Coronavirus Gene 7 Counteracts Host Defenses and Modulates Virus Virulence
Transmissible gastroenteritis virus (TGEV) genome contains three accessory genes:
3a, 3b and 7. Gene 7 is only present in members of coronavirus genus a1, and encodes a hydrophobic protein of 78 aa. To study gene 7 function, a recombinant TGEV virus lacking gene 7 was engineered (rTGEV-Δ7). Both the mutant and the parental (rTGEV-wt) viruses showed the same growth and viral RNA accumulation kinetics in tissue cultures. Nevertheless, cells infected with rTGEV-Δ7 virus showed an increased cytopathic effect caused by an enhanced apoptosis mediated by caspase activation. Macromolecular synthesis analysis showed that rTGEV-Δ7 virus infection led to host translational shut-off and increased cellular RNA degradation compared with rTGEV-wt infection. An increase of eukaryotic translation initiation factor 2 (eIF2α) phosphorylation and an enhanced nuclease, most likely RNase L, activity were observed in rTGEV-Δ7 virus infected cells. These results suggested that the removal of gene 7 promoted an intensified dsRNA-activated host antiviral response. In protein 7 a conserved sequence motif that potentially mediates binding to protein phosphatase 1 catalytic subunit (PP1c), a key regulator of the cell antiviral defenses, was identified. We postulated that TGEV protein 7 may counteract host antiviral response by its association with PP1c. In fact, pull-down assays demonstrated the interaction between TGEV protein 7, but not a protein 7 mutant lacking PP1c binding motif, with PP1. Moreover, the interaction between protein 7 and PP1 was required, during the infection, for eIF2α dephosphorylation and inhibition of cell RNA degradation. Inoculation of newborn piglets with rTGEV-Δ7 and rTGEV-wt viruses showed that rTGEV-Δ7 virus presented accelerated growth kinetics and pathology compared with the parental virus. Overall, the results indicated that gene 7 counteracted host cell defenses, and modified TGEV persistence increasing TGEV survival. Therefore, the acquisition of gene 7 by the TGEV genome most likely has provided a selective advantage to the virus.
Vyšlo v časopise:
Coronavirus Gene 7 Counteracts Host Defenses and Modulates Virus Virulence. PLoS Pathog 7(6): e32767. doi:10.1371/journal.ppat.1002090
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002090
Souhrn
Transmissible gastroenteritis virus (TGEV) genome contains three accessory genes:
3a, 3b and 7. Gene 7 is only present in members of coronavirus genus a1, and encodes a hydrophobic protein of 78 aa. To study gene 7 function, a recombinant TGEV virus lacking gene 7 was engineered (rTGEV-Δ7). Both the mutant and the parental (rTGEV-wt) viruses showed the same growth and viral RNA accumulation kinetics in tissue cultures. Nevertheless, cells infected with rTGEV-Δ7 virus showed an increased cytopathic effect caused by an enhanced apoptosis mediated by caspase activation. Macromolecular synthesis analysis showed that rTGEV-Δ7 virus infection led to host translational shut-off and increased cellular RNA degradation compared with rTGEV-wt infection. An increase of eukaryotic translation initiation factor 2 (eIF2α) phosphorylation and an enhanced nuclease, most likely RNase L, activity were observed in rTGEV-Δ7 virus infected cells. These results suggested that the removal of gene 7 promoted an intensified dsRNA-activated host antiviral response. In protein 7 a conserved sequence motif that potentially mediates binding to protein phosphatase 1 catalytic subunit (PP1c), a key regulator of the cell antiviral defenses, was identified. We postulated that TGEV protein 7 may counteract host antiviral response by its association with PP1c. In fact, pull-down assays demonstrated the interaction between TGEV protein 7, but not a protein 7 mutant lacking PP1c binding motif, with PP1. Moreover, the interaction between protein 7 and PP1 was required, during the infection, for eIF2α dephosphorylation and inhibition of cell RNA degradation. Inoculation of newborn piglets with rTGEV-Δ7 and rTGEV-wt viruses showed that rTGEV-Δ7 virus presented accelerated growth kinetics and pathology compared with the parental virus. Overall, the results indicated that gene 7 counteracted host cell defenses, and modified TGEV persistence increasing TGEV survival. Therefore, the acquisition of gene 7 by the TGEV genome most likely has provided a selective advantage to the virus.
Zdroje
1. EnjuanesLGorbalenyaAEde GrootRJCowleyJAZiebuhrJ 2008 The Nidovirales. MahyBWJVan RegenmortelMWalkerPMajumder-RussellD Encyclopedia of Virology, Third Edition Oxford Elsevier Ltd 419 430
2. MastersPS 2006 The molecular biology of coronaviruses. Adv Virus Res 66 193 292
3. DenisonMR 1999 The common cold. Rhinoviruses and coronaviruses. DolinRWringhtPF Viral infections of the respiratory tract New York Marcel Dekker, Inc 253 280
4. DrostenCGuntherSPreiserWvan der WerfSBrodtHR 2003 Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N Engl J Med 348 1967 1976
5. HolmesKVEnjuanesL 2003 The SARS coronavirus: a postgenomic era. Science 300 1377 1378
6. PerlmanSPeweL 1998 Role of CTL escape mutants in demyelination induced by mouse hepatitis virus, strain JHM. Adv Exp Med Biol 440 515 520
7. MedzhitovRJanewayCAJr 1997 Innate immunity: the virtues of a nonclonal system of recognition. Cell 91 295 298
8. DauberBWolffT 2009 Activation of the Antiviral Kinase PKR and Viral Countermeasures. Viruses 1 523 544
9. TaylorSSHasteNMGhoshG 2005 PKR and eIF2alpha: integration of kinase dimerization, activation, and substrate docking. Cell 122 823 825
10. BisbalCSilvermanRH 2007 Diverse functions of RNase L and implications in pathology. Biochimie 89 789 798
11. PlayerMRTorrencePF 1998 The 2-5A system: modulation of viral and cellular processes through acceleration of RNA degradation. Pharmacol Ther 78 55 113
12. ProudCG 1995 PKR: a new name and new roles. Trends Biochem Sci 20 241 246
13. CassadyKAGrossM 2002 The herpes simplex virus type 1 U(S)11 protein interacts with protein kinase R in infected cells and requires a 30-amino-acid sequence adjacent to a kinase substrate domain. J Virol 76 2029 2035
14. WatsonJCChangHWJacobsBL 1991 Characterization of a vaccinia virus-encoded double-stranded RNA-binding protein that may be involved in inhibition of the double-stranded RNA-dependent protein kinase. Virology 185 206 216
15. ChangHWWatsonJCJacobsBL 1992 The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. Proc Natl Acad Sci USA 89 4825 4829
16. BergmannMGarcia-SastreACarneroEPehambergerHWolffK 2000 Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. J Virol 74 6203 6206
17. LanglandJOPettifordSJiangBJacobsBL 1994 Products of the porcine group C rotavirus NSP3 gene bind specifically to double-stranded RNA and inhibit activation of the interferon-induced protein kinase PKR. J Virol 68 3821 3829
18. RivasCGilJMelkovaZEstebanMDiaz-GuerraM 1998 Vaccinia virus E3L protein is an inhibitor of the interferon (i.f.n.)-induced 2-5A synthetase enzyme. Virology 243 406 414
19. PetersGAKhooDMohrISenGC 2002 Inhibition of PACT-mediated activation of PKR by the herpes simplex virus type 1 Us11 protein. J Virol 76 11054 11064
20. RomanoPRZhangFTanSLGarcia-BarrioMTKatzeMG 1998 Inhibition of double-stranded RNA-dependent protein kinase PKR by vaccinia virus E3: role of complex formation and the E3 N-terminal domain. Mol Cell Biol 18 7304 7316
21. GaleMJJrKorthMJTangNMTanSLHopkinsDA 1997 Evidence that hepatitis C virus resistance to interferon is mediated through repression of the PKR protein kinase by the nonstructural 5A protein. Virology 230 217 227
22. DeverTESripriyaRMcLachlinJRLuJFabianJR 1998 Disruption of cellular translational control by a viral truncated eukaryotic translation initiation factor 2alpha kinase homolog. Proc Natl Acad Sci USA 95 4164 4169
23. O'MalleyRPMarianoTMSiekierkaJMathewsMB 1986 A mechanism for the control of protein synthesis by adenovirus VA RNAI. Cell 44 391 400
24. SharpTVSchwemmleMJeffreyILaingKMellorH 1993 Comparative analysis of the regulation of the interferon-inducible protein kinase PKR by Epstein-Barr virus RNAs EBER-1 and EBER-2 and adenovirus VAI RNA. Nucleic Acids Res 21 4483 4490
25. GunnerySRiceAPRobertsonHDMathewsMB 1990 Tat-responsive region RNA of human immunodeficiency virus 1 can prevent activation of the double-stranded-RNA-activated protein kinase. Proc Natl Acad Sci USA 87 8687 8691
26. PolyakSJTangNWambachMBarberGNKatzeMG 1996 The P58 cellular inhibitor complexes with the interferon-induced, double-stranded RNA-dependent protein kinase, PKR, to regulate its autophosphorylation and activity. J Biol Chem 271 1702 1707
27. GoodmanAGFornekJLMedigeshiGRPerroneLAPengX 2009 P58(IPK): a novel “CIHD” member of the host innate defense response against pathogenic virus infection. PLoS Pathog 5 e1000438
28. GosertRKanjanahaluethaiAEggerDBienzKBakerSC 2002 RNA replication of mouse hepatitis virus takes place at double-membrane vesicles. J Virol 76 3697 3708
29. SnijderEJvan der MeerYZevenhoven-DobbeJOnderwaterJJvan der MeulenJ 2006 Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex. J Virol 80 5927 5940
30. KamitaniWNarayananKHuangCLokugamageKIkegamiT 2006 Severe acute respiratory syndrome coronavirus nsp1 protein suppresses host gene expression by promoting host mRNA degradation. Proc Natl Acad Sci USA 103 12885 12890
31. TohyaYNarayananKKamitaniWHuangCLokugamageK 2009 Suppression of host gene expression by nsp1 proteins of group 2 bat coronaviruses. J Virol 83 5282 5288
32. WangXLiaoYYapPLPngKJTamJP 2009 Inhibition of protein kinase R activation and upregulation of GADD34 expression play a synergistic role in facilitating coronavirus replication by maintaining de novo protein synthesis in virus-infected cells. J Virol 83 12462 12472
33. YeYHaunsKLanglandJOJacobsBLHogueBG 2007 Mouse hepatitis coronavirus A59 nucleocapsid protein is a type I interferon antagonist. J Virol 81 2554 2563
34. BrierleyIDigardPInglisSC 1989 Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell 57 537 547
35. de GrootRJZiebuhrJPoonLLWooPCTalbotP 2010 Taxonomic structure of the Coronaviridae. FauquetCMMayoMAManiloffJDesselbergUKingA Virus Taxonomy International Committee on Taxonomy of Viruses: Academic Press
36. KoetznerCAKuoLGoebelSJDeanABParkerMM 2010 Accessory protein 5a is a major antagonist of the antiviral action of interferon against murine coronavirus. J Virol 84 8262 8274
37. YountBRobertsRSSimsACDemingDFriemanMB 2005 Severe acute respiratory syndrome coronavirus group-specific open reading frames encode nonessential functions for replication in cell cultures and mice. J Virol 79 14909 14922
38. DeDiegoMLPeweLAlvarezERejasMTPerlmanS 2008 Pathogenicity of severe acute respiratory coronavirus deletion mutants in hACE-2 transgenic mice. Virology 376 379 389
39. DeDiegoMLAlvarezEAlmazanFRejasMTLamirandeE 2007 A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J Virol 81 1701 1713
40. DediegoMLPeweLAlvarezERejasMTPerlmanS 2008 Pathogenicity of severe acute respiratory coronavirus deletion mutants in hACE-2 transgenic mice. Virology 376 379 389
41. TanguduCOlivaresHNetlandJPerlmanSGallagherT 2007 Severe acute respiratory syndrome coronavirus protein 6 accelerates murine coronavirus infections. J Virol 81 1220 1229
42. PeweLZhouHNetlandJTanguduCOlivaresH 2005 A severe acute respiratory syndrome-associated coronavirus-specific protein enhances virulence of an attenuated murine coronavirus. J Virol 79 11335 11342
43. BrianDABaricRS 2005 Coronavirus genome structure and replication. Curr Top Microbiol Immunol 287 1 30
44. EnjuanesLAlmazanFOrtegoJ 2003 Virus-based vectors for gene expression in mammalian cells: Coronavirus. MakridesSC Gene Transfer and Expression in Mammalian cells: Elsevier Science B.V 151 168
45. SolaIAlonsoSZúñigaSBalachMPlana-DuránJ 2003 Engineering transmissible gastroenteritis virus genome as an expression vector inducing latogenic immunity. J Virol 77 4357 4369
46. ChuDKPeirisJSChenHGuanYPoonLL 2008 Genomic characterizations of bat coronaviruses (1A, 1B and HKU8) and evidence for co-infections in Miniopterus bats. J Gen Virol 89 1282 1287
47. WooPCWangMLauSKXuHPoonRW 2007 Comparative analysis of twelve genomes of three novel group 2c and group 2d coronaviruses reveals unique group and subgroup features. J Virol 81 1574 1585
48. WooPCLauSKLamCSLaiKKHuangY 2009 Comparative analysis of complete genome sequences of three avian coronaviruses reveals a novel group 3c coronavirus. J Virol 83 908 917
49. JonassenCMKofstadTLarsenILLovlandAHandelandK 2005 Molecular identification and characterization of novel coronaviruses infecting graylag geese (Anser anser), feral pigeons (Columbia livia) and mallards (Anas platyrhynchos). J Gen Virol 86 1597 1607
50. GorbalenyaAEEnjuanesLZiebuhrJSnijderEJ 2006 Nidovirales: evolving the largest RNA virus genome. Virus Res 117 17 37
51. LaiMMCCavanaghD 1997 The molecular biology of coronaviruses. Adv Virus Res 48 1 100
52. OrtegoJSolaIAlmazanFCerianiJERiquelmeC 2003 Transmissible gastroenteritis coronavirus gene 7 is not essential but influences in vivo virus replication and virulence. Virology 308 13 22
53. de HaanCAMMastersPSShenSWeissSRottierPJM 2002 The group-specific murine coronavirus genes are not essential, but their deletion, by reverse genetics, is attenuating in the natural host. Virology 296 177 189
54. HaijemaBJVoldersHRottierPJ 2004 Live, attenuated coronavirus vaccines through the directed deletion of group-specific genes provide protection against feline infectious peritonitis. J Virol 78 3863 3871
55. HerreweghAAPMVennemaHHorzinekMCRottierPJMGrootPJ 1995 The molecular genetics of feline coronavirus comparative sequence analysis of the ORF7a/7b transcription unit of different biotypes. Virology 212 622 631
56. TungFYTAbrahamSSethnaMHungSLSethnaP 1992 The 9-kDa hydrophobic protein encoded at the 3′ end of the porcine transmissible gastroenteritis coronavirus genome is membrane-associated. Virology 186 676 683
57. SanchezCMIzetaASánchez-MorgadoJMAlonsoSSolaI 1999 Targeted recombination demonstrates that the spike gene of transmissible gastroenteritis coronavirus is a determinant of its enteric tropism and virulence. J Virol 73 7607 7618
58. IzetaASmerdouCAlonsoSPenzesZMendezA 1999 Replication and packaging of transmissible gastroenteritis coronavirus-derived synthetic minigenomes. J Virol 73 1535 1545
59. GalanCSolaINogalesAThomasBAkoulitchevA 2009 Host cell proteins interacting with the 3′ end of TGEV coronavirus genome influence virus replication. Virology 391 304 314
60. LaudeH 1981 Thermal inactivation studies of a coronavirus, transmissible gastroenteritis virus. J Gen Virol 56 235 240
61. van EngelandMRamaekersFCSchutteBReutelingspergerCP 1996 A novel assay to measure loss of plasma membrane asymmetry during apoptosis of adherent cells in culture. Cytometry 24 131 139
62. NicolettiIMiglioratiGPagliacciMCGrignaniFRiccardiC 1991 A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J Immunol Methods 139 271 279
63. EleouetJFChilmonczykSBesnardeauLLaudeH 1998 Transmissible gastroenteritis coronavirus induces programmed cell death in infected cells through a caspase-dependent pathway. J Virol 72 4918 4924
64. EleouetJFSleeEASauriniFCastagnéNPoncetD 2000 The viral nucleocapsid protein of transmissible gastroenteritis coronavirus (TGEV) is cleaved by caspase-6 and -7 during TGEV-induced apoptosis. J Virol 74 3975 3983
65. SirinarumitrTKlugeJPPaulPS 1998 Transmissible gastroenteritis virus induced apoptosis in swine testis cell cultures. Arch Virol 143 2471 2485
66. ZhangQLDingYQHeLWangWZhangJH 2003 Detection of cell apoptosis in the pathological tissues of patients with SARS and its significance. Di Yi Jun Yi Da Xue Xue Bao 23 770 773
67. WeiLSunSXuCHZhangJXuY 2007 Pathology of the thyroid in severe acute respiratory syndrome. Hum Pathol 38 95 102
68. NarayananKHuangCLokugamageKKamitaniWIkegamiT 2008 Severe acute respiratory syndrome coronavirus nsp1 suppresses host gene expression, including that of type I interferon, in infected cells. J Virol 82 4471 4479
69. SchwartzTFuLLaviE 2002 Differential induction of apoptosis in demyelinating and nondemyelinating infection by mouse hepatitis virus. J Neurovirol 8 392 399
70. RaabenMKoerkampMJRottierPJde HaanCA 2007 Mouse hepatitis coronavirus replication induces host translational shutoff and mRNA decay, with concomitant formation of stress granules and processing bodies. Cell Microbiol 9 2218 2229
71. LiuYZhangX 2007 Murine coronavirus-induced oligodendrocyte apoptosis is mediated through the activation of the Fas signaling pathway. Virology 360 364 375
72. DeregtDBabiuckLA 1987 Monoclonal antibodies to bovine coronavirus: characteristics and topographical mapping of neutralizing epitopes on the E2 and E3 glycoproteins. Virology 68 41 420
73. KyuwaSCohenMNelsonGTaharaSMStohlmanSA 1994 Modulation of cellular macromolecular synthesis by coronavirus: implication for pathogenesis. J Virol 68 6815 6819
74. EnjuanesLAlmazanFSolaIZunigaS 2006 Biochemical aspects of coronavirus replication and virus-host interaction. Annu Rev Microbiol 60 211 230
75. AuerHLyianarachchiSNewsomDKlisovicMIMarcucciG 2003 Chipping away at the chip bias: RNA degradation in microarray analysis. Nat Genet 35 292 293
76. LinRJYuHPChangBLTangWCLiaoCL 2009 Distinct antiviral roles for human 2′,5′-oligoadenylate synthetase family members against dengue virus infection. J Immunol 183 8035 8043
77. ScherbikSVParanjapeJMStockmanBMSilvermanRHBrintonMA 2006 RNase L plays a role in the antiviral response to West Nile virus. J Virol 80 2987 2999
78. IordanovMSParanjapeJMZhouAWongJWilliamsBR 2000 Activation of p38 mitogen-activated protein kinase and c-Jun NH(2)-terminal kinase by double-stranded RNA and encephalomyocarditis virus: involvement of RNase L, protein kinase R, and alternative pathways. Mol Cell Biol 20 617 627
79. WidlakPGarrardWT 2005 Discovery, regulation, and action of the major apoptotic nucleases DFF40/CAD and endonuclease G. J Cell Biochem 94 1078 1087
80. LoppAKuusksaluASamuelKKelveM 2000 Expression and activity of 2-5A synthetase in the course of differentiation and apoptosis of PC12 cells. Cytokine 12 737 741
81. HanJQBartonDJ 2002 Activation and evasion of the antiviral 2′-5′ oligoadenylate synthetase/ribonuclease L pathway by hepatitis C virus mRNA. RNA 8 512 525
82. SilvermanRH 2007 Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 81 12720 12729
83. HanJQWroblewskiGXuZSilvermanRHBartonDJ 2004 Sensitivity of hepatitis C virus RNA to the antiviral enzyme ribonuclease L is determined by a subset of efficient cleavage sites. J Interferon Cytokine Res 24 664 676
84. Domingo-GilEEstebanM 2006 Role of mitochondria in apoptosis induced by the 2-5A system and mechanisms involved. Apoptosis 11 725 738
85. SuAIPezackiJPWodickaLBrideauADSupekovaL 2002 Genomic analysis of the host response to hepatitis C virus infection. Proc Natl Acad Sci USA 99 15669 15674
86. WarkeRVXhajaKMartinKJFournierMFShawSK 2003 Dengue virus induces novel changes in gene expression of human umbilical vein endothelial cells. J Virol 77 11822 11832
87. BosworthBTMacLachlanNJJohnstonMI 1989 Induction of the 2-5A system by interferon and transmissible gastroenteritis virus. J Interferon Res 9 731 739
88. SchneiderRJMohrI 2003 Translation initiation and viral tricks. Trends Biochem Sci 28 130 136
89. HersheyJW 1991 Translational control in mammalian cells. Annu Rev Biochem 60 717 755
90. BrostromCOBrostromMA 1998 Regulation of translational initiation during cellular responses to stress. Prog Nucleic Acid Res Mol Biol 58 79 125
91. KaufmanRJ 1999 Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 13 1211 1233
92. ProudCG 2005 eIF2 and the control of cell physiology. Semin Cell Dev Biol 16 3 12
93. ScheunerDPatelRWangFLeeKKumarK 2006 Double-stranded RNA-dependent protein kinase phosphorylation of the alpha-subunit of eukaryotic translation initiation factor 2 mediates apoptosis. J Biol Chem 281 21458 21468
94. NovoaIZengHHardingHPRonD 2001 Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol 153 1011 1022
95. MeursEChongKGalabruJThomasNSKerrIM 1990 Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62 379 390
96. IrelandDDStohlmanSAHintonDRKapilPSilvermanRH 2009 RNase L mediated protection from virus induced demyelination. PLoS Pathog 5 e1000602
97. SchroderMKaufmanRJ 2005 The mammalian unfolded protein response. Annu Rev Biochem 74 739 789
98. HardingHPZhangYRonD 1999 Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397 271 274
99. ShiYVattemKMSoodRAnJLiangJ 1998 Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol Cell Biol 18 7499 7509
100. LuoSBaumeisterPYangSAbcouwerSFLeeAS 2003 Induction of Grp78/BiP by translational block: activation of the Grp78 promoter by ATF4 through and upstream ATF/CRE site independent of the endoplasmic reticulum stress elements. J Biol Chem 278 37375 37385
101. LeeAS 2001 The glucose-regulated proteins: stress induction and clinical applications. Trends Biochem Sci 26 504 510
102. HeBGrossMRoizmanB 1997 The gamma(1)34.5 protein of herpes simplex virus 1 complexes with protein phosphatase 1alpha to dephosphorylate the alpha subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc Natl Acad Sci USA 94 843 848
103. CohenPT 2002 Protein phosphatase 1–targeted in many directions. J Cell Sci 115 241 256
104. AggenJBNairnACChamberlinR 2000 Regulation of protein phosphatase-1. Chem Biol 7 R13 23
105. GouldCMDiellaFViaAPuntervollPGemundC 2010 ELM: the status of the 2010 eukaryotic linear motif resource. Nucleic Acids Res 38 1 14
106. PuntervollPLindingRGemundCChabanis-DavidsonSMattingsdalM 2003 ELM server: A new resource for investigating short functional sites in modular eukaryotic proteins. Nucleic Acids Res 31 3625 3630
107. Hsieh-WilsonLCAllenPBWatanabeTNairnACGreengardP 1999 Characterization of the neuronal targeting protein spinophilin and its interactions with protein phosphatase-1. Biochemistry 38 4365 4373
108. SchillaceRVVoltzJWSimATShenolikarSScottJD 2001 Multiple interactions within the AKAP220 signaling complex contribute to protein phosphatase 1 regulation. J Biol Chem 276 12128 12134
109. AjuhPMBrowneGJHawkesNACohenPTRobertsSG 2000 Association of a protein phosphatase 1 activity with the human factor C1 (HCF) complex. Nucleic Acids Res 28 678 686
110. KazemiSPapadopoulouSLiSSuQWangS 2004 Control of alpha subunit of eukaryotic translation initiation factor 2 (eIF2 alpha) phosphorylation by the human papillomavirus type 18 E6 oncoprotein: implications for eIF2 alpha-dependent gene expression and cell death. Mol Cell Biol 24 3415 3429
111. RiveraJAbramsCHernaezBAlcazarAEscribanoJM 2007 The MyD116 African swine fever virus homologue interacts with the catalytic subunit of protein phosphatase 1 and activates its phosphatase activity. J Virol 81 2923 2929
112. BrushMHWeiserDCShenolikarS 2003 Growth arrest and DNA damage-inducible protein GADD34 targets protein phosphatase 1 alpha to the endoplasmic reticulum and promotes dephosphorylation of the alpha subunit of eukaryotic translation initiation factor 2. Mol Cell Biol 23 1292 1303
113. NovoaIZhangYZengHJungreisRHardingHP 2003 Stress-induced gene expression requires programmed recovery from translational repression. EMBO J 22 1180 1187
114. EnjuanesLVan der ZeijstBAM 1995 Molecular basis of transmissible gastroenteritis coronavirus epidemiology. SiddellSG The Coronaviridae New York Plenum Press 337 376
115. SaifLJWesleyRD 1992 Transmissible gastroenteritis. LemanADStrawBEMengelingWLD'AllaireSTaylorDJ Diseases of Swine 7th ed. Ames. Iowa Wolfe Publishing Ltd 362 386
116. GantierMPWilliamsBR 2007 The response of mammalian cells to double-stranded RNA. Cytokine Growth Factor Rev 18 363 371
117. SilvermanRH 1985 Functional analysis of 2-5A-dependent RNase and 2-5a using 2′,5′-oligoadenylate-cellulose. Anal Biochem 144 450 460
118. DerSDYangYLWeissmannCWilliamsBR 1997 A double-stranded RNA-activated protein kinase-dependent pathway mediating stress-induced apoptosis. Proc Natl Acad Sci U S A 94 3279 3283
119. ZhouAParanjapeJBrownTLNieHNaikS 1997 Interferon action and apoptosis are defective in mice devoid of 2′,5′-oligoadenylate-dependent RNase L. EMBO J 16 6355 6363
120. RuschLZhouASilvermanRH 2000 Caspase-dependent apoptosis by 2′,5′-oligoadenylate activation of RNase L is enhanced by IFN-beta. J Interferon Cytokine Res 20 1091 1100
121. KrahlingVSteinDASpiegelMWeberFMuhlbergerE 2009 Severe acute respiratory syndrome coronavirus triggers apoptosis via protein kinase R but is resistant to its antiviral activity. J Virol 83 2298 2309
122. Kopecky-BrombergSAMartinez-SobridoLFriemanMBaricRAPaleseP 2007 Severe acute respiratory syndrome coronavirus open reading frame (ORF) 3b, ORF 6, and nucleocapsid proteins function as interferon antagonists. J Virol 81 548 557
123. WatheletMGOrrMFriemanMBBaricRS 2007 Severe acute respiratory syndrome coronavirus evades antiviral signaling: role of nsp1 and rational design of an attenuated strain. J Virol 81 11620 11633
124. Garcia-SastreABironCA 2006 Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312 879 882
125. BantelHSchulze-OsthoffK 2003 Apoptosis in hepatitis C virus infection. Cell Death Differ 10 Suppl 1 S48 S58
126. DelmasBGelfiJSjöströmHNorenOLaudeH 1993 Further characterization of aminopeptidase-N as a receptor for coronaviruses. Adv Exp Med Biol 342 293 298
127. McClurkinAWNormanJO 1966 Studies on transmissible gastroenteritis of swine. II. Selected characteristics of a cytopathogenic virus common to five isolates from transmissible gastroenteritis. Can J Comp Med Vet Sci 30 190 198
128. PenzesZGonzalezJMCalvoEIzetaASmerdouC 2001 Complete genome sequence of transmissible gastroenteritis coronavirus PUR46-MAD clone and evolution of the purdue virus cluster. Virus Genes 23 105 118
129. AlmazanFGonzalezJMPenzesZIzetaACalvoE 2000 Engineering the largest RNA virus genome as an infectious bacterial artificial chromosome. Proc Natl Acad Sci USA 97 5516 5521
130. JimenezGCorreaIMelgosaMPBullidoMJEnjuanesL 1986 Critical epitopes in transmissible gastroenteritis virus neutralization. J Virol 60 131 139
131. ZuñigaSSolaIAlonsoSEnjuanesL 2004 Sequence motifs involved in the regulation of discontinuous coronavirus subgenomic RNA synthesis. J Virol 78 980 994
132. MorenoJLZunigaSEnjuanesLSolaI 2008 Identification of a coronavirus transcription enhancer. J Virol 82 3882 3893
133. Diaz-GuerraMRivasCEstebanM 1997 Inducible expression of the 2-5A synthetase/RNase L system results in inhibition of vaccinia virus replication. Virology 227 220 228
134. SambrookJRussellDW 2001 Molecular cloning: A laboratory manual. Cold Spring Harbor, New York Cold Spring Harbor Laboratory Press
135. NotredameCHigginsDGHeringaJ 2000 T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302 205 217
136. RostBYachdavGLiuJ 2004 The PredictProtein server. Nucleic Acids Res 32 W321 W326
137. BendtsenJDNielsenHvon HeijneGBrunakS 2004 Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 783 795
138. BlomNGammeltoftSBrunakS 1999 Sequence and structure-based prediction of eukaryotic protein phosphorylation sites. J Mol Biol 294 1351 1362
139. NakaiKHortonP 1999 PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem Sci 24 34 36
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 6
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
Najčítanejšie v tomto čísle
- High Affinity Nanobodies against the VSG Are Potent Trypanolytic Agents that Block Endocytosis
- Structural and Mechanistic Studies of Measles Virus Illuminate Paramyxovirus Entry
- Sporangiospore Size Dimorphism Is Linked to Virulence of
- The Binding of Triclosan to SmeT, the Repressor of the Multidrug Efflux Pump SmeDEF, Induces Antibiotic Resistance in