The combined effect of environmental and host factors on the emergence of Viral RNA recombinants

PLoS Pathogens

Volumn 6, Issue 10, 2010, Pages

  Jaag, Hannah M ^a   Nagy, Peter D ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOTIDASE; RIBONUCLEASE; VIRUS RNA; BISPHOSPHOADENYLATE 3' NUCLEOTIDASE; BISPHOSPHOADENYLATE 3'-NUCLEOTIDASE; INORGANIC SALT; RNA; RNA, RECOMBINANT;

ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; ENZYME INHIBITION; GENE DELETION; HOST RESISTANCE; NONHUMAN; PLANT VIRUS; TOMATO BUSHY STUNT VIRUS; VIRUS REPLICATION; BIOLOGICAL MODEL; DRUG EFFECT; ENVIRONMENT; GENETIC RECOMBINATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MOLECULAR EVOLUTION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; RNA SPLICING; SACCHAROMYCES CEREVISIAE; TOBACCO; TOMBUSVIRUS; TRANSGENIC ORGANISM; VIROLOGY;

TOMATO BUSHY STUNT VIRUS;

ENVIRONMENT; EVOLUTION, MOLECULAR; HOST-PATHOGEN INTERACTIONS; MODELS, BIOLOGICAL; NUCLEOTIDASES; ORGANISMS, GENETICALLY MODIFIED; RECOMBINATION, GENETIC; RNA; RNA SPLICING; RNA, VIRAL; SACCHAROMYCES CEREVISIAE; SALTS; STRESS, PHYSIOLOGICAL; TOBACCO; TOMBUSVIRUS; VIRUS REPLICATION;

EID: 78449245042     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001156     Document Type: Article

References (57)

1. Drake JW, Holland JJ (1999) Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96: 13910-13913.
2. Domingo E, Escarmis C, Sevilla N, Moya A, Elena SF, et al. (1996) Basic concepts in RNA virus evolution. FASEB J 10: 859-864.
3. Roossinck MJ (2003) Plant RNA virus evolution. Curr Opin Microbiol 6: 406-409.
4. Crotty S, Cameron CE, Andino R (2001) RNA virus error catastrophe: direct molecular test by using ribavirin. Proc Natl Acad Sci U S A 98: 6895-6900.
5. Aaziz R, Tepfer M (1999) Recombination in RNA viruses and in virus-resistant transgenic plants. J Gen Virol 80 (Pt 6): 1339-1346.
6. Worobey M, Holmes EC (1999) Evolutionary aspects of recombination in RNA viruses. J Gen Virol 80 (Pt 10): 2535-2543.
7. Bujarski JJ, Nagy PD, Flasinski S (1994) Molecular studies of genetic RNA-RNA recombination in brome mosaic virus. Adv Virus Res 43: 275-302.
8. Fernandez-Cuartero B, Burgyan J, Aranda MA, Salanki K, Moriones E, et al. (1994) Increase in the relative fitness of a plant virus RNA associated with its recombinant nature. Virology 203: 373-377.
9. Rao AL, Hall TC (1993) Recombination and polymerase error facilitate restoration of infectivity in brome mosaic virus. J Virol 67: 969-979.
10. Hema M, Gopinath K, Kao C (2005) Repair of the tRNA-like CCA sequence in a multipartite positive-strand RNA virus. J Virol 79: 1417-1427.
11. Guan H, Simon AE (2000) Polymerization of nontemplate bases before transcription initiation at the 39 ends of templates by an RNA-dependent RNA polymerase: an activity involved in 39 end repair of viral RNAs. Proc Natl Acad Sci U S A 97: 12451-12456.
12. Nagy PD, Carpenter CD, Simon AE (1997) A novel 39-end repair mechanism in an RNA virus. Proc Natl Acad Sci U S A 94: 1113-1118.
13. Roossinck MJ (1997) Mechanisms of plant virus evolution. Annu Rev Phytopathol 35: 191-209.
14. Nagy PD, Simon AE (1997) New insights into the mechanisms of RNA recombination. Virology 235: 1-9.
15. 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.
16. Cheng CP, Nagy PD (2003) Mechanism of RNA recombination in carmo- and tombusviruses: evidence for template switching by the RNA-dependent RNA polymerase in vitro. J Virol 77: 12033-12047.
17. Kim MJ, Kao C (2001) Factors regulating template switch in vitro by viral RNAdependent RNA polymerases: implications for RNA-RNA recombination. Proc Natl Acad Sci U S A 98: 4972-4977.
18. Arnold JJ, Cameron CE (1999) Poliovirus RNA-dependent RNA polymerase (3Dpol) is sufficient for template switching in vitro. J Biol Chem 274: 2706-2716.
19. Tang RS, Barton DJ, Flanegan JB, Kirkegaard K (1997) Poliovirus RNA recombination in cell-free extracts. RNA 3: 624-633.
20. Jarvis TC, Kirkegaard K (1992) Poliovirus RNA recombination: mechanistic studies in the absence of selection. EMBO J 11: 3135-3145.
21. Figlerowicz M, Nagy PD, Tang N, Kao CC, Bujarski JJ (1998) Mutations in the N terminus of the brome mosaic virus polymerase affect genetic RNA-RNA recombination. J Virol 72: 9192-9200.
22. Nagy PD, Dzianott A, Ahlquist P, Bujarski JJ (1995) Mutations in the helicaselike domain of protein 1a alter the sites of RNA-RNA recombination in brome mosaic virus. J Virol 69: 2547-2556.
23. Nagy PD, Bujarski JJ (1998) Silencing homologous RNA recombination hot spots with GC-rich sequences in brome mosaic virus. J Virol 72: 1122-1130.
24. Nagy PD, Bujarski JJ (1997) Engineering of homologous recombination hotspots with AU-rich sequences in brome mosaic virus. J Virol 71: 3799-3810.
25. Nagy PD, Bujarski JJ (1993) Targeting the site of RNA-RNA recombination in brome mosaic virus with antisense sequences. Proc Natl Acad Sci U S A 90: 6390-6394.
26. Nagy PD, Zhang C, Simon AE (1998) Dissecting RNA recombination in vitro: role of RNA sequences and the viral replicase. Embo J 17: 2392-2403.
27. 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.
28. 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.
29. 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.
30. 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.
31. 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.
32. Jaag HM, Nagy PD (2009) Silencing of Nicotiana benthamiana Xrn4p exoribonuclease promotes tombusvirus RNA accumulation and recombination. Virology 386: 344-352.
33. Cheng CP, Jaag HM, Jonczyk M, Serviene E, Nagy PD (2007) Expression of the Arabidopsis Xrn4p 59-39 exoribonuclease facilitates degradation of tombusvirus RNA and promotes rapid emergence of viral variants in plants. Virology 368: 238-248.
34. Cheng CP, Serviene E, Nagy PD (2006) Suppression of viral RNA recombination by a host exoribonuclease. J Virol 80: 2631-2640.
35. Sun Q, Choi GH, Nuss DL (2009) A single Argonaute gene is required for induction of RNA silencing antiviral defense and promotes viral RNA recombination. Proc Natl Acad Sci U S A 106: 17927-17932.
36. Zhang X, Nuss DL (2008) A host dicer is required for defective viral RNA production and recombinant virus vector RNA instability for a positive sense RNA virus. Proc Natl Acad Sci U S A 105: 16749-16754.
37. Dichtl B, Stevens A, Tollervey D (1997) Lithium toxicity in yeast is due to the inhibition of RNA processing enzymes. EMBO J 16: 7184-7195.
38. Albert A, Yenush L, Gil-Mascarell MR, Rodriguez PL, Patel S, et al. (2000) Xray structure of yeast Hal2p, a major target of lithium and sodium toxicity, and identification of framework interactions determining cation sensitivity. J Mol Biol 295: 927-938.
39. Chernyakov I, Whipple JM, Kotelawala L, Grayhack EJ, Phizicky EM (2008) Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 59-39 exonucleases Rat1 and Xrn1. Genes Dev 22: 1369-1380.
40. Spiegelberg BD, Xiong JP, Smith JJ, Gu RF, York JD (1999) Cloning and characterization of a mammalian lithium-sensitive bisphosphate 39-nucleotidase inhibited by inositol 1,4-bisphosphate. J Biol Chem 274: 13619-13628.
41. Spiegelberg BD, Dela Cruz J, Law TH, York JD (2005) Alteration of lithium pharmacology through manipulation of phosphoadenosine phosphate metabolism. J Biol Chem 280: 5400-5405.
42. 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.
43. 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.
44. 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.
45. Todeschini AL, Condon C, Benard L (2006) Sodium-induced GCN4 expression controls the accumulation of the 59 to 39 RNA degradation inhibitor, 39- phosphoadenosine 59-phosphate. J Biol Chem 281: 3276-3282.
46. 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.
47. 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.
48. Gil-Mascarell R, Lopez-Coronado JM, Belles JM, Serrano R, Rodriguez PL (1999) The Arabidopsis HAL2-like gene family includes a novel sodium-sensitive phosphatase. Plant J 17: 373-383.
49. Rodriguez VM, Chetelat A, Majcherczyk P, Farmer EE (2010) Chloroplastic phosphoadenosine phosphosulfate metabolism regulates Basal levels of the prohormone jasmonic Acid in Arabidopsis leaves. Plant Physiol 152: 1335-1345.
50. Kim BH, von Arnim AG (2009) FIERY1 regulates light-mediated repression of cell elongation and flowering time via its 39(29),59-bisphosphate nucleotidase activity. Plant J 58: 208-219.
51. Nagy PD (2008) Yeast as a model host to explore plant virus-host interactions. Annu Rev Phytopathol 46: 217-242.
52. 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.
53. Gietz RD, Woods RA (2002) Transformation of yeast by lithium acetate/singlestranded carrier DNA/polyethylene glycol method. Methods Enzymol 350: 87-96.
54. 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.
55. 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.
56. Dinesh-Kumar SP, Anandalakshmi R, Marathe R, Schiff M, Liu Y (2003) Virusinduced gene silencing. Methods Mol Biol 236: 287-294.
57. Johnson AW (1997) Rat1p and Xrn1p are functionally interchangeable exoribonucleases that are restricted to and required in the nucleus and cytoplasm, respectively. Mol Cell Biol 17: 6122-6130.