydova,E.K., Rothman-Denes,L.B. and Murakami,K.S. (2008) Structural basis for DNA-hairpin promoter recognition by the bacteriophage N4 virion RNA polymerase. Mol. Cell, 32, 707-717.
32. Li,Y., Korolev,S. and Waksman,G. (1998) 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, 7514-7525.
33. Doublie,S., Tabor,S., Long,A.M., Richardson,C.C. and Ellenberger,T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2Å resolution. Nature, 391, 251-258.
34. Xu,X., Liu,Y., Weiss,S., Arnold,E., Sarafianos,S.G. and Ding,J. (2003) Molecular model of SARS coronavirus polymerase: Implications for biochemical functions and drug design. Nucleic Acids Res., 31, 7117-7120.
35. Gorbalenya,A.E., Pringle,D.M., Zeddam,J.L., Luke,B.T., Cameron,C.E., Kalmakoff,J., Hanzlik,T.N., Gordon,K.H.J. and Ward,V.K. (2002) The palm subdomain-based active site is nternally permuted in viral RNA-dependent RNA polymerases of an ancient lineage. J. Mol. Biol., 324, 47-62.
36. Bressanelli,S., Tomei,L., Roussel,A., Incitti,I., Vitale,R.L., Mathieu,M., DeFrancesco,R. and Rey,F.A. (1999) Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus. Proc. Natl. Acad. Sci. U.S.A., 96, 13034-13039.
37. Diamond,S.E. and Kirkegaard,K. (1994) Clustered charged-to-alanine mutagenesis of poliovirus RNA dependent RNA polymerase yields multiple temperature-sensitive mutants defective in RNA synthesis. J. Virol., 68, 863-876.
38. Bruenn,J.A. (2003) A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases. Nucleic Acids Res., 31, 1821-1829.
39. Thompson,A.A., Albertini,R.A. and Peersen,O.B. (2007) Stabilization of poliovirus polymerase by NTP binding and fingers-thumb interactions. J. Mol. Biol., 366, 1459-1474.
40. Cameron,C.E., Mostafa,I.M. and Arnold,J.J. (2009) Dynamics: The missing link between structure and function of the viral RNA-dependent RNA polymerase? Curr. Opin. Struct. Biol., 19, 768-774.
41. Ng,K.K., Arnold,J.J. and Cameron,C.E. (2008) Structure-function relationships among RNA-dependent RNA polymerases. Curr. Top. Microbiol. Immunol., 320, 137-156.
42. Burns,C.C., Lawson,M.A., Semier,B.L. and Ehrenfeld,E. (1989) Effects of mutations in poliovirus 3Dpol on RNA polymerase activity and on polyprotein cleavage. J. Virol., 63, 4866-4874.
43. Steitz,T.A. (1998) A mechanism for all polymerases. Nature, 391, 231-232.
44. Arnold,J.J., Vignuzzi,M., Stone,J.K., Andino,R. and Cameron,C.E. (2005) Remote site control of an active site fidelity checkpoint in a viral RNA-dependent RNA Polymerase. J. Biol. Chem., 280, 25706-25716.
45. Beese,L.S. and Steitz,T.A. (1991) Structural basis for the C-terminal-N-terminal exonuclease activity of Escherichia coli DNA polymerase I: A two metal ion mechanism. EMBO J., 10, 25-33.
46. Charini,W.A., Burns,C.C., Ehrenfeld,E. and Semler,B.L. (1991) trans rescue of a mutant poliovirus RNA polymerase function. J. Virol, 65, 2655-2665.
47. Hansen,J.L., Long,A.M. and Schultz,S.C. (1997) Structure of the RNA-dependent RNA polymerase of poliovirus. Structure, 5, 1109-1122.
48. Korneeva,V.S. and Cameron,C.E. (2007) Structure-function relationships of the viral RNA-dependent RNA polymerase: Fidelity, replication speed, and initiation mechanism determined by a residue in the ribose-binding pocket. J. Biol. Chem., 282, 16135-16145.
49. Richards,O.C., Spagnolo,J.F., Lyle,J.M., Vleck,S.E., Kuchta,R.D. and Kirkegaard,K. (1996) Intramolecular and intermolecular uridylylation by poliovirus RNA-dependent RNA polymerase. J. Virol., 80, 7405-7415.
50. Jablonski,S.A. and Morrow,C.D. (1995) Mutation of the aspartic acid residues of the GDD sequence motif of poliovirus RNA-dependent RNA polymerase results in enzymes with altered metal ion requirements for activity. J. Virol., 69, 1532-1539.
51. Lohmann,V., Korner,F., Herian,U. and Bartenschlager,R. (1997) Biochemical properties of Hepatitis C virus NS5B RNA-dependent RNA polymerase and identification of amino acid sequence motifs essential for enzymatic activity. J. Virol., 71, 8416-8428.
52. Okura,I., Horiike,N., Michitaka,K. and Onji,M. (2004) Effect of mutation in the hepatitis C virus nonstructural 5B region on HCV replication. J. Gastroenterol., 39, 449-454.
53. Hobson,S.D., Rosenblum,E.S., Richards,O.C., Richmond,K., Kirkegaard,K. and Schultz,S.C. (2001) Oligomeric structures of poliovirus polymerase are important for function. EMBO J., 0, 1153-1163.
54. Bernstein,H.D., Sarnow,P. and Baltimore,D. (1996) Genetic complementation among poliovirus mutants derived from an infectious cDNA clone. J. Virol., 60, 1040-1049.
55. Appleby,T.C., Luecke,H., Shim,J.H., Wu,J.Z., Cheney,I.W., Zhong,W., Vogeley,L., Hong,Z. and Yao,N. (2005) Crystal structure of complete rhinovirus RNA polymerase suggests front loading of protein primer. J. Virol., 79, 277-288.
56. Jacobo-Molina,A., Ding,J., Nanni,R.G., Clark,A.D. Jr, Lu,X., Tantillo,C., Williams,R.L., Kamer,G., Ferris,A.L., Clark,P. et al. (1992) Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA. Proc. Natl Acad. Sci. USA, 90, 6320-6324.