Membrane association of Wuhan nodavirus protein A is required for its ability to accumulate genomic RNA1 template

Virology

Volumn 439, Issue 2, 2013, Pages 140-151

  Qiu, Yang ^a   Wang, Zhaowei ^a   Liu, Yongxiang ^a   Qi, Nan ^a   Miao, Meng ^a   Si, Jie ^a   Xiang, Xue ^a   Cai, Dawei ^a   Hu, Yuanyang ^a   Zhou, Xi ^a  

^a School of Pharmaceutical Sciences   (China)

Author keywords

Genomic RNA accumulation; Membrane association; Mitochondrial localization; Protein A; Wuhan nodavirus

Indexed keywords

GENOMIC RNA; PROTEIN A; PROTEIN RNA1; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; INTRACELLULAR MEMBRANE; MEMBRANE STRUCTURE; MITOCHONDRIAL MEMBRANE; NODAVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA REPLICATION; RNA STABILITY; VIRUS GENOME; WUHAN NODAVIRUS;

ANIMALS; MITOCHONDRIAL MEMBRANES; NODAVIRIDAE; PROTEIN SORTING SIGNALS; RNA REPLICASE; RNA STABILITY; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION;

NODAVIRIDAE; RNA VIRUSES;

EID: 84875809495     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.02.010     Document Type: Article

References (62)

1. Ahlquist P. Parallels among positive-strand RNA viruses, reverse-transcribing viruses and double-stranded RNA viruses. Nat. Rev. Microbiol. 2006, 4:371-382.
2. Ahlquist P., Noueiry A.O., Lee W.M., Kushner D.B., Dye B.T. Host factors in positive-strand RNA virus genome replication. J. Virol. 2003, 77:8181-8186.
3. Ball L.A., Johnson K.L. Reverse genetics of nodaviruses. Adv. Virus Res. 1999, 53:229-244.
4. Cai D., Qiu Y., Qi N., Yan R., Lin M., Nie D., Zhang J., Hu Y. Characterization of Wuhan Nodavirus subgenomic RNA3 and the RNAi inhibition property of its encoded protein B2. Virus Res. 2010, 151:153-161.
5. Castorena K.M., Stapleford K.A., Miller D.J. Complementary transcriptomic, lipidomic, and targeted functional genetic analyses in cultured Drosophila cells highlight the role of glycerophospholipid metabolism in Flock House virus RNA replication. BMC Genomics 2010, 11:183.
6. Cserzo M., Wallin E., Simon I., von Heijne G., Elofsson A. Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng. 1997, 10:673-676.
7. den Boon J.A., Ahlquist P. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu. Rev. Microbiol. 2010, 64:241-256.
8. den Boon J.A., Diaz A., Ahlquist P. Cytoplasmic viral replication complexes. Cell Host Microbe 2010, 8:77-85.
9. Denison M.R. Seeking membranes: positive-strand RNA virus replication complexes. PLoS Biol. 2008, 6:e270.
10. Diaz A., Gallei A., Ahlquist P. Bromovirus RNA replication compartment formation requires concerted action of 1a's self-interacting RNA capping and helicase domains. J. Virol. 2012, 86:821-834.
11. Emanuelsson O., Nielsen H., Brunak S., von Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 2000, 300:1005-1016.
12. Froshauer S., Kartenbeck J., Helenius A. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J. Cell Biol. 1988, 107:2075-2086.
13. Gallagher T.M., Friesen P.D., Rueckert R.R. Autonomous replication and expression of RNA 1 from black beetle virus. J. Virol. 1983, 46:481-489.
14. Guo Y.X., Chan S.W., Kwang J. Membrane association of greasy grouper nervous necrosis virus protein A and characterization of its mitochondrial localization targeting signal. J. Virol. 2004, 78:6498-6508.
15. Heaton N.S., Randall G. Multifaceted roles for lipids in viral infection. Trends Microbiol. 2011, 19:368-375.
16. Hoffmann B., Beer M., Schelp C., Schirrmeier H., Depner K. Validation of a real-time RT-PCR assay for sensitive and specific detection of classical swine fever. J. Virol. Methods 2005, 130:36-44.
17. Huang Y., Wei H., Wang Y., Shi Z., Raoul H., Yuan Z. Rapid detection of filoviruses by real-time TaqMan polymerase chain reaction assays. Virol. Sin. 2012, 27:273-277.
18. Hugle T., Fehrmann F., Bieck E., Kohara M., Krausslich H.G., Rice C.M., Blum H.E., Moradpour D. The hepatitis C virus nonstructural protein 4B is an integral endoplasmic reticulum membrane protein. Virology 2001, 284:70-81.
19. Kampmueller K.M., Miller D.J. The cellular chaperone heat shock protein 90 facilitates Flock House virus RNA replication in Drosophila cells. J. Virol. 2005, 79:6827-6837.
20. Kopek B.G., Settles E.W., Friesen P.D., Ahlquist P. Nodavirus-induced membrane rearrangement in replication complex assembly requires replicase protein a, RNA templates, and polymerase activity. J. Virol. 2010, 84:12492-12503.
21. Kovalev N., Pogany J., Nagy P.D. A co-opted DEAD-box RNA helicase enhances tombusvirus plus-strand synthesis. PLoS Pathog. 2012, 8:e1002537.
22. Kujala P., Ikaheimonen A., Ehsani N., Vihinen H., Auvinen P., Kaariainen L. Biogenesis of the Semliki Forest virus RNA replication complex. J. Virol. 2001, 75:3873-3884.
23. Lee W.M., Ishikawa M., Ahlquist P. Mutation of host delta9 fatty acid desaturase inhibits brome mosaic virus RNA replication between template recognition and RNA synthesis. J. Virol. 2001, 75:2097-2106.
24. Li H., Li W.X., Ding S.W. Induction and suppression of RNA silencing by an animal virus. Science 2002, 296:1319-1321.
25. Liu C., Zhang J., Yi F., Wang J., Wang X., Jiang H., Xu J., Hu Y. Isolation and RNA1 nucleotide sequence determination of a new insect nodavirus from Pieris rapae larvae in Wuhan city, China. Virus Res. 2006, 120:28-35.
26. Lu R., Maduro M., Li F., Li H.W., Broitman-Maduro G., Li W.X., Ding S.W. Animal virus replication and RNAi-mediated antiviral silencing in Caenorhabditis elegans. Nature 2005, 436:1040-1043.
27. Lu R., Yigit E., Li W.X., Ding S.W. An RIG-I-Like RNA helicase mediates antiviral RNAi downstream of viral siRNA biogenesis in Caenorhabditis elegans. PLoS Pathog. 2009, 5:e1000286.
28. Mackenzie J.M., Jones M.K., Westaway E.G. Markers for trans-Golgi membranes and the intermediate compartment localize to induced membranes with distinct replication functions in flavivirus-infected cells. J. Virol. 1999, 73:9555-9567.
29. Magliano D., Marshall J.A., Bowden D.S., Vardaxis N., Meanger J., Lee J.Y. Rubella virus replication complexes are virus-modified lysosomes. Virology 1998, 240:57-63.
30. Mas P., Beachy R.N. 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. 1999, 147:945-958.
31. Mezeth K.B., Nylund S., Henriksen H., Patel S., Nerland A.H., Szilvay A.M. RNA-dependent RNA polymerase from Atlantic halibut nodavirus contains two signals for localization to the mitochondria. Virus Res. 2007, 130:43-52.
32. Miller D.J., Ahlquist P. Flock house virus RNA polymerase is a transmembrane protein with amino-terminal sequences sufficient for mitochondrial localization and membrane insertion. J. Virol. 2002, 76:9856-9867.
33. Miller D.J., Schwartz M.D., Ahlquist P. Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells. J. Virol. 2001, 75:11664-11676.
34. Miller D.J., Schwartz M.D., Dye B.T., Ahlquist P. Engineered retargeting of viral RNA replication complexes to an alternative intracellular membrane. J. Virol. 2003, 77:12193-12202.
35. Miller S., Krijnse-Locker J. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 2008, 6:363-374.
36. Nagy P.D., Pogany J. The dependence of viral RNA replication on co-opted host factors. Nat. Rev. Microbiol. 2012, 10:137-149.
37. Osman F., Leutenegger C., Golino D., Rowhani A. Real-time RT-PCR (TaqMan) assays for the detection of Grapevine Leafroll associated viruses 1-5 and 9. J. Virol. Methods 2007, 141:22-29.
38. Panavas T., Hawkins C.M., Panaviene Z., Nagy P.D. 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 2005, 338:81-95.
39. Panaviene Z., Baker J.M., Nagy P.D. The overlapping RNA-binding domains of p33 and p92 replicase proteins are essential for tombusvirus replication. Virology 2003, 308:191-205.
40. Pedersen K.W., van der Meer Y., Roos N., Snijder E.J. Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex. J. Virol. 1999, 73:2016-2026.
41. Pogany J., White K.A., Nagy P.D. Specific binding of tombusvirus replication protein p33 to an internal replication element in the viral RNA is essential for replication. J. Virol. 2005, 79:4859-4869.
42. Qi N., Cai D., Qiu Y., Xie J., Wang Z., Si J., Zhang J., Zhou X., Hu Y. RNA binding by a novel helical fold of b2 protein from wuhan nodavirus mediates the suppression of RNA interference and promotes b2 dimerization. J. Virol. 2011, 85:9543-9554.
43. Qi N., Zhang L., Qiu Y., Wang Z., Si J., Liu Y., Xiang X., Xie J., Qin C.F., Zhou X., Hu Y. Targeting of dicer-2 and RNA by a viral RNA silencing suppressor in Drosophila cells. J. Virol. 2012, 86:5763-5773.
44. Qiu Y., Cai D., Qi N., Wang Z., Zhou X., Zhang J., Hu Y. Internal initiation is responsible for synthesis of Wuhan nodavirus subgenomic RNA. J. Virol. 2011, 85:4440-4451.
45. Sasvari Z., Nagy P.D. Making of viral replication organelles by remodeling interior membranes. Viruses 2010, 2:2436-2442.
46. Schlegel A., Giddings T.H., Ladinsky M.S., Kirkegaard K. Cellular origin and ultrastructure of membranes induced during poliovirus infection. J. Virol. 1996, 70:6576-6588.
47. Schmidt-Mende J., Bieck E., Hugle T., Penin F., Rice C.M., Blum H.E., Moradpour D. Determinants for membrane association of the hepatitis C virus RNA-dependent RNA polymerase. J. Biol. Chem. 2001, 276:44052-44063.
48. Schneemann A., Reddy V., Johnson J.E. The structure and function of nodavirus particles: a paradigm for understanding chemical biology. Adv. Virus Res. 1998, 50:381-446.
49. Schneemann A., Zhong W., Gallagher T.M., Rueckert R.R. Maturation cleavage required for infectivity of a nodavirus. J. Virol. 1992, 66:6728-6734.
50. Selling B.H., Allison R.F., Kaesberg P. Genomic RNA of an insect virus directs synthesis of infectious virions in plants. Proc. Natl. Acad. Sci. USA 1990, 87:434-438.
51. Sharma M., Sasvari Z., Nagy P.D. Inhibition of phospholipid biosynthesis decreases the activity of the tombusvirus replicase and alters the subcellular localization of replication proteins. Virology 2011, 415:141-152.
52. Stapleford K.A., Rapaport D., Miller D.J. Mitochondrion-enriched anionic phospholipids facilitate flock house virus RNA polymerase membrane association. J. Virol. 2009, 83:4498-4507.
53. Suzuki R., Sakamoto S., Tsutsumi T., Rikimaru A., Tanaka K., Shimoike T., Moriishi K., Iwasaki T., Mizumoto K., Matsuura Y., Miyamura T., Suzuki T. Molecular determinants for subcellular localization of hepatitis C virus core protein. J. Virol. 2005, 79:1271-1281.
54. Tao Y.J., Ye Q. RNA virus replication complexes. PLoS Pathog. 2010, 6:e1000943.
55. Towner J.S., Ho T.V., Semler B.L. Determinants of membrane association for poliovirus protein 3AB. J. Biol. Chem. 1996, 271:26810-26818.
56. Van Der Heijden M.W., Carette J.E., Reinhoud P.J., Haegi A., Bol J.F. Alfalfa mosaic virus replicase proteins P1 and P2 interact and colocalize at the vacuolar membrane. J. Virol. 2001, 75:1879-1887.
57. Van Wynsberghe P.M., Chen H.R., Ahlquist P. Nodavirus RNA replication protein a induces membrane association of genomic RNA. J. Virol. 2007, 81:4633-4644.
58. Venter P.A., Schneemann A. Recent insights into the biology and biomedical applications of Flock House virus. Cell. Mol. Life Sci. 2008, 65:2675-2687.
59. von Heijne G. Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J. Mol. Biol. 1992, 225:487-494.
60. Wang X., Lee W.M., Watanabe T., Schwartz M., Janda M., Ahlquist P. Brome mosaic virus 1a nucleoside triphosphatase/helicase domain plays crucial roles in recruiting RNA replication templates. J. Virol. 2005, 79:13747-13758.
61. Weeks S.A., Shield W.P., Sahi C., Craig E.A., Rospert S., Miller D.J. A targeted analysis of cellular chaperones reveals contrasting roles for heat shock protein 70 in flock house virus RNA replication. J. Virol. 2010, 84:330-339.
62. Xu K., Huang T.S., Nagy P.D. Authentic in vitro replication of two tombusviruses in isolated mitochondrial and endoplasmic reticulum membranes. J. Virol. 2012, 86:12779-12794.