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PMID: 18414501 Published · ppublish English Journal Article Review

Modification of intracellular membrane structures for virus replication.

Nature reviews. Microbiology ·Vol. 6 ·No. 5 ·2008-05-00 ·Pages 363-74

Miller S, Krijnse-Locker J

Abstract

Viruses are intracellular parasites that use the host cell they infect to produce new infectious progeny. Distinct steps of the virus life cycle occur in association with the cytoskeleton or cytoplasmic membranes, which are often modified during infection. Plus-stranded RNA viruses induce membrane proliferations that support the replication of their genomes. Similarly, cytoplasmic replication of some DNA viruses occurs in association with modified cellular membranes. We describe how viruses modify intracellular membranes, highlight similarities between the structures that are induced by viruses of different families and discuss how these structures could be formed.

MeSH Terms
Animals Autophagy Humans Intracellular Membranes/ultrastructure,virology Mice Virus Replication
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Miller Sven
3-V Biosciences, Institute of Biochemistry, Schafmattstrasse 18, ETH Hoenggerberg, HPME 17, CH8093 Zurich, Switzerland. [email protected]
Krijnse-Locker Jacomine
References (116)
116 references, click to expand
  1. Non-structural proteins 2 and 3 interact to modify host cell membranes during the formation of the arterivirus replication complex.
    J Gen Virol. 2001 May;82(Pt 5):985-994 PMID: 11297673
  2. Differential regulation of endoplasmic reticulum structure through VAP-Nir protein interaction.
    J Biol Chem. 2005 Feb 18;280(7):5934-44 PMID: 15545272
  3. Detection and subcellular localization of the turnip yellow mosaic virus 66K replication protein in infected cells.
    Virology. 2001 Mar 1;281(1):88-101 PMID: 11222099
  4. Kunjin RNA replication and applications of Kunjin replicons.
    Adv Virus Res. 2003;59:99-140 PMID: 14696328
  5. The role of the Nir/rdgB protein family in membrane trafficking and cytoskeleton remodeling.
    Exp Cell Res. 2004 Jul 1;297(1):1-10 PMID: 15194420
  6. Subversion of cellular autophagosomal machinery by RNA viruses.
    PLoS Biol. 2005 May;3(5):e156 PMID: 15884975
  7. The non-structural protein 4A of dengue virus is an integral membrane protein inducing membrane alterations in a 2K-regulated manner.
    J Biol Chem. 2007 Mar 23;282(12):8873-82 PMID: 17276984
  8. 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
  9. Involvement of cellular membrane traffic proteins in poliovirus replication.
    Cell Cycle. 2007 Jan 1;6(1):36-8 PMID: 17245115
  10. Inhibition of cellular protein secretion by poliovirus proteins 2B and 3A.
    EMBO J. 1995 Mar 1;14(5):894-907 PMID: 7889939
  11. Biochemistry of vaccinia-infected mouse fibroblasts (strain L-M). III. Radioautographic and biochemical studies of thymidine-H3 uptake into DNA of L-M cells and rabbit cells in primary culture.
    Virology. 1963 Jan;19:13-22 PMID: 14033126
  12. Kunjin virus: an Australian variant of West Nile?
    Ann N Y Acad Sci. 2001 Dec;951:153-60 PMID: 11797773
  13. 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
  14. Poliovirus 3A protein limits interleukin-6 (IL-6), IL-8, and beta interferon secretion during viral infection.
    J Virol. 2001 Sep;75(17):8158-65 PMID: 11483761
  15. Molecular cloning and characterization of mammalian homologues of vesicle-associated membrane protein-associated (VAMP-associated) proteins.
    Biochem Biophys Res Commun. 1999 Jan 8;254(1):21-6 PMID: 9920726
  16. Endoplasmic reticulum and Golgi complex: Contributions to, and turnover by, autophagy.
    Traffic. 2006 Dec;7(12):1590-5 PMID: 17040485
  17. Membrane deformation by protein coats.
    Curr Opin Cell Biol. 2006 Aug;18(4):386-94 PMID: 16782321
  18. Virus factories: associations of cell organelles for viral replication and morphogenesis.
    Biol Cell. 2005 Feb;97(2):147-72 PMID: 15656780
  19. ERG30, a VAP-33-related protein, functions in protein transport mediated by COPI vesicles.
    J Cell Biol. 1999 Jul 26;146(2):301-11 PMID: 10427086
  20. Human VAP-B is involved in hepatitis C virus replication through interaction with NS5A and NS5B.
    J Virol. 2005 Nov;79(21):13473-82 PMID: 16227268
  21. Role of the amphipathic peptide of Semliki forest virus replicase protein nsP1 in membrane association and virus replication.
    J Virol. 2007 Jan;81(2):872-83 PMID: 17093195
  22. Host factors involved in the replication of hepatitis C virus.
    Rev Med Virol. 2007 Sep-Oct;17(5):343-54 PMID: 17563922
  23. 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
  24. Wrapping things up about virus RNA replication.
    Traffic. 2005 Nov;6(11):967-77 PMID: 16190978
  25. Tobacco mosaic virus infection induces severe morphological changes of the endoplasmic reticulum.
    Proc Natl Acad Sci U S A. 1998 Sep 15;95(19):11169-74 PMID: 9736708
  26. Cellular autophagy machinery is not required for vaccinia virus replication and maturation.
    Autophagy. 2006 Apr-Jun;2(2):91-5 PMID: 16874104
  27. Analysis of the interaction of viral RNA replication proteins by using the yeast two-hybrid assay.
    J Virol. 1997 Oct;71(10):7526-32 PMID: 9311832
  28. Cellular origin and ultrastructure of membranes induced during poliovirus infection.
    J Virol. 1996 Oct;70(10):6576-88 PMID: 8794292
  29. Visualization and functional analysis of RNA-dependent RNA polymerase lattices.
    Science. 2002 Jun 21;296(5576):2218-22 PMID: 12077417
  30. Specific membranous structures associated with the replication of group A arboviruses.
    J Virol. 1972 Sep;10(3):492-503 PMID: 4672392
  31. Amphipathic helix-dependent localization of NS5A mediates hepatitis C virus RNA replication.
    J Virol. 2003 May;77(10):6055-61 PMID: 12719597
  32. Intracellular distribution of rubella virus nonstructural protein P150.
    J Virol. 1999 Sep;73(9):7805-11 PMID: 10438871
  33. Regulation of Sar1 NH2 terminus by GTP binding and hydrolysis promotes membrane deformation to control COPII vesicle fission.
    J Cell Biol. 2005 Dec 19;171(6):919-24 PMID: 16344311
  34. Poliovirus proteins induce membrane association of GTPase ADP-ribosylation factor.
    J Virol. 2005 Jun;79(11):7207-16 PMID: 15890959
  35. Cytoplasmic organization of POXvirus DNA replication.
    Traffic. 2005 Oct;6(10):839-46 PMID: 16138898
  36. Quantitative analysis of the hepatitis C virus replication complex.
    J Virol. 2005 Nov;79(21):13594-605 PMID: 16227280
  37. Inhibition of endoplasmic reticulum-to-Golgi traffic by poliovirus protein 3A: genetic and ultrastructural analysis.
    J Virol. 1997 Dec;71(12):9054-64 PMID: 9371562
  38. Viral RNA replication in association with cellular membranes.
    Curr Top Microbiol Immunol. 2005;285:139-73 PMID: 15609503
  39. An N-terminal amphipathic helix in hepatitis C virus (HCV) NS4B mediates membrane association, correct localization of replication complex proteins, and HCV RNA replication.
    J Virol. 2004 Oct;78(20):11393-400 PMID: 15452261
  40. Secretory pathway function, but not cytoskeletal integrity, is required in poliovirus infection.
    Arch Virol Suppl. 1994;9:159-72 PMID: 8032247
  41. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells.
    Virology. 1994 Jul;202(1):129-45 PMID: 8009827
  42. Testing the modularity of the N-terminal amphipathic helix conserved in picornavirus 2C proteins and hepatitis C NS5A protein.
    Virology. 2006 Jan 20;344(2):453-67 PMID: 16226781
  43. SNARE function analyzed in synaptobrevin/VAMP knockout mice.
    Science. 2001 Nov 2;294(5544):1117-22 PMID: 11691998
  44. Three ways to make a vesicle.
    Nat Rev Mol Cell Biol. 2000 Dec;1(3):187-98 PMID: 11252894
  45. ELECTRON MICROSCOPIC STUDY OF THE FORMATION OF POLIOVIRUS.
    Virology. 1965 Jul;26:379-89 PMID: 14319710
  46. Hijacking components of the cellular secretory pathway for replication of poliovirus RNA.
    J Virol. 2007 Jan;81(2):558-67 PMID: 17079330
  47. Subcellular localization and membrane topology of the Dengue virus type 2 Non-structural protein 4B.
    J Biol Chem. 2006 Mar 31;281(13):8854-63 PMID: 16436383
  48. How proteins produce cellular membrane curvature.
    Nat Rev Mol Cell Biol. 2006 Jan;7(1):9-19 PMID: 16365634
  49. Evidence for a COP-I-independent transport route from the Golgi complex to the endoplasmic reticulum.
    Nat Cell Biol. 1999 Nov;1(7):423-30 PMID: 10559986
  50. Biogenesis of the Semliki Forest virus RNA replication complex.
    J Virol. 2001 Apr;75(8):3873-84 PMID: 11264376
  51. Semliki Forest virus mRNA capping enzyme requires association with anionic membrane phospholipids for activity.
    EMBO J. 1999 Jun 1;18(11):3164-72 PMID: 10357827
  52. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses.
    Nat Med. 2004 Dec;10(12 Suppl):S98-109 PMID: 15577938
  53. Cellular autophagy: surrender, avoidance and subversion by microorganisms.
    Nat Rev Microbiol. 2004 Apr;2(4):301-14 PMID: 15031729
  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. Sar1p N-terminal helix initiates membrane curvature and completes the fission of a COPII vesicle.
    Cell. 2005 Aug 26;122(4):605-17 PMID: 16122427
  56. Replication of tobacco mosaic virus on endoplasmic reticulum and role of the cytoskeleton and virus movement protein in intracellular distribution of viral RNA.
    J Cell Biol. 1999 Nov 29;147(5):945-58 PMID: 10579716
  57. Characterization of rubella virus replication complexes using antibodies to double-stranded RNA.
    Virology. 1994 Apr;200(1):307-12 PMID: 8128633
  58. A small region of the dengue virus-encoded RNA-dependent RNA polymerase, NS5, confers interaction with both the nuclear transport receptor importin-beta and the viral helicase, NS3.
    J Gen Virol. 2001 Apr;82(Pt 4):735-745 PMID: 11257177
  59. Exploiting alternative subcellular location for replication: tombusvirus replication switches to the endoplasmic reticulum in the absence of peroxisomes.
    Virology. 2007 Jun 5;362(2):320-30 PMID: 17292435
  60. Cytoplasmic structures associated with an arbovirus infection: loci of viral ribonucleic acid synthesis.
    J Virol. 1968 Nov;2(11):1326-38 PMID: 5750316
  61. Towards an understanding of the poliovirus replication complex: the solution structure of the soluble domain of the poliovirus 3A protein.
    J Mol Biol. 2003 Jul 4;330(2):225-34 PMID: 12823963
  62. VAP-33 localizes to both an intracellular vesicle population and with occludin at the tight junction.
    J Cell Sci. 1999 Nov;112 ( Pt 21):3723-32 PMID: 10523508
  63. Vaccinia virus DNA replication occurs in endoplasmic reticulum-enclosed cytoplasmic mini-nuclei.
    Mol Biol Cell. 2001 Jul;12(7):2031-46 PMID: 11452001
  64. Assembly of vaccinia virus revisited: de novo membrane synthesis or acquisition from the host?
    Trends Microbiol. 2002 Jan;10(1):15-24 PMID: 11755081
  65. Brome mosaic virus helicase- and polymerase-like proteins colocalize on the endoplasmic reticulum at sites of viral RNA synthesis.
    J Virol. 1996 Dec;70(12):8908-16 PMID: 8971020
  66. 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
  67. Regulated cleavages at the West Nile virus NS4A-2K-NS4B junctions play a major role in rearranging cytoplasmic membranes and Golgi trafficking of the NS4A protein.
    J Virol. 2006 May;80(9):4623-32 PMID: 16611922
  68. Replication of hepatitis C virus.
    Nat Rev Microbiol. 2007 Jun;5(6):453-63 PMID: 17487147
  69. Identification of the domains required for direct interaction of the helicase-like and polymerase-like RNA replication proteins of brome mosaic virus.
    J Virol. 1992 Dec;66(12):7293-302 PMID: 1433519
  70. 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
  71. Inhibition of poliovirus RNA synthesis by brefeldin A.
    J Virol. 1992 Apr;66(4):1985-94 PMID: 1312615
  72. Conserved determinants for membrane association of nonstructural protein 5A from hepatitis C virus and related viruses.
    J Virol. 2007 Mar;81(6):2745-57 PMID: 17192310
  73. 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
  74. A human virus protein, poliovirus protein 2BC, induces membrane proliferation and blocks the exocytic pathway in the yeast Saccharomyces cerevisiae.
    EMBO J. 1995 Jul 17;14(14):3349-64 PMID: 7628436
  75. Transport between ER and Golgi.
    Curr Opin Cell Biol. 2000 Aug;12(4):445-9 PMID: 10873822
  76. NMR structure and molecular dynamics of the in-plane membrane anchor of nonstructural protein 5A from bovine viral diarrhea virus.
    Biochemistry. 2006 Feb 21;45(7):2221-33 PMID: 16475810
  77. Interactions between viral nonstructural proteins and host protein hVAP-33 mediate the formation of hepatitis C virus RNA replication complex on lipid raft.
    J Virol. 2004 Apr;78(7):3480-8 PMID: 15016871
  78. A viral protein that blocks Arf1-mediated COP-I assembly by inhibiting the guanine nucleotide exchange factor GBF1.
    Dev Cell. 2006 Aug;11(2):191-201 PMID: 16890159
  79. Mouse VAP33 is associated with the endoplasmic reticulum and microtubules.
    Proc Natl Acad Sci U S A. 2000 Feb 1;97(3):1101-6 PMID: 10655491
  80. Intracellular location and translocation of silent and active poliovirus replication complexes.
    J Gen Virol. 2005 Mar;86(Pt 3):707-718 PMID: 15722531
  81. Poliovirus-encoded 2C polypeptide specifically binds to the 3'-terminal sequences of viral negative-strand RNA.
    J Virol. 1997 Dec;71(12):9570-8 PMID: 9371621
  82. Rubella virus replication complexes are virus-modified lysosomes.
    Virology. 1998 Jan 5;240(1):57-63 PMID: 9448689
  83. Molecular machinery of autophagosome formation in yeast, Saccharomyces cerevisiae.
    FEBS Lett. 2007 May 22;581(11):2156-61 PMID: 17382324
  84. 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
  85. The initiation of vaccinia infection.
    Virology. 1960 Jul;11:603-23 PMID: 13806834
  86. Brefeldin A inhibits cell-free, de novo synthesis of poliovirus.
    J Virol. 1998 Aug;72(8):6456-64 PMID: 9658088
  87. Coronavirus replication complex formation utilizes components of cellular autophagy.
    J Biol Chem. 2004 Mar 12;279(11):10136-41 PMID: 14699140
  88. New views of cells in 3D: an introduction to electron tomography.
    Trends Cell Biol. 2005 Jan;15(1):43-51 PMID: 15653077
  89. The intracellular sites of early replication and budding of SARS-coronavirus.
    Virology. 2007 May 10;361(2):304-15 PMID: 17210170
  90. Structural and functional characterization of the poliovirus replication complex.
    J Virol. 1992 May;66(5):2740-7 PMID: 1313898
  91. A functional role for VAP-33 in insulin-stimulated GLUT4 traffic.
    Traffic. 2000 Jun;1(6):512-21 PMID: 11208137
  92. 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
  93. COPI activity coupled with fatty acid biosynthesis is required for viral replication.
    PLoS Pathog. 2006 Oct;2(10):e102 PMID: 17040126
  94. Partial purification and characterization of foxtail mosaic potexvirus RNA-dependent RNA polymerase.
    Virology. 1993 Dec;197(2):695-703 PMID: 8249292
  95. Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex.
    J Virol. 2006 Jun;80(12):5927-40 PMID: 16731931
  96. Palmitoylation and polymerization of hepatitis C virus NS4B protein.
    J Virol. 2006 Jun;80(12):6013-23 PMID: 16731940
  97. Flock house virus RNA replicates on outer mitochondrial membranes in Drosophila cells.
    J Virol. 2001 Dec;75(23):11664-76 PMID: 11689648
  98. A VAMP-binding protein from Aplysia required for neurotransmitter release.
    Science. 1995 Sep 15;269(5230):1580-3 PMID: 7667638
  99. Efficient rescue of hepatitis C virus RNA replication by trans-complementation with nonstructural protein 5A.
    J Virol. 2005 Jan;79(2):896-909 PMID: 15613318
  100. Intracellular distribution of poliovirus proteins and the induction of virus-specific cytoplasmic structures.
    Virology. 1983 Nov;131(1):39-48 PMID: 6316654
  101. Effects of palmitoylation of replicase protein nsP1 on alphavirus infection.
    J Virol. 2000 Aug;74(15):6725-33 PMID: 10888610
  102. Coxsackie B3 virus protein 2B contains cationic amphipathic helix that is required for viral RNA replication.
    J Virol. 1996 Jun;70(6):3876-86 PMID: 8648724
  103. Membrane curvature and mechanisms of dynamic cell membrane remodelling.
    Nature. 2005 Dec 1;438(7068):590-6 PMID: 16319878
  104. Studies of a putative amphipathic helix in the N-terminus of poliovirus protein 2C.
    Virology. 1994 Feb 15;199(1):188-99 PMID: 8116242
  105. Localization of the tomato bushy stunt virus replication protein p33 reveals a peroxisome-to-endoplasmic reticulum sorting pathway.
    Plant Cell. 2005 Dec;17(12):3513-31 PMID: 16284309
  106. ARF proteins: roles in membrane traffic and beyond.
    Nat Rev Mol Cell Biol. 2006 May;7(5):347-58 PMID: 16633337
  107. Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle.
    PLoS Biol. 2007 Sep;5(9):e220 PMID: 17696647
  108. 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
  109. 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
  110. Phosphorylation of cucumber mosaic virus RNA polymerase 2a protein inhibits formation of replicase complex.
    EMBO J. 2002 May 1;21(9):2292-300 PMID: 11980726
  111. 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
  112. Flock house virus RNA polymerase is a transmembrane protein with amino-terminal sequences sufficient for mitochondrial localization and membrane insertion.
    J Virol. 2002 Oct;76(19):9856-67 PMID: 12208963
  113. 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
  114. Alfalfa mosaic virus replicase proteins P1 and P2 interact and colocalize at the vacuolar membrane.
    J Virol. 2001 Feb;75(4):1879-87 PMID: 11160687
  115. An amino-terminal amphipathic alpha-helix mediates membrane association of the hepatitis C virus nonstructural protein 5A.
    J Biol Chem. 2002 Mar 8;277(10):8130-9 PMID: 11744739
  116. A class of membrane proteins with a C-terminal anchor.
    Trends Cell Biol. 1993 Mar;3(3):72-5 PMID: 14731773
Article Info
Journal
Nature reviews. Microbiology
Abbr.
Nat Rev Microbiol
ISSN
1740-1534
DOI
10.1038/nrmicro1890
Email
[email protected]
Published
2008-05-00
Pages
363-74
Language
English
Region
England
NLM ID
101190261
PMCID
PMC7096853
Subset
IM
External Links
PubMed source DOI: 10.1038/nrmicro1890 PMC Full Text View journal details
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