Home LiteratureArticle Details
PMID: 15890959 Published · ppublish English Journal Article

Poliovirus proteins induce membrane association of GTPase ADP-ribosylation factor.

Journal of virology ·Vol. 79 ·No. 11 ·2005-06-00 ·Pages 7207-16

Belov GA, Fogg MH, Ehrenfeld E

Abstract

Poliovirus infection results in the disintegration of intracellular membrane structures and formation of specific vesicles that serve as sites for replication of viral RNA. The mechanism of membrane rearrangement has not been clearly defined. Replication of poliovirus is sensitive to brefeldin A (BFA), a fungal metabolite known to prevent normal function of the ADP-ribosylation factor (ARF) family of small GTPases. During normal membrane trafficking in uninfected cells, ARFs are involved in vesicle formation from different intracellular sites through interaction with numerous regulatory and coat proteins as well as in regulation of phospholipase D activity and cytoskeleton modifications. We demonstrate here that ARFs 3 and 5, but not ARF6, are translocated to membranes in HeLa cell extracts that are engaged in translation of poliovirus RNA. The accumulation of ARFs on membranes correlates with active replication of poliovirus RNA in vitro, whereas ARF translocation to membranes does not occur in the presence of BFA. ARF translocation can be induced independently by synthesis of poliovirus 3A or 3CD proteins, and we describe mutations that abolished this activity. In infected HeLa cells, an ARF1-enhanced green fluorescent protein fusion redistributes from Golgi stacks to the perinuclear region, where poliovirus RNA replication occurs. Taken together, the data suggest an involvement of ARF in poliovirus RNA replication.

MeSH Terms
ADP-Ribosylation Factor 1/genetics,metabolism ADP-Ribosylation Factors/metabolism Biological Transport, Active/drug effects Brefeldin A/pharmacology Green Fluorescent Proteins/genetics,metabolism HeLa Cells Humans In Vitro Techniques Intracellular Membranes/metabolism,virology Mutation Poliovirus/genetics,pathogenicity,physiology RNA, Viral/metabolism Recombinant Fusion Proteins/genetics,metabolism Viral Proteins/genetics,physiology Virus Replication
Chemicals
RNA, Viral Recombinant Fusion Proteins Viral Proteins enhanced green fluorescent protein Green Fluorescent Proteins Brefeldin A ADP-Ribosylation Factor 1 ADP-Ribosylation Factors
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Belov George A
Laboratory of Infectious Diseases, NIAID, NIH, Building 50, Room 6120, Bethesda, MD 20892-8011, USA.
Fogg Mark H
Ehrenfeld Ellie
References (83)
83 references, click to expand
  1. Biochemical dissection of AP-1 recruitment onto Golgi membranes.
    J Cell Biol. 1993 Nov;123(3):561-73 PMID: 8227126
  2. Stepwise assembly of functionally active transport vesicles.
    Cell. 1993 Dec 3;75(5):1015-25 PMID: 8252615
  3. ADP-ribosylation factor, a small GTP-dependent regulatory protein, stimulates phospholipase D activity.
    Cell. 1993 Dec 17;75(6):1137-44 PMID: 8261513
  4. Dominant inhibitory mutants of ARF1 block endoplasmic reticulum to Golgi transport and trigger disassembly of the Golgi apparatus.
    J Biol Chem. 1994 Jan 14;269(2):1437-48 PMID: 8288610
  5. An activating mutation in ARF1 stabilizes coatomer binding to Golgi membranes.
    J Biol Chem. 1994 Feb 4;269(5):3135-8 PMID: 8106346
  6. ADP-ribosylation factor and coatomer couple fusion to vesicle budding.
    J Cell Biol. 1994 Feb;124(4):415-24 PMID: 8106543
  7. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells.
    Virology. 1994 Jul;202(1):129-45 PMID: 8009827
  8. Cytosolic ARFs are required for vesicle formation but not for cell-free intra-Golgi transport: evidence for coated vesicle-independent transport.
    Mol Biol Cell. 1994 Feb;5(2):237-52 PMID: 8019009
  9. Characteristics of the poliovirus replication complex.
    Arch Virol Suppl. 1994;9:147-57 PMID: 8032246
  10. Secretory pathway function, but not cytoskeletal integrity, is required in poliovirus infection.
    Arch Virol Suppl. 1994;9:159-72 PMID: 8032247
  11. ARF1(2-17) does not specifically interact with ARF1-dependent pathways. Inhibition by peptide of phospholipases C beta, D and exocytosis in HL60 cells.
    FEBS Lett. 1994 Jul 25;349(1):34-8 PMID: 8045298
  12. Induction of membrane proliferation by poliovirus proteins 2C and 2BC.
    Biochem Biophys Res Commun. 1995 Jan 5;206(1):64-76 PMID: 7818552
  13. Inhibition of cellular protein secretion by poliovirus proteins 2B and 3A.
    EMBO J. 1995 Mar 1;14(5):894-907 PMID: 7889939
  14. Poliovirus requires a precise 5' end for efficient positive-strand RNA synthesis.
    J Virol. 2000 Jul;74(14):6394-400 PMID: 10864650
  15. Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments.
    J Cell Biol. 1995 Mar;128(6):1003-17 PMID: 7896867
  16. Interaction between the 5'-terminal cloverleaf and 3AB/3CDpro of poliovirus is essential for RNA replication.
    J Virol. 1995 Jun;69(6):3658-67 PMID: 7745714
  17. Inefficient complementation activity of poliovirus 2C and 3D proteins for rescue of lethal mutations.
    J Virol. 1995 Jul;69(7):4245-54 PMID: 7769684
  18. Arf proteins: the membrane traffic police?
    Trends Biochem Sci. 1995 Apr;20(4):147-50 PMID: 7770914
  19. 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
  20. Complete replication of poliovirus in vitro: preinitiation RNA replication complexes require soluble cellular factors for the synthesis of VPg-linked RNA.
    J Virol. 1995 Sep;69(9):5516-27 PMID: 7636997
  21. Human protein Sam68 relocalization and interaction with poliovirus RNA polymerase in infected cells.
    Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2296-301 PMID: 8637866
  22. ADP-ribosylation factor-1 stimulates formation of nascent secretory vesicles from the trans-Golgi network of endocrine cells.
    J Biol Chem. 1996 Mar 8;271(10):5297-300 PMID: 8621377
  23. Evidence that phospholipase D mediates ADP ribosylation factor-dependent formation of Golgi coated vesicles.
    J Cell Biol. 1996 Jul;134(2):295-306 PMID: 8707816
  24. Intracellular distribution of Arf proteins in mammalian cells. Arf6 is uniquely localized to the plasma membrane.
    J Biol Chem. 1996 Sep 6;271(36):21767-74 PMID: 8702973
  25. Cellular origin and ultrastructure of membranes induced during poliovirus infection.
    J Virol. 1996 Oct;70(10):6576-88 PMID: 8794292
  26. The ARF GTPases: defining roles in membrane traffic and organelle structure.
    Cold Spring Harb Symp Quant Biol. 1995;60:229-34 PMID: 8824395
  27. Isolation of a brefeldin A-inhibited guanine nucleotide-exchange protein for ADP ribosylation factor (ARF) 1 and ARF3 that contains a Sec7-like domain.
    Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):12856-60 PMID: 8917509
  28. Comparative activity of ADP-ribosylation factor family members in the early steps of coated vesicle formation on rat liver Golgi membranes.
    J Biol Chem. 1997 Feb 14;272(7):4141-8 PMID: 9020126
  29. 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
  30. Requirement of poly(rC) binding protein 2 for translation of poliovirus RNA.
    J Virol. 1997 Aug;71(8):6243-6 PMID: 9223526
  31. Phospholipase D stimulates release of nascent secretory vesicles from the trans-Golgi network.
    J Cell Biol. 1997 Aug 11;138(3):495-504 PMID: 9245781
  32. The role of ADP-ribosylation factor and phospholipase D in adaptor recruitment.
    J Cell Biol. 1997 Sep 22;138(6):1239-54 PMID: 9298980
  33. Effects of brefeldin A on autophagy in cultured rat fibroblasts.
    Eur J Cell Biol. 1997 Sep;74(1):63-7 PMID: 9309391
  34. ADP-ribosylation factor 6 regulates a novel plasma membrane recycling pathway.
    J Cell Biol. 1997 Oct 6;139(1):49-61 PMID: 9314528
  35. Poly (rC) binding protein 2 forms a ternary complex with the 5'-terminal sequences of poliovirus RNA and the viral 3CD proteinase.
    RNA. 1997 Oct;3(10):1124-34 PMID: 9326487
  36. Poliovirus 2C protein determinants of membrane binding and rearrangements in mammalian cells.
    J Virol. 1997 Dec;71(12):8962-72 PMID: 9371552
  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. Brefeldin A-inhibited guanine nucleotide-exchange activity of Sec7 domain from yeast Sec7 with yeast and mammalian ADP ribosylation factors.
    Proc Natl Acad Sci U S A. 1998 Apr 14;95(8):4204-8 PMID: 9539714
  39. The distribution and translocation of the G protein ADP-ribosylation factor 1 in live cells is determined by its GTPase activity.
    J Cell Sci. 1998 May;111 ( Pt 9):1277-85 PMID: 9547306
  40. Identification of regions of poliovirus 2BC protein that are involved in cytotoxicity.
    J Virol. 1998 May;72(5):3560-70 PMID: 9557636
  41. Brefeldin A inhibits cell-free, de novo synthesis of poliovirus.
    J Virol. 1998 Aug;72(8):6456-64 PMID: 9658088
  42. Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirus-infected cells.
    J Virol. 1998 Aug;72(8):6699-709 PMID: 9658117
  43. Building a secretory apparatus: role of ARF1/COPI in Golgi biogenesis and maintenance.
    Histochem Cell Biol. 1998 May-Jun;109(5-6):449-62 PMID: 9681627
  44. ADP-Ribosylation factor 1 (ARF1) regulates recruitment of the AP-3 adaptor complex to membranes.
    J Cell Biol. 1998 Jul 27;142(2):391-402 PMID: 9679139
  45. Switch from translation to RNA replication in a positive-stranded RNA virus.
    Genes Dev. 1998 Aug 1;12(15):2293-304 PMID: 9694795
  46. Molecules in the ARF orbit.
    J Biol Chem. 1998 Aug 21;273(34):21431-4 PMID: 9705267
  47. ADP-ribosylation factor and phosphatidic acid levels in Golgi membranes during budding of coatomer-coated vesicles.
    Proc Natl Acad Sci U S A. 1998 Nov 10;95(23):13676-80 PMID: 9811859
  48. Structural basis for the inhibitory effect of brefeldin A on guanine nucleotide-exchange proteins for ADP-ribosylation factors.
    Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):2752-7 PMID: 10077583
  49. Brefeldin A acts to stabilize an abortive ARF-GDP-Sec7 domain protein complex: involvement of specific residues of the Sec7 domain.
    Mol Cell. 1999 Mar;3(3):275-85 PMID: 10198630
  50. Phospholipase D as an effector for ADP-ribosylation factor in the regulation of vesicular traffic.
    Chem Phys Lipids. 1999 Apr;98(1-2):141-52 PMID: 10358936
  51. 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
  52. 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
  53. 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
  54. Nucleolin stimulates viral internal ribosome entry site-mediated translation.
    Virus Res. 2001 Jul;76(1):17-29 PMID: 11376843
  55. Involvement of ADP-ribosylation factor 1 in cholera toxin-induced morphological changes of Chinese hamster ovary cells.
    J Biol Chem. 2001 Jun 22;276(25):22838-43 PMID: 11279243
  56. 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
  57. 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
  58. 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
  59. Molecular aspects of the cellular activities of ADP-ribosylation factors.
    Sci STKE. 2000 Nov 21;2000(59):re1 PMID: 11752622
  60. The viral protein 3CD induces an equilibrium between the viral protein and RNA synthesis in a cell-free system for poliovirus replication.
    Arch Virol. 2002 Apr;147(4):731-44 PMID: 12038684
  61. 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
  62. ARF1 regulatory factors and COPI vesicle formation.
    Curr Opin Cell Biol. 2002 Aug;14(4):423-7 PMID: 12383792
  63. Arf and its many interactors.
    Curr Opin Cell Biol. 2003 Aug;15(4):396-404 PMID: 12892779
  64. Membrane requirements for uridylylation of the poliovirus VPg protein and viral RNA synthesis in vitro.
    J Virol. 2003 Nov;77(21):11408-16 PMID: 14557626
  65. A role for Arf1 in mitotic Golgi disassembly, chromosome segregation, and cytokinesis.
    Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13314-9 PMID: 14585930
  66. 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
  67. Structural basis for proteolysis-dependent activation of the poliovirus RNA-dependent RNA polymerase.
    EMBO J. 2004 Sep 1;23(17):3462-71 PMID: 15306852
  68. Intracellular distribution of poliovirus proteins and the induction of virus-specific cytoplasmic structures.
    Virology. 1983 Nov;131(1):39-48 PMID: 6316654
  69. The host protein required for in vitro replication of poliovirus is a protein kinase that phosphorylates eukaryotic initiation factor-2.
    Cell. 1985 Apr;40(4):913-21 PMID: 2985268
  70. Poliovirus protein 3CD is the active protease for processing of the precursor protein P1 in vitro.
    J Gen Virol. 1988 Jul;69 ( Pt 7):1627-36 PMID: 2839599
  71. Poliovirus mutant that contains a cold-sensitive defect in viral RNA synthesis.
    J Virol. 1988 Aug;62(8):2922-8 PMID: 2839711
  72. Protein 3CD is the major poliovirus proteinase responsible for cleavage of the P1 capsid precursor.
    Virology. 1988 Sep;166(1):265-70 PMID: 2842953
  73. 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
  74. ADP-ribosylation factor is a subunit of the coat of Golgi-derived COP-coated vesicles: a novel role for a GTP-binding protein.
    Cell. 1991 Oct 18;67(2):239-53 PMID: 1680566
  75. Cell-free, de novo synthesis of poliovirus.
    Science. 1991 Dec 13;254(5038):1647-51 PMID: 1661029
  76. Inhibition of poliovirus RNA synthesis by brefeldin A.
    J Virol. 1992 Apr;66(4):1985-94 PMID: 1312615
  77. Structural and functional characterization of the poliovirus replication complex.
    J Virol. 1992 May;66(5):2740-7 PMID: 1313898
  78. ADP-ribosylation factor is required for vesicular trafficking between the endoplasmic reticulum and the cis-Golgi compartment.
    J Biol Chem. 1992 Jun 25;267(18):13053-61 PMID: 1618803
  79. Involvement of membrane traffic in the replication of poliovirus genomes: effects of brefeldin A.
    Virology. 1992 Nov;191(1):166-75 PMID: 1329315
  80. Intracellular localization of poliovirus RNA by in situ hybridization at the ultrastructural level using single-stranded riboprobes.
    Virology. 1992 Dec;191(2):687-97 PMID: 1333118
  81. Effects of brefeldin A and accessory proteins on association of ADP-ribosylation factors 1, 3, and 5 with Golgi.
    J Biol Chem. 1993 May 25;268(15):10820-5 PMID: 8496147
  82. The binding of AP-1 clathrin adaptor particles to Golgi membranes requires ADP-ribosylation factor, a small GTP-binding protein.
    Cell. 1993 Jun 4;73(5):999-1005 PMID: 8500185
  83. Coated vesicle assembly in the Golgi requires only coatomer and ARF proteins from the cytosol.
    Nature. 1993 Aug 19;364(6439):732-4 PMID: 8355790
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2005-06-00
Pages
7207-16
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC1112117
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]