Formation and working mechanism of the picornavirus VPg uridylylation complex

Current Opinion in Virology

Volumn 9, Issue , 2014, Pages 24-30

  Sun, Yuna ^a,b   Guo, Yu ^c   Lou, Zhiyong ^b,d,e  

^a INSTITUTE OF BIOPHYSICS   (China)

^b Tsinghua University   (China)

^c NANKAI UNIVERSITY   (China)

^d TSINGHUA UNIVERSITY   (China)

^e SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

URIDINE PHOSPHATE; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; BINDING SITE; COMPLEX FORMATION; GENETIC VARIABILITY; NONHUMAN; OPEN READING FRAME; PICORNAVIRUS; URIDYLYLATION COMPLEX; VIRUS GENOME; VIRUS REPLICATION; BIOSYNTHESIS; METABOLISM; PHYSIOLOGY; PICORNAVIRIDAE; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING;

PICORNAVIRIDAE; PROTEIN MULTIMERIZATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, VIRAL; URIDINE MONOPHOSPHATE; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84907920692     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2014.09.003     Document Type: Review

References (55)

1. J.B. Flanegan, R.F. Petterson, V. Ambros, N.J. Hewlett, and D. Baltimore Covalent linkage of a protein to a defined nucleotide sequence at the 5′-terminus of virion and replicative intermediate RNAs of poliovirus Proc Natl Acad Sci U S A 74 1977 961 965
2. F.L. Schaffer, D.W. Ehresmann, M.K. Fretz, and M.I. Soergel A protein, VPg, covalently linked to 36S calicivirus RNA J Gen Virol 47 1980 215 220
3. Y.F. Lee, A. Nomoto, B.M. Detjen, and E. Wimmer A protein covalently linked to poliovirus genome RNA Proc Natl Acad Sci U S A 74 1977 59 63
4. A. Nomoto, B. Detjen, R. Pozzatti, and E. Wimmer The location of the polio genome protein in viral RNAs and its implication for RNA synthesis Nature 268 1977 208 213
5. A. Nomoto, N. Kitamura, F. Golini, and E. Wimmer The 5′-terminal structures of poliovirion RNA and poliovirus mRNA differ only in the genome-linked protein VPg Proc Natl Acad Sci U S A 74 1977 5345 5349
6. B. Al-Mutairy, J.E. Walter, A. Pothen, and D.K. Mitchell Genome prediction of putative genome-linked viral protein (VPg) of astroviruses Virus Genes 31 2005 21 30
7. I. Goodfellow The genome-linked protein VPg of vertebrate viruses - a multifaceted protein Curr Opin Virol 1 2011 355 362
8. I. Goodfellow, Y. Chaudhry, I. Gioldasi, A. Gerondopoulos, A. Natoni, L. Labrie, J.F. Laliberte, and L. Roberts Calicivirus translation initiation requires an interaction between VPg and eIF 4 E EMBO Rep 6 2005 968 972
9. Y. Chaudhry, M.A. Skinner, and I.G. Goodfellow Recovery of genetically defined murine norovirus in tissue culture by using a fowlpox virus expressing T7 RNA polymerase J Gen Virol 88 2007 2091 2100
10. W.J. Kaiser, Y. Chaudhry, S.V. Sosnovtsev, and I.G. Goodfellow Analysis of protein-protein interactions in the feline calicivirus replication complex J Gen Virol 87 2006 363 368
11. V. Ambros, R.F. Pettersson, and D. Baltimore An enzymatic activity in uninfected cells that cleaves the linkage between poliovirion RNA and the 5′ terminal protein Cell 15 1978 1439 1446
12. R. Virgen-Slane, J.M. Rozovics, K.D. Fitzgerald, T. Ngo, W. Chou, G.J. van der Heden van Noort, D.V. Filippov, P.D. Gershon, and B.L. Semler An RNA virus hijacks an incognito function of a DNA repair enzyme Proc Natl Acad Sci U S A 109 2012 14634 14639
13. J.N. Burroughs, and F. Brown Presence of a covalently linked protein on calicivirus RNA J Gen Virol 41 1978 443 446
14. S. van der Werf, J. Bradley, E. Wimmer, F.W. Studier, and J.J. Dunn Synthesis of infectious poliovirus RNA by purified T7 RNA polymerase Proc Natl Acad Sci U S A 83 1986 2330 2334
15. T.P. Herbert, I. Brierley, and T.D. Brown Identification of a protein linked to the genomic and subgenomic mRNAs of feline calicivirus and its role in translation J Gen Virol 78 Pt 5 1997 1033 1040
16. K.D. Fitzgerald, and B.L. Semler Bridging IRES elements in mRNAs to the eukaryotic translation apparatus Biochim Biophys Acta 1789 2009 518 528
17. A.M.Q. King, F. Brown, P. Christian, T. Hovi, and T. Hyypia Picornaviridae In Virus Taxonomy M.H.V. Van Regen-mortel, C.M. Fauquet, D.H.L. Bishop, C.H. Calisher, Seventh Report of the International Committee for the Taxonomy of Viruses 2000 657 673
18. P.C. McMinn An overview of the evolution of enterovirus 71 and its clinical and public health significance FEMS Microbiol Rev 26 2002 91 107
19. A.V. Gamarnik, and R. Andino Switch from translation to RNA replication in a positive-stranded RNA virus Genes Dev 12 1998 2293 2304
20. J. Pelletier, and N. Sonenberg Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA Nature 334 1988 320 325
21. B.I. Hillman, R. Foglia, and W. Yuan Satellite and defective RNAs of Cryphonectria hypovirus 3-grand haven 2, a virus species in the family Hypoviridae with a single open reading frame Virology 276 2000 181 189
22. H.B. Pathak, H.S. Oh, I.G. Goodfellow, J.J. Arnold, and C.E. Cameron Picornavirus genome replication: roles of precursor proteins and rate-limiting steps in oriI-dependent VPg uridylylation J Biol Chem 283 2008 30677 30688
23. M.A. Lawson, and B.L. Semler Alternate poliovirus nonstructural protein processing cascades generated by primary sites of 3C proteinase cleavage Virology 191 1992 309 320
24. J.J. DeStefano, and O. Titilope Poliovirus protein 3AB displays nucleic acid chaperone and helix-destabilizing activities J Virol 80 2006 1662 1671
25. S.J. Plotch, and O. Palant Poliovirus protein 3AB forms a complex with and stimulates the activity of the viral RNA polymerase, 3Dpol J Virol 69 1995 7169 7179
26. A.V. Paul, G.A. Belov, E. Ehrenfeld, and E. Wimmer Model of picornavirus RNA replication C.E. Cameron, M. Götte, K.D. Raney, Viral Genome Replication 1st edn 2009 Springer 3 23
27. A.V. Paul, J.H. van Boom, D. Filippov, and E. Wimmer Protein-primed RNA synthesis by purified poliovirus RNA polymerase Nature 393 1998 280 284
28. C. Chen, Y. Wang, C. Shan, Y. Sun, P. Xu, H. Zhou, C. Yang, P.Y. Shi, Z. Rao, and B. Zhang Crystal structure of enterovirus 71 RNA-dependent RNA polymerase complexed with its protein primer VPg: implication for a trans mechanism of VPg uridylylation J Virol 87 2013 5755 5768
29. Y. Sun, Y. Wang, C. Shan, C. Chen, P. Xu, M. Song, H. Zhou, C. Yang, W. Xu, and P.Y. Shi Enterovirus 71 VPg uridylation uses a two-molecular mechanism of 3D polymerase J Virol 86 2012 13662 13671
30. A.V. Paul, E. Rieder, D.W. Kim, J.H. van Boom, and E. Wimmer Identification of an RNA hairpin in poliovirus RNA that serves as the primary template in the in vitro uridylylation of VPg J Virol 74 2000 10359 10370
31. L. Tiley, A.M. King, and G.J. Belsham The foot-and-mouth disease virus cis-acting replication element (cre) can be complemented in trans within infected cells J Virol 77 2003 2243 2246
32. A. Nayak, I.G. Goodfellow, K.E. Woolaway, J. Birtley, S. Curry, and G.J. Belsham Role of RNA structure and RNA binding activity of foot-and-mouth disease virus 3C protein in VPg uridylylation and virus replication J Virol 80 2006 9865 9875
33. I.G. Goodfellow, D. Kerrigan, and D.J. Evans Structure and function analysis of the poliovirus cis-acting replication element (CRE) RNA 9 2003 124 137
34. B.P. Steil, and D.J. Barton Cis-active RNA elements (CREs) and picornavirus RNA replication Virus Res 139 2009 240 252
35. S. Cordey, D. Gerlach, T. Junier, E.M. Zdobnov, L. Kaiser, and C. Tapparel The cis-acting replication elements define human enterovirus and rhinovirus species Rna 14 2008 1568 1578
36. A. Nayak, I.G. Goodfellow, and G.J. Belsham Factors required for the uridylylation of the foot-and-mouth disease virus 3B1, 3B2, and 3B3 peptides by the RNA-dependent RNA polymerase (3Dpol) in vitro J Virol 79 2005 7698 7706
37. L.L. Marcotte, A.B. Wass, D.W. Gohara, H.B. Pathak, J.J. Arnold, D.J. Filman, C.E. Cameron, and J.M. Hogle Crystal structure of poliovirus 3CD protein: virally encoded protease and precursor to the RNA-dependent RNA polymerase J Virol 81 2007 3583 3596
38. J.M. Lyle, A. Clewell, K. Richmond, O.C. Richards, D.A. Hope, S.C. Schultz, and K. Kirkegaard Similar structural basis for membrane localization and protein priming by an RNA-dependent RNA polymerase J Biol Chem 277 2002 16324 16331
39. S.A. Ogram, C.D. Boone, R. McKenna, and J.B. Flanegan Amiloride inhibits the initiation of Coxsackievirus and poliovirus RNA replication by inhibiting VPg uridylylation Virology 464-465C 2014 87 97
40. C.E. Cameron, H.S. Oh, and I.M. Moustafa Expanding knowledge of P3 proteins in the poliovirus lifecycle Future Microbiol 5 2010 867 881
41. T.C. Appleby, H. Luecke, J.H. Shim, J.Z. Wu, I.W. Cheney, W. Zhong, L. Vogeley, Z. Hong, and N. Yao Crystal structure of complete rhinovirus RNA polymerase suggests front loading of protein primer J Virol 79 2005 277 288
42. C. Ferrer-Orta, A. Arias, R. Agudo, R. Perez-Luque, C. Escarmis, E. Domingo, and N. Verdaguer The structure of a protein primer-polymerase complex in the initiation of genome replication Embo J 25 2006 880 888
43. A. Gruez, B. Selisko, M. Roberts, G. Bricogne, C. Bussetta, I. Jabafi, B. Coutard, A.M. De Palma, J. Neyts, and B. Canard The crystal structure of coxsackievirus B3 RNA-dependent RNA polymerase in complex with its protein primer VPg confirms the existence of a second VPg binding site on Picornaviridae polymerases J Virol 82 2008 9577 9590
44. M. Shen, Z.J. Reitman, Y. Zhao, I. Moustafa, Q. Wang, J.J. Arnold, H.B. Pathak, and C.E. Cameron Picornavirus genome replication. Identification of the surface of the poliovirus (PV) 3C dimer that interacts with PV 3Dpol during VPg uridylylation and construction of a structural model for the PV 3C2-3Dpol complex J Biol Chem 283 2008 875 888
45. H.B. Pathak, J.J. Arnold, P.N. Wiegand, M.R. Hargittai, and C.E. Cameron Picornavirus genome replication: assembly and organization of the VPg uridylylation ribonucleoprotein (initiation) complex J Biol Chem 282 2007 16202 16213
46. J.M. Lyle, E. Bullitt, K. Bienz, and K. Kirkegaard Visualization and functional analysis of RNA-dependent RNA polymerase lattices Science 296 2002 2218 2222
47. J.L. Hansen, A.M. Long, and S.C. Schultz Structure of the RNA-dependent RNA polymerase of poliovirus Structure 5 1997 1109 1122
48. S.D. Hobson, E.S. Rosenblum, O.C. Richards, K. Richmond, K. Kirkegaard, and S.C. Schultz Oligomeric structures of poliovirus polymerase are important for function Embo J 20 2001 1153 1163
49. J. Wang, J.M. Lyle, and E. Bullitt Surface for catalysis by poliovirus RNA-dependent RNA polymerase J Mol Biol 425 2013 2529 2540
50. P. Gong, and O.B. Peersen Structural basis for active site closure by the poliovirus RNA-dependent RNA polymerase Proc Natl Acad Sci U S A 107 2010 22505 22510
51. R. Andino, G.E. Rieckhof, P.L. Achacoso, and D. Baltimore Poliovirus RNA synthesis utilizes an RNP complex formed around the 5′-end of viral RNA Embo J 12 1993 3587 3598
52. W. Xiang, K.S. Harris, L. Alexander, and E. Wimmer Interaction between the 5′-terminal cloverleaf and 3AB/3CDpro of poliovirus is essential for RNA replication J Virol 69 1995 3658 3667
53. J.K. Claridge, S.J. Headey, J.Y. Chow, M. Schwalbe, P.J. Edwards, C.M. Jeffries, H. Venugopal, J. Trewhella, and S.M. Pascal A picornaviral loop-to-loop replication complex J Struct Biol 166 2009 251 262
54. A. Totsuka, and Y. Moritsugu Hepatitis A virus proteins Intervirology 42 1999 63 68
55. Y. Wu, Z. Lou, Y. Miao, Y. Yu, H. Dong, W. Peng, M. Bartlam, X. Li, and Z. Rao Structures of EV71 RNA-dependent RNA polymerase in complex with substrate and analogue provide a drug target against the hand-foot-and-mouth disease pandemic in China Protein Cell 1 2010 491 500