Dual roles for an arginine-rich motif in specific genome recognition and localization of viral coat protein to rna replication sites in flock house virus-infected cells

Journal of Virology

Volumn 83, Issue 7, 2009, Pages 2872-2882

  Venter, P Arno ^a   Marshall, Dawn ^a   Schneemann, Anette ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; COAT PROTEIN; GREEN FLUORESCENT PROTEIN; LYSINE; VIRUS PROTEIN; VIRUS RNA; CAPSID PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL MIGRATION; CONFOCAL MICROSCOPY; DROSOPHILA MELANOGASTER; ENCAPSULATION; FLOCK HOUSE VIRUS; GENOMICS; MICROENVIRONMENT; MITOCHONDRION; NODAVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; RNA ANALYSIS; RNA GENE; RNA REPLICATION; RNA VIRUS; VIRION; VIRUS INFECTION; AMINO ACID SUBSTITUTION; CHEMISTRY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TRANSPORT; SITE DIRECTED MUTAGENESIS; VIRUS ASSEMBLY; VIRUS REPLICATION;

FLOCK HOUSE VIRUS; NODAVIRIDAE; RNA VIRUSES;

AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; ARGININE; CAPSID PROTEINS; MITOCHONDRIA; MUTAGENESIS, SITE-DIRECTED; NODAVIRIDAE; PROTEIN BINDING; PROTEIN TRANSPORT; RNA, VIRAL; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 63149184752     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01780-08     Document Type: Article

References (61)

1. 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, New York, NY.
2. Basnayake, V. R., T. L. Sit, and S. A. Lommel. 2006. The genomic RNA packaging scheme of Red clover necrotic mosaic virus. Virology 345:532-539.
3. Battiste, J. L., H. Mao, N. S. Rao, R. Tan, D. R. Muhandiram, L. E. Kay, A. D. Frankel, and J. R. Williamson. 1996. Alpha helix-RNA major groove recognition in an HIV-1 Rev peptide-RRE RNA complex. Science 273: 1547-1551.
4. Bohnlein, E., J. Berger, and J. Hauber. 1991. Functional mapping of the human immunodeficiency virus type 1 Rev RNA binding domain: new in sights into the domain structure of Rev and Rex. J. Virol. 65:7051-7055.
5. Cai, Z., A. Gorin, R. Frederick, X. Ye, W. Hu, A. Majumdar, A. Kettani, and D. J. Patel. 1998. Solution structure of P22 transcriptional antitermination N peptide-box B RNA complex. Nat. Struct. Biol. 5:203-212.
6. Cochrane, A. W., A Perkins, and C. A. Rosen. 1990. Identification of se quences important in the nucleolar localization of human immunodeficiency virus Rev: relevance of nucleolar localization to function. J. Virol. 64:881-885.
7. Dasgupta, R., L. L. Cheng, L. C. Bartholomay, and B. M. Christensen. 2003. Flock house virus replicates and expresses green fluorescent protein in mos quitoes. J. Gen. Virol. 84:1789-1797.
8. Dearing, S. C., P. D. Scotti, P. J. Wigley, and S. D. Dhana. 1980. A small RNA virus isolated from the grass grub, Costelytra zealandica (Coleoptera: Scarabaeidae). N.Z. J. Zool. 7:267.
9. Dong, X. F., P. Natarajan, M. Tihova, J. E. Johnson, and A. Schneemann. 1998. Particle polymorphism caused by deletion of a peptide molecular switch in a quasiequivalent icosahedral virus. J. Virol. 72:6024-6033.
10. Fisher, A. J., and J. E. Johnson. 1993. Ordered duplex RNA controls capsid architecture in an icosahedral animal virus. Nature 361:176-179.
11. Friesen, P. D., and R. R. Rueckert. 1984. Early and late functions in a bipartite RNA virus: evidence for translational control by competition be tween viral mRNAs. J. Virol. 49:116-124.
12. 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.
13. 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.
14. Garzon, S., H. Strykowski, and G. Charpentier. 1990. Implication of mito chondria in the replication of Nodamura virus in larvae of the Lepidoptera, Galleria mellonella (L.) and in suckling mice. Arch. Virol. 113:165-176.
15. Habib, S. J., W. Neupert, and D. Rapaport. 2007. Analysis and prediction of mitochondrial targeting signals. Methods Cell Biol. 80:761-781.
16. Hoogenraad, N. J., L. A. Ward, and M. T. Ryan. 2002. Import and assembly of proteins into mitochondria of mammalian cells. Biochim. Biophys. Acta 1592:97-105.
17. Hope, T. J., D. McDonald, X. J. Huang, J. Low, and T. G. Parslow. 1990. Mutational analysis of the human immunodeficiency virus type 1 Rev trans activator: essential residues near the amino terminus. J. Virol. 64:5360-5366.
18. Horton, R. M., S. N. Ho, J. K. Pullen, H. D. Hunt, Z. Cai, and L. R. Pease. 1993. Gene splicing by overlap extension. Methods Enzymol. 217:270-279.
19. Kanaji, S., J. Iwahashi, Y. Kida, M. Sakaguchi, and K. Mihara. 2000. Characterization of the signal that directs Tom20 to the mitochondrial outer membrane. J. Cell Biol. 151:277-288.
20. Kopek, B. G., G. Perkins, D. J. Miller, M. H. Ellisman, and P. Ahlquist. 2007. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol. 5:e220.
21. Kramvis, A., and M. C. Kew. 1998. Structure and function of the encapsi dation signal of Hepadnaviridae. J. Viral Hepat. 5:357-367.
22. Krishna, N. K., D. Marshall, and A. Schneemann. 2003. Analysis of RNA packaging in wild-type and mosaic protein capsids of flock house virus using recombinant baculovirus vectors. Virology 305:10-24.
23. Krishna, N. K., and A. Schneemann. 1999. Formation of an RNA het erodimer upon heating of nodavirus particles. J. Virol. 73:1699-1703.
24. Kubota, S., H. Siomi, T. Satoh, S. Endo, M. Maki, and M. Hatanaka. 1989. Functional similarity of HIV-I rev and HTLV-I rex proteins: identification of a new nucleolar-targeting signal in rev protein. Biochem. Biophys. Res. Commun. 162:963-970.
25. Kuroda, R., T. Ikenoue, M. Honsho, S. Tsujimoto, J. Y. Mitoma, and A. Ito. 1998. Charged amino acids at the carboxyl-terminal portions determine the intracellular locations of two isoforms of cytochrome b5. J. Biol. Chem. 273:31097-31102.
26. Lanman, J., J. Crum, T. J. Deerinck, G. M. Gaietta, A, Schneemann, G. E. Sosinsky, M. H. Ellisman, and J. E. Johnson. 2008. Visualizing flock house virus infection in Drosophila cells with correlated fluorescence and electron microscopy. J. Struct. Biol. 161:439-446.
27. Lever, A. M. 2007. HIV-1 RNA packaging. Adv. Pharmacol. 55:1-32.
28. Malim, M. H., S. Bohnlein, J. Hauber, and B. R. Cullen. 1989. Functional dissection of the HIV-1 Rev trans-activator-derivation of a trans-dominant repressor of Rev function. Cell 58:205-214.
29. Marshall, D., and A. Schneemann. 2001. Specific packaging of nodaviral RNA2 requires the N-terminus of the capsid protein. Virology 285:165-175.
30. Miller, D. J., and P. Ahlquist. 2002. Flock house virus RNA polymerase is a transmembrane protein with amino-terminal sequences sufficient for mito chondrial localization and membrane insertion. J. Virol. 76:9856-9867.
31. 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.
32. Mindich, L. 1999. Precise packaging of the three genomic segments of the double-stranded-RNA bacteriophage ø6. Microbiol. Mol. Biol. Rev. 63:149 160.
33. Murphy, F. A., W. F. Scherer, A. K. Harrison, H. W. Dunne, and G. W. Gary, Jr. 1970. Characterization of Nodamura virus, an arthropod transmissible picornavirus. Virology 40:1008-1021.
34. Netherton, C., K. Moffat, E. Brooks, and T. Wileman. 2007. A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication. Adv. Virus Res. 70:101-182.
35. Nicchitta, C. V., R. S. Lerner, S. B. Stephens, R. D. Dodd, and B. Pyhtila. 2005. Pathways for compartmentalizing protein synthesis in eukaryotic cells: the template-partitioning model. Biochem. Cell Biol. 83:687-695.
36. Owen, K. E., and R. J. Kuhn. 1996. Identification of a region in the Sindbis virus nucleocapsid protein that is involved in specificity of RNA encapsida tion. J. Virol. 70:2757-2763.
37. Palese, P. 1977. The genes of influenza virus. Cell 10:1-10.
38. Patton, J. T., and E. Spencer. 2000. Genome replication and packaging of segmented double-stranded RNA viruses. Virology 277:217-225.
39. Puglisi, J. D., L. Chen, S. Blanchard, and A D. Frankel. 1995. Solution structure of a bovine immunodeficiency virus Tat-TAR peptide-RNA com plex. Science 270:1200-1203.
40. Pyhtila, B., T. Zheng, P. J. Lager, J. D. Keene, M. C. Reedy, and C. V. Nicchitta. 2008. Signal sequence- and translation-independent mRNA local ization to the endoplasmic reticulum. RNA 14:445-53.
41. Qu, F., and T. J. Morris. 1997. Encapsidation of turnip crinkle virus is defined by a specific packaging signal and RNA size. J. Virol. 71:1428-1435.
42. Rein, A. 1994. Retroviral RNA packaging: a review. Arch. Virol. Suppl. 9:513-522.
43. Rogers, S. L., G. C. Rogers, D. J. Sharp, and R. D. Vale. 2002. Drosophila EB1 is important for proper assembly, dynamics, and positioning of the mitotic spindle. J. Cell Biol. 158:873-884.
44. Schneemann, A. 2006. The structural and functional role of RNA in icosahedral virus assembly. Annu. Rev. Microbiol. 60:51-67.
45. Schneemann, A., and D. Marshall. 1998. Specific encapsidation of nodavirus RNAs is mediated through the C terminus of capsid precursor protein alpha. J. Virol. 72:8738-8746.
46. Schneemann, A., V. Reddy, and J. E. Johnson. 1998. The structure and function of nodavirus particles: a paradigm for understanding chemical bi ology. Adv. Virus Res. 50:381-46.
47. Schneemann, A., W. Zhong, T. M. Gallagher, and R. R. Rueckert. 1992. Maturation cleavage required for infectivity of a nodavirus. J. Virol. 66:6728-6734.
48. Schneider, P. A., A. Schneemann, and W. I. Lipkin. 1994. RNA splicing in Borna disease virus, a nonsegmented, negative-strand RNA virus. J. Virol. 68:5007-5012.
49. Scotti, P. D., S. Dearing, and D. W. Mossop. 1983. Flock House virus: a nodavirus isolated from Costelytra zealandica (White) (Coleoptera: Scar abaeidae). Arch. Virol. 75:181-189.
50. Seibel, N. M., J. Eljouni, M. M. Nalaskowski, and W. Hampe. 2007. Nuclear localization of enhanced green fluorescent protein homomultimers. Anal. Biochem. 368:95-99.
51. Stauber, R. H., E. Afonina, S. Gulnik, J. Erickson, and G. N. Pavlakis. 1998. Analysis of intracellular trafficking and interactions of cytoplasmic HIV-1 Rev mutants in living cells. Virology 251:38-8.
52. Szilvay, A, M., K. A. Brokstad, S. O. Boe, G. Haukenes, and K. H. Kalland. 1997. Oligomerization of HIV-1 Rev. mutants in the cytoplasm and during nuclear import. Virology 235:73-81.
53. Tang, L., K. N. Johnson, L. A. Ball, T. Lin, M. Yeager, and J. E. Johnson. 2001. The structure of pariacoto virus reveals a dodecahedral cage of duplex RNA. Nat. Struct. Biol. 8:77-83.
54. Tihova, M., K. A. Dryden, T. V. Le, S. C. Harvey, J. E. Johnson, M. Yeager, and A. Schneemann. 2004. Nodavirus coat protein imposes dodecahedral RNA structure independent of nucleotide sequence and length. J. Virol. 78:2897-2905.
55. Truscott, K. N., K. Brandner, and N. Planner. 2003. Mechanisms of protein import into mitochondria. Curr. Biol. 13:R326-R337.
56. Venkatesh, L. K., S. Mohammed, and G. Chinnadurai. 1990. Functional domains of the HIV-1 rev gene required for trans-regulation and subcellular localization. Virology 176:39-47.
57. Venter, P. A., N. K. Krishna, and A. Schneemann. 2005. Capsid protein synthesis from replicating RNA directs specific packaging of the genome of a multipartite, positive-strand RNA virus. J. Virol. 79:6239-6248.
58. Weiss, M. A., and N. Narayana. 1998. RNA recognition by arginine-rich peptide motifs. Biopolymers 48:167-180.
59. Wileman, T. 2007. Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design? Annu. Rev. Microbiol. 61:149-167.
60. Ye, X., R. A. Kumar, and D. J. Patel. 1995. Molecular recognition in the bovine immunodeficiency virus Tat peptide-TAR RNA complex. Chem. Biol. 2:827-840.
61. Zhong, W., R. Dasgupta, and R. Rueckert. 1992. Evidence that the packaging signal for nodaviral RNA2 is a bulged stem-loop. Proc. Natl. Acad. Sci. USA 89:11146-11150.