Non-template functions of viral RNA in picornavirus replication

Current Opinion in Virology

Volumn 1, Issue 5, 2011, Pages 339-346

  Ogram, Sushma A ^a   Flanegan, James B ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; RIBONUCLEOPROTEIN; VIRUS PROTEIN; VIRUS RNA;

ARTICLE; NONHUMAN; PICORNAVIRUS; POLIOMYELITIS VIRUS; PRIORITY JOURNAL; RNA ANALYSIS; RNA SEQUENCE; VIRUS GENOME; VIRUS REPLICATION;

EID: 81755165920     PISSN: 18796257     EISSN: 18796265     Source Type: Journal    
DOI: 10.1016/j.coviro.2011.09.005     Document Type: Review

References (72)

1. D.J. Barton, E.P. Black, and J.B. Flanegan Complete replication of poliovirus in vitro: preinitiation RNA replication complexes require soluble cellular factors for the synthesis of VPg-linked RNA J Virol 69 1995 5516 5527
2. D.J. Barton, and J.B. Flanegan Coupled translation and replication of poliovirus RNA in vitro: synthesis of functional 3D polymerase and infectious virus J Virol 67 1993 822 831
3. A. Molla, A.V. Paul, and E. Wimmer Cell-free, de novo synthesis of poliovirus Science 254 1991 1647 1651
4. S. Nagashima, J. Sasaki, and K. Taniguchi The 5′-terminal region of the Aichi virus genome encodes cis-acting replication elements required for positive- and negative-strand RNA synthesis J Virol 79 2005 6918 6931
5. N. Sharma, S.A. Ogram, B.J. Morasco, A. Spear, N.M. Chapman, and J.B. Flanegan Functional role of the 5′ terminal cloverleaf in Coxsackievirus RNA replication Virology 393 2009 238 249
6. M.J. van Ooij, D.A. Vogt, A. Paul, C. Castro, J. Kuijpers, F.J. van Kuppeveld, C.E. Cameron, E. Wimmer, R. Andino, and W.J. Melchers Structural and functional characterization of the Coxsackievirus B3 CRE(2C): role of CRE(2C) in negative- and positive-strand RNA synthesis J Gen Virol 87 2006 103 113
7. D.J. Barton, and J.B. Flanegan Synchronous replication of poliovirus RNA: initiation of negative-strand RNA synthesis requires the guanidine-inhibited activity of protein 2C J Virol 71 1997 8482 8489
8. J.E. Novak, and K. Kirkegaard Coupling between genome translation and replication in an RNA virus Genes Dev 8 1994 1726 1737
9. B.J. Morasco, N. Sharma, J. Parilla, and J.B. Flanegan Poliovirus cre(2C)-dependent synthesis of VPgpUpU is required for positive- but not negative-strand RNA synthesis J Virol 77 2003 5136 5144
10. D.J. Barton, B.J. O'Donnell, and J.B. Flanegan 5′ Cloverleaf in poliovirus RNA is a cis-acting replication element required for negative-strand synthesis EMBO J 20 2001 1439 1448
11. N. Sharma, B.J. O'Donnell, and J.B. Flanegan 3′-Terminal sequence in poliovirus negative-strand templates is the primary cis-acting element required for VPgpUpU-primed positive-strand initiation J Virol 79 2005 3565 3577
12. Y. Liu, E. Wimmer, and A.V. Paul Cis-acting RNA elements in human and animal plus-strand RNA viruses Biochim Biophys Acta 1789 2009 495 517
13. B.P. Steil, and D.J. Barton Cis-active RNA elements (CREs) and picornavirus RNA replication Virus Res 139 2009 240 252
14. R.F. Pettersson, J.B. Flanegan, J.K. Rose, and D. Baltimore 5′-Terminal nucleotide sequences of polio virus polyribosomal RNA and virion RNA are identical Nature 268 1977 270 272
15. 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
16. E. Wimmer Genome-linked proteins of viruses Cell 28 1982 199 201
17. N. Takeda, C.F. Yang, R.J. Kuhn, and E. Wimmer Uridylylation of the genome-linked protein of poliovirus in vitro is dependent upon an endogenous RNA template Virus Res 8 1987 193 204
18. H. Toyoda, C.F. Yang, N. Takeda, A. Nomoto, and E. Wimmer Analysis of RNA synthesis of type 1 poliovirus by using an in vitro molecular genetic approach J Virol 61 1987 2816 2822
19. K.L. McKnight, and S.M. Lemon The rhinovirus type 14 genome contains an internally located RNA structure that is required for viral replication RNA 4 1998 1569 1584
20. P.E. Lobert, N. Escriou, J. Ruelle, and T. Michiels A coding RNA sequence acts as a replication signal in cardioviruses Proc Natl Acad Sci U S A 96 1999 11560 11565
21. E. Rieder, A.V. Paul, D.W. Kim, J.H. van Boom, and E. Wimmer Genetic and biochemical studies of poliovirus cis-acting replication element cre in relation to VPg uridylylation J Virol 74 2000 10371 10380
22. I. Goodfellow, Y. Chaudhry, A. Richardson, J. Meredith, J.W. Almond, W. Barclay, and D.J. Evans Identification of a cis-acting replication element within the poliovirus coding region J Virol 74 2000 4590 4600
23. 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
24. K. Gerber, E. Wimmer, and A.V. Paul Biochemical and genetic studies of the initiation of human rhinovirus 2 RNA replication: identification of a cis-replicating element in the coding sequence of 2A(pro) J Virol 75 2001 10979 10990
25. P.W. Mason, S.V. Bezborodova, and T.M. Henry Identification and characterization of a cis-acting replication element (cre) adjacent to the internal ribosome entry site of foot-and-mouth disease virus J Virol 76 2002 9686 9694
26. I.G. Goodfellow, C. Polacek, R. Andino, and D.J. Evans The poliovirus 2C cis-acting replication element-mediated uridylylation of VPg is not required for synthesis of negative-sense genomes J Gen Virol 84 2003 2359 2363
27. J. Yin, A.V. Paul, E. Wimmer, and E. Rieder Functional dissection of a poliovirus cis-acting replication element [PV-cre(2C)]: analysis of single- and dual-cre viral genomes and proteins that bind specifically to PV-cre RNA J Virol 77 2003 5152 5166
28. A.V. Paul, J. Yin, J. Mugavero, E. Rieder, Y. Liu, and E. Wimmer A 'slide-back' mechanism for the initiation of protein-primed RNA synthesis by the RNA polymerase of poliovirus J Biol Chem 278 2003 43951 43960
29. V. Thiviyanathan, Y. Yang, K. Kaluarachchi, R. Rijnbrand, D.G. Gorenstein, and S.M. Lemon High-resolution structure of a picornaviral internal cis-acting RNA replication element (cre) Proc Natl Acad Sci U S A 101 2004 12688 12693
30. Y. Yang, R. Rijnbrand, K.L. McKnight, E. Wimmer, A. Paul, A. Martin, and S.M. Lemon Sequence requirements for viral RNA replication and VPg uridylylation directed by the internal cis-acting replication element (cre) of human rhinovirus type 14 J Virol 76 2002 7485 7494
31. 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
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. H.B. Pathak, S.K. Ghosh, A.W. Roberts, S.D. Sharma, J.D. Yoder, J.J. Arnold, D.W. Gohara, D.J. Barton, A.V. Paul, and C.E. Cameron Structure-function relationships of the RNA-dependent RNA polymerase from poliovirus (3Dpol). A surface of the primary oligomerization domain functions in capsid precursor processing and VPg uridylylation J Biol Chem 277 2002 31551 31562
34. 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
35. M. Shen, Q. Wang, Y. Yang, H.B. Pathak, J.J. Arnold, C. Castro, S.M. Lemon, and C.E. Cameron Human rhinovirus type 14 gain-of-function mutants for oriI utilization define residues of 3C(D) and 3Dpol that contribute to assembly and stability of the picornavirus VPg uridylylation complex J Virol 81 2007 12485 12495
36. 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
37. Y. Yang, R. Rijnbrand, S. Watowich, and S.M. Lemon Genetic evidence for an interaction between a picornaviral cis-acting RNA replication element and 3CD protein J Biol Chem 279 2004 12659 12667
38. T. Lyons, K.E. Murray, A.W. Roberts, and D.J. Barton Poliovirus 5′-terminal cloverleaf RNA is required in cis for VPg uridylylation and the initiation of negative-strand RNA synthesis J Virol 75 2001 10696 10708
39. H. Toyoda, D. Franco, K. Fujita, A.V. Paul, and E. Wimmer Replication of poliovirus requires binding of the poly(rC) binding protein to the cloverleaf as well as to the adjacent C-rich spacer sequence between the cloverleaf and the internal ribosomal entry site J Virol 81 2007 10017 10028
40. R. Andino, G.E. Rieckhof, and D. Baltimore A functional ribonucleoprotein complex forms around the 5′ end of poliovirus RNA Cell 63 1990 369 380
41. 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
42. T.B. Parsley, J.S. Towner, L.B. Blyn, E. Ehrenfeld, and B.L. Semler Poly (rC) binding protein 2 forms a ternary complex with the 5′-terminal sequences of poliovirus RNA and the viral 3CD proteinase RNA 3 1997 1124 1134
43. E.V. Pilipenko, S.V. Maslova, A.N. Sinyakov, and V.I. Agol Towards identification of cis-acting elements involved in the replication of enterovirus and rhinovirus RNAs: a proposal for the existence of tRNA-like terminal structures Nucleic Acids Res 20 1992 1739 1745
44. H. Duque, and A.C. Palmenberg Phenotypic characterization of three phylogenetically conserved stem-loop motifs in the mengovirus 3′ untranslated region J Virol 75 2001 3111 3120
45. M. Saiz, S. Gomez, E. Martinez-Salas, and F. Sobrino Deletion or substitution of the aphthovirus 3′ NCR abrogates infectivity and virus replication J Gen Virol 82 2001 93 101
46. J. Zoll, H.A. Heus, F.J. van Kuppeveld, and W.J. Melchers The structure-function relationship of the enterovirus 3′-UTR Virus Res 139 2009 209 216
47. W.J.G. Melchers, J.G.J. Hoenderop, H.J. Bruins Slot, C.W.A. Pleij, E.V. Pilipenko, V.I. Agol, and J.M.D. Galama Kissing of the two predominant hairpin loops in the Coxsackie B virus 3′ untranslated region is the essential structural feature of the origin of replication required for negative-strand RNA synthesis J Virol 71 1997 686 696
48. E.V. Pilipenko, K. Poperechny, S.V. Maslova, W.J.G. Melchers, H.J. Bruins Slot, and V.I. Agol Cis-element, oriR, involved in the initiation of (-) strand poliovirus RNA: a quasi-globular multi-domain RNA structure maintained by tertiary ('kissing') interactions EMBO J 15 1996 5428 5436
49. M.H. Mirmomeni, P.J. Hughes, and G. Stanway An RNA tertiary structure in the 3′ untranslated region of enteroviruses is necessary for efficient replication J Virol 71 1997 2363 2370
50. B.P. Steil, and D.J. Barton Conversion of VPg into VPgpUpUOH before and during poliovirus negative-strand RNA synthesis J Virol 83 2009 12660 12670
51. D.M. Brown, C.T. Cornell, G.P. Tran, J.H. Nguyen, and B.L. Semler An authentic 3′ noncoding region is necessary for efficient poliovirus replication J Virol 79 2005 11962 11973
52. S. Todd, J.S. Towner, D.M. Brown, and B.L. Semler Replication-competent picornaviruses with complete genomic RNA 3′ noncoding region deletions J Virol 71 1997 8868 8874
53. S. Waggoner, and P. Sarnow Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirus-infected cells J Virol 72 1998 6699 6709
54. pro with the 5′ and 3′ termini of the poliovirus genome: Identification of viral and cellular cofactors needed for efficient binding J Biol Chem 269 1994 27004 27014
55. D.H. Spector, and D. Baltimore Requirement of 3′-terminal poly(adenylic acid) for the infectivity of poliovirus RNA Proc Natl Acad Sci U S A 71 1974 2983 2987
56. P. Sarnow Role of 3′-end sequences in infectivity of poliovirus transcripts made in vitro J Virol 63 1989 467 470
57. L.S. Silvestri, J.M. Parilla, B.J. Morasco, S.A. Ogram, and J.B. Flanegan Relationship between poliovirus negative-strand RNA synthesis and the length of the 3′ poly(A) tail Virology 345 2006 509 519
58. J. Herold, and R. Andino Poliovirus RNA replication requires genome circularization through a protein-protein bridge Mol Cell 7 2001 581 591
59. B.P. Steil, and D.J. Barton Poliovirus cis-acting replication element-dependent VPg uridylylation lowers the Km of the initiating nucleoside triphosphate for viral RNA replication J Virol 82 2008 9400 9408
60. B.P. Steil, B.J. Kempf, and D.J. Barton Poly(A) at the 3′ end of positive-strand RNA and VPg-linked poly(U) at the 5′ end of negative-strand RNA are reciprocal templates during replication of poliovirus RNA J Virol 84 2010 2843 2858
61. A. Spear, N. Sharma, and J.B. Flanegan Protein-RNA tethering: the role of poly(C) binding protein 2 in poliovirus RNA replication Virology 374 2008 280 291
62. N.L. Teterina, D. Egger, K. Bienz, D.M. Brown, B.L. Semler, and E. Ehrenfeld Requirements for assembly of poliovirus replication complexes and negative-strand RNA synthesis J Virol 75 2001 3841 3850
63. A.V. Gamarnik, and R. Andino Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA RNA 3 1997 882 892
64. R. Zell, Y. Ihle, S. Seitz, U. Gundel, P. Wutzler, and M. Gorlach Poly(rC)-binding protein 2 interacts with the oligo(rC) tract of coxsackievirus B3 Biochem Biophys Res Commun 366 2008 917 921
65. K.E. Murray, and D.J. Barton Poliovirus CRE-dependent VPg uridylylation is required for positive-strand RNA synthesis but not for negative-strand RNA synthesis J Virol 77 2003 4739 4750
66. S. Crowder, and K. Kirkegaard Trans-dominant inhibition of RNA viral replication can slow growth of drug-resistant viruses Nat Genet 37 2005 701 709
67. S.A. Harmon, O.C. Richards, D.F. Summers, and E. Ehrenfeld The 5′-terminal nucleotides of hepatitis A virus RNA, but not poliovirus RNA, are required for infectivity J Virol 65 1991 2757 2760
68. W.M. Klump, I. Bergmann, B.C. M:uller, D. Ameis, and R. Kandolf Complete nucleotide sequence of infectious Coxsackievirus B3 cDNA: two initial 5′ uridine residues are regained during plus-strand RNA synthesis J Virol 64 1990 1573 1583
69. J.E. Brunner, J.H. Nguyen, H.H. Roehl, T.V. Ho, K.M. Swiderek, and B.L. Semler Functional interaction of heterogeneous nuclear ribonucleoprotein C with poliovirus RNA synthesis initiation complexes J Virol 79 2005 3254 3266
70. J.E. Brunner, K.J. Ertel, J.M. Rozovics, and B.L. Semler Delayed kinetics of poliovirus RNA synthesis in a human cell line with reduced levels of hnRNP C proteins Virology 400 2010 240 247
71. K.J. Ertel, J.E. Brunner, and B.L. Semler Mechanistic consequences of hnRNP C binding to both RNA termini of poliovirus negative-strand RNA intermediates J Virol 84 2010 4229 4242
72. D.A. Vogt, and R. Andino An RNA element at the 5′-end of the poliovirus genome functions as a general promoter for RNA synthesis PLoS Pathog 6 2010 e1000936