Proteome-wide overexpression of host proteins for identification of factors affecting tombusvirus RNA replication: An inhibitory role of protein kinase C

Journal of Virology

Volumn 86, Issue 17, 2012, Pages 9384-9395

  Nawaz ul Rehman, Muhammad Shah ^a   Martinez Ochoa, Natalia ^a   Pascal, Helene ^a   Sasvari, Zsuzsanna ^a   Herbst, Christin ^a   Xu, Kai ^a   Baker, Jannine ^a   Sharma, Monika ^a   Herbst, Alan ^a   Nagy, Peter D ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CERCOSPORAMIDE; PROTEIN KINASE C; PROTEIN KINASE C1P; PROTEIN KINASE INHIBITOR; RIBOSOME RNA; UNCLASSIFIED DRUG; VESICULAR TRANSPORT PROTEIN; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GENE IDENTIFICATION; GENE OVEREXPRESSION; NICOTIANA BENTHAMIANA; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTOPLAST; RNA REPLICATION; SACCHAROMYCES CEREVISIAE; TOMBUSVIRUS; VIRUS CELL INTERACTION; VIRUS INHIBITION; VIRUS REPLICATION;

DOWN-REGULATION; HOST-PATHOGEN INTERACTIONS; PLANT DISEASES; PLANT PROTEINS; PROTEIN KINASE C; PROTEOME; RNA, VIRAL; SACCHAROMYCES CEREVISIAE PROTEINS; TOBACCO; TOMBUSVIRUS; VIRUS REPLICATION;

RNA VIRUSES; SACCHAROMYCES CEREVISIAE; TOMATO BUSHY STUNT VIRUS; TOMBUSVIRUS;

EID: 84866156147     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00019-12     Document Type: Article

References (88)

1. Alfonzo JD, Crother TR, Guetsova ML, Daignan-Fornier B, Taylor MW. 1999. APT1, but not APT2, codes for a functional adenine phosphoribosyltransferase in Saccharomyces cerevisiae. J. Bacteriol. 181:347-352.
2. Ali A, Sivakami S, Raghuram N. 2007. Regulation of activity and transcript levels of NR in rice (Oryza sativa): roles of protein kinase and Gproteins. Plant Science. 172:406-413.
3. Barajas D, Jiang Y, Nagy PD. 2009. A unique role for the host ESCRT proteins in replication of tomato bushy stunt virus. PLoS Pathog. 5: e1000705. doi:10.1371/journal.ppat.1000705.
4. Barajas D, Li Z, Nagy PD. 2009. The Nedd4-type Rsp5p ubiquitin ligase inhibits tombusvirus replication by regulating degradation of the p92 replication protein and decreasing the activity of the tombusvirus replicase. J. Virol. 83:11751-11764.
5. Barajas D, Nagy PD. 2010. Ubiquitination of tombusvirus p33 replication protein plays a role in virus replication and binding to the host Vps23p ESCRT protein. Virology. 397:358-368.
6. Cheng C-P, Panavas T, Luo G, Nagy PD. 2005. Heterologous RNA replication enhancer stimulates in vitro RNA synthesis and templateswitching by the carmovirus, but not by the tombusvirus, RNAdependent RNA polymerase: Implication for modular evolution of RNA viruses. Virology. 341:107-121.
7. Cherry S, et al. 2005. Genome-wide RNAi screen reveals a specific sensitivity of IRES-containing RNA viruses to host translation inhibition. Genes Dev. 19:445-452.
8. De BP, Gupta S, Banerjee AK. 1995. Cellular protein kinase C isoform zeta regulates human parainfluenza virus type 3 replication. Proc. Natl. Acad. Sci. U. S. A. 92:5204-5208.
9. den Boon JA, Diaz A, Ahlquist P. 2010. Cytoplasmic viral replication complexes. Cell Host Microbe. 8:77-85.
10. Gancarz BL, Hao L, He Q, Newton MA, Ahlquist P. 2011. Systematic identification of novel, essential host genes affecting bromovirus RNA replication. PLoS One 6:e23988. doi:10.1371/journal.pone.0023988.
11. Gelperin DM, et al. 2005. Biochemical and genetic analysis of the yeast proteome with a movable ORF collection. Genes Dev. 19:2816-2826.
12. Gietz RD, Woods RA. 2002. Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol. 350:87-96.
13. Huang TS, Nagy PD. 2011. Direct inhibition of tombusvirus plus-strand RNA synthesis by a dominant negative mutant of a host metabolic enzyme, glyceraldehyde-3-phosphate dehydrogenase, in yeast and plants. J. Virol. 85:9090-9102.
14. Huntley CC, De BP, Banerjee AK. 1997. Phosphorylation of Sendai virus phosphoprotein by cellular protein kinase C zeta. J. Biol. Chem. 272:16578-16584.
15. Huntley CC, De BP, Murray NR, Fields AP, Banerjee AK. 1995. Human parainfluenza virus type 3 phosphoprotein: identification of serine 333 as the major site for PKC zeta phosphorylation. Virology. 211:561-567.
16. Jaag HM, Nagy PD. 2010. The combined effect of environmental and host factors on the emergence of viral RNA recombinants. PLoS Pathog. 6:e1001156. doi:10.1371/journal.ppat.1001156.
17. Jaag HM, Pogany J, Nagy PD. 2010. A host Ca2+/Mn2+ ion pump is a factor in the emergence of viral RNA recombinants. Cell Host Microbe. 7:74-81.
18. Jiang Y, Li Z, Nagy PD. 2010. Nucleolin/Nsr1p binds to the 3= noncoding region of the tombusvirus RNA and inhibits replication. Virology. 396:10-20.
19. Jiang Y, Serviene E, Gal J, Panavas T, Nagy PD. 2006. Identification of essential host factors affecting tombusvirus RNA replication based on the yeast Tet promoters Hughes Collection. J. Virol. 80:7394-7404.
20. Kasparovsky T, Blein JP, Mikes V. 2004. Ergosterol elicits oxidative burst in tobacco cells via phospholipase A(2) and protein kinase C signal pathway. Plant Physiol. Biochem. 42:429-435.
21. Konicek BW, et al. 2011. Therapeutic inhibition of MAP kinase interacting kinase blocks eukaryotic initiation factor 4E phosphorylation and suppresses outgrowth of experimental lung metastases. Cancer Res. 71:1849-1857.
22. Kovalev N, Pogany J, Nagy PD. 2012. A co-opted DEAD-box RNA helicase enhances tombusvirus plus-strand synthesis. PLoS Pathog. 8:e1002537. doi:10.1371/journal.ppat.1002537.
23. Kushner DB, et al. 2003. Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc. Natl. Acad. Sci. U. S. A. 100:15764-15769.
24. Li Q, et al. 2009. A genome-wide genetic screen for host factors required for hepatitis C virus propagation. Proc. Natl. Acad. Sci. U. S. A. 106:16410-16415.
25. Li Z, Barajas D, Panavas T, Herbst DA, Nagy PD. 2008. Cdc34p ubiquitin-conjugating enzyme is a component of the tombusvirus replicase complex and ubiquitinates p33 replication protein. J. Virol. 82:6911-6926.
26. Li Z, Nagy PD. 2011. Diverse roles of host RNA binding proteins in RNA virus replication. RNA Biol. 8:305-315.
27. Li Z, et al. 2009. Translation elongation factor 1A is a component of the tombusvirus replicase complex and affects the stability of the p33 replication co-factor. Virology. 385:245-260.
28. Li Z, et al. 2010. Translation elongation factor 1A facilitates the assembly of the tombusvirus replicase and stimulates minus-strand synthesis. PLoS Pathog. 6:e1001175. doi:10.1371/journal.ppat.1001175.
29. Li Z, et al. 2011. Systematic exploration of essential yeast gene function with temperature-sensitive mutants. Nat. Biotechnol. 29:361-367.
30. Lin JY, Mendu V, Pogany J, Qin J, Nagy PD. 2012. The TPR domain in the host Cyp40-like cyclophilin binds to the viral replication protein and inhibits the assembly of the tombusviral replicase. PLoS Pathog. 8:e1002491. doi:10.1371/journal.ppat.1002491.
31. McCartney AW, Greenwood JS, Fabian MR, White KA, Mullen RT. 2005. Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway. Plant Cell. 17:3513-3531.
32. Mendu V, Chiu M, Barajas D, Li Z, Nagy PD. 2010. Cpr1 cyclophilin and Ess1 parvulin prolyl isomerases interact with the tombusvirus replication protein and inhibit viral replication in yeast model host. Virology. 406:342-351.
33. Miller S, Krijnse-Locker J. 2008. Modification of intracellular membrane structures for virus replication. Nat. Rev. Microbiol. 6:363-374.
34. Monkewich S, et al. 2005. The p92 polymerase coding region contains an internal RNA element required at an early step in Tombusvirus genome replication. J. Virol. 79:4848-4858.
35. Moser TS, Jones RG, Thompson CB, Coyne CB, Cherry S. 2010. A kinome RNAi screen identified AMPK as promoting poxvirus entry through the control of actin dynamics. PLoS Pathog. 6:e1000954. doi: 10.1371/journal.ppat.1000954.
36. Munnik T, Testerink C. 2009. Plant phospholipid signaling: "in a nutshell." J. Lipid Res. 50: S260-S265.
37. Nagy PD. 2011. The roles of host factors in tombusvirus RNA recombination. Adv. Virus Res. 81:63-84.
38. Nagy PD. 2008. Yeast as a model host to explore plant virus-host interactions. Annu. Rev. Phytopathol. 46:217-242.
39. Nagy PD, Pogany J. 2012. The dependence of viral RNA replication on co-opted host factors. Nat. Rev. Microbiol. 10:137-149.
40. Nagy PD, Pogany J. 2010. Global genomics and proteomics approaches to identify host factors as targets to induce resistance against tomato bushy stunt virus. Adv. Virus Res. 76:123-177.
41. Nagy PD, Pogany J. 2008. Multiple roles of viral replication proteins in plant RNA virus replication. Methods Mol. Biol. 451:55-68.
42. Nagy PD, Wang RY, Pogany J, Hafren A, Makinen K. 2011. Emerging picture of host chaperone and cyclophilin roles in RNA virus replication. Virology. 411:374-382.
43. Navarro B, Rubino L, Russo M. 2004. Expression of the Cymbidium ringspot virus 33-kilodalton protein in Saccharomyces cerevisiae and molecular dissection of the peroxisomal targeting signal. J. Virol. 78:4744-4752.
44. Ng TI, et al. 2007. Identification of host genes involved in hepatitis C virus replication by small interfering RNA technology. Hepatology. 45:1413-1421.
45. Novoa RR, et al. 2005. Virus factories: associations of cell organelles for viral replication and morphogenesis. Biol. Cell. 97:147-172.
46. Panavas T, Hawkins CM, Panaviene Z, Nagy PD. 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.
47. Panavas T, Nagy PD. 2003. Yeast as a model host to study replication and recombination of defective interfering RNA of Tomato bushy stunt virus. Virology. 314:315-325.
48. Panavas T, Serviene E, Brasher J, Nagy PD. 2005. Yeast genome-wide screen reveals dissimilar sets of host genes affecting replication of RNA viruses. Proc. Natl. Acad. Sci. U. S. A. 102:7326-7331.
49. Panaviene Z, Baker JM, Nagy PD. 2003. The overlapping RNA-binding domains of p33 and p92 replicase proteins are essential for tombusvirus replication. Virology. 308:191-205.
50. Panaviene Z, Panavas T, Serva S, Nagy PD. 2004. Purification of the cucumber necrosis virus replicase from yeast cells: role of coexpressed viral RNA in stimulation of replicase activity. J. Virol. 78:8254-8263.
51. Pathak KB, Pogany J, Xu K, White KA, Nagy PD. 2012. Defining the roles of cis-acting RNA elements in tombusvirus replicase assembly in vitro. J. Virol. 86:156-171.
52. Pathak KB, Sasvari Z, Nagy PD. 2008. The host Pex19p plays a role in peroxisomal localization of tombusvirus replication proteins. Virology. 379:294-305.
53. Pogany J, Nagy PD. 2008. Authentic replication and recombination of Tomato bushy stunt virus RNA in a cell-free extract from yeast. J. Virol. 82:5967-5980.
54. Pogany J, Panavas T, Serviene E, Nawaz-Ul-Rehman MS, and, DNP. 2010. A high-throughput approach for studying virus replication in yeast. Curr. Protoc. Microbiol. 19: 16J.1.1-16J.1.15.
55. Pogany J, Stork J, Li Z, Nagy PD. 2008. In vitro assembly of the Tomato bushy stunt virus replicase requires the host Heat shock protein 70. Proc. Natl. Acad. Sci. U. S. A. 105:19956-19961.
56. Pogany J, White KA, Nagy PD. 2005. Specific binding of tombusvirus replication protein p33 to an internal replication element in the viral RNA is essential for replication. J. Virol. 79:4859-4869.
57. Qatsha KA, Rudolph C, Marme D, Schachtele C, May WS. 1993. Go 6976, a selective inhibitor of protein kinase C, is a potent antagonist of human immunodeficiency virus 1 induction from latent/low-levelproducing reservoir cells in vitro. Proc. Natl. Acad. Sci. U. S. A. 90:4674-4678.
58. Qin J, Barajas D, Nagy PD. 2012. An inhibitory function ofWWdomaincontaining host proteins in RNA virus replication. Virology. 426:106-119.
59. Rajendran KS, Nagy PD. 2003. Characterization of the RNA-binding domains in the replicase proteins of tomato bushy stunt virus. J. Virol. 77:9244-9258.
60. Rajendran KS, Nagy PD. 2004. Interaction between the replicase proteins of Tomato bushy stunt virus in vitro and in vivo. Virology. 326:250-261.
61. Rajendran KS, Nagy PD. 2006. Kinetics and functional studies on interaction between the replicase proteins of Tomato Bushy Stunt Virus: Requirement of p33:p92 interaction for replicase assembly. Virology. 345:270-279.
62. Randall G, et al. 2007. Cellular cofactors affecting hepatitis C virus infection and replication. Proc. Natl. Acad. Sci. U. S. A. 104:12884-12889.
63. Reich NC, Pfeffer LM. 1990. Evidence for involvement of protein kinase Cin the cellular response to interferon alpha. Proc. Natl. Acad. Sci. U. S. A. 87:8761-8765.
64. Salonen A, Ahola T, Kaariainen L. 2005. Viral RNA replication in association with cellular membranes. Curr. Top. Microbiol. Immunol. 285:139-173.
65. Sasvari Z, Izotova L, Kinzy TG, Nagy PD. 2011. Synergistic roles of eukaryotic translation elongation factors 1Bgamma and 1A in stimulation of tombusvirus minus-strand synthesis. PLoS Pathog. 7:e1002438. doi: 10.1371/journal.ppat.1002438.
66. Schmitz HP, Heinisch JJ. 2003. Evolution, biochemistry and genetics of protein kinase C in fungi. Curr. Genet. 43:245-254.
67. Serva S, Nagy PD. 2006. Proteomics analysis of the tombusvirus replicase: Hsp70 molecular chaperone is associated with the replicase and enhances viral RNA replication. J. Virol. 80:2162-2169.
68. Serviene E, Jiang Y, Cheng CP, Baker J, Nagy PD. 2006. Screening of the yeast yTHC collection identifies essential host factors affecting tombusvirus RNA recombination. J. Virol. 80:1231-1241.
69. Serviene E, et al. 2005. Genome-wide screen identifies host genes affecting viral RNA recombination. Proc. Natl. Acad. Sci. U. S. A. 102:10545-10550.
70. Sessions OM, et al. 2009. Discovery of insect and human dengue virus host factors. Nature. 458:1047-1050.
71. Shapka N, Stork J, Nagy PD. 2005. Phosphorylation of the p33 replication protein of Cucumber necrosis tombusvirus adjacent to the RNA binding site affects viral RNA replication. Virology. 343:65-78.
72. Sopko R, et al. 2006. Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell. 21:319-330.
73. Stork J, Kovalev N, Sasvari Z, Nagy PD. 2011. RNA chaperone activity of the tombusviral p33 replication protein facilitates initiation of RNA synthesis by the viral RdRp in vitro. Virology. 409:338-347.
74. Stork J, Panaviene Z, Nagy PD. 2005. Inhibition of in vitro RNA binding and replicase activity by phosphorylation of the p33 replication protein of Cucumber necrosis tombusvirus. Virology. 343:79-92.
75. Subramaniam R, Despres C, Brisson N. 1997. A functional homolog of mammalian protein kinase C participates in the elicitor-induced defense response in potato. Plant Cell. 9:653-664.
76. Supekova L, et al. 2008. Identification of human kinases involved in hepatitisCvirus replication by small interferenceRNAlibrary screening. J. Biol. Chem. 283:29-36.
77. Sussman A, et al. 2004. Discovery of cercosporamide, a known antifungal natural product, as a selective Pkc1 kinase inhibitor through highthroughput screening. Eukaryot. Cell. 3:932-943.
78. Tai AW, et al. 2009. A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host Microbe. 5:298-307.
79. Vaillancourt FH, et al. 2009. Identification of a lipid kinase as a host factor involved in hepatitis C virus RNA replication. Virology. 387:5-10.
80. Vasconsuelo A, Boland R. 2007. Molecular aspects of the early stages of elicitation of secondary metabolites in plants. Plant Science. 172:861-875.
81. Vasconsuelo A, Giuletti AM, Picotto G, Rodriguez-Talou J, Boland R. 2003. Involvement of the PLC/PKC pathway in Chitosan-induced anthraquinone production by Rubia tinctorum L. cell cultures. Plant Science. 165:429-436.
82. Vasconsuelo A, Giulietti AM, Boland R. 2004. Signal transduction events mediating chitosan stimulation of anthraquinone synthesis in Rubia tinctorum. Plant Science. 166:405-413.
83. Vasconsuelo A, Morelli S, Picotto G, Giulietti AM, Boland R. 2005. Intracellular calcium mobilization: a key step for chitosan-induced anthraquinone production in Rubia tinctorum L. Plant Science. 169:712-720.
84. Wang RY, Nagy PD. 2008. Tomato bushy stunt virus co-opts the RNAbinding function of a host metabolic enzyme for viral genomic RNA synthesis. Cell Host Microbe. 3:178-187.
85. Wang RY, Stork J, Nagy PD. 2009. A key role for heat shock protein 70 in the localization and insertion of tombusvirus replication proteins to intracellular membranes. J. Virol. 83:3276-3287.
86. Wang RY, Stork J, Pogany J, Nagy PD. 2009. A temperature sensitive mutant of heat shock protein 70 reveals an essential role during the early steps of tombusvirus replication. Virology. 394:28-38.
87. White KA, Nagy PD. 2004. Advances in the molecular biology of tombusviruses: gene expression, genome replication, and recombination. Prog. Nucleic Acids Res. Mol. Biol. 78:187-226.
88. Wu B, et al. 2009. A discontinuous RNA platform mediates RNA virus replication: building an integrated model for RNA-based regulation of viral processes. PLoS Pathog. 5:e1000323. doi:10.1371/journal. ppat.1000323.