Home LiteratureArticle Details
PMID: 8794292 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Cellular origin and ultrastructure of membranes induced during poliovirus infection.

Journal of virology ·Vol. 70 ·No. 10 ·1996-10-00 ·Pages 6576-88

Schlegel A, Giddings TH, Ladinsky MS, Kirkegaard K

Abstract

Poliovirus RNA replicative complexes are associated with cytoplasmic membranous structures that accumulate during viral infection. These membranes were immunoisolated by using a monoclonal antibody against the viral nonstructural protein 2C. Biochemical analysis of the isolated membranes revealed that several organelles of the host cell (lysosomes, trans-Golgi stack and trans-Golgi network, and endoplasmic reticulum) contributed to the virus-induced membranous structures. Electron microscopy of infected cells preserved by high-pressure freezing revealed that the virus-induced membranes contain double lipid bilayers that surround apparently cytosolic material. Immunolabeling experiments showed that poliovirus proteins 2C and 3D were localized to the same membranes as the cellular markers tested. The morphological and biochemical data are consistent with the hypothesis that autophagy or a similar host process is involved in the formation of the poliovirus-induced membranes.

MeSH Terms
Cell Membrane/ultrastructure,virology HeLa Cells Humans Microscopy, Electron Poliomyelitis/pathology Poliovirus
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Schlegel A
Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder 80309, USA.
Giddings T H
Ladinsky M S
Kirkegaard K
References (66)
66 references, click to expand
  1. Reassessment of the subcellular localization of p63.
    J Cell Sci. 1995 Jun;108 ( Pt 6):2477-85 PMID: 7673362
  2. Intracellular distribution of poliovirus proteins and the induction of virus-specific cytoplasmic structures.
    Virology. 1983 Nov;131(1):39-48 PMID: 6316654
  3. Mechanisms of intracellular protein transport.
    Nature. 1994 Nov 3;372(6501):55-63 PMID: 7969419
  4. Autophagic degradation of N-linked glycoproteins is downregulated in differentiated human colon adenocarcinoma cells.
    Biochem Biophys Res Commun. 1993 Dec 15;197(2):805-11 PMID: 8267619
  5. ELECTRON MICROSCOPIC STUDY OF THE FORMATION OF POLIOVIRUS.
    Virology. 1965 Jul;26:379-89 PMID: 14319710
  6. Localization of the Lys, Asp, Glu, Leu tetrapeptide receptor to the Golgi complex and the intermediate compartment in mammalian cells.
    J Cell Biol. 1994 Dec;127(6 Pt 1):1557-74 PMID: 7798312
  7. Association of the polioviral RNA polymerase complex with phospholipid membranes.
    J Virol. 1976 Aug;19(2):457-66 PMID: 183011
  8. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex.
    J Biol Chem. 1982 Dec 25;257(24):14806-10 PMID: 6294080
  9. Cytoplasmic membrane-bound vesicles in echovirus 12-infected cells.
    Virology. 1968 Oct;36(2):241-53 PMID: 4879189
  10. Poliovirus proteinase 3C converts an active form of transcription factor IIIC to an inactive form: a mechanism for inhibition of host cell polymerase III transcription by poliovirus.
    EMBO J. 1991 Oct;10(10):2941-7 PMID: 1915271
  11. Expression and subcellular localization of poliovirus VPg-precursor protein 3AB in eukaryotic cells: evidence for glycosylation in vitro.
    J Virol. 1994 Jul;68(7):4468-77 PMID: 8207820
  12. A DESCRIPTION OF ECHO-9 VIRUS INFECTION IN CULTURED CELLS. II. CYTOCHEMICAL OBSERVATIONS.
    Am J Pathol. 1964 Feb;44:215-45 PMID: 14119168
  13. Transport and topology of galactosyltransferase in endomembranes of HeLa cells.
    J Cell Biol. 1983 Sep;97(3):723-7 PMID: 6411739
  14. Studies on the mechanisms of autophagy: formation of the autophagic vacuole.
    J Cell Biol. 1990 Jun;110(6):1923-33 PMID: 2351689
  15. Initiation of poliovirus plus-strand RNA synthesis in a membrane complex of infected HeLa cells.
    J Virol. 1986 Oct;60(1):43-53 PMID: 3018300
  16. Immunocytochemical localization of the Golgi apparatus using protein-specific antibodies to galactosyltransferase.
    Eur J Cell Biol. 1991 Dec;56(2):451-8 PMID: 1724963
  17. Functional oligomerization of poliovirus RNA-dependent RNA polymerase.
    RNA. 1995 Jul;1(5):466-77 PMID: 7489508
  18. Structural and functional characterization of the poliovirus replication complex.
    J Virol. 1992 May;66(5):2740-7 PMID: 1313898
  19. Poliovirus subviral particles associated with progeny RNA in the replication complex.
    J Gen Virol. 1995 Jan;76 ( Pt 1):63-71 PMID: 7844543
  20. 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
  21. Poliovirus 2Apro expression inhibits growth of yeast cells.
    FEBS Lett. 1995 Aug 28;371(1):4-8 PMID: 7664881
  22. The role of cytoplasmic membranes in poliovirus biosynthesis.
    Virology. 1970 Sep;42(1):100-11 PMID: 4318974
  23. Enhanced intracellular calcium concentration during poliovirus infection.
    J Virol. 1995 Aug;69(8):5142-6 PMID: 7609085
  24. 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
  25. 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
  26. Induction of membrane proliferation by poliovirus proteins 2C and 2BC.
    Biochem Biophys Res Commun. 1995 Jan 5;206(1):64-76 PMID: 7818552
  27. Autophagic vacuoles rapidly fuse with pre-existing lysosomes in cultured hepatocytes.
    J Cell Sci. 1992 Jul;102 ( Pt 3):515-26 PMID: 1324248
  28. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  29. Cytopathology of Mengovirus infection. I. Relationship between cellular disintegration and virulence.
    Virology. 1967 Jun;32(2):184-200 PMID: 4290639
  30. The N-glycan processing in HT-29 cells is a function of their state of enterocytic differentiation. Evidence for an atypical traffic associated with change in polypeptide stability in undifferentiated HT-29 cells.
    J Biol Chem. 1991 Nov 5;266(31):20849-55 PMID: 1834650
  31. Inhibition of cellular protein secretion by poliovirus proteins 2B and 3A.
    EMBO J. 1995 Mar 1;14(5):894-907 PMID: 7889939
  32. Inhibition of poliovirus RNA synthesis by brefeldin A.
    J Virol. 1992 Apr;66(4):1985-94 PMID: 1312615
  33. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5'-end of viral RNA.
    EMBO J. 1993 Sep;12(9):3587-98 PMID: 8253083
  34. A quantitative method for assessing protein abundance using enhanced chemiluminescence.
    Biotechniques. 1993 Nov;15(5):790, 792, 794 passim PMID: 8267963
  35. A comparison of the changes in fine structure of L cells during single cycles of viral multiplication, following their infection with the viruses of Mengo and encephalomyocarditis.
    J Cell Biol. 1962 Aug;14:281-302 PMID: 13883195
  36. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma.
    J Cell Biol. 1975 Dec;67(3):835-51 PMID: 811671
  37. Production of monoclonal and monospecific antibodies against non-capsid proteins of poliovirus.
    J Gen Virol. 1986 Nov;67 ( Pt 11):2415-22 PMID: 2431100
  38. Involvement of membrane traffic in the replication of poliovirus genomes: effects of brefeldin A.
    Virology. 1992 Nov;191(1):166-75 PMID: 1329315
  39. Autophagic vacuoles fuse with the prelysosomal compartment in cultured rat fibroblasts.
    Eur J Cell Biol. 1993 Jun;61(1):54-66 PMID: 8223708
  40. Autophagy and related mechanisms of lysosome-mediated protein degradation.
    Trends Cell Biol. 1994 Apr;4(4):139-43 PMID: 14731737
  41. Association of poliovirus proteins with the endoplasmic reticulum.
    J Virol. 1984 Dec;52(3):777-83 PMID: 6092710
  42. Isolation and characterization of human lysosomal membrane glycoproteins, h-lamp-1 and h-lamp-2. Major sialoglycoproteins carrying polylactosaminoglycan.
    J Biol Chem. 1988 Dec 15;263(35):18911-9 PMID: 3143719
  43. The cytochemical examination of poliovirus-induced cell damage.
    J Cell Biol. 1973 Nov;59(2 Pt 1):530-6 PMID: 4375684
  44. 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
  45. Membrane fractions active in poliovirus RNA replication contain VPg precursor polypeptides.
    Virology. 1983 Jul 15;128(1):33-47 PMID: 6308897
  46. The dynamic nature of the Golgi complex.
    J Cell Biol. 1989 Feb;108(2):277-97 PMID: 2537312
  47. Cytopathology of Mengovirus infection. II. Proliferation of membranous cisternae.
    Virology. 1967 Jun;32(2):201-15 PMID: 4290640
  48. A DESCRIPTION OF ECHO-9 VIRUS INFECTION IN CULTURED CELLS. I. THE CYTOPATHIC EFFECT.
    Am J Pathol. 1964 Jan;44:1-27 PMID: 14103199
  49. Inhibition of protein synthesis separates autophagic sequestration from the delivery of lysosomal enzymes.
    J Cell Sci. 1993 Jun;105 ( Pt 2):473-80 PMID: 8408278
  50. 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
  51. Immuno-isolation of Sec7p-coated transport vesicles from the yeast secretory pathway.
    Nature. 1992 Jan 9;355(6356):173-5 PMID: 1729652
  52. Radiocarbon dates related to the Scottish Late-Glacial Sea in the Firth of Clyde.
    Nature. 1970 Aug 1;227(5257):480-2 PMID: 16058010
  53. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides.
    J Cell Sci. 1995 Apr;108 ( Pt 4):1617-27 PMID: 7615680
  54. Analysis of RNA synthesis of type 1 poliovirus by using an in vitro molecular genetic approach.
    J Virol. 1987 Sep;61(9):2816-22 PMID: 3039171
  55. Characterization of a novel 63 kDa membrane protein. Implications for the organization of the ER-to-Golgi pathway.
    J Cell Sci. 1993 Mar;104 ( Pt 3):671-83 PMID: 8314869
  56. Active complete in vitro replication of nodavirus RNA requires glycerophospholipid.
    Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11136-40 PMID: 1454791
  57. Some ultrastructural and histochemical aspects of Coxsackie virus-cell interactions.
    Lab Invest. 1966 Jun;15(6):1055-83 PMID: 5911943
  58. Direct cleavage of human TATA-binding protein by poliovirus protease 3C in vivo and in vitro.
    Mol Cell Biol. 1993 Feb;13(2):1232-7 PMID: 8380894
  59. Inhibition of transcription factor activity by poliovirus.
    Cell. 1981 Dec;27(3 Pt 2):555-61 PMID: 6086108
  60. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells.
    Virology. 1994 Jul;202(1):129-45 PMID: 8009827
  61. High-pressure freezing for the preservation of biological structure: theory and practice.
    J Electron Microsc Tech. 1989 Nov;13(3):165-74 PMID: 2685196
  62. Immunocytochemical localization of capsid-related particles in subcellular fractions of poliovirus-infected cells.
    Virology. 1992 Jun;188(2):676-84 PMID: 1316678
  63. Studies on the mechanisms of autophagy: maturation of the autophagic vacuole.
    J Cell Biol. 1990 Jun;110(6):1935-45 PMID: 2161853
  64. Interaction of poliovirus polypeptide 3CDpro with the 5' and 3' termini of the poliovirus genome. Identification of viral and cellular cofactors needed for efficient binding.
    J Biol Chem. 1994 Oct 28;269(43):27004-14 PMID: 7929441
  65. Patterns of cytopathology and lysosomal enzyme release in poliovirus-infected HEp-2 cells treated with either 2-(alpha-hydroxybenzyl)-benzimidazole or guanidine HCl.
    J Gen Virol. 1970 Jan;6(1):151-61 PMID: 4313397
  66. 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
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1996-10-00
Pages
6576-88
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC190698
Subset
IM
Grants
NIAID NIH HHS · AI 25166 · United States
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]