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PMID: 16190978 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Wrapping things up about virus RNA replication.

Traffic (Copenhagen, Denmark) ·Vol. 6 ·No. 11 ·2005-11-00 ·Pages 967-77

Mackenzie J

Abstract

All single-stranded 'positive-sense' RNA viruses that infect mammalian, insect or plant cells rearrange internal cellular membranes to provide an environment facilitating virus replication. A striking feature of these unique membrane structures is the induction of 70-100 nm vesicles (either free within the cytoplasm, associated with other induced vesicles or bound within a surrounding membrane) harbouring the viral replication complex (RC). Although similar in appearance, the cellular composition of these vesicles appears to vary for different viruses, implying different organelle origins for the intracellular sites of viral RNA replication. Genetic analysis has revealed that induction of these membrane structures can be attributed to a particular viral gene product, usually a non-structural protein. This review will highlight our current knowledge of the formation and composition of virus RCs and describe some of the similarities and differences in RNA-membrane interactions observed between the virus families Flaviviridae and Picornaviridae.

MeSH Terms
Animals Cell Membrane/genetics Genome, Viral Humans RNA Viruses/classification,genetics,physiology RNA, Viral/biosynthesis,metabolism Virus Replication
Chemicals
RNA, Viral
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Mackenzie Jason
School of Molecular and Microbial Sciences, University of Queensland, St. Lucia, Queensland 4072, Australia. [email protected]
References (100)
100 references, click to expand
  1. Structural organization of poliovirus RNA replication is mediated by viral proteins of the P2 genomic region.
    J Virol. 1990 Mar;64(3):1156-63 PMID: 2154600
  2. Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex.
    J Virol. 2002 Jun;76(12):5974-84 PMID: 12021330
  3. Unstable receptors disappear from cell surface during poliovirus infection.
    Med Sci Monit. 2002 Oct;8(10):BR391-6 PMID: 12388911
  4. Identification of the hepatitis C virus RNA replication complex in Huh-7 cells harboring subgenomic replicons.
    J Virol. 2003 May;77(9):5487-92 PMID: 12692249
  5. Kunjin RNA replication and applications of Kunjin replicons.
    Adv Virus Res. 2003;59:99-140 PMID: 14696328
  6. 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
  7. Recombination of poliovirus RNA proceeds in mixed replication complexes originating from distinct replication start sites.
    J Virol. 2002 Nov;76(21):10960-71 PMID: 12368339
  8. Poliovirus 2C protein determinants of membrane binding and rearrangements in mammalian cells.
    J Virol. 1997 Dec;71(12):8962-72 PMID: 9371552
  9. Subversion of cellular autophagosomal machinery by RNA viruses.
    PLoS Biol. 2005 May;3(5):e156 PMID: 15884975
  10. Inhibition of cellular protein secretion by poliovirus proteins 2B and 3A.
    EMBO J. 1995 Mar 1;14(5):894-907 PMID: 7889939
  11. ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex.
    J Virol. 1998 Aug;72(8):6689-98 PMID: 9658116
  12. Replication and gene function in Kunjin virus.
    Curr Top Microbiol Immunol. 2002;267:323-51 PMID: 12082996
  13. Transcription of infectious yellow fever RNA from full-length cDNA templates produced by in vitro ligation.
    New Biol. 1989 Dec;1(3):285-96 PMID: 2487295
  14. ER-to-Golgi carriers arise through direct en bloc protrusion and multistage maturation of specialized ER exit domains.
    Dev Cell. 2003 Oct;5(4):583-94 PMID: 14536060
  15. Open reading frame 1a-encoded subunits of the arterivirus replicase induce endoplasmic reticulum-derived double-membrane vesicles which carry the viral replication complex.
    J Virol. 1999 Mar;73(3):2016-26 PMID: 9971782
  16. Identification, by a monoclonal antibody, of a 53-kD protein associated with a tubulo-vesicular compartment at the cis-side of the Golgi apparatus.
    J Cell Biol. 1988 Nov;107(5):1643-53 PMID: 3182932
  17. ARF: a key regulatory switch in membrane traffic and organelle structure.
    Curr Opin Cell Biol. 1994 Aug;6(4):527-32 PMID: 7986529
  18. Virus factories: associations of cell organelles for viral replication and morphogenesis.
    Biol Cell. 2005 Feb;97(2):147-72 PMID: 15656780
  19. Differential requirements for COPI coats in formation of replication complexes among three genera of Picornaviridae.
    J Virol. 2002 Nov;76(21):11113-22 PMID: 12368353
  20. 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
  21. trans-Complementation of yellow fever virus NS1 reveals a role in early RNA replication.
    J Virol. 1997 Dec;71(12):9608-17 PMID: 9371625
  22. Inefficient complementation activity of poliovirus 2C and 3D proteins for rescue of lethal mutations.
    J Virol. 1995 Jul;69(7):4245-54 PMID: 7769684
  23. Poliovirus infection and expression of the poliovirus protein 2B provoke the disassembly of the Golgi complex, the organelle target for the antipoliovirus drug Ro-090179.
    J Virol. 1997 Jun;71(6):4679-93 PMID: 9151862
  24. Poliovirus protein 2C contains two regions involved in RNA binding activity.
    J Biol Chem. 1995 Apr 28;270(17):10105-12 PMID: 7730315
  25. Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step.
    J Cell Biol. 1994 Jan;124(1-2):55-70 PMID: 8294506
  26. Foot-and-mouth disease virus replication sites form next to the nucleus and close to the Golgi apparatus, but exclude marker proteins associated with host membrane compartments.
    J Gen Virol. 2005 Mar;86(Pt 3):687-696 PMID: 15722529
  27. Proteolytic activation of tick-borne encephalitis virus by furin.
    J Virol. 1997 Nov;71(11):8475-81 PMID: 9343204
  28. Immunolocalization of the dengue virus nonstructural glycoprotein NS1 suggests a role in viral RNA replication.
    Virology. 1996 Jun 1;220(1):232-40 PMID: 8659120
  29. Cellular origin and ultrastructure of membranes induced during poliovirus infection.
    J Virol. 1996 Oct;70(10):6576-88 PMID: 8794292
  30. Improved membrane preservation of flavivirus-infected cells with cryosectioning.
    J Virol Methods. 1996 Jan;56(1):67-75 PMID: 8690769
  31. The poliovirus replication machinery can escape inhibition by an antiviral drug that targets a host cell protein.
    J Virol. 2004 Apr;78(7):3378-86 PMID: 15016860
  32. Nonstructural protein precursor NS4A/B from hepatitis C virus alters function and ultrastructure of host secretory apparatus.
    J Virol. 2003 Jul;77(14):7843-55 PMID: 12829824
  33. Visualization and functional analysis of RNA-dependent RNA polymerase lattices.
    Science. 2002 Jun 21;296(5576):2218-22 PMID: 12077417
  34. Intracellular distribution of rubella virus nonstructural protein P150.
    J Virol. 1999 Sep;73(9):7805-11 PMID: 10438871
  35. Poliovirus proteins induce membrane association of GTPase ADP-ribosylation factor.
    J Virol. 2005 Jun;79(11):7207-16 PMID: 15890959
  36. Sorting and retrieval between the endoplasmic reticulum and Golgi apparatus.
    Curr Opin Cell Biol. 1995 Aug;7(4):530-5 PMID: 7495573
  37. Viral RNA replication in association with cellular membranes.
    Curr Top Microbiol Immunol. 2005;285:139-73 PMID: 15609503
  38. Subgenomic replicons of the flavivirus Kunjin: construction and applications.
    J Virol. 1997 Feb;71(2):1497-505 PMID: 8995675
  39. Immunocytochemistry and in situ hybridization in the electron microscope: combined application in the study of virus-infected cells.
    Histochem Cell Biol. 1995 May;103(5):325-38 PMID: 7641067
  40. Molecular and ultrastructural analysis of heavy membrane fractions associated with the replication of Kunjin virus RNA.
    Arch Virol. 1992;125(1-4):177-91 PMID: 1322651
  41. Completion of Kunjin virus RNA sequence and recovery of an infectious RNA transcribed from stably cloned full-length cDNA.
    J Virol. 1994 Jul;68(7):4580-8 PMID: 8207832
  42. Fine structure of vesicles induced in chloroplasts of Chinese cabbage leaves by infection with turnip yellow mosaic virus.
    J Gen Virol. 1973 Jul;20(1):37-50 PMID: 4584930
  43. Development by self-digestion: molecular mechanisms and biological functions of autophagy.
    Dev Cell. 2004 Apr;6(4):463-77 PMID: 15068787
  44. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells.
    Virology. 1994 Jul;202(1):129-45 PMID: 8009827
  45. Nascent flavivirus RNA colocalized in situ with double-stranded RNA in stable replication complexes.
    Virology. 1999 May 25;258(1):108-17 PMID: 10329573
  46. Assembly and maturation of the flavivirus Kunjin virus appear to occur in the rough endoplasmic reticulum and along the secretory pathway, respectively.
    J Virol. 2001 Nov;75(22):10787-99 PMID: 11602720
  47. Maintenance of Golgi structure and function depends on the integrity of ER export.
    J Cell Biol. 2001 Nov 12;155(4):557-70 PMID: 11706049
  48. Biogenesis of the Semliki Forest virus RNA replication complex.
    J Virol. 2001 Apr;75(8):3873-84 PMID: 11264376
  49. 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
  50. Poliovirus protein 3A inhibits tumor necrosis factor (TNF)-induced apoptosis by eliminating the TNF receptor from the cell surface.
    J Virol. 2001 Nov;75(21):10409-20 PMID: 11581409
  51. Cellular autophagy: surrender, avoidance and subversion by microorganisms.
    Nat Rev Microbiol. 2004 Apr;2(4):301-14 PMID: 15031729
  52. Synthesis of Semliki Forest virus RNA requires continuous lipid synthesis.
    Virology. 1991 Jul;183(1):74-82 PMID: 1647077
  53. Cytopathology in the identification and classification of tombusviruses.
    Intervirology. 1987;28(3):134-43 PMID: 3450676
  54. Formation of the poliovirus replication complex requires coupled viral translation, vesicle production, and viral RNA synthesis.
    J Virol. 2000 Jul;74(14):6570-80 PMID: 10864671
  55. Meeting report: EMBO workshop 'Cell Biology of Virus Infection', September 25-29, 2004, EMBL, Heidelberg, Germany.
    Traffic. 2005 Apr;6(4):351-6 PMID: 15752140
  56. RNA replication of mouse hepatitis virus takes place at double-membrane vesicles.
    J Virol. 2002 Apr;76(8):3697-708 PMID: 11907209
  57. Subcellular distribution of the foot-and-mouth disease virus 3A protein in cells infected with viruses encoding wild-type and bovine-attenuated forms of 3A.
    Virology. 2001 Aug 15;287(1):151-62 PMID: 11504550
  58. Characterization of rubella virus replication complexes using antibodies to double-stranded RNA.
    Virology. 1994 Apr;200(1):307-12 PMID: 8128633
  59. Effects of brefeldin A on autophagy in cultured rat fibroblasts.
    Eur J Cell Biol. 1997 Sep;74(1):63-7 PMID: 9309391
  60. Effects of foot-and-mouth disease virus nonstructural proteins on the structure and function of the early secretory pathway: 2BC but not 3A blocks endoplasmic reticulum-to-Golgi transport.
    J Virol. 2005 Apr;79(7):4382-95 PMID: 15767438
  61. Subcellular localization and some biochemical properties of the flavivirus Kunjin nonstructural proteins NS2A and NS4A.
    Virology. 1998 Jun 5;245(2):203-15 PMID: 9636360
  62. Cerulenin, an inhibitor of lipid synthesis, blocks vesicular stomatitis virus RNA replication.
    FEBS Lett. 1991 Mar 11;280(1):129-33 PMID: 1849089
  63. Inhibition of poliovirus RNA synthesis by brefeldin A.
    J Virol. 1992 Apr;66(4):1985-94 PMID: 1312615
  64. Replication complex of human parechovirus 1.
    J Virol. 2003 Aug;77(15):8512-23 PMID: 12857920
  65. A cytopathic and a cell culture adapted hepatitis A virus strain differ in cell killing but not in intracellular membrane rearrangements.
    Virology. 2000 Jan 5;266(1):157-69 PMID: 10612670
  66. Intracellular localisation of dengue-2 RNA in mosquito cell culture using electron microscopic in situ hybridisation.
    Arch Virol. 1997;142(12):2347-57 PMID: 9672599
  67. Markers for trans-Golgi membranes and the intermediate compartment localize to induced membranes with distinct replication functions in flavivirus-infected cells.
    J Virol. 1999 Nov;73(11):9555-67 PMID: 10516064
  68. A positive-strand RNA virus replication complex parallels form and function of retrovirus capsids.
    Mol Cell. 2002 Mar;9(3):505-14 PMID: 11931759
  69. Brome mosaic virus RNA replication proteins 1a and 2a colocalize and 1a independently localizes on the yeast endoplasmic reticulum.
    J Virol. 1999 Dec;73(12):10303-9 PMID: 10559348
  70. Ultrastructural studies of Kunjin virus-infected Aedes albopictus cells.
    J Gen Virol. 1987 Feb;68 ( Pt 2):577-82 PMID: 3029292
  71. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes.
    J Cell Biol. 1988 Dec;107(6 Pt 1):2075-86 PMID: 2904446
  72. Induction of membrane proliferation by poliovirus proteins 2C and 2BC.
    Biochem Biophys Res Commun. 1995 Jan 5;206(1):64-76 PMID: 7818552
  73. Rubella virus replication complexes are virus-modified lysosomes.
    Virology. 1998 Jan 5;240(1):57-63 PMID: 9448689
  74. Phospholipid biosynthesis and poliovirus genome replication, two coupled phenomena.
    EMBO J. 1990 Jun;9(6):2011-6 PMID: 2161336
  75. The ultrastructure of the developing replication site in foot-and-mouth disease virus-infected BHK-38 cells.
    J Gen Virol. 2004 Apr;85(Pt 4):933-946 PMID: 15039536
  76. Brefeldin A inhibits cell-free, de novo synthesis of poliovirus.
    J Virol. 1998 Aug;72(8):6456-64 PMID: 9658088
  77. Coronavirus replication complex formation utilizes components of cellular autophagy.
    J Biol Chem. 2004 Mar 12;279(11):10136-41 PMID: 14699140
  78. Structural and functional characterization of the poliovirus replication complex.
    J Virol. 1992 May;66(5):2740-7 PMID: 1313898
  79. Replication complexes associated with the morphogenesis of rubella virus.
    Arch Virol. 1992;122(1-2):95-106 PMID: 1729987
  80. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles.
    J Virol. 2000 Oct;74(19):8953-65 PMID: 10982339
  81. In situ hybridization for light and electron microscopy: a comparison of methods for the localization of viral RNA using biotinylated DNA and RNA probes.
    J Virol Methods. 1990 Oct;30(1):1-14 PMID: 1964937
  82. Genetic interaction of flavivirus nonstructural proteins NS1 and NS4A as a determinant of replicase function.
    J Virol. 1999 Jun;73(6):4611-21 PMID: 10233920
  83. Immunocytochemical localization of capsid-related particles in subcellular fractions of poliovirus-infected cells.
    Virology. 1992 Jun;188(2):676-84 PMID: 1316678
  84. Complementation analysis of the flavivirus Kunjin NS3 and NS5 proteins defines the minimal regions essential for formation of a replication complex and shows a requirement of NS3 in cis for virus assembly.
    J Virol. 2002 Nov;76(21):10766-75 PMID: 12368319
  85. Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells.
    J Virol. 2001 Dec;75(23):11664-76 PMID: 11689648
  86. Reassessment of the subcellular localization of p63.
    J Cell Sci. 1995 Jun;108 ( Pt 6):2477-85 PMID: 7673362
  87. Cowpea mosaic virus infection induces a massive proliferation of endoplasmic reticulum but not Golgi membranes and is dependent on de novo membrane synthesis.
    J Virol. 2000 Jul;74(14):6556-63 PMID: 10864669
  88. Intracellular distribution of poliovirus proteins and the induction of virus-specific cytoplasmic structures.
    Virology. 1983 Nov;131(1):39-48 PMID: 6316654
  89. Localization of mouse hepatitis virus nonstructural proteins and RNA synthesis indicates a role for late endosomes in viral replication.
    J Virol. 1999 Sep;73(9):7641-57 PMID: 10438855
  90. Proteins C and NS4B of the flavivirus Kunjin translocate independently into the nucleus.
    Virology. 1997 Jul 21;234(1):31-41 PMID: 9234944
  91. ERGIC-53 and traffic in the secretory pathway.
    J Cell Sci. 2000 Feb;113 ( Pt 4):587-96 PMID: 10652252
  92. Poliovirus protein 2C has ATPase and GTPase activities.
    J Biol Chem. 1993 Apr 15;268(11):8105-10 PMID: 8385138
  93. Stable expression of noncytopathic Kunjin replicons simulates both ultrastructural and biochemical characteristics observed during replication of Kunjin virus.
    Virology. 2001 Jan 5;279(1):161-72 PMID: 11145899
  94. Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures.
    J Virol. 1997 Sep;71(9):6650-61 PMID: 9261387
  95. Cellular COPII proteins are involved in production of the vesicles that form the poliovirus replication complex.
    J Virol. 2001 Oct;75(20):9808-18 PMID: 11559814
  96. Induction of intracellular membrane rearrangements by HAV proteins 2C and 2BC.
    Virology. 1997 Oct 13;237(1):66-77 PMID: 9344908
  97. MHC I-dependent antigen presentation is inhibited by poliovirus protein 3A.
    Proc Natl Acad Sci U S A. 2000 Dec 5;97(25):13790-5 PMID: 11095746
  98. Association of polioviral proteins of the P2 genomic region with the viral replication complex and virus-induced membrane synthesis as visualized by electron microscopic immunocytochemistry and autoradiography.
    Virology. 1987 Sep;160(1):220-6 PMID: 2820130
  99. Membrane permeabilization by poliovirus proteins 2B and 2BC.
    J Biol Chem. 1996 Sep 20;271(38):23134-7 PMID: 8798506
  100. Reversible dissociation of the poliovirus replication complex: functions and interactions of its components in viral RNA synthesis.
    J Virol. 1996 Dec;70(12):8675-83 PMID: 8970994
Article Info
Journal
Traffic (Copenhagen, Denmark)
Abbr.
Traffic
ISSN
1398-9219
Published
2005-11-00
Pages
967-77
Language
English
Region
England
NLM ID
100939340
PMCID
PMC7169867
Subset
IM
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