Structures of the compact helical core domains of feline calicivirus and murine norovirus VPg proteins

Journal of Virology

Volumn 87, Issue 10, 2013, Pages 5318-5330

  Leen, Eoin N ^a   Rex Kwok, K Y ^a   Birtley, James R ^a,e   Simpson, Peter J ^a   Subba Reddy, Chennareddy V ^d   Chaudhry, Yasmin ^a,h   Sosnovtsev, Stanislav V ^c   Green, Kim Y ^c   Prater, Sean N ^a,f   Tong, Michael ^a,g   Young, Joanna C ^a   Chung, Liliane M W ^a   Marchant, Jan ^a   Roberts, Lisa O ^b   Kao, C Cheng ^d   Matthews, Stephen ^a   Goodfellow, Ian G ^a,h   Curry, Stephen ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF SURREY   (United Kingdom)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d INDIANA UNIVERSITY   (United States)

^e UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

^g STONY BROOK UNIVERSITY   (United States)

^h UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 5; TYROSINE; UNCLASSIFIED DRUG; VIRAL NS7 POLYMERASE; VIRUS ENZYME;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHEMICAL MODIFICATION; COMPACT HELICAL CORE DOMAIN; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA FLANKING REGION; ENZYME ACTIVE SITE; HYDROPHOBICITY; NONHUMAN; NOROVIRUS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; NUCLEOTIDYLATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RNA REPLICATION; SITE DIRECTED MUTAGENESIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; VESIVIRUS; VIRUS INFECTIVITY;

ANIMALS; CALICIVIRUS, FELINE; MAGNETIC RESONANCE SPECTROSCOPY; MODELS, MOLECULAR; NOROVIRUS; PROTEIN CONFORMATION; VIRAL PROTEINS;

EID: 84877343659     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03151-12     Document Type: Article

References (75)

1. Radford AD, Coyne KP, Dawson S, Porter CJ, Gaskell RM. 2007. Feline calicivirus. Vet. Res. 38:319-335.
2. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. 2008. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg. Infect. Dis. 14:1224-1231.
3. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17:7-15.
4. Cheetham S, Souza M, Meulia T, Grimes S, Han MG, Saif LJ. 2006. Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J. Virol. 80:10372-10381.
5. Jung K, Wang Q, Kim Y, Scheuer K, Zhang Z, Shen Q, Chang K-O, Saif LJ. 2012. The effects of simvastatin or interferon- on infectivity of human norovirus using a gnotobiotic pig model for the study of antivirals. PLoS One 7:e41619. doi:10.1371/journal.pone.0041619.
6. Vashist S, Bailey D, Putics A, Goodfellow I. 2009. Model systems for the study of human norovirus biology. Future Virol. 4:353-367.
7. Chaudhry Y, Skinner MA, Goodfellow IG. 2007. Recovery of genetically defined murine norovirus in tissue culture by using a fowlpox virus expressing T7 RNA polymerase. J. Gen. Virol. 88:2091-2100.
8. Sosnovtsev S, Green KY. 1995. RNA transcripts derived from a cloned full-length copy of the feline calicivirus genome do not require VpG for infectivity. Virology 210:383-390.
9. Ward VK, McCormick CJ, Clarke IN, Salim O, Wobus CE, Thackray LB, Virgin HW, IV, Lambden PR. 2007. Recovery of infectious murine norovirus using pol II-driven expression of full-length cDNA. Proc. Natl. Acad. Sci. U. S. A. 104:11050-11055.
10. Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV, Belliot G, Krug A, Mackenzie JM, Green KY, Virgin HW. 2004. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2:e432. doi:10.1371/journal.pbio.0020432.
11. Yunus MA, Chung LM, Chaudhry Y, Bailey D, Goodfellow I. 2010. Development of an optimized RNA-based murine norovirus reverse genetics system. J. Virol. Methods 169:112-118.
12. Kahan SM, Liu G, Reinhard MK, Hsu CC, Livingston RS, Karst SM. 2011. Comparative murine norovirus studies reveal a lack of correlation between intestinal virus titers and enteric pathology. Virology 421:202- 210.
13. Karst SM, Wobus CE, Lay M, Davidson J, Virgin HW, IV. 2003. STAT1-dependent innate immunity to a Norwalk-like virus. Science. 299: 1575-1578.
14. McFadden N, Bailey D, Carrara G, Benson A, Chaudhry Y, Shortland A, Heeney J, Yarovinsky F, Simmonds P, Macdonald A, Goodfellow I. 2011. Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog. 7:e1002413. doi:10.1371/journal.ppat.1002413.
15. Belliot G, Sosnovtsev SV, Mitra T, Hammer C, Garfield M, Green KY. 2003. In vitro proteolytic processing of the MD145 norovirus ORF1 nonstructural polyprotein yields stable precursors and products similar to those detected in calicivirus-infected cells. J. Virol. 77:10957-10974.
16. Blakeney SJ, Cahill A, Reilly PA. 2003. Processing of Norwalk virus nonstructural proteins by a 3C-like cysteine proteinase. Virology 308: 216-224.
17. Liu B, Clarke IN, Lambden PR. 1996. Polyprotein processing in Southampton virus: identification of 3C-like protease cleavage sites by in vitro mutagenesis. J. Virol. 70:2605-2610.
18. Sosnovtsev SV, Belliot G, Chang KO, Prikhodko VG, Thackray LB, Wobus CE, Karst SM, Virgin HW, Green KY. 2006. Cleavage map and proteolytic processing of the murine norovirus nonstructural polyprotein in infected cells. J. Virol. 80:7816-7831.
19. Ettayebi K, Hardy ME. 2003. Norwalk virus nonstructural protein p48 forms a complex with the SNARE regulator VAP-A and prevents cell surface expression of vesicular stomatitis virus G protein. J. Virol. 77:11790- 11797.
20. Nakamura K, Someya Y, Kumasaka T, Ueno G, Yamamoto M, Sato T, Takeda N, Miyamura T, Tanaka N. 2005. A norovirus protease structure provides insights into active and substrate binding site integrity. J. Virol. 79:13685-13693.
21. Ng KK, Cherney MM, Vazquez AL, Machin A, Alonso JM, Parra F, James MN. 2002. Crystal structures of active and inactive conformations of a caliciviral RNA-dependent RNA polymerase. J. Biol. Chem. 277: 1381-1387.
22. Pfister T, Wimmer E. 2001. Polypeptide p41 of a Norwalk-like virus is a nucleic acid-independent nucleoside triphosphatase. J. Virol. 75:1611- 1619.
23. Sharp TM, Guix S, Katayama K, Crawford SE, Estes MK. 2010. Inhibition of cellular protein secretion by Norwalk virus nonstructural protein p22 requires a mimic of an endoplasmic reticulum export signal. PLoS One 5:e13130. doi:10.1371/journal.pone.0013130.
24. Burroughs JN, Brown F. 1978. Presence of a covalently linked protein on calicivirus RNA. J. Gen. Virol. 41:443- 446.
25. Herbert TP, Brierley I, Brown TD. 1997. Identification of a protein linked to the genomic and subgenomic mRNAs of feline calicivirus and its role in translation. J. Gen. Virol. 78(Part 5):1033-1040.
26. Schaffer FL, Ehresmann DW, Fretz MK, Soergel MI. 1980. A protein, VPg, covalently linked to 36S calicivirus RNA. J. Gen. Virol. 47:215-220.
27. Daubert SD, Bruening G, Najarian RC. 1978. Protein bound to the genome RNAs of cowpea mosaic virus. Eur. J. Biochem. 92:45-51.
28. Fuentes C, Bosch A, Pinto RM, Guix S. 2012. Identification of human astrovirus genome-linked protein (VPg) essential for viral infectivity. J. Virol. 86:10070-10078.
29. Harding NE, Ito J, David GS. 1978. Identification of the protein firmly bound to the ends of bacteriophage phi 29 DNA. Virology 84:279-292.
30. Lee YF, Nomoto A, Detjen BM, Wimmer E. 1977. A protein covalently linked to poliovirus genome RNA. Proc. Natl. Acad. Sci. U. S. A. 74: 59-63.
31. Mayo MA, Barker H, Harrison BD. 1979. Evidence for a protein covalently linked to tobacco ringspot virus-RNA. J. Gen. Virol. 43:735-740.
32. Rekosh DM, Russell WC, Bellet AJ, Robinson AJ. 1977. Identification of a protein linked to the ends of adenovirus DNA. Cell 11:283-295.
33. Salas M, Mellado RP, Vinuela E. 1978. Characterization of a protein covalently linked to the 5= termini of the DNA of Bacillus subtilis phage phi29. J. Mol. Biol. 119:269-291.
34. Siaw MF, Shahabuddin M, Ballard S, Shaw JG, Rhoads RE. 1985. Identification of a protein covalently linked to the 5= terminus of tobacco vein mottling virus RNA. Virology 142:134-143.
35. Chaudhry Y, Nayak A, Bordeleau ME, Tanaka J, Pelletier J, Belsham GJ, Roberts LO, Goodfellow IG. 2006. Caliciviruses differ in their functional requirements for eIF4F components. J. Biol. Chem. 281:25315-25325.
36. Goodfellow I, Chaudhry Y, Gioldasi I, Gerondopoulos A, Natoni A, Labrie L, Laliberte JF, Roberts L. 2005. Calicivirus translation initiation requires an interaction between VPg and eIF 4 E. EMBO Rep. 6:968-972.
37. Daughenbaugh KF, Fraser CS, Hershey JW, Hardy ME. 2003. The genome-linked protein VPg of the Norwalk virus binds eIF3, suggesting its role in translation initiation complex recruitment. EMBO J. 22:2852- 2859.
38. Leonard S, Chisholm J, Laliberte JF, Sanfacon H. 2002. Interaction in vitro between the proteinase of Tomato ringspot virus (genus Nepovirus) and the eukaryotic translation initiation factor iso4E from Arabidopsis thaliana. J. Gen. Virol. 83:2085-2089.
39. Leonard S, Plante D, Wittmann S, Daigneault N, Fortin MG, Laliberte JF. 2000. Complex formation between potyvirus VPg and translation eukaryotic initiation factor 4E correlates with virus infectivity. J. Virol. 74: 7730-7737.
40. Leonard S, Viel C, Beauchemin C, Daigneault N, Fortin MG, Laliberte JF. 2004. Interaction of VPg-Pro of turnip mosaic virus with the transla-tion initiation factor 4E and the poly(A)-binding protein in planta. J. Gen. Virol. 85:1055-1063.
41. Wittmann S, Chatel H, Fortin MG, Laliberte JF. 1997. Interaction of the viral protein genome linked of turnip mosaic potyvirus with the translational eukaryotic initiation factor (iso) 4E of Arabidopsis thaliana using the yeast two-hybrid system. Virology 234:84-92.
42. Velazquez-Moctezuma R, Banos-Lara MdR, Acevedo Y, Mendez E. 2012. Alternative cell lines to improve the rescue of infectious human astrovirus from a cDNA clone. J. Virol. Methods 179:295-302.
43. Belliot G, Sosnovtsev SV, Chang KO, McPhie P, Green KY. 2008. Nucleotidylylation of the VPg protein of a human norovirus by its proteinase-polymerase precursor protein. Virology 374:33- 49.
44. Mitra T, Sosnovtsev SV, Green KY. 2004. Mutagenesis of tyrosine 24 in the VPg protein is lethal for feline calicivirus. J. Virol. 78:4931- 4935.
45. Subba-Reddy CV, Goodfellow I, Kao CC. 2011. VPg-primed RNA synthesis of norovirus RNA-dependent RNA polymerases by using a novel cell-based assay. J. Virol. 85:13027-13037.
46. Rohayem J, Robel I, Jager K, Scheffler U, Rudolph W. 2006. Proteinprimed and de novo initiation of RNA synthesis by norovirus 3Dpol. J. Virol. 80:7060-7069.
47. Kaiser WJ, Chaudhry Y, Sosnovtsev SV, Goodfellow IG. 2006. Analysis of protein-protein interactions in the feline calicivirus replication complex. J. Gen. Virol. 87:363-368.
48. Schein CH, Oezguen N, van der Heden van Noort GJ, Filippov DV, Paul A, Kumar E, Braun W. 2010. NMR solution structure of poliovirus uridylyated peptide linked to the genome (VPgpU). Peptides 31:1441- 1448.
49. Schein CH, Oezguen N, Volk DE, Garimella R, Paul A, Braun W. 2006. NMR structure of the viral peptide linked to the genome (VPg) of poliovirus. Peptides 27:1676-1684.
50. Ferrer-Orta C, Arias A, Perez-Luque R, Escarmis C, Domingo E, Verdaguer N. 2004. Structure of foot-and-mouth disease virus RNAdependent RNA polymerase and its complex with a template-primer RNA. J. Biol. Chem. 279:47212- 47221.
51. Hebrard E, Bessin Y, Michon T, Longhi S, Uversky VN, Delalande F, Van Dorsselaer A, Romero P, Walter J, Declerck N, Fargette D. 2009. Intrinsic disorder in viral proteins genome-linked: experimental and predictive analyses. Virol. J. 6:23.
52. Grzela R, Szolajska E, Ebel C, Madern D, Favier A, Wojtal I, Zagorski W, Chroboczek J. 2008. Virulence factor of potato virus Y, genomeattached terminal protein VPg, is a highly disordered protein. J. Biol. Chem. 283:213-221.
53. Rantalainen KI, Eskelin K, Tompa P, Makinen K. 2011. Structural flexibility allows the functional diversity of potyvirus genome-linked protein VPg. J. Virol. 85:2449-2457.
54. Rantalainen KI, Uversky VN, Permi P, Kalkkinen N, Dunker AK, Makinen K. 2008. Potato virus A genome-linked protein VPg is an intrinsically disordered molten globule-like protein with a hydrophobic core. Virology 377:280-288.
55. Jiang J, Laliberté J-F. 2011. The genome-linked protein VPg of plant viruses-a protein with many partners. Curr. Opin. Virol. 1:347-354.
56. Zou P, Gautel M, Geerlof A, Wilmanns M, Koch MH, Svergun DI. 2003. Solution scattering suggests cross-linking function of telethonin in the complex with titin. J. Biol. Chem. 278:2636-2644.
57. Bertani G. 2004. Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J. Bacteriol. 186:595- 600.
58. Marchant J, Sawmynaden K, Saouros S, Simpson P, Matthews S. 2008. Complete resonance assignment of the first and second apple domains of MIC4 from Toxoplasma gondii, using a new NMRView-based assignment aid. Biomol. NMR Assign. 2:119-121.
59. Jung YS, Zweckstetter M. 2004. Mars-robust automatic backbone assignment of proteins. J. Biomol. NMR 30:11-23.
60. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. 1998. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D. 54:905-921.
61. Linge JP, Williams MA, Spronk CAEM, Bonvin AMJJ, Nilges M. 2003. Refinement of protein structures in explicit solvent. Proteins 50:496-506.
62. Rieping W, Habeck M, Bardiaux B, Bernard A, Malliavin TE, Nilges M. 2007. ARIA2: automated NOE assignment and data integration in NMR structure calculation. Bioinformatics 23:381-382.
63. Shen Y, Delaglio F, Cornilescu G, Bax A. 2009. TALOS plus: a hybrid method for predicting protein backbone torsion angles fromNMRchemical shifts. J. Biomol. NMR 44:213-223.
64. Bhattacharya A, Tejero R, Montelione GT. 2007. Evaluating protein structures determined by structural genomics consortia. Proteins 66:778- 795.
65. Sosnovtsev SV, Garfield M, Green KY. 2002. Processing map and essential cleavage sites of the nonstructural polyprotein encoded by ORF1 of the feline calicivirus genome. J. Virol. 76:7060-7072.
66. Ohnishi M, Urry DW. 1969. Temperature dependence of amide proton chemical shifts: the secondary structures of gramicidin S and valinomycin. Biochem. Biophys. Res. Commun. 36:194-202.
67. Lee JH, Alam I, Han KR, Cho S, Shin S, Kang S, Yang JM, Kim KH. 2011. Crystal structures of murine norovirus-1 RNA-dependent RNA polymerase. J. Gen. Virol. 92:1607-1616.
68. Ng KK, Pendas-Franco N, Rojo J, Boga JA, Machin A, Alonso JM, Parra F. 2004. Crystal structure of Norwalk virus polymerase reveals the carboxyl terminus in the active site cleft. J. Biol. Chem. 279:16638-16645.
69. Zamyatkin DF, Parra F, Alonso JM, Harki DA, Peterson BR, Grochulski P, Ng KK. 2008. Structural insights into mechanisms of catalysis and inhibition in Norwalk virus polymerase. J. Biol. Chem. 283:7705-7712.
70. Han KR, Choi Y, Min BS, Jeong H, Cheon D, Kim J, Jee Y, Shin S, Yang JM. 2010. Murine norovirus-1 3Dpol exhibits RNA-dependent RNA polymerase activity and nucleotidylylates on Tyr of the VPg. J. Gen. Virol. 91:1713-1722.
71. Subba-Reddy CV, Yunus MA, Goodfellow IG, Kao CC. 2012. Norovirus RNA synthesis is modulated by an interaction between the viral RNAdependent RNA polymerase and the major capsid protein, VP1. J. Virol. 86:10138-10149.
72. Goodfellow I. 2011. The genome-linked protein VPg of vertebrate viruses- a multifaceted protein. Curr. Opin. Virol. 1:355-362.
73. Eskelin K, Hafrén A, Rantalainen KI, Mäkinen K. 2011. Potyviral VPg enhances viralRNAtranslation and inhibits reportermRNAtranslation in planta. J. Virol. 85:9210-9221.
74. Dunham DM, Jiang X, Berke T, Smith AW, Matson DO. 1998. Genomic mapping of a calicivirus VPg. Arch. Virol. 143:2421-2430.
75. Ferrer-Orta C, Arias A, Agudo R, Pérez-Luque R, Escarmís C, Domingo E, Verdaguer N. 2006. The structure of a protein primer-polymerase complex in the initiation of genome replication. EMBO J. 25:880-888.