#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

The Hypervariable Amino-Terminus of P1 Protease Modulates Potyviral Replication and Host Defense Responses


RNA viruses are ideal systems for the study of population dynamics, relationships among pathogen traits such as fitness and virulence, and of host immune responses to pathogen attacks. Based on experimental evolution studies, early models equated parasite virulence with fitness. Some reports showed that viral virulence and fitness can be unlinked. Here we present evidence that the highly disordered N-terminal region of a potyviral P1 protein negatively regulates its self-cleavage activity. Removal of this regulator domain greatly affects viral infection, which is characterized by accelerated early replication and enhanced symptom severity. These properties are nonetheless associated with low viral accumulation and high induction of antiviral resistance markers. Finally, we propose that host-dependent regulation of P1 processing efficiency modulates viral virulence and alleviates the host antiviral responses.


Vyšlo v časopise: The Hypervariable Amino-Terminus of P1 Protease Modulates Potyviral Replication and Host Defense Responses. PLoS Pathog 10(3): e32767. doi:10.1371/journal.ppat.1003985
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003985

Souhrn

RNA viruses are ideal systems for the study of population dynamics, relationships among pathogen traits such as fitness and virulence, and of host immune responses to pathogen attacks. Based on experimental evolution studies, early models equated parasite virulence with fitness. Some reports showed that viral virulence and fitness can be unlinked. Here we present evidence that the highly disordered N-terminal region of a potyviral P1 protein negatively regulates its self-cleavage activity. Removal of this regulator domain greatly affects viral infection, which is characterized by accelerated early replication and enhanced symptom severity. These properties are nonetheless associated with low viral accumulation and high induction of antiviral resistance markers. Finally, we propose that host-dependent regulation of P1 processing efficiency modulates viral virulence and alleviates the host antiviral responses.


Zdroje

1. WalshD, MathewsMB, MohrI (2013) Tinkering with translation: protein synthesis in virus-infected cells. Cold Spring Harb Perspect Biol 5: a012351 doi:10.1101/cshperspect.a012351

2. SummersDF, Maizel JrJV (1968) Evidence for large precursor proteins in poliovirus synthesis. Proc Natl Acad Sci U S A 59: 966.

3. DoughertyWG, Dawn ParksT (1989) Molecular genetic and biochemical evidence for the involvement of the heptapeptide cleavage sequence in determining the reaction profile at two tobacco etch virus cleavage sites in cell-free assays. Virology 172: 145–155 doi:10.1016/0042-6822(89)90116-5

4. GarcíaJA, MartínMT, CerveraMT, RiechmannJL (1992) Proteolytic processing of the plum pox potyvirus polyprotein by the Nla protease at a novel cleavage site. Virology 188: 697–703 doi:10.1016/0042-6822(92)90524-S

5. TongL (2002) Viral proteases. Chem Rev 102: 4609–4626 doi:10.1021/cr010184f

6. SatheshkumarPS, GayathriP, PrasadK, SavithriHS (2005) “Natively unfolded” VPg is essential for Sesbania mosaic virus serine protease activity. J Biol Chem 280: 30291–30300 doi:10.1074/jbc.M504122200

7. MathurC, JimsheenaVK, BanerjeeS, MakinenK, GowdaLR, et al. (2012) Functional regulation of PVBV Nuclear Inclusion protein-a protease activity upon interaction with Viral Protein genome-linked and phosphorylation. Virology 422: 254–264 doi:10.1016/j.virol.2011.10.009

8. Saalau-BethellSM, WoodheadAJ, ChessariG, CarrMG, CoyleJ, et al. (2012) Discovery of an allosteric mechanism for the regulation of HCV NS3 protein function. Nat Chem Biol 8: 920–925 doi:10.1038/nchembio.1081

9. PozziN, VogtAD, GoharaDW, Di CeraE (2012) Conformational selection in trypsin-like proteases. Curr Opin Struct Biol 22: 421–431 doi:10.1016/j.sbi.2012.05.006

10. GorbalenyaAE, DonchenkoAP, BlinovVM, KooninEV (1989) Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases: a distinct protein superfamily with a common structural fold. FEBS Lett 243: 103–114 doi:10.1016/0014-5793(89)80109-7

11. Valli A (2013) Potyvirus P1 proteinase. Handbook of proteolytic enzymes (3rd edition). Elsevier. pp. 3130–3133.

12. KooninEV, WolfYI, NagasakiK, DoljaVV (2008) The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat Rev Microbiol 6: 925–939 doi:10.1038/nrmicro2030

13. GibbsA, OhshimaK (2010) Potyviruses and the digital revolution. Annu Rev Phytopathol 48: 205–223 doi:10.1146/annurev-phyto-073009-114404

14. ChungBY-W, MillerWA, AtkinsJF, FirthAE (2008) An overlapping essential gene in the Potyviridae. Proc Natl Acad Sci U S A 105: 5897–5902 doi:10.1073/pnas.0800468105

15. WeiT, ZhangC, HongJ, XiongR, KasschauKD, et al. (2010) Formation of complexes at plasmodesmata for potyvirus intercellular movement is mediated by the viral protein P3N-PIPO. PLoS Pathog 6: e1000962 doi:10.1371/journal.ppat.1000962

16. López-Moya JJ, Valli A, García JA (2009) Potyviridae. Encyclopedia of life sciences. John Wiley & Sons, Ltd. pp. 1–10.

17. CarringtonJC, FreedDD, SandersTC (1989) Autocatalytic processing of the potyvirus helper component proteinase in Escherichia coli and in vitro. J Virol 63: 4459–4463.

18. VerchotJ, HerndonKL, CarringtonJC (1992) Mutational analysis of the tobacco etch potyviral 35-kDa proteinase: identification of essential residues and requirements for autoproteolysis. Virology 190: 298–306 doi:10.1016/0042-6822(92)91216-H

19. GuoB, LinJ, YeK (2011) Structure of the autocatalytic cysteine protease domain of potyvirus helper-component proteinase. J Biol Chem 286: 21937–21943 doi:10.1074/jbc.M111.230706

20. VerchotJ, CarringtonJC (1995) Debilitation of plant potyvirus infectivity by P1 proteinase-inactivating mutations and restoration by second-site modifications. J Virol 69: 1582–1590.

21. ValliA, López-MoyaJJ, GarcíaJA (2007) Recombination and gene duplication in the evolutionary diversification of P1 proteins in the family Potyviridae. J Gen Virol 88: 1016–1028 doi:10.1099/vir.0.82402-0

22. SalvadorB, SaénzP, YangüezE, QuiotJB, QuiotL, et al. (2008) Host-specific effect of P1 exchange between two potyviruses. Mol Plant Pathol 9: 147–155 doi:10.1111/j.1364-3703.2007.00450.x

23. MaliogkaVI, SalvadorB, CarbonellA, SáenzP, San LeónD, et al. (2012) Virus variants with differences in the P1 protein coexist in a Plum pox virus population and display particular host-dependent pathogenicity features. Mol Plant Pathol 13: 877–886 doi:10.1111/j.1364-3703.2012.00796.x

24. RohožkováJ, NavrátilM (2011) P1 peptidase – a mysterious protein of family Potyviridae. J Biosci 36: 189–200 doi:10.1007/s12038-011-9020-6

25. AnandalakshmiR, PrussGJ, GeX, MaratheR, MalloryAC, et al. (1998) A viral suppressor of gene silencing in plants. Proc Natl Acad Sci U S A 95: 13079–13084 doi:10.1073/pnas.95.22.13079

26. KasschauKD, CarringtonJC (1998) A counterdefensive strategy of plant viruses: suppression of posttranscriptional gene silencing. Cell 95: 461–470 doi:10.1016/S0092-8674(00)81614-1

27. RajamakiML, KelloniemiJ, AlminaiteA, KekarainenT, RabensteinF, et al. (2005) A novel insertion site inside the potyvirus P1 cistron allows expression of heterologous proteins and suggests some P1 functions. Virology 342: 88–101 doi:10.1016/j.virol.2005.07.019

28. ValliA, Martín-HernándezAM, López-MoyaJJ, GarcíaJA (2006) RNA silencing suppression by a second copy of the P1 serine protease of Cucumber vein yellowing ipomovirus, a member of the family Potyviridae that lacks the cysteine protease HCPro. J Virol 80: 10055–10063 doi:10.1128/JVI.00985-06

29. Garcia-RuizH, TakedaA, ChapmanEJ, SullivanCM, FahlgrenN, et al. (2010) Arabidopsis RNA-dependent RNA polymerases and Dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip mosaic virus infection. Plant Cell 22: 481–496 doi:10.1105/tpc.109.073056

30. RiechmannJL, LaínS, GarcíaJA (1990) Infectious in vitro transcripts from a plum pox potyvirus cDNA clone. Virology 177: 710–716 doi:10.1016/0042-6822(90)90537-2

31. Fernández-FernándezMR, MouriñoM, RiveraJ, RodríguezF, Plana-DuránJ, et al. (2001) Protection of rabbits against rabbit hemorrhagic disease virus by immunization with the VP60 protein expressed in plants with a potyvirus-based vector. Virology 280: 283–291 doi:10.1006/viro.2000.0762

32. VerchotJ, CarringtonJC (1995) Evidence that the potyvirus P1 proteinase functions in trans as an accessory factor for genome amplification. J Virol 69: 3668–3674.

33. WardJJ, McGuffinLJ, BrysonK, BuxtonBF, JonesDT (2004) The DISOPRED server for the prediction of protein disorder. Bioinformatics 20: 2138–2139 doi:10.1093/bioinformatics/bth195

34. KozlowskiLP, BujnickiJM (2012) MetaDisorder: a meta-server for the prediction of intrinsic disorder in proteins. BMC Bioinformatics 13: 111 doi:10.1186/1471-2105-13-111

35. AbresciaNGA, BamfordDH, GrimesJM, StuartDI (2012) Structure unifies the viral universe. Annu Rev Biochem 81: 795–822 doi:10.1146/annurev-biochem-060910-095130

36. DonnellyMLL, HughesLE, LukeG, MendozaH, ten DamE, et al. (2001) The “cleavage” activities of foot-and-mouth disease virus 2A site-directed mutants and naturally occurring “2A-like” sequences. J Gen Virol 82: 1027–1041.

37. KelloniemiJ, MäkinenK, ValkonenJPT (2008) Three heterologous proteins simultaneously expressed from a chimeric potyvirus: infectivity, stability and the correlation of genome and virion lengths. Virus Res 135: 282–291 doi:10.1016/j.virusres.2008.04.006

38. RawlingsND, BarrettAJ, BatemanA (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40: D343–D350 doi:10.1093/nar/gkr987

39. KhanAR, JamesMNG (1998) Molecular mechanisms for the conversion of zymogens to active proteolytic enzymes. Protein Sci 7: 815–836 doi:10.1002/pro.5560070401

40. VerchotJ, KooninEV, CarringtonJC (1991) The 35-kDa protein from the N-terminus of the potyviral polyprotein functions as a third virus-encoded proteinase. Virology 185: 527–535 doi:10.1016/0042-6822(91)90522-D

41. DoljaVV, McBrideHJ, CarringtonJC (1992) Tagging of plant potyvirus replication and movement by insertion of beta-glucuronidase into the viral polyprotein. Proc Natl Acad Sci U S A 89: 10208–10212.

42. HafrénA, HofiusD, RönnholmG, SonnewaldU, MäkinenK (2010) HSP70 and its cochaperone CPIP promote potyvirus infection in Nicotiana benthamiana by regulating viral coat protein functions. Plant Cell 22: 523–535 doi:10.1105/tpc.109.072413

43. LinthorstHJ, MelchersLS, MayerA, van RoekelJS, CornelissenBJ, et al. (1990) Analysis of gene families encoding acidic and basic beta-1,3-glucanases of tobacco. Proc Natl Acad Sci U S A 87: 8756–8760 doi:10.1073/pnas.87.22.8756

44. KauffmannS, LegrandM, GeoffroyP, FritigB (1987) Biological function of “pathogenesis-related” proteins: four PR proteins of tobacco have 1,3-beta-glucanase activity. EMBO J 6: 3209–3212.

45. Leubner-Metzger G, Meins Jr F (1999) Functions and regulation of plant beta-1,3-glucanases (PR-2). Pathogenesis-related proteins in plants. CRC Press. pp. 1–31.

46. Van LoonLC, GerritsenYAM, RitterCE (1987) Identification, purification, and characterization of pathogenesis-related proteins from virus-infected Samsun NN tobacco leaves. Plant Mol Biol 9: 593–609 doi:10.1007/BF00020536

47. LegrandM, KauffmannS, GeoffroyP, FritigB (1987) Biological function of pathogenesis-related proteins: Four tobacco pathogenesis-related proteins are chitinases. Proc Natl Acad Sci U S A 84: 6750–6754.

48. WardER, UknesSJ, WilliamsSC, DincherSS, WiederholdDL, et al. (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3: 1085–1094 doi:10.1105/tpc.3.10.1085

49. HeitzT, FritigB, LegrandM (1994) Local and systemic accumulation of pathogenesis-related proteins in tobacco plants infected with tobacco mosaic virus. Mol Plant Microbe Interact 7: 776–779.

50. Van LoonLC, RepM, PieterseCMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44: 135–162 doi:10.1146/annurev.phyto.44.070505.143425

51. HennigJ, DeweyRE, CuttJR, KlessigDF (1993) Pathogen, salicylic acid and developmental dependent expression of a β-1,3-glucanase/GUS gene fusion in transgenic tobacco plants. Plant J 4: 481–493 doi:10.1046/j.1365-313X.1993.04030481.x

52. NikiT, MitsuharaI, SeoS, OhtsuboN, OhashiY (1998) Antagonistic effect of salicylic acid and jasmonic acid on the expression of pathogenesis-related (PR) protein genes in wounded mature tobacco leaves. Plant Cell Physiol 39: 500–507 doi:10.1093/oxfordjournals.pcp.a029397

53. WhiteRF (1979) Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99: 410–412 doi:10.1016/0042-6822(79)90019-9

54. YalpaniN, SilvermanP, WilsonTM, KleierDA, RaskinI (1991) Salicylic acid is a systemic signal and an inducer of pathogenesis-related proteins in virus-infected tobacco. Plant Cell 3: 809–818 doi:10.1105/tpc.3.8.809

55. GaffneyT, FriedrichL, VernooijB, NegrottoD, NyeG, et al. (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754–756 doi:10.1126/science.261.5122.754

56. YingX-B, DongL, ZhuH, DuanC-G, DuQ-S, et al. (2010) RNA-dependent RNA polymerase 1 from Nicotiana tabacum suppresses RNA silencing and enhances viral infection in Nicotiana benthamiana. Plant Cell 22: 1358–1372 doi:10.1105/tpc.109.072058

57. RossPL, HuangYN, MarcheseJN, WilliamsonB, ParkerK, et al. (2004) Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 3: 1154–1169 doi:10.1074/mcp.M400129-MCP200

58. BombarelyA, RosliHG, VrebalovJ, MoffettP, MuellerLA, et al. (2012) A draft genome sequence of Nicotiana benthamiana to enhance molecular plant-microbe biology research. Mol Plant Microbe Interact 25: 1523–1530 doi:10.1094/MPMI-06-12-0148-TA

59. BombarelyA, MendaN, TecleIY, BuelsRM, StricklerS, et al. (2011) The Sol Genomics Network (solgenomics.net): growing tomatoes using Perl. Nucleic Acids Res 39: D1149–D1155 doi:10.1093/nar/gkq866

60. MemelinkJ, LinthorstHJ, SchilperoortRA, HogeJHC (1990) Tobacco genes encoding acidic and basic isoforms of pathogenesis-related proteins display different expression patterns. Plant Mol Biol 14: 119–126 doi:10.1007/BF00018553

61. BrederodeFT, LinthorstHJ, BolJF (1991) Differential induction of acquired resistance and PR gene expression in tobacco by virus infection, ethephon treatment, UV light and wounding. Plant Mol Biol 17: 1117–1125 doi:10.1007/BF00028729

62. EyalY, MellerY, Lev-YadunS, FluhrR (1993) A basic-type PR-1 promoter directs ethylene responsiveness, vascular and abscission zone-specific expression. Plant J 4: 225–234 doi:10.1046/j.1365-313X.1993.04020225.x

63. XuYI, ChangP-FL, LiuD, NarasimhanML, RaghothamaKG, et al. (1994) Plant defense genes are synergistically induced by ethylene and methyl jasmonate. Plant Cell 6: 1077–1085 doi:10.1105/tpc.6.8.1077

64. XieW, GoodwinPH (2009) A PRp27 gene of Nicotiana benthamiana contributes to resistance to Pseudomonas syringae pv. tabaci but not to Colletotrichum destructivum or Colletotrichum orbiculare. Funct Plant Biol 36: 351–361 doi:10.1071/FP08241

65. SinghNK, NelsonDE, KuhnD, HasegawaPM, BressanRA (1989) Molecular cloning of osmotin and regulation of its expression by ABA and adaptation to low water potential. Plant Physiol 90: 1096–1101 doi:10.1104/pp.90.3.1096

66. HaninM, BriniF, EbelC, TodaY, TakedaS, et al. (2011) Plant dehydrins and stress tolerance: versatile proteins for complex mechanisms. Plant Signal Behav 6: 1503–1509 doi:10.4161/psb.6.10.17088

67. ChenZ, SilvaH, KlessigDF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262: 1883–1886 doi:10.1126/science.8266079

68. WeigelM, VarottoC, PesaresiP, FinazziG, RappaportF, et al. (2003) Plastocyanin is indispensable for photosynthetic electron flow in Arabidopsis thaliana. J Biol Chem 278: 31286–31289 doi:10.1074/jbc.M302876200

69. FermaniS, TrivelliX, SparlaF, ThumigerA, CalvaresiM, et al. (2012) Conformational selection and folding-upon-binding of intrinsically disordered protein CP12 regulate photosynthetic enzymes assembly. J Biol Chem 287: 21372–21383 doi:10.1074/jbc.M112.350355

70. KubotaK, TsudaS, TamaiA, MeshiT (2003) Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J Virol 77: 11016–11026 doi:10.1128/JVI.77.20.11016-11026.2003

71. IshibashiK, MeshiT, IshikawaM (2011) Gaining replicability in a nonhost compromises the silencing suppression activity of Tobacco mild green mosaic virus in a host. J Virol 85: 1893–1895 doi:10.1128/JVI.01741-10

72. Tena FernándezF, GonzálezI, DoblasP, RodríguezC, SahanaN, et al. (2013) The influence of cis-acting P1 protein and translational elements on the expression of Potato virus Y helper-component proteinase (HCPro) in heterologous systems and its suppression of silencing activity. Mol Plant Pathol 14: 530–541 doi:10.1111/mpp.12025

73. AdamsMJ, AntoniwJF, FauquetCM (2005) Molecular criteria for genus and species discrimination within the family Potyviridae. Arch Virol 150: 459–479 doi:10.1007/s00705-004-0440-6

74. CarrascoP, de la IglesiaF, ElenaSF (2007) Distribution of fitness and virulence effects caused by single-nucleotide substitutions in Tobacco etch virus. J Virol 81: 12979–12984 doi:10.1128/JVI.00524-07

75. RollandM, KerlanC, JacquotE (2009) The acquisition of molecular determinants involved in potato virus Y necrosis capacity leads to fitness reduction in tobacco plants. J Gen Virol 90: 244–252 doi:10.1099/vir.0.005140-0

76. HerreraM, García-ArriazaJ, ParienteN, EscarmísC, DomingoE (2007) Molecular basis for a lack of correlation between viral fitness and cell killing capacity. PLoS Pathog 3: e53 doi:10.1371/journal.ppat.0030053

77. CollNS, EppleP, DanglJL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18: 1247–1256 doi:10.1038/cdd.2011.37

78. LancasterKZ, PfeifferJK (2012) Viral population dynamics and virulence thresholds. Curr Opin Microbiol 15: 525–530 doi:10.1016/j.mib.2012.05.007

79. RyalsJA, NeuenschwanderUH, WillitsMG, MolinaA, SteinerHY, et al. (1996) Systemic acquired resistance. Plant Cell 8: 1809–1819 doi:10.1105/tpc.8.10.1809

80. Robert-SeilaniantzA, GrantM, JonesJD (2011) Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Annu Rev Phytopathol 49: 317–343 doi:10.1146/annurev-phyto-073009-114447

81. PieterseCM, Leon-ReyesA, Van der EntS, Van WeesSC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5: 308–316 doi:10.1038/nchembio.164

82. García-MarcosA, PachecoR, ManzanoA, AguilarE, TenlladoF (2013) Oxylipin biosynthesis genes positively regulate programmed cell death during compatible infections with the synergistic pair Potato virus X-Potato virus Y and Tomato spotted wilt virus. J Virol 87: 5769–5783 doi:10.1128/JVI.03573-12

83. Gimenez-IbanezS, SolanoR (2013) Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens. Front Plant Sci 4: 72 doi:10.3389/fpls.2013.00072

84. Díaz-VivancosP, RubioM, MesoneroV, PeriagoPM, BarcelóAR, et al. (2006) The apoplastic antioxidant system in Prunus: response to long-term plum pox virus infection. J Exp Bot 57: 3813–3824 doi:10.1093/jxb/erl138

85. ElviraMI, GaldeanoMM, GilardiP, Garcia-LuqueI, SerraMT (2008) Proteomic analysis of pathogenesis-related proteins (PRs) induced by compatible and incompatible interactions of pepper mild mottle virus (PMMoV) in Capsicum chinense L3 plants. J Exp Bot 59: 1253–1265 doi:10.1093/jxb/ern032

86. Di CarliM, BenvenutoE, DoniniM (2012) Recent insights into plant-virus interactions through proteomic analysis. J Proteome Res 11: 4765–4780 doi:10.1021/pr300494e

87. JiLH, DingSW (2001) The suppressor of transgene RNA silencing encoded by Cucumber mosaic virus interferes with salicylic acid-mediated virus resistance. Mol Plant Microbe Interact 14: 715 doi:10.1094/MPMI.2001.14.6.715

88. WangX, GoregaokerSP, CulverJN (2009) Interaction of the Tobacco mosaic virus replicase protein with a NAC domain transcription factor is associated with the suppression of systemic host defenses. J Virol 83: 9720–9730 doi:10.1128/JVI.00941-09

89. LoveAJ, GeriC, LairdJ, CarrC, YunB-W, et al. (2012) Cauliflower mosaic virus protein P6 inhibits signaling responses to salicylic acid and regulates innate immunity. PLoS One 7: e47535 doi:10.1371/journal.pone.0047535

90. RinckG, BirghanC, HaradaT, MeyersG, ThielH-J, et al. (2001) A cellular J-domain protein modulates polyprotein processing and cytopathogenicity of a pestivirus. J Virol 75: 9470–9482 doi:10.1128/JVI.75.19.9470-9482.2001

91. LacknerT, MüllerA, PankrazA, BecherP, ThielH-J, et al. (2004) Temporal modulation of an autoprotease is crucial for replication and pathogenicity of an RNA virus. J Virol 78: 10765–10775 doi:10.1128/JVI.78.19.10765-10775.2004

92. LacknerT, MullerA, KonigM, ThielH-J, TautzN (2005) Persistence of bovine viral diarrhea virus is determined by a cellular cofactor of a viral autoprotease. J Virol 79: 9746–9755 doi:10.1128/JVI.79.15.9746-9755.2005

93. PrussG, GeX, ShiXM, CarringtonJC, VanceVB (1997) Plant viral synergism: the potyviral genome encodes a broad-range pathogenicity enhancer that transactivates replication of heterologous viruses. Plant Cell 9: 859–868 doi:10.1105/tpc.9.6.859

94. ChoiH-K, TongL, MinorW, DumasP, BoegeU, et al. (1991) Structure of Sindbis virus core protein reveals a chymotrypsin-like serine proteinase and the organization of the virion. Nature 354: 37–43 doi:10.1038/354037a0

95. PengC-W, PeremyslovVV, MushegianAR, DawsonWO, DoljaVV (2001) Functional specialization and evolution of leader proteinases in the family Closteroviridae. J Virol 75: 12153–12160 doi:10.1128/JVI.75.24.12153-12160.2001

96. HiltonL, MoganeradjK, ZhangG, ChenY-H, RandallRE, et al. (2006) The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. J Virol 80: 11723–11732 doi:10.1128/JVI.01145-06

97. WaterhouseAM, ProcterJB, MartinDMA, ClampM, BartonGJ (2009) Jalview version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25: 1189–1191 doi:10.1093/bioinformatics/btp033

98. EdgarRC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797 doi:10.1093/nar/gkh340

99. CuffJA, BartonGJ (2000) Application of multiple sequence alignment profiles to improve protein secondary structure prediction. Proteins 40: 502–511 doi:;10.1002/1097-0134(20000815)40:3<502::AID-PROT170>3.0.CO;2-Q

100. JonesDT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195–202 doi:10.1006/jmbi.1999.3091

101. ChengJ, RandallAZ, SweredoskiMJ, BaldiP (2005) SCRATCH: a protein structure and structural feature prediction server. Nucleic Acids Res 33: W72–W76 doi:10.1093/nar/gki396

102. DelerisA, Gallego-BartolomeJ, BaoJ, KasschauKD, CarringtonJC, et al. (2006) Hierarchical action and inhibition of plant Dicer-like proteins in antiviral defense. Science 313: 68–71 doi:10.1126/science.1128214

103. ChiuW, NiwaY, ZengW, HiranoT, KobayashiH, et al. (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6: 325–330 doi:10.1016/S0960-9822(02)00483-9

104. Lucini C (2004) Expresión de proteínas heterólogas en plantas por medio del virus de la sharka (PPV) Madrid: Universidad Politécnica de Madrid.

105. HartleyJL, TempleGF, BraschMA (2000) DNA cloning using in vitro site-specific recombination. Genome Res 10: 1788–1795 doi:10.1101/gr.143000

106. GibsonDG, YoungL, ChuangR-Y, VenterJC, Hutchison IIICA, et al. (2009) Enzymatic assembly of DNA molecules up to several hundred kilobases. Nat Methods 6: 343–345 doi:10.1038/nmeth.1318

107. SchäggerH, von JagowG (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166: 368–379 doi:10.1016/0003-2697(87)90587-2

108. MurashigeT, SkoogF (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15: 473–497 doi:10.1111/j.1399-3054.1962.tb08052.x

109. EskelinK, SuntioT, HyvärinenS, HafrenA, MäkinenK (2010) Renilla luciferase-based quantitation of Potato virus A infection initiated with Agrobacterium infiltration of N. benthamiana leaves. J Virol Methods 164: 101–110 doi:10.1016/j.jviromet.2009.12.006

110. SchneiderCA, RasbandWS, EliceiriKW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9: 671–675 doi:10.1038/nmeth.2089

111. LanfordRE, SureauC, JacobJR, WhiteR, FuerstTR (1994) Demonstration of in vitro infection of chimpanzee hepatocytes with hepatitis C virus using strand-specific RT/PCR. Virology 202: 606–614 doi:10.1006/viro.1994.1381

112. Komurian-PradelF, PerretM, DeimanB, SodoyerM, LotteauV, et al. (2004) Strand specific quantitative real-time PCR to study replication of hepatitis C virus genome. J Virol Methods 116: 103–106 doi:10.1016/j.jviromet.2003.10.004

113. PlaskonNE, AdelmanZN, MylesKM (2009) Accurate strand-specific quantification of viral RNA. PLoS One 4: e7468 doi:10.1371/journal.pone.0007468

114. PfafflMW, HageleitM (2001) Validities of mRNA quantification using recombinant RNA and recombinant DNA external calibration curves in real-time RT-PCR. Biotechnol Lett 23: 275–282 doi:10.1023/A:1005658330108

115. MaB, JohnsonR (2012) De novo sequencing and homology searching. Mol Cell Proteomics 11: 1–16 doi:10.1074/mcp.O111.014902

116. ZhangJ, XinL, ShanB, ChenW, XieM, et al. (2012) PEAKS DB: de novo sequencing assisted database search for sensitive and accurate peptide identification. Mol Cell Proteomics 11: 1–8 doi:10.1074/mcp.M111.010587

117. SaeedA, SharovV, WhiteJ, LiJ, LiangW, et al. (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34: 374–378.

118. EisenMB, SpellmanPT, BrownPO, BotsteinD (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863–14868.

119. Maere S, Heymans K, Kuiper M (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 21: : 3448–3449. doi:10.1093/bioinformatics/bti551.

120. ProcterJB, ThompsonJ, LetunicI, CreeveyC, JossinetF, et al. (2010) Visualization of multiple alignments, phylogenies and gene family evolution. Nat Methods 7: S16–S25 doi:10.1038/nmeth.1434

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2014 Číslo 3
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#