Crystal structure of complete rhinovirus RNA polymerase suggests front loading of protein primer

Journal of Virology

Volumn 79, Issue 1, 2005, Pages 277-288

  Appleby, Todd C ^a   Luecke, Hartmut ^b   Jae, Hoon Shim ^a   Wu, Jim Z ^a   Cheney, I Wayne ^a   Zhong, Weidong ^a   Vogeley, Lutz ^b   Hong, Zhi ^a   Yao, Nanhua ^a  

^a Valeant Pharmaceuticals International   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE;

AMINO TERMINAL SEQUENCE; ARTICLE; COMPARATIVE STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME ACTIVE SITE; ENZYME STRUCTURE; HUMAN RHINOVIRUS; PRIORITY JOURNAL; PROTEIN DOMAIN; THREE DIMENSIONAL IMAGING; VIRUS REPLICATION;

CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RHINOVIRUS; RNA REPLICASE; RNA, VIRAL; URIDINE;

EID: 10644250663     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.1.277-288.2005     Document Type: Article

References (52)

1. Ago, H., T. Adachi, A. Yoshida, M. Yamamoto, N. Habuka, K. Yatsunami, and M. Miyano. 1999. Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus. Structure Fold Des. 7:1417-1426.
2. Beese, L. S., and T. A. Steitz. 1991. Structural basis for the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J. 10:25-33.
3. Blessing, R. H., and G. D. Smith. 1999. Difference structure factor normalization for determining heavy-atom or anomalous scattering substructures. J. Appl. Cryst. 32:664-670.
4. Bressanelli, S., L. Tomei, A. Roussel, I. Incitti, R. L. Vitale, M. Mathieu, R. De Francesco, and F. A. Rey. 1999. Crystal structure of the RNA-dependent RNA polymerase of hepatitis C virus. Proc. Natl. Acad. Sci. USA 96:13034-13039.
5. Butcher, S. J., J. M. Grimes, E. V. Makeyev, D. H. Bamford, and D. I. Stuart. 2001. A mechanism for initiating RNA-dependent RNA polymerization. Nature 410:235-240.
6. Calhoun, W. J., C. A. Swenson, E. C. Dick, L. B. Schwartz, R. F. Lemanske, Jr., and W. W. Busse. 1991. Experimental rhinovirus 16 infection potentiates histamine release after antigen bronchoprovocation in allergic subjects. Am. Rev. Respir. Dis. 144:1267-1273.
7. Carroll, S. S., J. E. Tomassini, M. Bosserman, K. Getty, M. W. Stahlhut, A. B. Eldrup, B. Bhat, D. Hall, A. L. Simcoe, R. LaFemina, C. A. Rutkowski, B. Wolanski, Z. Yang, G. Migliaccio, R. De Francesco, L. C. Kuo, M. MacCoss, and D. B. Olsen. 2003. Inhibition of hepatitis C virus RNA replication by 2′-modified nucleoside analogs. J. Biol. Chem. 278:11979-11984.
8. Cheney, I. W., S. Naim, J. H. Shim, M. Reinhardt, B. Pai, J. Z. Wu, Z. Hong, and W. Zhong. 2003. Viability of poliovirus/rhinovirus VPg chimeric viruses and identification of an amino acid residue in the VPg gene critical for viral RNA replication. J. Virol. 77:7434-7443.
9. Choi, K. H., J. M. Groarke, D. C. Young, R. J. Kuhn, J. L. Smith, D. C. Pevear, and M. G. Rossmann. 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.
10. Collaborative Computational Project, Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D 50:760-763.
11. Cowtan, K. 1994. DM: an automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsl. Protein Crystallogr. 31:34-38.
12. Gohara, D. W., J. J. Arnold, and C. E. Cameron. 2004. Poliovirus RNA-dependent RNA polymerase (3Dpol): kinetic, thermodynamic, and structural analysis of ribonucleotide selection. Biochemistry 43:5149-5158.
13. Gohara, D. W., S. Crotty, J. J. Arnold, J. D. Yoder, R. Andino, and C. E. Cameron. 2000. Poliovirus RNA-dependent RNA polymerase (3Dpol): structural, biochemical, and biological analysis of conserved structural motifs A and B. J. Biol. Chem. 275:25523-25532.
14. Hadfield, A. T., G. D. Diana, and M. G. Rossmann. 1999. Analysis of three structurally related antiviral compounds in complex with human rhinovirus 16. Proc. Natl. Acad. Sci. USA 96:14730-14735.
15. Hansen, J. L., A. M. Long, and S. C. Schultz. 1997. Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 5:1109-1122.
16. Harris, K. S., S. R. Reddigari, M. J. Nicklin, T. Hammerle, and E. Wimmer. 1992. Purification and characterization of poliovirus polypeptide 3CD, a proteinase and a precursor for RNA polymerase. J. Virol. 66:7481-7489.
17. Harris, K. S., W. Xiang, L. Alexander, W. S. Lane, A. V. Paul, and E. Wimmer. 1994. Interaction of poliovirus polypeptide 3CDpro with the 5′ and 3′ termini of the poliovirus genome. Identification of viral and cellular cofactors needed for efficient binding. J. Biol. Chem. 269:27004-27014.
18. Hobson, S. D., E. S. Rosenblum, O. C. Richards, K. Richmond, K. Kirkegaard, and S. C. Schultz. 2001. Oligomeric structures of poliovirus polymerase are important for function. EMBO J. 20:1153-1163.
19. Hong, Z., C. E. Cameron, M. P. Walker, C. Castro, N. Yao, J. Y. Lau, and W. Zhong. 2001. A novel mechanism to ensure terminal initiation by hepatitis C virus NS5B polymerase. Virology 285:6-11.
20. Huang, H., R. Chopra, G. L. Verdine, and S. C. Harrison. 1998. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282:1669-1675.
21. Hung, M., C. S. Gibbs, and M. Tsiang. 2002. Biochemical characterization of rhinovirus RNA-dependent RNA polymerase. Antivir. Res. 56:99-114.
22. Jacobo-Molina, A., J. Ding, R. G. Nanni, A. D. Clark, Jr., X. Lu, C. Tantillo, R. L. Williams, G. Kamer, A. L. Ferris, P. Clark, A. Hizi, S. H. Hughes, and E. Arnold. 1993. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA. Proc. Natl. Acad. Sci. USA 90:6320-6324.
23. Jones, T. A., J. Y. Zou, S. W. Cowan, and M. Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr Sect. A 47:110-119.
24. Kaiser, L., C. E. Crump, and F. G. Hayden. 2000. In vitro activity of pleconaril and AG7088 against selected serotypes and clinical isolates of human rhinoviruses. Antivir. Res. 47:215-220.
25. Laurila, M. R., E. V. Makeyev, and D. H. Bamford. 2002. Bacteriophage phi 6 RNA-dependent RNA polymerase: molecular details of initiating nucleic acid synthesis without primer. J. Biol. Chem. 277:17117-17124.
26. Lee, W. M., W. Wang, and R. R. Rueckert. 1995. Complete sequence of the RNA genome of human rhinovirus 16, a clinically useful common cold virus belonging to the ICAM-1 receptor group. Virus Genes 9:177-181.
27. Leong, L. E.-C., C. T. Cornell, and B. L. Semler. 2002. Processing determinants and functions of cleavage products of picornavirus polyproteins, p. 187-197. In B. L. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. American Society for Microbiology, Washington, D.C.
28. Lesburg, C. A., M. B. Cable, E. Ferrari, Z. Hong, A. F. Mannarino, and P. C. Weber. 1999. Crystal structure of the RNA-dependent RNA polymerase from hepatitis C virus reveals a fully encircled active site. Nat. Struct. Biol. 6:937-943.
29. Lu, G. 1999. FINDNCS: A program to detect non-crystallographic symmetries in protein crystals from heavy atom sites. J. Appl. Crystallogr. 32:365.
30. Lyle, J. M., E. Bullitt, K. Bienz, and K. Kirkegaard. 2002. Visualization and functional analysis of RNA-dependent RNA polymerase lattices. Science 296:2218-2222.
31. Lyle, J. M., A. Clewell, K. Richmond, O. C. Richards, D. A. Hope, S. C. Schultz, and K. Kirkegaard. 2002. Similar structural basis for membrane localization and protein priming by an RNA-dependent RNA polymerase. J. Biol. Chem. 277:16324-16331.
32. Machin, A., J. M. Martin Alonso, and F. Parra. 2001. Identification of the amino acid residue involved in rabbit hemorrhagic disease virus VPg uridylylation. J. Biol. Chem. 276:27787-27792.
33. Matthews, D. A., P. S. Dragorich, S. E. Webber, S. A. Fuhrman, A. K. Patick, L. S. Zalman, T. F. Hendrickson, R. A. Love, T. J. Prins, J. T. Marakovits, R. Zhou, J. Tikhe, C. E. Ford, J. W. Meador, R. A. Ferre, E. L. Brown, S. L. Binford, M. A. Brothers, D. M. DeLisle, and S. T. Worland. 1999. Structure-assisted design of mechanism-based irreversible inhibitors of human rhinovirus 3C protease with potent antiviral activity against multiple rhinovirus serotypes. Proc. Natl. Acad. Sci. USA 96:11000-11007.
34. Migliaccio, G., J. E. Tomassini, S. S. Carroll, L. Tomei, S. Altamura, B. Bhat, L. Bartholomew, M. R. Bosserman, A. Ceccacci, L. F. Colwell, R. Cortese, R. De Francesco, A. B. Eldrup, K. L. Getty, X. S. Hou, R. L. LaFemina, S. W. Ludmerer, M. MacCoss, D. R. McMasters, M. W. Stahlhut, D. B. Olsen, D. J. Hazuda, and O. A. Flores. 2003. Characterization of resistance to nonobligate chain-terminating ribonucleoside analogs that inhibit hepatitis C virus replication in vitro. J. Biol. Chem. 278:49164-49170.
35. Musher, D. M. 2003. How contagious are common respiratory tract infections? N. Engl. J. Med. 348:1256-1266.
36. Ng, K. K., M. M. Cherney, A. L. Vazquez, A. Machin, J. M. Alonso, F. Parra, and M. N. James. 2002. Crystal structures of active and inactive conformations of a caliciviral RNA-dependent RNA polymerase. J. Biol. Chem. 277:1381-1387.
37. Ng, K. K., N. Pendas-Franco, J. Rojo, J. A. Boga, A. Machin, J. M. Alonso, and F. Parra. 2004. Crystal structure of Norwalk virus polymerase reveals the carboxyl terminus in the active site cleft. J. Biol. Chem. 279:16638-16645.
38. O'Farrell, D., R. Trowbridge, D. Rowlands, and J. Jager. 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.
39. Otwinowski, Z. 1991. Maximum likelihood refinement of heavy atom parameters, p. 80-85. In W. Wolf, P. R. Evans, and A. G. W. Leslie (ed.), Isomorphous replacement and anomalous scattering. Proceedings of the Daresbury Study Weekend. SERC Daresbury Laboratory, Warrington, United Kingdom.
40. Paul, A. V., J. Peters, J. Mugavero, J. Yin, J. H. van Boom, and E. Wimmer. 2003. Biochemical and genetic studies of the VPg uridylylation reaction catalyzed by the RNA polymerase of poliovirus. J. Virol. 77:891-904.
41. Paul, A. V., J. Yin, J. Mugavero, E. Rieder, Y. Liu, and E. Wimmer. 2003. A "slide-back" mechanism for the initiation of protein-primed RNA synthesis by the RNA polymerase of poliovirus. J. Biol. Chem. 278:43951-43960.
42. Racaniello, V. R., and D. Baltimore. 1981. Molecular cloning of poliovirus cDNA and determination of the complete nucleotide sequence of the viral genome. Proc. Natl. Acad. Sci. USA 78:4887-4891.
43. Rieder, E., A. V. Paul, D. W. Kim, J. H. van Boom, and E. Wimmer. 2000. Genetic and biochemical studies of poliovirus cis-acting replication element cre in relation to VPg uridylylation. J. Virol. 74:10371-10380.
44. Rossmann, M. G., E. Arnold, J. W. Ericksort, E. A. Frankenberger, J. P. Griffith, H. J. Hecht, J. E. Johnson, G. Kamer, M. Luo, and A. G. Mosser. 1985. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317:145-153.
45. Schwede, T., J. Kopp, N. Guex, and M. C. Peitsch. 2003. SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res. 31:3381-3385.
46. Sousa, R. 1996. Structural and mechanistic relationships between nucleic acid polymerases. Trends Biochem. Sci. 21:186-190.
47. Steitz, T. A. 1998. A mechanism for all polymerases. Nature 391:231-232.
48. Steitz, T. A., S. J. Smerdon, J. Jager, and C. M. Joyce. 1994. A unified polymerase mechanism for nonhomologous DNA and RNA polymerases. Science 266:2022-2025.
49. Tao, Y., D. L. Farsetta, M. L. Nibert, and S. C. Harrison. 2002. RNA synthesis in a cage-structural studies of reovirus polymerase lambda3. Cell 111:733-745.
50. Weeks, C. M., and R. Miller. 1999. The design and implementation of SnB version 2.0. J. Appl. Cryst. 32:120-124.
51. pol with VPg and with genetic variants of 3AB. J. Virol. 72:6732-6741.
52. Yang, Y., R. Rijnbrand, K. L. McKnight, E. Wimmer, A. Paul, A. Martin, and S. M. Lemon. 2002. Sequence requirements for viral RNA replication and VPg uridylylation directed by the internal cis-acting replication element (cre) of human rhinovirus type 14. J. Virol. 76:7485-7494.