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PMID: 25184560 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Review

Picornavirus morphogenesis.

Microbiology and molecular biology reviews : MMBR ·Vol. 78 ·No. 3 ·2014-09-00 ·Pages 418-37

Jiang P, Liu Y, Ma HC, Paul AV, Wimmer E

Abstract

The Picornaviridae represent a large family of small plus-strand RNA viruses that cause a bewildering array of important human and animal diseases. Morphogenesis is the least-understood step in the life cycle of these viruses, and this process is difficult to study because encapsidation is tightly coupled to genome translation and RNA replication. Although the basic steps of assembly have been known for some time, very few details are available about the mechanism and factors that regulate this process. Most of the information available has been derived from studies of enteroviruses, in particular poliovirus, where recent evidence has shown that, surprisingly, the specificity of encapsidation is governed by a viral protein-protein interaction that does not involve an RNA packaging signal. In this review, we make an attempt to summarize what is currently known about the following topics: (i) encapsidation intermediates, (ii) the specificity of encapsidation (iii), viral and cellular factors that are required for encapsidation, (iv) inhibitors of encapsidation, and (v) a model of enterovirus encapsidation. Finally, we compare some features of picornavirus morphogenesis with those of other plus-strand RNA viruses.

MeSH Terms
Animals Antiviral Agents/pharmacology Capsid/physiology,ultrastructure Genome, Viral Host-Pathogen Interactions Humans Morphogenesis Picornaviridae/drug effects,physiology,ultrastructure Picornaviridae Infections/virology RNA, Viral/physiology Virus Assembly
Chemicals
Antiviral Agents RNA, Viral
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Jiang Ping
Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, New York, USA.
Liu Ying
Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, New York, USA.
Ma Hsin-Chieh
Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, New York, USA.
Paul Aniko V
Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, New York, USA.
Wimmer Eckard
Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, New York, USA eckard.wimmer@stonybrook.edu.
References (196)
196 references, click to expand
  1. Myristoylation is important at multiple stages in poliovirus assembly.
    J Virol. 1991 May;65(5):2372-80 PMID: 1850017
  2. Mutations in the yellow fever virus nonstructural protein NS2A selectively block production of infectious particles.
    J Virol. 2002 May;76(10):4773-84 PMID: 11967294
  3. Genetics of poliovirus.
    Annu Rev Genet. 1993;27:353-436 PMID: 8122908
  4. Poliovirus 2C protein determinants of membrane binding and rearrangements in mammalian cells.
    J Virol. 1997 Dec;71(12):8962-72 PMID: 9371552
  5. Fine-tuning translation kinetics selection as the driving force of codon usage bias in the hepatitis A virus capsid.
    PLoS Pathog. 2010 Mar 05;6(3):e1000797 PMID: 20221432
  6. Subversion of cellular autophagosomal machinery by RNA viruses.
    PLoS Biol. 2005 May;3(5):e156 PMID: 15884975
  7. Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery.
    Exp Biol Med (Maywood). 2003 Feb;228(2):111-33 PMID: 12563018
  8. The changing faces of glutathione, a cellular protagonist.
    Biochem Pharmacol. 2003 Oct 15;66(8):1499-503 PMID: 14555227
  9. Antibiotic radicicol binds to the N-terminal domain of Hsp90 and shares important biologic activities with geldanamycin.
    Cell Stress Chaperones. 1998 Jun;3(2):100-8 PMID: 9672245
  10. The Src family kinase c-Yes is required for maturation of West Nile virus particles.
    J Virol. 2005 Sep;79(18):11943-51 PMID: 16140770
  11. Topology of double-membraned vesicles and the opportunity for non-lytic release of cytoplasm.
    Autophagy. 2005 Oct-Dec;1(3):182-4 PMID: 16874042
  12. Identification of domains in rubella virus genomic RNA and capsid protein necessary for specific interaction.
    J Virol. 1996 Apr;70(4):2184-90 PMID: 8642641
  13. Knockdown of autophagy-related gene decreases the production of infectious hepatitis C virus particles.
    Autophagy. 2009 Oct;5(7):937-45 PMID: 19625776
  14. Analysis of the cloverleaf element in a human rhinovirus type 14/poliovirus chimera: correlation of subdomain D structure, ternary protein complex formation and virus replication.
    J Gen Virol. 2003 Aug;84(Pt 8):2203-2216 PMID: 12867653
  15. Chemical cross-linking of proteins of Semliki Forest virus: virus particles and plasma membranes from BHK-21 cells treated with colchicine or dibucaine.
    J Virol. 1978 Oct;28(1):193-8 PMID: 702646
  16. The coronavirus E protein: assembly and beyond.
    Viruses. 2012 Mar;4(3):363-82 PMID: 22590676
  17. Differences between poliovirus empty capsids formed in vivo and those formed in vitro: a role for the morphopoietic factor.
    J Virol. 1981 Oct;40(1):173-83 PMID: 6270373
  18. The amino-terminal nine amino acid sequence of poliovirus capsid VP4 protein is sufficient to confer N-myristoylation and targeting to detergent-insoluble membranes.
    Biochemistry. 2000 Feb 8;39(5):1083-90 PMID: 10653654
  19. Picornavirus-receptor interactions.
    Trends Microbiol. 2002 Jul;10(7):324-31 PMID: 12110211
  20. Poliovirus mutants at histidine 195 of VP2 do not cleave VP0 into VP2 and VP4.
    J Virol. 1999 Nov;73(11):9072-9 PMID: 10516013
  21. Poliovirus single-stranded RNA and double-stranded RNA: differential infectivity in enucleate cells.
    J Virol. 1978 Sep;27(3):582-6 PMID: 212582
  22. Complete nucleotide sequence and genetic organization of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans.
    J Virol. 1998 Oct;72(10):8408-12 PMID: 9733894
  23. Complete protein linkage map between the P2 and P3 non-structural proteins of poliovirus.
    J Gen Virol. 2007 Aug;88(Pt 8):2259-2267 PMID: 17622630
  24. Processing determinants required for in vitro cleavage of the poliovirus P1 precursor to capsid proteins.
    J Virol. 1987 Oct;61(10):3181-9 PMID: 3041039
  25. Conservation of a packaging signal and the viral genome RNA packaging mechanism in alphavirus evolution.
    J Virol. 2011 Aug;85(16):8022-36 PMID: 21680508
  26. A novel coding-region RNA element modulates infectious dengue virus particle production in both mammalian and mosquito cells and regulates viral replication in Aedes aegypti mosquitoes.
    Virology. 2012 Oct 25;432(2):511-26 PMID: 22840606
  27. Functional analysis of the murine coronavirus genomic RNA packaging signal.
    J Virol. 2013 May;87(9):5182-92 PMID: 23449786
  28. Guanidine-selected mutants of poliovirus: mapping of point mutations to polypeptide 2C.
    J Virol. 1986 Feb;57(2):638-46 PMID: 3003395
  29. The structure of antiviral agents that inhibit uncoating when complexed with viral capsids.
    Antiviral Res. 1989 Feb;11(1):3-13 PMID: 2540708
  30. 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. 1996 Oct 1;15(19):5428-36 PMID: 8895586
  31. MAP-kinase regulated cytosolic phospholipase A2 activity is essential for production of infectious hepatitis C virus particles.
    PLoS Pathog. 2012;8(7):e1002829 PMID: 22911431
  32. Reticulon 3 binds the 2C protein of enterovirus 71 and is required for viral replication.
    J Biol Chem. 2007 Feb 23;282(8):5888-98 PMID: 17182608
  33. Identification of probable genomic packaging signal sequence from SARS-CoV genome by bioinformatics analysis.
    Acta Pharmacol Sin. 2003 Jun;24(6):489-96 PMID: 12791173
  34. Role of annexin A2 in the production of infectious hepatitis C virus particles.
    J Virol. 2010 Jun;84(11):5775-89 PMID: 20335258
  35. Coupling between replication and packaging of flavivirus RNA: evidence derived from the use of DNA-based full-length cDNA clones of Kunjin virus.
    J Virol. 2001 May;75(10):4633-40 PMID: 11312333
  36. Morphogenesis of hepatitis A virus: isolation and characterization of subviral particles.
    J Virol. 1990 Nov;64(11):5284-9 PMID: 2170672
  37. Hepatitis C virus (HCV) induces formation of stress granules whose proteins regulate HCV RNA replication and virus assembly and egress.
    J Virol. 2012 Oct;86(20):11043-56 PMID: 22855484
  38. Poliovirus protein 2C contains two regions involved in RNA binding activity.
    J Biol Chem. 1995 Apr 28;270(17):10105-12 PMID: 7730315
  39. Defined recombinants of poliovirus and coxsackievirus: sequence-specific deletions and functional substitutions in the 5'-noncoding regions of viral RNAs.
    Virology. 1988 Jan;162(1):47-57 PMID: 2827387
  40. Intrinsic signals for the assembly of hepatitis A virus particles. Role of structural proteins VP4 and 2A.
    J Biol Chem. 1999 Feb 19;274(8):4527-31 PMID: 9988685
  41. The transformation of enterovirus replication structures: a three-dimensional study of single- and double-membrane compartments.
    mBio. 2011 Oct 04;2(5): PMID: 21972238
  42. Poliovirus empty capsid morphogenesis: evidence for conformational differences between self- and extract-assembled empty capsids.
    J Virol. 1982 Mar;41(3):792-800 PMID: 6284971
  43. Structure of a human common cold virus and functional relationship to other picornaviruses.
    Nature. 1985 Sep 12-18;317(6033):145-53 PMID: 2993920
  44. Interaction between the yellow fever virus nonstructural protein NS3 and the host protein Alix contributes to the release of infectious particles.
    Microbes Infect. 2011 Jan;13(1):85-95 PMID: 21044891
  45. Analysis of deletion mutants indicates that the 2A polypeptide of hepatitis A virus participates in virion morphogenesis.
    J Virol. 2002 Aug;76(15):7495-505 PMID: 12097562
  46. Functional coupling between replication and packaging of poliovirus replicon RNA.
    J Virol. 1999 Jan;73(1):427-35 PMID: 9847348
  47. Demonstration of the specificity of poliovirus encapsidation using a novel replicon which encodes enzymatically active firefly luciferase.
    Virology. 1998 Mar 30;243(1):1-11 PMID: 9527910
  48. Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1839-42 PMID: 8127891
  49. Myristate modification does not function as a membrane association signal during poliovirus capsid assembly.
    Virology. 1992 Apr;187(2):814-20 PMID: 1312279
  50. Icosahedral RNA virus structure.
    Annu Rev Biochem. 1989;58:533-73 PMID: 2673017
  51. Coupling between genome translation and replication in an RNA virus.
    Genes Dev. 1994 Jul 15;8(14):1726-37 PMID: 7958852
  52. Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding.
    J Virol. 1994 Oct;68(10):6523-34 PMID: 8083990
  53. Isolation of poliovirus 2C mutants defective in viral RNA synthesis.
    J Virol. 1988 Nov;62(11):4016-21 PMID: 2845120
  54. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells.
    Virology. 1994 Jul;202(1):129-45 PMID: 8009827
  55. An assembly defect as a result of an attenuating mutation in the capsid proteins of the poliovirus type 3 vaccine strain.
    J Virol. 1991 Oct;65(10):5225-31 PMID: 1654440
  56. Mouse hepatic cells support assembly of infectious hepatitis C virus particles.
    Gastroenterology. 2011 Sep;141(3):1057-66 PMID: 21699799
  57. Implications of the picornavirus capsid structure for polyprotein processing.
    Proc Natl Acad Sci U S A. 1987 Jan;84(1):21-5 PMID: 3467351
  58. New aspects of glutathione metabolism and translocation in mammals.
    Ciba Found Symp. 1979;(72):135-61 PMID: 45011
  59. Essential role of domain III of nonstructural protein 5A for hepatitis C virus infectious particle assembly.
    PLoS Pathog. 2008 Mar 28;4(3):e1000035 PMID: 18369481
  60. (+)RNA viruses rewire cellular pathways to build replication organelles.
    Curr Opin Virol. 2012 Dec;2(6):740-7 PMID: 23036609
  61. Hepatitis C virus p7 and NS2 proteins are essential for production of infectious virus.
    J Virol. 2007 Aug;81(16):8374-83 PMID: 17537845
  62. Hepatitis C virus NS2 protein contributes to virus particle assembly via opposing epistatic interactions with the E1-E2 glycoprotein and NS3-NS4A enzyme complexes.
    J Virol. 2009 Sep;83(17):8379-95 PMID: 19515772
  63. Encapsidation studies of poliovirus subgenomic replicons.
    J Gen Virol. 1998 Jul;79 ( Pt 7):1725-34 PMID: 9680136
  64. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes.
    Nature. 2013 Apr 18;496(7445):367-71 PMID: 23542590
  65. Intracellular vesicle acidification promotes maturation of infectious poliovirus particles.
    PLoS Pathog. 2012;8(11):e1003046 PMID: 23209416
  66. Hepadnaviral assembly is initiated by polymerase binding to the encapsidation signal in the viral RNA genome.
    EMBO J. 1992 Sep;11(9):3413-20 PMID: 1380455
  67. Cell-free synthesis of poliovirus: 14S subunits are the key intermediates in the encapsidation of poliovirus RNA.
    J Gen Virol. 2000 Nov;81(Pt 11):2751-2754 PMID: 11038388
  68. Poliovirus 2C region functions during encapsidation of viral RNA.
    J Virol. 1997 Nov;71(11):8759-65 PMID: 9343235
  69. Regulation of poliovirus 3C protease by the 2C polypeptide.
    J Virol. 2004 Sep;78(17):9243-56 PMID: 15308719
  70. Poliovirus morphogenesis. I. Identification of 80S dissociable particles and evidence for the artifactual production of procapsids.
    J Virol. 1981 Aug;39(2):341-7 PMID: 6268826
  71. A chimeric plasmid from cDNA clones of poliovirus and coxsackievirus produces a recombinant virus that is temperature-sensitive.
    Proc Natl Acad Sci U S A. 1986 Mar;83(6):1777-81 PMID: 3006071
  72. A distinct picornavirus group identified by sequence analysis.
    Proc Natl Acad Sci U S A. 1992 Sep 15;89(18):8847-51 PMID: 1528901
  73. Isolation and characterization of defective-interfering particles of poliovirus Sabin 1 strain.
    Virology. 1985 Apr 30;142(2):307-16 PMID: 2997988
  74. The ins and outs of hepatitis C virus entry and assembly.
    Nat Rev Microbiol. 2013 Oct;11(10):688-700 PMID: 24018384
  75. Effects of temperature and lipophilic agents on poliovirus formation and RNA synthesis in a cell-free system.
    J Virol. 1993 Oct;67(10):5932-8 PMID: 8396661
  76. A second virus-encoded proteinase involved in proteolytic processing of poliovirus polyprotein.
    Cell. 1986 Jun 6;45(5):761-70 PMID: 3011278
  77. Replication-competent picornaviruses with complete genomic RNA 3' noncoding region deletions.
    J Virol. 1997 Nov;71(11):8868-74 PMID: 9343250
  78. Picornaviral structure and assembly.
    Microbiol Rev. 1981 Jun;45(2):287-315 PMID: 7022155
  79. The effect of colchicine and dibucaine on the morphogenesis of Semliki Forest virus.
    J Biol Chem. 1978 Jul 10;253(13):4584-9 PMID: 659435
  80. Vaccine-derived polioviruses and the endgame strategy for global polio eradication.
    Annu Rev Microbiol. 2005;59:587-635 PMID: 16153180
  81. Structural and functional studies of nonstructural protein 2 of the hepatitis C virus reveal its key role as organizer of virion assembly.
    PLoS Pathog. 2010 Dec 16;6(12):e1001233 PMID: 21187906
  82. Behind closed membranes: the secret lives of picornaviruses?
    PLoS Pathog. 2013;9(5):e1003262 PMID: 23658516
  83. Aichi virus leader protein is involved in viral RNA replication and encapsidation.
    J Virol. 2003 Oct;77(20):10799-807 PMID: 14512530
  84. Viral reorganization of the secretory pathway generates distinct organelles for RNA replication.
    Cell. 2010 May 28;141(5):799-811 PMID: 20510927
  85. Poliovirus neutralization by antibodies to internal epitopes of VP4 and VP1 results from reversible exposure of these sequences at physiological temperature.
    J Virol. 1994 Jun;68(6):3965-70 PMID: 7514682
  86. Role of nonstructural protein NS2A in flavivirus assembly.
    J Virol. 2008 May;82(10):4731-41 PMID: 18337583
  87. The heat shock cognate protein 70 is associated with hepatitis C virus particles and modulates virus infectivity.
    Hepatology. 2009 Jun;49(6):1798-809 PMID: 19434724
  88. Interactions of viral protein 3CD and poly(rC) binding protein with the 5' untranslated region of the poliovirus genome.
    J Virol. 2000 Mar;74(5):2219-26 PMID: 10666252
  89. Analysis of a potential myristoylation site in hepatitis A virus capsid protein VP4.
    Virology. 1993 Jun;194(2):616-26 PMID: 8389076
  90. Composition and three-dimensional architecture of the dengue virus replication and assembly sites.
    Cell Host Microbe. 2009 Apr 23;5(4):365-75 PMID: 19380115
  91. Analysis of poliovirus protein 3A interactions with viral and cellular proteins in infected cells.
    J Virol. 2011 May;85(9):4284-96 PMID: 21345960
  92. Dimerization-driven interaction of hepatitis C virus core protein with NS3 helicase.
    J Gen Virol. 2011 Jan;92(Pt 1):101-11 PMID: 20881089
  93. An intragenic revertant of a poliovirus 2C mutant has an uncoating defect.
    J Virol. 1990 Mar;64(3):1102-7 PMID: 2154595
  94. Temperature-sensitive poliovirus mutant fails to cleave VP0 and accumulates provirions.
    J Virol. 1990 Sep;64(9):4067-75 PMID: 2166805
  95. Defective interfering particles of poliovirus: mapping of the deletion and evidence that the deletions in the genomes of DI(1), (2) and (3) are located in the same region.
    J Mol Biol. 1979 Feb 25;128(2):179-96 PMID: 219204
  96. 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. 2008 Jan 11;283(2):875-88 PMID: 17993457
  97. A critical role of a cellular membrane traffic protein in poliovirus RNA replication.
    PLoS Pathog. 2008 Nov;4(11):e1000216 PMID: 19023417
  98. Polyadenylation of genomic RNA and initiation of antigenomic RNA in a positive-strand RNA virus are controlled by the same cis-element.
    Nucleic Acids Res. 2006 May 31;34(10):2953-65 PMID: 16738134
  99. Lack of myristoylation of poliovirus capsid polypeptide VP0 prevents the formation of virions or results in the assembly of noninfectious virus particles.
    J Virol. 1990 Sep;64(9):4099-107 PMID: 2166807
  100. Envelope lipid-packing as a critical factor for the biological activity and stability of alphavirus particles isolated from mammalian and mosquito cells.
    J Biol Chem. 2011 Jan 21;286(3):1730-6 PMID: 21075845
  101. The acidic domain of hepatitis C virus NS4A contributes to RNA replication and virus particle assembly.
    J Virol. 2011 Feb;85(3):1193-204 PMID: 21047963
  102. Reduction of the rate of poliovirus protein synthesis through large-scale codon deoptimization causes attenuation of viral virulence by lowering specific infectivity.
    J Virol. 2006 Oct;80(19):9687-96 PMID: 16973573
  103. A comparison of the anti-rhinoviral drug binding pocket in HRV14 and HRV1A.
    J Mol Biol. 1993 Mar 5;230(1):206-27 PMID: 8383771
  104. Phosphatidylinositol-4 kinase III beta and oxysterol-binding protein accumulate unesterified cholesterol on poliovirus-induced membrane structure.
    Microbiol Immunol. 2014 Apr;58(4):239-56 PMID: 24527995
  105. How positive-strand RNA viruses benefit from autophagosome maturation.
    J Virol. 2013 Sep;87(18):9966-72 PMID: 23760248
  106. Yellow Fever virus NS3 plays an essential role in virus assembly independent of its known enzymatic functions.
    J Virol. 2008 Apr;82(7):3342-52 PMID: 18199634
  107. Functional specificity of co-chaperone interactions with Hsp90 client proteins.
    Crit Rev Biochem Mol Biol. 2004 Sep-Dec;39(5-6):279-95 PMID: 15763706
  108. Catalysis of poliovirus VP0 maturation cleavage is not mediated by serine 10 of VP2.
    J Virol. 1991 Jan;65(1):326-34 PMID: 1845893
  109. Hepatitis C virus proteins: from structure to function.
    Curr Top Microbiol Immunol. 2013;369:113-42 PMID: 23463199
  110. Binding of glutathione to enterovirus capsids is essential for virion morphogenesis.
    PLoS Pathog. 2014 Apr 10;10(4):e1004039 PMID: 24722756
  111. Direct interaction between two viral proteins, the nonstructural protein 2C and the capsid protein VP3, is required for enterovirus morphogenesis.
    PLoS Pathog. 2010 Aug 26;6(8):e1001066 PMID: 20865167
  112. Characterization of the nucleoside triphosphatase activity of poliovirus protein 2C reveals a mechanism by which guanidine inhibits poliovirus replication.
    J Biol Chem. 1999 Mar 12;274(11):6992-7001 PMID: 10066753
  113. Activity of pleconaril against enteroviruses.
    Antimicrob Agents Chemother. 1999 Sep;43(9):2109-15 PMID: 10471549
  114. The 5'-end sequence of the genome of Aichi virus, a picornavirus, contains an element critical for viral RNA encapsidation.
    J Virol. 2003 Mar;77(6):3542-8 PMID: 12610129
  115. Cell-free, de novo synthesis of poliovirus.
    Science. 1991 Dec 13;254(5038):1647-51 PMID: 1661029
  116. Myristylation of picornavirus capsid protein VP4 and its structural significance.
    Nature. 1987 Jun 11-17;327(6122):482-6 PMID: 3035380
  117. The site of attachment in human rhinovirus 14 for antiviral agents that inhibit uncoating.
    Science. 1986 Sep 19;233(4770):1286-93 PMID: 3018924
  118. Stimulation of poliovirus RNA synthesis and virus maturation in a HeLa cell-free in vitro translation-RNA replication system by viral protein 3CDpro.
    Virol J. 2005 Nov 21;2:86 PMID: 16300678
  119. Glutathione is required for efficient production of infectious picornavirus virions.
    Virology. 2006 Sep 30;353(2):258-67 PMID: 16860836
  120. Myristylation of poliovirus capsid precursor P1 is required for assembly of subviral particles.
    J Virol. 1992 Jul;66(7):4556-63 PMID: 1318418
  121. Identification of a cis-acting replication element within the poliovirus coding region.
    J Virol. 2000 May;74(10):4590-600 PMID: 10775595
  122. Poliovirus subviral particles associated with progeny RNA in the replication complex.
    J Gen Virol. 1995 Jan;76 ( Pt 1):63-71 PMID: 7844543
  123. Conserved RNA secondary structures in Picornaviridae genomes.
    Nucleic Acids Res. 2001 Dec 15;29(24):5079-89 PMID: 11812840
  124. Alanine scanning of poliovirus 2CATPase reveals new genetic evidence that capsid protein/2CATPase interactions are essential for morphogenesis.
    J Virol. 2012 Sep;86(18):9964-75 PMID: 22761387
  125. Production of guanidine-resistant and -dependent poliovirus mutants from cloned cDNA: mutations in polypeptide 2C are directly responsible for altered guanidine sensitivity.
    J Virol. 1986 Nov;60(2):793-6 PMID: 3022012
  126. Efficient encapsidation of human immunodeficiency virus type 1 vectors and further characterization of cis elements required for encapsidation.
    J Virol. 1997 Jun;71(6):4544-54 PMID: 9151848
  127. Virus attenuation by genome-scale changes in codon pair bias.
    Science. 2008 Jun 27;320(5884):1784-7 PMID: 18583614
  128. Proteinase 3C of hepatitis A virus (HAV) cleaves the HAV polyprotein P2-P3 at all sites including VP1/2A and 2A/2B.
    Virology. 1994 Jan;198(1):275-81 PMID: 8259663
  129. The unique role of domain 2A of the hepatitis A virus precursor polypeptide P1-2A in viral morphogenesis.
    BMB Rep. 2008 Sep 30;41(9):678-83 PMID: 18823593
  130. Mouse adaptation determinants of poliovirus type 1 enhance viral uncoating.
    J Virol. 1996 Jan;70(1):305-12 PMID: 8523541
  131. Decay-accelerating factor (CD55), a glycosylphosphatidylinositol-anchored complement regulatory protein, is a receptor for several echoviruses.
    Proc Natl Acad Sci U S A. 1994 Jun 21;91(13):6245-8 PMID: 7517044
  132. Three-dimensional structure of poliovirus at 2.9 A resolution.
    Science. 1985 Sep 27;229(4720):1358-65 PMID: 2994218
  133. The atomic structure of Mengo virus at 3.0 A resolution.
    Science. 1987 Jan 9;235(4785):182-91 PMID: 3026048
  134. The rhinovirus type 14 genome contains an internally located RNA structure that is required for viral replication.
    RNA. 1998 Dec;4(12):1569-84 PMID: 9848654
  135. Interaction of hepatitis C virus nonstructural protein 5A with core protein is critical for the production of infectious virus particles.
    J Virol. 2008 Aug;82(16):7964-76 PMID: 18524832
  136. Synthesis and assembly of hepatitis A virus-specific proteins in BS-C-1 cells.
    J Virol. 1993 Jun;67(6):3095-102 PMID: 8388489
  137. Morphogenesis of poliovirus 3. Formation of provirion in cell-free extracts.
    J Virol. 1973 Nov;12(5):1181-3 PMID: 4358165
  138. Identification of AHBA biosynthetic genes related to geldanamycin biosynthesis in Streptomyces hygroscopicus 17997.
    Curr Microbiol. 2006 Mar;52(3):197-203 PMID: 16502293
  139. Mutations in VP1 of poliovirus specifically affect both encapsidation and release of viral RNA.
    J Virol. 1990 Jan;64(1):195-206 PMID: 2152812
  140. Morphogenesis of poliovirus. IV. existence of particles sedimenting at 150S and having the properties of provirion.
    J Virol. 1977 Aug;23(2):363-7 PMID: 196114
  141. The antigenic structure of poliovirus.
    Philos Trans R Soc Lond B Biol Sci. 1989 Jun 12;323(1217):467-78 PMID: 2569204
  142. Protein 3CD is the major poliovirus proteinase responsible for cleavage of the P1 capsid precursor.
    Virology. 1988 Sep;166(1):265-70 PMID: 2842953
  143. Evolutionary constraints on chaperone-mediated folding provide an antiviral approach refractory to development of drug resistance.
    Genes Dev. 2007 Jan 15;21(2):195-205 PMID: 17234885
  144. Intracellular location and translocation of silent and active poliovirus replication complexes.
    J Gen Virol. 2005 Mar;86(Pt 3):707-718 PMID: 15722531
  145. Dissecting the roles of VP0 cleavage and RNA packaging in picornavirus capsid stabilization: the structure of empty capsids of foot-and-mouth disease virus.
    J Virol. 1997 Dec;71(12):9743-52 PMID: 9371640
  146. Stimulation of poliovirus synthesis in a HeLa cell-free in vitro translation-RNA replication system by viral protein 3CDpro.
    J Virol. 2005 May;79(10):6358-67 PMID: 15858019
  147. Morphogenesis of poliovirus. II. Demonstration of a new intermediate, the proviron.
    J Virol. 1973 Nov;12(5):1122-30 PMID: 4358164
  148. The 3' untranslated region of picornavirus RNA: features required for efficient genome replication.
    J Virol. 1995 Dec;69(12):7835-44 PMID: 7494295
  149. A "slide-back" mechanism for the initiation of protein-primed RNA synthesis by the RNA polymerase of poliovirus.
    J Biol Chem. 2003 Nov 7;278(45):43951-60 PMID: 12937178
  150. An authentic 3' noncoding region is necessary for efficient poliovirus replication.
    J Virol. 2005 Sep;79(18):11962-73 PMID: 16140772
  151. Identification of an RNA hairpin in poliovirus RNA that serves as the primary template in the in vitro uridylylation of VPg.
    J Virol. 2000 Nov;74(22):10359-70 PMID: 11044080
  152. Structural and functional characterization of the poliovirus replication complex.
    J Virol. 1992 May;66(5):2740-7 PMID: 1313898
  153. Replication complexes associated with the morphogenesis of rubella virus.
    Arch Virol. 1992;122(1-2):95-106 PMID: 1729987
  154. An interaction between glutathione and the capsid is required for the morphogenesis of C-cluster enteroviruses.
    PLoS Pathog. 2014 Apr 10;10(4):e1004052 PMID: 24722315
  155. Capsid protein VP4 of poliovirus is N-myristoylated.
    Proc Natl Acad Sci U S A. 1987 Nov;84(22):7827-31 PMID: 2825164
  156. A poliovirus replicon containing the chloramphenicol acetyltransferase gene can be used to study the replication and encapsidation of poliovirus RNA.
    J Virol. 1992 Aug;66(8):5040-6 PMID: 1321286
  157. 5'-Terminal deletions occur in coxsackievirus B3 during replication in murine hearts and cardiac myocyte cultures and correlate with encapsidation of negative-strand viral RNA.
    J Virol. 2005 Jun;79(11):7024-41 PMID: 15890942
  158. Immunocytochemical localization of capsid-related particles in subcellular fractions of poliovirus-infected cells.
    Virology. 1992 Jun;188(2):676-84 PMID: 1316678
  159. Role and mechanism of the maturation cleavage of VP0 in poliovirus assembly: structure of the empty capsid assembly intermediate at 2.9 A resolution.
    Protein Sci. 1994 Oct;3(10):1651-69 PMID: 7849583
  160. Replication of coronavirus MHV-A59 in sac- cells: determination of the first site of budding of progeny virions.
    Eur J Cell Biol. 1984 Mar;33(2):281-93 PMID: 6325194
  161. Interactions between the West Nile virus capsid protein and the host cell-encoded phosphatase inhibitor, I2PP2A.
    Cell Microbiol. 2007 Nov;9(11):2756-66 PMID: 17868381
  162. Identification of two functionally redundant RNA elements in the coding sequence of poliovirus using computer-generated design.
    Proc Natl Acad Sci U S A. 2012 Sep 4;109(36):14301-7 PMID: 22886087
  163. Genetic analysis of an NTP-binding motif in poliovirus polypeptide 2C.
    Virology. 1992 Aug;189(2):547-55 PMID: 1322588
  164. RNA binding properties of poliovirus subviral particles.
    J Virol. 1995 Jan;69(1):13-22 PMID: 7983702
  165. Foot-and-mouth disease virus assembly: processing of recombinant capsid precursor by exogenous protease induces self-assembly of pentamers in vitro in a myristoylation-dependent manner.
    J Virol. 2009 Nov;83(21):11275-82 PMID: 19710148
  166. Defective interfering particles of poliovirus. I. Isolation and physical properties.
    J Virol. 1971 Apr;7(4):478-85 PMID: 4329564
  167. Coxsackievirus B3 adapted to growth in RD cells binds to decay-accelerating factor (CD55).
    J Virol. 1995 Mar;69(3):1903-6 PMID: 7531780
  168. Studies of a putative amphipathic helix in the N-terminus of poliovirus protein 2C.
    Virology. 1994 Feb 15;199(1):188-99 PMID: 8116242
  169. Inhibitors of viral uncoating.
    Pharmacol Ther. 1989;42(3):289-305 PMID: 2672048
  170. Role of the transmembrane domains of prM and E proteins in the formation of yellow fever virus envelope.
    J Virol. 2003 Jan;77(2):813-20 PMID: 12502797
  171. Structural and functional characterization of nonstructural protein 2 for its role in hepatitis C virus assembly.
    J Biol Chem. 2008 Oct 17;283(42):28546-62 PMID: 18644781
  172. A cysteine-rich motif in poliovirus protein 2C(ATPase) is involved in RNA replication and binds zinc in vitro.
    J Virol. 2000 Jan;74(1):334-43 PMID: 10590122
  173. Guanidine-dependent mutants of poliovirus: identification of three classes with different growth requirements.
    Virology. 1987 Mar;157(1):83-8 PMID: 3029969
  174. Genetic and biochemical studies of poliovirus cis-acting replication element cre in relation to VPg uridylylation.
    J Virol. 2000 Nov;74(22):10371-80 PMID: 11044081
  175. Myristoyl modification of viral proteins: assays to assess functional roles.
    Methods Enzymol. 1995;250:495-509 PMID: 7651174
  176. Evidence for emergence of diverse polioviruses from C-cluster coxsackie A viruses and implications for global poliovirus eradication.
    Proc Natl Acad Sci U S A. 2007 May 29;104(22):9457-62 PMID: 17517601
  177. Assembly of severe acute respiratory syndrome coronavirus RNA packaging signal into virus-like particles is nucleocapsid dependent.
    J Virol. 2005 Nov;79(22):13848-55 PMID: 16254320
  178. Primary structure of poliovirus defective-interfering particle genomes and possible generation mechanisms of the particles.
    J Mol Biol. 1986 Dec 5;192(3):473-87 PMID: 3031313
  179. The transmembrane domains of the prM and E proteins of yellow fever virus are endoplasmic reticulum localization signals.
    J Virol. 2004 Nov;78(22):12591-602 PMID: 15507646
  180. Induction of intracellular membrane rearrangements by HAV proteins 2C and 2BC.
    Virology. 1997 Oct 13;237(1):66-77 PMID: 9344908
  181. Venezuelan equine encephalitis virus nsP2 protein regulates packaging of the viral genome into infectious virions.
    J Virol. 2013 Apr;87(8):4202-13 PMID: 23365438
  182. Molecular determinants and dynamics of hepatitis C virus secretion.
    PLoS Pathog. 2012 Jan;8(1):e1002466 PMID: 22241992
  183. Molecular dissection of the multifunctional poliovirus RNA-binding protein 3AB.
    RNA. 1995 Nov;1(9):892-904 PMID: 8548654
  184. Identification of poliovirus particles of different antigenicity by specific agglutination as seen in the electron microscope.
    Virology. 1962 Jan;16:84-90 PMID: 14449962
  185. Encapsidation of poliovirus replicons encoding the complete human immunodeficiency virus type 1 gag gene by using a complementation system which provides the P1 capsid protein in trans.
    J Virol. 1995 Mar;69(3):1548-55 PMID: 7853488
  186. Identification and targeting of an interaction between a tyrosine motif within hepatitis C virus core protein and AP2M1 essential for viral assembly.
    PLoS Pathog. 2012;8(8):e1002845 PMID: 22916011
  187. NS3 helicase domains involved in infectious intracellular hepatitis C virus particle assembly.
    J Virol. 2008 Aug;82(15):7624-39 PMID: 18508894
  188. A pH-dependent antigenic conversion of empty capsids of poliovirus studied with the aid of monoclonal antibodies to N and H antigen.
    Virology. 1982 Oct 15;122(1):215-8 PMID: 6291235
  189. Membrane permeabilization by poliovirus proteins 2B and 2BC.
    J Biol Chem. 1996 Sep 20;271(38):23134-7 PMID: 8798506
  190. New evidence for the precursor role of 14 S subunits in poliovirus morphogenesis.
    Virology. 1990 Jul;177(1):411-4 PMID: 2162113
  191. Quantitative study of the formation of poliovirus antigens in infected HeLa cells.
    Virology. 1963 Apr;19:491-500 PMID: 13976714
  192. Protein-primed RNA synthesis by purified poliovirus RNA polymerase.
    Nature. 1998 May 21;393(6682):280-4 PMID: 9607767
  193. Association of heat shock protein 70 with enterovirus capsid precursor P1 in infected human cells.
    J Virol. 1992 Mar;66(3):1520-7 PMID: 1310763
  194. A genetic interaction between the core and NS3 proteins of hepatitis C virus is essential for production of infectious virus.
    J Virol. 2011 Dec;85(23):12351-61 PMID: 21957313
  195. NS2 protein of hepatitis C virus interacts with structural and non-structural proteins towards virus assembly.
    PLoS Pathog. 2011 Feb 10;7(2):e1001278 PMID: 21347350
  196. Packaging signals in alphaviruses.
    J Virol. 1997 Jan;71(1):248-58 PMID: 8985344
Article Info
Journal
Microbiology and molecular biology reviews : MMBR
Abbr.
Microbiol Mol Biol Rev
ISSN
1098-5557
Published
2014-09-00
Pages
418-37
Language
English
Region
United States
NLM ID
9706653
PMCID
PMC4187686
Subset
IM
Grants
NIAID NIH HHS · R01 AI015122 · United States
NIAID NIH HHS · R37 AI015122 · United States
NIAID NIH HHS · AI 15122 · United States
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