Brome mosaic virus 1a nucleoside triphosphatase/helicase domain plays crucial roles in recruiting RNA replication templates

Journal of Virology

Volumn 79, Issue 21, 2005, Pages 13747-13758

  Wang, Xiaofeng ^a   Lee, Wai Ming ^a,c   Watanabe, Tokiko ^a   Schwartz, Michael ^a,b   Janda, Michael ^a   Ahlquist, Paul ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; HELICASE; MUTANT PROTEIN; NUCLEASE; NUCLEOSIDE TRIPHOSPHATASE; RNA POLYMERASE; RNA REPLICATION FACTOR 1A; RNA REPLICATION FACTOR 2A; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; MOSAIC VIRUS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA REPLICATION; RNA STABILITY; RNA TRANSPORT; RNA VIRUS; VIRUS REPLICATION;

BROMOVIRUS; ENDOPLASMIC RETICULUM; NUCLEOSIDE-TRIPHOSPHATASE; PROTEIN STRUCTURE, TERTIARY; RNA HELICASES; RNA, VIRAL; SACCHAROMYCES CEREVISIAE; TEMPLATES, GENETIC;

BROME MOSAIC VIRUS; RNA VIRUSES;

EID: 27144503011     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.21.13747-13758.2005     Document Type: Article

References (59)

1. Ahlquist, P., E. G. Strauss, C. M. Rice, J. H. Strauss, J. Haseloff, and D. Zimmern. 1985. Sindbis virus proteins nsP1 and nsP2 contain homology to nonstructural proteins from several RNA plant viruses. J. Virol. 53:536-542.
2. Ahola, T., and P. Ahlquist. 1999. Putative RNA capping activities encoded by brome mosaic virus: methylation and covalent binding of guanylate by replicase protein 1a. J. Virol. 73:10061-10069.
3. Ahola, T., J. A. den Boon, and P. Ahlquist. 2000. Helicase and capping enzyme active site mutations in brome mosaic virus protein 1a cause defects in template recruitment, negative-strand RNA synthesis, and viral RNA capping. J. Virol. 74:8803-8811.
4. Allison, R., C. Thompson, and P. Ahlquist. 1990. Regeneration of a functional RNA virus genome by recombination between deletion mutants and requirement for cowpea chlorotic mottle virus 3a and coat genes for systemic infection. Proc. Natl. Acad. Sci. USA 87:1820-1824.
5. Bagnat, M., S. Keranen, A. Shevchenko, and K. Simons. 2000. Lipid rafts function in biosynthetic delivery of proteins to the cell surface in yeast. Proc. Natl. Acad. Sci. USA 97:3254-3259.
6. Caruthers, J. M., and D. B. McKay. 2002. Helicase structure and mechanism. Curr. Opin. Struct. Biol. 12:123-133.
7. Chen, J., and P. Ahlquist. 2000. Brome mosaic virus polymerase-like protein 2a is directed to the endoplasmic reticulum by helicase-like viral protein 1a. J. Virol. 74:4310-4318.
8. Chen, J., A. Noueiry, and P. Ahlquist. 2001. Brome mosaic virus protein 1a recruits viral RNA2 to RNA replication through a 5′ proximal RNA2 signal. J. Virol. 75:3207-3219.
9. den Boon, J. A., J. Chen, and P. Ahlquist. 2001. Identification of sequences in Brome mosaic virus replicase protein 1a that mediate association with endoplasmic reticulum membranes. J. Virol. 75:12370-12381.
10. Diez, J., M. Ishikawa, M. Kaido, and P. Ahlquist. 2000. Identification and characterization of a host protein required for efficient template selection in viral RNA replication. Proc. Natl. Acad. Sci. USA 97:3913-3918.
11. Dillingham, M. S., P. Soultanas, and D. B. Wigley. 1999. Site-directed mutagenesis of motif III in PcrA helicase reveals a role in coupling ATP hydrolysis to strand separation. Nucleic Acids Res. 27:3310-3317.
12. Dillingham, M. S., P. Soultanas, P. Wiley, M. R. Webb, and D. B. Wigley. 2001. Defining the roles of individual residues in the single-stranded DNA binding site of PcrA helicase. Proc. Natl. Acad. Sci. USA 98:8381-8387.
13. Egehnan, E. H. 2001. Structural biology. Pumping DNA. Nature 409:573-575.
14. Fairman, M. E., P. A. Maroney, W. Wang, H. A. Bowers, P. Gollnick, T. W. Nilsen, and E. Jankowsky. 2004. Protein displacement by DExH/D "RNA helicases" without duplex unwinding. Science 304:730-734.
15. Froshauer, S., J. Kartenbeck, and A. Helenius. 1988. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J. Cell Biol. 107:2075-2086.
16. Gomis-Ruth, F. X., G. Moncalian, R. Perez-Luque, A. Gonzalez, E. Cabezon, F. de la Cruz, and M. Coll. 2001. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409:637-641.
17. Gorbalenya, A. E., and E. V. Koonin. 1993. Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3:419-429.
18. Goregaoker, S. P., and J. N. Culver. 2003. Oligomerization and activity of the helicase domain of the tobacco mosaic virus 126- and 183-kilodalton replicase proteins. J. Virol. 77:3549-3556.
19. Grassmann, C. W., O. Isken, and S. E. Behrens. 1999. Assignment of the multifunctional NS3 protein of bovine viral diarrhea virus during RNA replication: an in vivo and in vitro study. J. Virol. 73:9196-9205.
20. Gu, B., C. Liu, J. Lin-Goerke, D. R. Maley, L. L. Gutshall, C. A. Feltenberger, and A. M. Del Vecchio. 2000. The RNA helicase and nucleotide triphosphatase activities of the bovine viral diarrhea virus NS3 protein are essential for viral replication. J. Virol. 74:1794-1800.
21. Hatta, T., S. Bullivant, and R. E. Matthews. 1973. Fine structure of vesicles induced in chloroplasts of Chinese cabbage leaves by infection with turnip yellow mosaic virus. J. Gen. Virol. 20:37-50.
22. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
23. Ishikawa, M., M. Janda, M. A. Krol, and P. Ahlquist. 1997. In vivo DNA expression of functional brome mosaic virus RNA replicons in Saccharomyces cerevisiae. J. Virol. 71:7781-7790.
24. Janda, M., and P. Ahlquist. 1993. RNA-dependent replication, transcription, and persistence of brome mosaic virus RNA replicons in S. cerevisiae. Cell 72:961-970.
25. Janda, M., and P. Ahlquist. 1998. Brome mosaic virus RNA replication protein 1a dramatically increases in vivo stability but not translation of viral genomic RNA3. Proc. Natl. Acad. Sci. USA 95:2227-2232.
26. Kainov, D. E., M. Pirttimaa, R. Tuma, S. J. Butcher, G. J. Thomas, Jr., D. H. Bamford, and E. V. Makeyev. 2003. RNA packaging device of double-stranded RNA bacteriophages, possibly as simple as hexamer of P4 protein. J. Biol. Chem. 278:48084-48091.
27. Kao, C. C., and P. Ahlquist. 1992. Identification of the domains required for direct interaction of the helicase-like and polymerase-like RNA replication proteins of brome mosaic virus. J. Virol. 66:7293-7302.
28. Kim, K. S. 1977. An ultrastructural study of inclusions and disease in plant cells infected by cowpea chlorotic mottle virus. J. Gen. Virol. 35:535-543.
29. King, J. A., R. Dubielzig, D. Grimm, and J. A. Kleinschmidt. 2001. DNA helicase-mediated packaging of adeno-associated virus type 2 genomes into preformed capsids. EMBO J. 20:3282-3291.
30. Kong, F., K. Sivakumaran, and C. Kao. 1999. The N-terminal half of the brome mosaic virus 1 a protein has RNA capping-associated activities: specificity for GTP and S-adenosylmethionine. Virology 259:200-210.
31. Koonin, E. V., and V. V. Dolja. 1993. Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit. Rev. Biochem. Mol. Biol. 28:375-430.
32. Korolev, S., J. Hsieh, G. H. Gauss, T. M. Lohman, and G. Waksman. 1997. Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell 90:635-647.
33. Krol, M. A., N. H. Olson, J. Tate, J. E. Johnson, T. S. Baker, and P. Ahlquist. 1999. RNA-controlled polymorphism in the in vivo assembly of 180-subunit and 120-subunit virions from a single capsid protein. Proc. Natl. Acad. Sci. USA 96:13650-13655.
34. Kroner, P. A., B. M. Young, and P. Ahlquist. 1990. Analysis of the role of brome mosaic virus 1a protein domains in RNA replication, using linker insertion mutagenesis. J. Virol. 64:6110-6120.
35. Kujala, P., T. Ahola, N. Ehsani, P. Auvinen, H. Vihinen, and L. Kaariainen. 1999. Intracellular distribution of rubella virus nonstructural protein P150. J. Virol. 73:7805-7811.
36. Lee, W. M., and P. Ahlquist. 2003. Membrane synthesis, specific lipid requirements, and localized lipid composition changes associated with a positive-strand RNA virus RNA replication protein. J. Virol. 77:12819-12828.
37. Li, Y. I., T. W. Shih, Y. H. Hsu, Y. T. Han, Y. L. Huang, and M. Meng. 2001. The helicase-like domain of plant potexvirus replicase participates in formation of RNA 5′ cap structure by exhibiting RNA 5′- triphosphatase activity. J. Virol. 75:12114-12120.
38. Lin, C., and J. L. Kim. 1999. Structure-based mutagenesis study of hepatitis C virus NS3 helicase. J. Virol. 73:8798-8807.
39. Linder, P. 2004. Molecular biology. The life of RNA with proteins. Science 304:694-695.
40. Marchler-Bauer, A., J. B. Anderson, C. DeWeese-Scott, N. D. Fedorova, L. Y. Geer, S. He, D. I. Hurwitz, J. D. Jackson, A. R. Jacobs, C. J. Lanczycki, C. A. Liebert, C. Liu, T. Madej, G. H. Marchler, R. Mazumder, A. N. Nikolskaya, A. R. Panchenko, B. S. Rao, B. A. Shoemaker, V. Simonyan, J. S. Song, P. A. Thiessen, S. Vasudevan, Y. Wang, R. A. Yamashita, J. J. Yin, and S. H. Bryant. 2003. CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res. 31:383-387.
41. Matusan, A. E., M. J. Pryor, A. D. Davidson, and P. J. Wright. 2001. Mutagenesis of the dengue virus type 2 NS3 protein within and outside helicase motifs: effects on enzyme activity and virus replication. J. Virol. 75:9633-9643.
42. Mise, K., and P. Ahlquist. 1995. Host-specificity restriction by bromovirus cell-to-cell movement protein occurs after initial cell-to-cell spread of infection in nonhost plants. Virology 206:276-286.
43. Moore, S. D., and P. E. Prevelige, Jr. 2002. A P22 scaffold protein mutation increases the robustness of head assembly in the presence of excess portal protein. J. Virol. 76:10245-10255.
44. Noueiry, A. O., J. Diez, S. P. Falk, J. Chen, and P. Ahlquist. 2003. Yeast Lsm1p-7p/Pat1p deadenylation-dependent mRNA-decapping factors are required for brome mosaic virus genomic RNA translation. Mol. Cell. Biol. 23:4094-4106.
45. O'Reilly, E. K., N. Tang, P. Ahlquist, and C. C. Kao. 1995. Biochemical and genetic analyses of the interaction between the helicase-like and polymerase-like proteins of the brome mosaic virus. Virology 214:59-71.
46. O'Reilly, E. K., Z. Wang, R. French, and C. C. Kao. 1998. Interactions between the structural domains of the RNA replication proteins of plant-infecting RNA viruses. J. Virol.72:7160-7169.
47. Pirttimaa, M. J., A. O. Paatero, M. J. Frilander, and D. H. Bamford. 2002. Nonspecific nucleoside triphosphatase P4 of double-stranded RNA bacteriophage φ6 is required for single-stranded RNA packaging and transcription. J. Virol. 76:10122-10127.
48. Restrepo-Hartwig, M., and P. Ahlquist. 1999. Brome mosaic virus RNA replication proteins 1a and 2a colocalize and 1a independently localizes on the yeast endoplasmic reticulum. J. Virol. 73:10303-10309.
49. Restrepo-Hartwig, M. A., and P. Ahlquist. 1996. Brome mosaic virus helicase- and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral RNA synthesis. J. Virol. 70:8908-8916.
50. Rikkonen, M., J. Peranen, and L. Kaariainen. 1994. ATPase and GTPase activities associated with Semliki Forest virus nonstructural protein nsP2. J. Virol. 68:5804-5810.
51. Salonen, A., T. Ahola, and L. Kaariainen. 2005. Viral RNA replication in association with cellular membranes. Curr. Top. Microbiol. Immunol. 285:139-173.
52. Schwartz, M., J. Chen, M. Janda, M. Sullivan, J. den Boon, and P. Ahlquist. 2002. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids. Mol. Cell 9:505-514.
53. Singleton, M. R., and D. B. Wigley. 2002. Modularity and specialization in superfamily 1 and 2 helicases. J. Bacteriol. 184:1819-1826.
54. Sullivan, M. L., and P. Ahlquist. 1999. A brome mosaic virus intergenic RNA3 replication signal functions with viral replication protein 1a to dramatically stabilize RNA in vivo. J. Virol. 73:2622-2632.
55. Tai, C. L., W. C. Pan, S. H. Liaw, U. C. Yang, L. H. Hwang, and D. S. Chen. 2001. Structure-based mutational analysis of the hepatitis C virus NS3 helicase. J. Virol. 75:8289-8297.
56. Tanner, N. K., and P. Linden 2001. DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol. Cell 8:251-262.
57. Vasiljeva, L., A. Merits, P. Auvinen, and L. Kaariainen. 2000. Identification of a novel function of the alphavirus capping apparatus. RNA 5′-triphosphatase activity of Nsp2. J. Biol. Chem. 275:17281-17287.
58. Velankar, S. S., P. Soultanas, M. S. Dillingham, H. S. Subramanya, and D. B. Wigley. 1999. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell 97:75-84.
59. Westaway, E., J. Mackenzie, M. Kenney, M. Jones, and A. Khromykh. 1997. Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures. J. Virol. 71:6650-6661.