The TPR domain in the host Cyp40-like cyclophilin binds to the viral replication protein and inhibits the assembly of the tombusviral replicase

PLoS Pathogens

Volumn 8, Issue 2, 2012, Pages

  Lin, Jing Yi ^a   Mendu, Venugopal ^a   Pogany, Judit ^a   Qin, Jun ^a,b   Nagy, Peter D ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b NORTHWEST A F UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CPR7P PROTEIN; CYCLOPHILIN; CYP40 PROTEIN; RNA DIRECTED RNA POLYMERASE; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; IN VITRO STUDY; INSECT VIRUS; NODAMURA VIRUS; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; RNA STRUCTURE; RNA SYNTHESIS; TETRATRICOPEPTIDE REPEAT; TOMBUSVIRUS; VIRUS REPLICATION;

ARABIDOPSIS; CYCLOPHILINS; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MUTATION; PEPTIDYLPROLYL ISOMERASE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RNA REPLICASE; RNA, VIRAL; SACCHAROMYCES CEREVISIAE; TOMBUSVIRUS; VIRAL PROTEINS; VIRUS ASSEMBLY; VIRUS REPLICATION;

HEXAPODA; LYCOPERSICON ESCULENTUM; NODAMURA VIRUS; RNA VIRUSES; TOMATO BUSHY STUNT VIRUS; TOMBUSVIRUS;

EID: 84860913468     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002491     Document Type: Article

References (82)

1. Nagy PD, (2008) Yeast as a model host to explore plant virus-host interactions. Annu Rev Phytopathol 46: 217-242.
2. Nagy PD, Pogany J, (2008) Multiple roles of viral replication proteins in plant RNA virus replication. Methods Mol Biol 451: 55-68.
3. 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.
4. Li Z, Nagy PD, (2011) Diverse roles of host RNA binding proteins in RNA virus replication. RNA Biol 8: 305-315.
5. den Boon JA, Diaz A, Ahlquist P, (2010) Cytoplasmic viral replication complexes. Cell Host Microbe 8: 77-85.
6. Salonen A, Ahola T, Kaariainen L, (2005) Viral RNA replication in association with cellular membranes. Curr Top Microbiol Immunol 285: 139-173.
7. Miller S, Krijnse-Locker J, (2008) Modification of intracellular membrane structures for virus replication. Nat Rev Microbiol 6: 363-374.
8. Fernandez-Garcia MD, Mazzon M, Jacobs M, Amara A, (2009) Pathogenesis of flavivirus infections: using and abusing the host cell. Cell Host Microbe 5: 318-328.
9. 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.
10. Cherry S, Doukas T, Armknecht S, Whelan S, Wang H, 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.
11. 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.
12. Kushner DB, Lindenbach BD, Grdzelishvili VZ, Noueiry AO, Paul SM, 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.
13. Krishnan MN, Ng A, Sukumaran B, Gilfoy FD, Uchil PD, et al. (2008) RNA interference screen for human genes associated with West Nile virus infection. Nature 455: 242-245.
14. Li Q, Brass AL, Ng A, Hu Z, Xavier RJ, 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.
15. Randall G, Panis M, Cooper JD, Tellinghuisen TL, Sukhodolets KE, et al. (2007) Cellular cofactors affecting hepatitis C virus infection and replication. Proc Natl Acad Sci U S A 104: 12884-12889.
16. Sessions OM, Barrows NJ, Souza-Neto JA, Robinson TJ, Hershey CL, et al. (2009) Discovery of insect and human dengue virus host factors. Nature 458: 1047-1050.
17. Tai AW, Benita Y, Peng LF, Kim SS, Sakamoto N, et al. (2009) A functional genomic screen identifies cellular cofactors of hepatitis C virus replication. Cell Host Microbe 5: 298-307.
18. Nagy PD, Pogany J, (2006) Yeast as a model host to dissect functions of viral and host factors in tombusvirus replication. Virology 344: 211-220.
19. White KA, Nagy PD, (2004) Advances in the molecular biology of tombusviruses: gene expression, genome replication, and recombination. Prog Nucleic Acid Res Mol Biol 78: 187-226.
20. 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.
21. 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.
22. Serviene E, Shapka N, Cheng CP, Panavas T, Phuangrat B, et al. (2005) Genome-wide screen identifies host genes affecting viral RNA recombination. Proc Natl Acad Sci U S A 102: 10545-10550.
23. 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.
24. Li Z, Pogany J, Panavas T, Xu K, Esposito AM, 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.
25. 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.
26. 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.
27. Wang RY, Nagy PD, (2008) Tomato bushy stunt virus Co-Opts the RNA-Binding Function of a Host Metabolic Enzyme for Viral Genomic RNA Synthesis. Cell Host Microbe 3: 178-187.
28. Huang TS, Nagy PD, (2011) Direct inhibition of tombusvirus plus-strand RNA synthesis by a dominant-negative mutant of a host metabolic enzyme, GAPDH, in yeast and plants. J Virol 85: 9090-9102.
29. Li Z, Pogany J, Tupman S, Esposito AM, Kinzy TG, et al. (2010) Translation Elongation Factor 1A Facilitates the Assembly of the Tombusvirus Replicase and Stimulates Minus-Strand Synthesis. PLoS Pathog 6: e1001175.
30. 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.
31. 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.
32. Jonczyk M, Pathak KB, Sharma M, Nagy PD, (2007) Exploiting alternative subcellular location for replication: tombusvirus replication switches to the endoplasmic reticulum in the absence of peroxisomes. Virology 362: 320-330.
33. 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.
34. 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.
35. 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.
36. Panaviene Z, Panavas T, Nagy PD, (2005) Role of an internal and two 3′-terminal RNA elements in assembly of tombusvirus replicase. J Virol 79: 10608-10618.
37. 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.
38. 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.
39. 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.
40. Wang P, Heitman J, (2005) The cyclophilins. Genome Biol 6: 226.
41. Arevalo-Rodriguez M, Wu X, Hanes SD, Heitman J, (2004) Prolyl isomerases in yeast. Front Biosci 9: 2420-2446.
42. Lee J, Kim SS, (2010) Current implications of cyclophilins in human cancers. J Exp Clin Cancer Res 29: 97.
43. Galat A, Bua J, (2010) Molecular aspects of cyclophilins mediating therapeutic actions of their ligands. Cell Mol Life Sci 67: 3467-3488.
44. Monkewich S, Lin HX, Fabian MR, Xu W, Na H, 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.
45. Panavas T, Pogany J, Nagy PD, (2002) Internal initiation by the cucumber necrosis virus RNA-dependent RNA polymerase is facilitated by promoter-like sequences. Virology 296: 275-287.
46. Cheng CP, Pogany J, Nagy PD, (2002) Mechanism of DI RNA formation in tombusviruses: dissecting the requirement for primer extension by the tombusvirus RNA dependent RNA polymerase in vitro. Virology 304: 460-473.
47. Nagy PD, Pogany J, (2000) Partial purification and characterization of Cucumber necrosis virus and Tomato bushy stunt virus RNA-dependent RNA polymerases: similarities and differences in template usage between tombusvirus and carmovirus RNA-dependent RNA polymerases. Virology 276: 279-288.
48. Pogany J, Panavas T, Serviene E, Nawaz-Ul-Rehman MS, P DN, (2010) A high-throughput approach for studying virus replication in yeast. Curr Protoc Microbiol Chapter 16: Unit16J 11.
49. 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.
50. Jaag HM, Nagy PD, (2010) The combined effect of environmental and host factors on the emergence of viral RNA recombinants. PLoS Pathog 6: e1001156.
51. Galat A, (2004) Function-dependent clustering of orthologues and paralogues of cyclophilins. Proteins 56: 808-820.
52. Weeks SA, Shield WP, Sahi C, Craig EA, Rospert S, et al. (2010) A targeted analysis of cellular chaperones reveals contrasting roles for heat shock protein 70 in flock house virus RNA replication. J Virol 84: 330-339.
53. Smith MR, Willmann MR, Wu G, Berardini TZ, Moller B, et al. (2009) Cyclophilin 40 is required for microRNA activity in Arabidopsis. Proc Natl Acad Sci U S A 106: 5424-5429.
54. 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.
55. 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.
56. Mayr C, Richter K, Lilie H, Buchner J, (2000) Cpr6 and Cpr7, two closely related Hsp90-associated immunophilins from Saccharomyces cerevisiae, differ in their functional properties. J Biol Chem 275: 34140-34146.
57. Duina AA, Chang HC, Marsh JA, Lindquist S, Gaber RF, (1996) A cyclophilin function in Hsp90-dependent signal transduction. Science 274: 1713-1715.
58. Duina AA, Marsh JA, Kurtz RB, Chang HC, Lindquist S, et al. (1998) The peptidyl-prolyl isomerase domain of the CyP-40 cyclophilin homolog Cpr7 is not required to support growth or glucocorticoid receptor activity in Saccharomyces cerevisiae. J Biol Chem 273: 10819-10822.
59. Liu X, Sun L, Yu M, Wang Z, Xu C, et al. (2009) Cyclophilin A interacts with influenza A virus M1 protein and impairs the early stage of the viral replication. Cell Microbiol 11: 760-741.
60. Sokolskaja E, Luban J, (2006) Cyclophilin, TRIM5, and innate immunity to HIV-1. Curr Opin Microbiol 9: 404-408.
61. Strebel K, Luban J, Jeang KT, (2009) Human cellular restriction factors that target HIV-1 replication. BMC Med 7: 48.
62. Berthoux L, Sebastian S, Sokolskaja E, Luban J, (2005) Cyclophilin A is required for TRIM5{alpha}-mediated resistance to HIV-1 in Old World monkey cells. Proc Natl Acad Sci U S A 102: 14849-14853.
63. Brennan G, Kozyrev Y, Hu SL, (2008) TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc Natl Acad Sci U S A 105: 3569-3574.
64. Franke EK, Yuan HE, Luban J, (1994) Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372: 359-362.
65. Luban J, Bossolt KL, Franke EK, Kalpana GV, Goff SP, (1993) Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 73: 1067-1078.
66. Takeuchi H, Buckler-White A, Goila-Gaur R, Miyagi E, Khan MA, et al. (2007) Vif counteracts a cyclophilin A-imposed inhibition of simian immunodeficiency viruses in human cells. J Virol 81: 8080-8090.
67. Krishnan MN, Ng A, Sukumaran B, Gilfoy FD, Uchil PD, et al. (2008) RNA interference screen for human genes associated with West Nile virus infection. Nature 455: 242-245.
68. Nakagawa M, Sakamoto N, Enomoto N, Tanabe Y, Kanazawa N, et al. (2004) Specific inhibition of hepatitis C virus replication by cyclosporin A. Biochem Biophys Res Commun 313: 42-47.
69. Watashi K, Hijikata M, Hosaka M, Yamaji M, Shimotohno K, (2003) Cyclosporin A suppresses replication of hepatitis C virus genome in cultured hepatocytes. Hepatology 38: 1282-1288.
70. Kaul A, Stauffer S, Berger C, Pertel T, Schmitt J, et al. (2009) Essential role of cyclophilin A for hepatitis C virus replication and virus production and possible link to polyprotein cleavage kinetics. PLoS Pathog 5: e1000546.
71. Coelmont L, Hanoulle X, Chatterji U, Berger C, Snoeck J, et al. (2010) DEB025 (Alisporivir) inhibits hepatitis C virus replication by preventing a cyclophilin A induced cis-trans isomerisation in domain II of NS5A. PLoS One 5: e13687.
72. Yang F, Robotham JM, Grise H, Frausto S, Madan V, et al. (2010) A major determinant of cyclophilin dependence and cyclosporine susceptibility of hepatitis C virus identified by a genetic approach. PLoS Pathog 6: e1001118.
73. Qing M, Yang F, Zhang B, Zou G, Robida JM, et al. (2009) Cyclosporine inhibits flavivirus replication through blocking the interaction between host cyclophilins and viral NS5 protein. Antimicrob Agents Chemother 53: 3226-3235.
74. Okamoto T, Nishimura Y, Ichimura T, Suzuki K, Miyamura T, et al. (2006) Hepatitis C virus RNA replication is regulated by FKBP8 and Hsp90. Embo J 25: 5015-5025.
75. Wang J, Tong W, Zhang X, Chen L, Yi Z, et al. (2006) Hepatitis C virus non-structural protein NS5A interacts with FKBP38 and inhibits apoptosis in Huh7 hepatoma cells. FEBS Lett 580: 4392-4400.
76. Dolinski K, Muir S, Cardenas M, Heitman J, (1997) All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable for viability in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 94: 13093-13098.
77. Janke C, Magiera MM, Rathfelder N, Taxis C, Reber S, et al. (2004) A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21: 947-962.
78. Jaag HM, Stork J, Nagy PD, (2007) Host transcription factor Rpb11p affects tombusvirus replication and recombination via regulating the accumulation of viral replication proteins. Virology 368: 388-404.
79. 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.
80. 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.
81. Cheng CP, Panavas T, Luo G, Nagy PD, (2005) Heterologous RNA replication enhancer stimulates in vitro RNA synthesis and template-switching by the carmovirus, but not by the tombusvirus, RNA-dependent RNA polymerase: implication for modular evolution of RNA viruses. Virology 341: 107-121.
82. Rajendran KS, Pogany J, Nagy PD, (2002) Comparison of turnip crinkle virus RNA-dependent RNA polymerase preparations expressed in Escherichia coli or derived from infected plants. J Virol 76: 1707-1717.