Nodavirus RNA replication protein A induces membrane association of genomic RNA

Journal of Virology

Volumn 81, Issue 9, 2007, Pages 4633-4644

  Van Wynsberghe, Priscilla M ^a   Chen, Hau Ren ^a,b   Ahlquist, Paul ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NATIONAL CHUNG CHENG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; GENOMIC RNA; PHOSPHORUS 32; PROTEIN A; RNA POLYMERASE; VIRUS RNA; YELLOW FLUORESCENT PROTEIN;

ARTICLE; COMPLEX FORMATION; DROSOPHILA MELANOGASTER; ISOTOPE LABELING; NODAVIRUS; NONHUMAN; NORTHERN BLOTTING; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA REPLICATION; RNA STABILITY; RNA SYNTHESIS; RNA VIRUS; SACCHAROMYCES CEREVISIAE; VIRUS ISOLATION; VIRUS REPLICATION; WESTERN BLOTTING; YEAST CELL;

ANIMALS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CELLS, CULTURED; DROSOPHILA MELANOGASTER; GENOMIC INSTABILITY; MUTATION; NODAVIRIDAE; PROTEIN STRUCTURE, TERTIARY; REPLICATION PROTEIN A; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA REPLICASE; RNA, VIRAL; SACCHAROMYCES CEREVISIAE; VIRUS REPLICATION;

DROSOPHILA MELANOGASTER; FLOCK HOUSE VIRUS; NODAVIRIDAE; RNA VIRUSES; SACCHAROMYCES CEREVISIAE;

EID: 34247574570     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02267-06     Document Type: Article

References (70)

1. Ahlquist, P. 2006. Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat. Rev. Microbiol. 4:371-382.
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., and L. Kaariainen. 1995. Reaction in alphavirus mRNA capping: formation of a covalent complex of nonstructural protein nsP1 with 7-methyl-GMP. Proc. Natl. Acad. Sci. USA 92:507-511.
4. Argos, P. 1988. A sequence motif in many polymerases. Nucleic Acids Res. 16:9909-9916.
5. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.). 1987. Current protocols in molecular biology. John Wiley & Sons, Inc., New York, NY.
6. Ball, L. A. 1992. Cellular expression of a functional nodavirus RNA replicon from vaccinia virus vectors. J. Virol. 66:2335-2345.
7. Ball, L. A. 1995. Requirements for the self-directed replication of flock house virus RNA 1. J. Virol. 69:720-727.
8. Ball, L. A., and K. L. Johnson. 1998. Nodaviruses of insects, p. 225-267. In L. K. Miller and L. A. Ball (ed.), The insect viruses. Plenum Publishing Corporation, New York, NY.
9. Benzaghou, I., I. Bougie, and M. Bisaillon. 2004. Effect of metal ion binding on the structural stability of the hepatitis C virus RNA polymerase. J. Biol. Chem. 279:49755-49761.
10. Cartier, J. L., P. A. Hershberger, and P. D. Friesen. 1994. Suppression of apoptosis in insect cells stably transfected with baculovirus p35: dominant interference by N-terminal sequences p35(1-76). J. Virol. 68:7728-7737.
11. 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.
12. 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.
13. Dasgupta, R., A. Ghosh, B. Dasmahapatra, L. A. Guarino, and P. Kaesberg. 1984. Primary and secondary structure of black beetle virus RNA2, the genomic messenger for BBV coat protein precursor. Nucleic Acids Res. 12:7215-7223.
14. Dunigan, D. D., and M. Zaitlin. 1990. Capping of tobacco mosaic virus RNA. Analysis of viral-coded guanylyltransferase-like activity. J. Biol. Chem. 265:7779-7786.
15. Dye, B. T., D. J. Miller, and P. Ahlquist. 2005. In vivo self-interaction of nodavirus RNA replicase protein A revealed by fluorescence resonance energy transfer. J. Virol. 79:8909-8919.
16. Egger, D., and K. Bienz. 2005. Intracellular location and translocation of silent and active poliovirus replication complexes. J. Gen. Virol. 86:707-718.
17. Egger, D., B. Wolk, R. Gosert, L. Bianchi, H. E. Blum, D. Moradpour, and K. Bienz. 2002. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J. Virol. 76:5974-5984.
18. Elazar, M., P. Liu, C. M. Rice, and J. S. Glenn. 2004. An N-terminal amphipathic helix in hepatitis C virus (HCV) NS4B mediates membrane association, correct localization of replication complex proteins, and HCV RNA replication. J. Virol. 78:11393-11400.
19. Ferrer-Orta, C., A. Arias, R. Perez-Luque, C. Escarmis, E. Domingo, and N. Verdaguer. 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.
20. Friesen, P. D., and R. R. Rueckert. 1982. Black beetle virus: messenger for protein B is a subgenomic viral RNA. J. Virol. 42:986-995.
21. Friesen, P. D., and R. R. Rueckert. 1981. Synthesis of black beetle virus proteins in cultured Drosophila cells: differential expression of RNAs 1 and 2. J. Virol. 37:876-886.
22. Gallagher, T. M., P. D. Friesen, and R. R. Rueckert. 1983. Autonomous replication and expression of RNA 1 from black beetle virus. J. Virol. 46:481-489.
23. Gallagher, T. M., and R. R. Rueckert. 1988. Assembly-dependent maturation cleavage in provirions of a small icosahedral insect ribovirus. J. Virol. 62:3399-3406.
24. Gamarnik, A. V., and R. Andino. 1998. Switch from translation to RNA replication in a positive-stranded RNA virus. Genes Dev. 12:2293-2304.
25. Gopinath, K., B. Dragnea, and C. Kao. 2005. Interaction between brome mosaic virus proteins and RNAs: effects on RNA replication, protein expression, and RNA stability. J. Virol. 79:14222-14234.
26. Gosert, R., D. Egger, V. Lohmann, R. Bartenschlager, H. E. Blum, K. Bienz, and D. Moradpour. 2003. Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons. J. Virol. 77:5487-5492.
27. Guarino, L. A., A. Ghosh, B. Dasmahapatra, R. Dasgupta, and P. Kaesberg. 1984. Sequence of the black beetle virus subgenomic RNA and its location in the viral genome. Virology 139:199-203.
28. Heinlein, M., H. S. Padgett, J. S. Gens, B. G. Pickard, S. J. Casper, B. L. Epel, and R. N. Beachy. 1998. Changing patterns of localization of the tobacco mosaic virus movement protein and replicase to the endoplasmic reticulum and microtubules during infection. Plant Cell 10:1107-1120.
29. Herrick, D., R. Parker, and A. Jacobson. 1990. Identification and comparison of stable and unstable mRNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:2269-2284.
30. Huang, Y. L., Y. H. Hsu, Y. T. Han, and M. Meng. 2005. mRNA guanylation catalyzed by the S-adenosylmethionine-dependent guanylyltransferase of bamboo mosaic virus. J. Biol. Chem. 280:13153- 13162.
31. Jablonski, S. A., and C. D. Morrow. 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.
32. 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.
33. Johnson, K. N., K. L. Johnson, R. Dasgupta, T. Gratsch, and L. A. Ball. 2001. Comparisons among the larger genome segments of six nodaviruses and their encoded RNA replicases. J. Gen. Virol. 82:1855-1866.
34. Kamer, G., and P. Argos. 1984. Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acids Res. 12:7269-7282.
35. Koonin, E. V. 1991. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72:2197-2206.
36. Kujala, P., A. Ikaheimonen, N. Ehsani, H. Vihinen, P. Auvinen, and L. Kaariainen. 2001. Biogenesis of the Semliki Forest virus RNA replication complex. J. Virol. 75:3873-3884.
37. Larimer, F. W., C. L. Hsu, M. K. Maupin, and A. Stevens. 1992. Characterization of the XRN1 gene encoding a 5′→3′ exoribonuclease: sequence data and analysis of disparate protein and mRNA levels of gene-disrupted yeast cells. Gene 120:51-57.
38. Li, H., W. X. Li, and S. W. Ding. 2002. Induction and suppression of RNA silencing by an animal virus. Science 296:1319-1321.
39. Lindenbach, B. D., J. Y. Sgro, and P. Ahlquist. 2002. Long-distance base pairing in flock house virus RNA1 regulates subgenomic RNA3 synthesis and RNA2 replication. J. Virol. 76:3905-3919.
40. Lu, R., M. Maduro, F. Li, H. W. Li, G. Broitman-Maduro, W. X. Li, and S. W. Ding. 2005. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 436:1040-1043.
41. Magden, J., N. Takeda, T. Li, P. Auvinen, T. Ahola, T. Miyamura, A. Merits, and L. Kaariainen. 2001. Virus-specific mRNA capping enzyme encoded by hepatitis E virus. J. Virol. 75:6249-6255.
42. Magliano, D., J. A. Marshall, D. S. Bowden, N. Vardaxis, J. Meanger, and J. Y. Lee. 1998. Rubella virus replication complexes are virus-modified lysosomes. Virology 240:57-63.
43. Mas, P., and R. N. Beachy. 1999. Replication of tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement protein in intracellular distribution of viral RNA. J. Cell Biol. 147:945-958.
44. Miller, D. J., and P. Ahlquist. 2002. Flock house virus RNA polymerase is a transmembrane protein with amino-terminal sequences sufficient for mitochondrial localization and membrane insertion. J. Virol. 76:9856-9867.
45. Miller, D. J., M. D. Schwartz, and P. Ahlquist. 2001. Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells. J. Virol. 75:11664-11676.
46. Miller, D. J., M. D. Schwartz, B. T. Dye, and P. Ahlquist. 2003. Engineered retargeting of viral RNA replication complexes to an alternative intracellular membrane. J. Virol. 77:12193-12202.
47. Panavas, T., C. M. Hawkins, Z. Panaviene, and P. D. Nagy. 2005. The role of the p33:p33/p92 interaction domain in RNA replication and intracellular localization of p33 and p92 proteins of cucumber necrosis tombusvirus. Virology 338:81-95.
48. Panaviene, Z., T. Panavas, and P. D. Nagy. 2005. Role of an internal and two 3′-terminal RNA elements in assembly of tombusvirus replicase. J. Virol. 79:10608-10618.
49. Pantaleo, V., L. Rubino, and M. Russo. 2004. The p36 and p95 replicase proteins of carnation Italian ringspot virus cooperate in stabilizing defective interfering RNA. J. Gen. Virol. 85:2429-2433.
50. Perrigoue, J. G., J. A. den Boon, A. Friedl, M. A. Newton, P. Ahlquist, and B. Sugden. 2005. Lack of association between EBV and breast carcinoma. Cancer Epidemiol. Biomarkers Prev. 14:809-814.
51. Pogany, J., K. A. White, and P. D. Nagy. 2005. Specific binding of tombus-virus replication protein p33 to an internal replication element in the viral RNA is essential for replication. J. Virol. 79:4859-4869.
52. Price, B. D., R. R. Rueckert, and P. Ahlquist. 1996. Complete replication of an animal virus and maintenance of expression vectors derived from it in Saccharomyces cerevisiac. Proc. Natl. Acad. Sci. USA 93:9465-9470.
53. Price, B. D., M. Roeder, and P. Ahlquist. 2000. DNA-directed expression of functional flock house virus RNA1 derivatives in Saccharomyces cerevisiae, heterologous gene expression, and selective effects on subgenomic mRNA synthesis. J. Virol. 74:11724-11733.
54. Rajendran, K. S., and P. D. Nagy. 2003. Characterization of the RNA-binding domains in the replicase proteins of tomato bushy stunt virus. J. Virol. 77:9244-9258.
55. 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.
56. Rubino, L., and M. Russo. 1998. Membrane targeting sequences in tombus-virus infections. Virology 252:431-437.
57. Rubino, L., F. Weber-Lotfi, A. Dietrich, C. Stussi-Garaud, and M. Russo. 2001. The open reading frame 1-encoded ('36K') protein of carnation Italian ringspot virus localizes to mitochondria. J. Gen. Virol. 82:29-34.
58. Salonen, A., T. Ahola, and L. Kaariainen. 2005. Viral RNA replication in association with cellular membranes. Curr. Top. Microbiol. Immunol. 285:139-173.
59. Sambrook, J., and D. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
60. Schlegel, A., T. H. Giddings, Jr., M. S. Ladinsky, and K. Kirkegaard. 1996. Cellular origin and ultrastructure of membranes induced during poliovirus infection. J. Virol. 70:6576-6588.
61. Schneemann, A., V. Reddy, and J. E. Johnson. 1998. The structure and function of nodavirus particles: a paradigm for understanding chemical biology. Adv. Virus Res. 50:381-446.
62. 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.
63. Scotti, P. D., S. Dearing, and D. W. Mossop. 1983. Flock house virus: a nodavirus isolated from Costelytra zealandica (White) (Coleoptera: Scarabaeidae). Arch. Virol. 75:181-189.
64. Selling, B. H., R. F. Allison, and P. Kaesberg. 1990. Genomic RNA of an insect virus directs synthesis of infectious virions in plants. Proc. Natl. Acad. Sci. USA 87:434-438.
65. Stevens, A. 1980. Purification and characterization of a Saccharomyces cerevisiae exoribonuclease which yields 5′-mononucleotides by a 5′ leads to 3′ mode of hydrolysis. J. Biol. Chem. 255:3080-3085.
66. 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.
67. Tucker, M., and R. Parker. 2000. Mechanisms and control of mRNA decapping in Saccharomyces cerevisiae. Annu. Rev. Biochem. 69:571-595.
68. Wang, X., W. M. Lee, T. Watanabe, M. Schwartz, M. Janda, and P. Ahlquist. 2005. Brome mosaic virus 1a nucleoside triphosphatase/helicase domain plays crucial roles in recruiting RNA replication templates. J. Virol. 79:13747-13758.
69. Yang, Y., R. Rijnbrand, S. Watowich, and S. M. Lemon. 2004. Genetic evidence for an interaction between a picornaviral cis-acting RNA replication element and 3CD protein. J. Biol. Chem. 279:12659-12667.
70. Yin, J., A. V. Paul, E. Wimmer, and E. Rieder. 2003. Functional dissection of a poliovirus cis-acting replication clement [PV-cre(2C)]: analysis of single-and dual-cre viral genomes and proteins that bind specifically to PV-cre RNA. J. Virol. 77:5152-5166.