Analysis of the subcellular targeting of the smaller replicase protein of Pelargonium flower break virus

Virus Research

Volumn 163, Issue 2, 2012, Pages 580-591

  Martínez Turiño, Sandra ^a   Hernández, Carmen ^a  

^a Universitat Politècnica de València   (Spain)

Author keywords

Carmovirus; Membrane association; Mitochondria; Pelargonium flower break virus; Subcellular localization; Viral replicase

Indexed keywords

GREEN FLUORESCENT PROTEIN; PROTEIN P27;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FRACTIONATION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE DELETION; INTRACELLULAR MEMBRANE; MITOCHONDRION; NONHUMAN; PELARGONIUM FLOWER BREAK VIRUS; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; VIRUS REPLICATION;

ARTIFICIAL GENE FUSION; CARMOVIRUS; CELL FRACTIONATION; CELLS, CULTURED; DNA MUTATIONAL ANALYSIS; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; MICROSCOPY, CONFOCAL; MITOCHONDRIAL MEMBRANES; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; RNA REPLICASE; SEQUENCE DELETION; STAINING AND LABELING; TOBACCO; VIRAL PROTEINS; VIRUS REPLICATION;

CARMOVIRUS; PELARGONIUM FLOWER BREAK VIRUS; RNA VIRUSES; TOMBUSVIRIDAE;

EID: 84856509840     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2011.12.011     Document Type: Article

References (66)

1. 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.
2. Arai M., Mitsuke H., Ikeda M., Xia J.X., Kikuchi T., Satake M., Shimizu T. ConPred II: a consensus prediction method for obtaining transmembrane topology models with high reliability. Nucleic Acids Res. 2004, 32:W390-W393.
3. Batten J.S., Turina M., Scholthof K.B. Panicovirus accumulation is governed by two membrane-associated proteins with a newly identified conserved motif that contributes to pathogenicity. Virol. J. 2006, 3:12.
4. Beddoe T., Lithgow T. Delivery of nascent polypeptides to the mitochondrial surface. Biochim. Biophys. Acta 2002, 1592:35-39.
5. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
6. Chacinska A., Koehler C.M., Milenkovic D., Lithgow T., Pfanner N. Importing mitochondrial proteins: machineries and mechanisms. Cell 2009, 138:628-644.
7. Ciuffreda P., Rubino L., Russo M. Molecular cloning and complete nucleotide sequence of galinsoga mosaic virus genomic RNA. Arch. Virol. 1998, 143:173-180.
8. Combet C., Blanchet C., Geourjon C., Deléage G. NPS@: network protein sequence analysis. Trends Biochem. Sci. 2000, 25:147-150.
9. Cserzö 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.
10. Denison M.R. Seeking membranes: positive-strand RNA virus replication complexes. PLoS Biol. 2008, 6:e270.
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. Fernández-Miragall O., Hernández C. An internal ribosome entry site directs translation of the 3'-gene from Pelargonium flower break virus genomic RNA: implications for infectivity. PLoS One 2011, 6:e22617.
13. Galao R.P., Scheller N., Alves-Rodrígues I., Breinig T., Meyerhans A., Díez J. Saccharomyces cerevisiae: a versatile eukaryotic system in virology. Microb. Cell Fact. 2007, 6:32.
14. Garavito R.M., Picot D., Loll P.J. The 3.1A X-ray crystal structure of the integral membrane enzyme prostaglandin H2 synthase-1. Adv. Prostaglandin Thromboxane Leukot. Res. 1995, 23:99-103.
15. Hua S., Sun Z. Support vector machine approach for protein subcellular localization prediction. Bioinformatics 2001, 17:721-728.
16. Hawkins J., Bodén M. Detecting and sorting targeting peptides with neural networks and support vector machines. J. Bioinform. Comput. Biol. 2006, 4:1-18.
17. Hofmann K., Stoffel W. TMBASE - a database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 1993, 374:166-170.
18. Hwang Y.T., McCartney A.W., Gidda S.K., Mullen R.T. Localization of the Carnation Italian ringspot virus replication protein p36 to the mitochondrial outer membrane is mediated by an internal targeting signal and the TOM complex. BMC Cell Biol. 2008, 9:54.
19. Ishibashi K., Nishikiori M., Ishikawa M. Interactions between tobamovirus replication proteins and cellular factors: their impacts on virus multiplication. Mol. Plant Microbe Interact. 2010, 23:1413-1419.
20. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 1983, 153:163-168.
21. Juretić D., Zoranić L., Zucić D. Basic charge clusters and predictions of membrane protein topology. J. Chem. Inf. Comput. Sci. 2002, 42:620-632.
22. Käll L., Krogh A., Sonnhammer E.L. Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Nucleic Acids Res. 2007, 35:W429-W432.
23. Kemper C., Habib S.J., Engl G., Heckmeyer P., Dimmer K.S., Rapaport D. Integration of tail-anchored proteins into the mitochondrial outer membrane does not require any known import components. J. Cell Sci. 2008, 121:1990-1998.
24. Koenig R., Lesemann D.E., Pfeilstetter E. New isolates of carnation Italian ringspot virus differ from the original one by having replication-associated proteins with a typical tombusvirus-like N-terminus and by inducing peroxisome- rather than mitochondrion-derived multivesicular bodies. Arch. Virol. 2009, 154:1695-1698.
25. Koonin E.V. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 1991, 72:2197-2206.
26. Koonin E.V., Dolja V.V. Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit. Rev. Biochem. Mol. Biol. 1993, 28:375-430.
27. Kuo-Chen Ch, Hong-Bin S. A new method for predicting the subcellular localization of eukaryotic proteins with both single and multiple sites: Euk-mPLoc 2.0. PLoS One 2010, 5:e9931.
28. Lesemann D.E., Adam G. Electron microscopical and serological studies on four isometrical pelargonium viruses. Acta Hortic. 1994, 377:41-54.
29. Lomize M.A., Lomize A.L., Pogozheva I.D., Mosberg H.I. OPM: orientations of proteins in membranes database. Bioinformatics 2006, 22:623-625.
30. McCartney A.W., Greenwood J.S., Fabian M.R., White K.A., Mullen R.T. Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell 2005, 17:3513-3531.
31. Mackenzie J. Wrapping things up about virus RNA replication. Traffic 2005, 6:967-977.
32. Martínez-Turiño S., Hernández C. Inhibition of RNA silencing by the coat protein of Pelargonium flower break virus: distinctions from closely related suppressors. J. Gen. Virol. 2009, 90:519-525.
33. Martínez-Turiño S., Hernández C. Identification and characterization of RNA binding activity in the ORF1-encoded replicase protein of Pelargonium flower break virus. J. Gen. Virol. 2010, 91:3075-3084.
34. Martínez-Turiño S., Hernández C. A membrane-associated movement protein of Pelargonium flower break virus shows RNA-binding activity and contains a biologically relevant leucine zipper-like motif. Virology 2011, 413:310-319.
35. 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.
36. Mochizuki T., Hirai K., Kanda A., Ohnishi J., Ohki T., Tsuda S. Induction of necrosis via mitochondrial targeting of Melon necrotic spot virus replication protein p29 by its second transmembrane domain. Virology 2009, 390:239-249.
37. Nagy P.D. Yeast as a model host to explore plant virus-host interactions. Annu. Rev. Phytopathol. 2008, 46:217-242.
38. Nakai T., Yasuhara T., Fujiki Y., Ohashi A. Multiple genes, including a member of the AAA family, are essential for degradation of unassembled subunit 2 of cytochrome c oxidase in yeast mitochondria. Mol. Cell. Biol. 1995, 15:4441-4452.
39. Navarro B., Rubino L., Russo M. Expression of the Cymbidium ringspot virus 33-kilodalton protein in Saccharomyces cerevisiae and molecular dissection of the peroxisomal targeting signal. J. Virol. 2004, 78:4744-4752.
40. Orgel J.P. Sequence context and modified hydrophobic moment plots help identify 'horizontal' surface helices in transmembrane protein structure prediction. J. Struct. Biol. 2004, 148:51-65.
41. Orgel J.P. Surface-active helices in transmembrane proteins. Curr. Protein Pept. Sci. 2006, 7:553-560.
42. 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.
43. Peña L., Cervera M., Ghorbel R., Domínguez A., Fagoaga C., Juárez J., Pina J.A., Navarro L. Transgenic citrus. Plant Genetic Engineering, Improvement of Commercial Plants 2003, vol. 3:261-282. SCI Tech Publishing LLC, Houston, TX, USA.
44. 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.
45. Poot M., Zhang Y.Z., Krämer J.A., Wells K.S., Jones L.J., Hanzel D.K., Lugade A.G., Singer V.L., Haugland R.P. Analysis of mitochondrial morphology and function with novel fixable fluorescent stains. J. Histochem. Cytochem. 1996, 44:1363-1372.
46. Rajendran K.S., Nagy P.D. Characterization of the RNA-binding domains in the replicase proteins of tomato bushy stunt virus. J. Virol. 2003, 77:9244-9258.
47. Rajendran K.S., Nagy P.D. Kinetics and functional studies on interaction between the replicase proteins of Tomato bushy stunt virus: requirement of p33:p92 interaction for replicase assembly. Virology 2006, 345:270-279.
48. Rico P., Hernández C. Complete nucleotide sequence and genome organization of Pelargonium flower break virus. Arch. Virol. 2004, 149:641-651.
49. Rico P., Hernández C. Infectivity of in vitro transcripts from a full-length cDNA clone of Pelargonium flower break virus in an experimental and a natural host. J. Plant Pathol. 2006, 88:103-106.
50. Rose A., Lorenzen S., Goede A., Gruening B., Hildebrand P.W. RHYTHM - a server to predict the orientation of transmembrane helices in channels and membrane-coils. Nucleic Acids Res. 2009, 37:W575-W580.
51. Rost B. PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol. 1996, 266:525-539.
52. Rubino L., Di Franco A., Russo M. Expression of a plant virus non-structural protein in Saccharomyces cerevisiae causes membrane proliferation and altered mitochondrial morphology. J. Gen. Virol. 2000, 81:279-286.
53. Rubino L., Weber-Lotfi F., Dietrich A., Stussi-Garaud C., Russo M. The open reading frame 1-encoded (36K) protein of Carnation Italian ringspot virus localizes to mitochondria. J. Gen. Virol. 2001, 82:29-34.
54. Salonen A., Ahola T., Kääriäinen L. Viral RNA replication in association with cellular membranes. Curr. Top. Microbiol. Immunol. 2005, 285:139-173.
55. Setoguchi K., Otera H., Mihara K. Cytosolic factor- and TOM-independent import of C-tail-anchored mitochondrial outer membrane proteins. EMBO J. 2006, 25:5635-5647.
56. Siggers K.A., Lesser C.F. The yeast Saccharomyces cerevisiae: a versatile model system for the identification and characterization of bacterial virulence proteins. Cell Host Microbe 2008, 4:8-15.
57. Stork J., Kovalev N., Sasvari Z., Nagy P.D. RNA chaperone activity of the tombusviral p33 replication protein facilitates initiation of RNA synthesis by the viral RdRp in vitro. Virology 2011, 409:338-347.
58. Schwer B., Ren S., Pietschmann T., Kartenbeck J., Kaehlcke K., Bartenschlager R., Yen T.S., Ott M. Targeting of hepatitis C virus core protein to mitochondria through a novel C-terminal localization motif. J. Virol. 2004, 78:7958-7968.
59. Turner K.A., Sit T.L., Callaway A.S., Allen N.S., Lommel S.A. Red clover necrotic mosaic virus replication proteins accumulate at the endoplasmic reticulum. Virology 2004, 320:276-290.
60. Viklund H., Elofsson A. OCTOPUS: improving topology prediction by two-track ANN-based preference scores and an extended topological grammar. Bioinformatics 2008, 24:1662-1668.
61. Wallis J.W., Chrebet G., Brodsky G., Rolfe M., Rothstein R. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 1989, 58:409-419.
62. Weber-Lotfi F., Dietrich A., Russo M., Rubino L. Mitochondrial targeting and membrane anchoring of a viral replicase in plant and yeast cells. J. Virol. 2002, 76:10485-10496.
63. Winzeler E.A., Shoemaker D.D., Astromoff A., Liang H., Anderson K., Andre B., Bangham R., Benito R., Boeke J.D., Bussey H., Chu A.M., Connelly C., Davis K., Dietrich F., Dow S.W., El Bakkoury M., Foury F., Friend S.H., Gentalen E., Giaever G., Hegemann J.H., Jones T., Laub M., Liao H., Liebundguth N., Lockhart D.J., Lucau-Danila A., Lussier M., M'Rabet N., Menard P., Mittmann M., Pai C., Rebischung C., Revuelta J.L., Riles L., Roberts C.J., Ross-MacDonald P., Scherens B., Snyder M., Sookhai-Mahadeo S., Storms R.K., Véronneau S., Voet M., Volckaert G., Ward T.R., Wysocki R., Yen G.S., Yu K., Zimmermann K., Philippsen P., Johnston M., Davis R.W. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 1999, 285:901-906.
64. Yu C.S., Chen Y.C., Lu C.H., Hwang J.K. Prediction of protein subcellular localization. Proteins 2006, 64:643-651.
65. Yuan Z., Mattick J.S., Teasdale R.D. SVMtm: support vector machines to predict transmembrane segments. J. Comput. Chem. 2004, 25:632-636.
66. Zinser E., Paltauf F., Daum G. Sterol composition of yeast organelle membranes and subcellular distribution of enzymes involved in sterol metabolism. J. Bacteriol. 1993, 175:2853-2858.