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Cellular origin and ultrastructure of membranes induced during poliovirus infection.

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  • 1. Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder 80309, USA.
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    • Schlegel A 1
    (1 author)

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Journal of Virology, 01 Oct 1996, 70(10):6576-6588
https://doi.org/10.1128/jvi.70.10.6576-6588.1996 PMID: 8794292 PMCID: PMC190698

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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.

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J Virol. 1996 Oct; 70(10): 6576–6588.
PMCID: PMC190698
PMID: 8794292

Cellular origin and ultrastructure of membranes induced during poliovirus infection.

A Schlegel, T H Giddings, Jr, M S Ladinsky, and K Kirkegaard
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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.

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Selected References
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  • Aldabe R, Carrasco L. Induction of membrane proliferation by poliovirus proteins 2C and 2BC. Biochem Biophys Res Commun. 1995 Jan 5;206(1):64–76. [Abstract] [Google Scholar]
  • Amako K, Dales S. Cytopathology of Mengovirus infection. I. Relationship between cellular disintegration and virulence. Virology. 1967 Jun;32(2):184–200. [Abstract] [Google Scholar]
  • Amako K, Dales S. Cytopathology of Mengovirus infection. II. Proliferation of membranous cisternae. Virology. 1967 Jun;32(2):201–215. [Abstract] [Google Scholar]
  • Andino R, Rieckhof GE, Achacoso PL, Baltimore D. Poliovirus RNA synthesis utilizes an RNP complex formed around the 5'-end of viral RNA. EMBO J. 1993 Sep;12(9):3587–3598. [Europe PMC free article] [Abstract] [Google Scholar]
  • Barco A, Carrasco L. 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):3349–3364. [Europe PMC free article] [Abstract] [Google Scholar]
  • Barco A, Carrasco L. Poliovirus 2Apro expression inhibits growth of yeast cells. FEBS Lett. 1995 Aug 28;371(1):4–8. [Abstract] [Google Scholar]
  • Bienz K, Egger D, Pasamontes L. 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):220–226. [Abstract] [Google Scholar]
  • Bienz K, Egger D, Pfister T, Troxler M. Structural and functional characterization of the poliovirus replication complex. J Virol. 1992 May;66(5):2740–2747. [Europe PMC free article] [Abstract] [Google Scholar]
  • Bienz K, Egger D, Rasser Y, Bossart W. Intracellular distribution of poliovirus proteins and the induction of virus-specific cytoplasmic structures. Virology. 1983 Nov;131(1):39–48. [Abstract] [Google Scholar]
  • Bienz K, Egger D, Troxler M, Pasamontes L. Structural organization of poliovirus RNA replication is mediated by viral proteins of the P2 genomic region. J Virol. 1990 Mar;64(3):1156–1163. [Europe PMC free article] [Abstract] [Google Scholar]
  • Blobel G, Dobberstein B. 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):835–851. [Europe PMC free article] [Abstract] [Google Scholar]
  • Butterworth BE, Shimshick EJ, Yin FH. Association of the polioviral RNA polymerase complex with phospholipid membranes. J Virol. 1976 Aug;19(2):457–466. [Europe PMC free article] [Abstract] [Google Scholar]
  • Caliguiri LA, Tamm I. The role of cytoplasmic membranes in poliovirus biosynthesis. Virology. 1970 Sep;42(1):100–111. [Abstract] [Google Scholar]
  • Carlsson SR, Roth J, Piller F, Fukuda M. 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):18911–18919. [Abstract] [Google Scholar]
  • Cho MW, Teterina N, Egger D, Bienz K, Ehrenfeld E. Membrane rearrangement and vesicle induction by recombinant poliovirus 2C and 2BC in human cells. Virology. 1994 Jul;202(1):129–145. [Abstract] [Google Scholar]
  • Clark ME, Hämmerle T, Wimmer E, Dasgupta A. 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):2941–2947. [Europe PMC free article] [Abstract] [Google Scholar]
  • Clark ME, Lieberman PM, Berk AJ, Dasgupta A. Direct cleavage of human TATA-binding protein by poliovirus protease 3C in vivo and in vitro. Mol Cell Biol. 1993 Feb;13(2):1232–1237. [Europe PMC free article] [Abstract] [Google Scholar]
  • Crawford N, Fire A, Samuels M, Sharp PA, Baltimore D. Inhibition of transcription factor activity by poliovirus. Cell. 1981 Dec;27(3 Pt 2):555–561. [Abstract] [Google Scholar]
  • Dahl R, Staehelin LA. High-pressure freezing for the preservation of biological structure: theory and practice. J Electron Microsc Tech. 1989 Nov;13(3):165–174. [Abstract] [Google Scholar]
  • DALES S, EGGERS HJ, TAMM I, PALADE GE. ELECTRON MICROSCOPIC STUDY OF THE FORMATION OF POLIOVIRUS. Virology. 1965 Jul;26:379–389. [Abstract] [Google Scholar]
  • DALES S, FRANKLIN RM. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Datta U, Dasgupta A. Expression and subcellular localization of poliovirus VPg-precursor protein 3AB in eukaryotic cells: evidence for glycosylation in vitro. J Virol. 1994 Jul;68(7):4468–4477. [Europe PMC free article] [Abstract] [Google Scholar]
  • Doedens JR, Kirkegaard K. Inhibition of cellular protein secretion by poliovirus proteins 2B and 3A. EMBO J. 1995 Mar 1;14(5):894–907. [Europe PMC free article] [Abstract] [Google Scholar]
  • Dunn WA., Jr Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J Cell Biol. 1990 Jun;110(6):1923–1933. [Europe PMC free article] [Abstract] [Google Scholar]
  • Dunn WA., Jr Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. J Cell Biol. 1990 Jun;110(6):1935–1945. [Europe PMC free article] [Abstract] [Google Scholar]
  • Dunn WA., Jr Autophagy and related mechanisms of lysosome-mediated protein degradation. Trends Cell Biol. 1994 Apr;4(4):139–143. [Abstract] [Google Scholar]
  • Etchison D, Milburn SC, Edery I, Sonenberg N, Hershey JW. 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):14806–14810. [Abstract] [Google Scholar]
  • Franzusoff A, Lauzé E, Howell KE. Immuno-isolation of Sec7p-coated transport vesicles from the yeast secretory pathway. Nature. 1992 Jan 9;355(6356):173–175. [Abstract] [Google Scholar]
  • Froshauer S, Kartenbeck J, Helenius A. Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. J Cell Biol. 1988 Dec;107(6 Pt 1):2075–2086. [Europe PMC free article] [Abstract] [Google Scholar]
  • GODMAN GC, RIFKIND RA, HOWE C, ROSE HM. A DESCRIPTION OF ECHO-9 VIRUS INFECTION IN CULTURED CELLS. I. THE CYTOPATHIC EFFECT. Am J Pathol. 1964 Jan;44:1–27. [Europe PMC free article] [Abstract] [Google Scholar]
  • GODMAN GC, RIFKIND RA, PAGE RB, HOWE C, ROSE HM. A DESCRIPTION OF ECHO-9 VIRUS INFECTION IN CULTURED CELLS. II. CYTOCHEMICAL OBSERVATIONS. Am J Pathol. 1964 Feb;44:215–245. [Europe PMC free article] [Abstract] [Google Scholar]
  • Griffiths G, Ericsson M, Krijnse-Locker J, Nilsson T, Goud B, Söling HD, Tang BL, Wong SH, Hong W. 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):1557–1574. [Europe PMC free article] [Abstract] [Google Scholar]
  • Griffiths G, Fuller SD, Back R, Hollinshead M, Pfeiffer S, Simons K. The dynamic nature of the Golgi complex. J Cell Biol. 1989 Feb;108(2):277–297. [Europe PMC free article] [Abstract] [Google Scholar]
  • Guskey LE, Smith PC, Wolff DA. 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):151–161. [Abstract] [Google Scholar]
  • Harris KS, Xiang W, Alexander L, Lane WS, Paul AV, Wimmer E. 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):27004–27014. [Abstract] [Google Scholar]
  • Heding LD, Wolff DA. The cytochemical examination of poliovirus-induced cell damage. J Cell Biol. 1973 Nov;59(2 Pt 1):530–536. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hershman KM, Fleming WW, Taylor DA. A quantitative method for assessing protein abundance using enhanced chemiluminescence. Biotechniques. 1993 Nov;15(5):790–passim. [Abstract] [Google Scholar]
  • Houri JJ, Ogier-Denis E, Trugnan G, Codogno P. Autophagic degradation of N-linked glycoproteins is downregulated in differentiated human colon adenocarcinoma cells. Biochem Biophys Res Commun. 1993 Dec 15;197(2):805–811. [Abstract] [Google Scholar]
  • Irurzun A, Arroyo J, Alvarez A, Carrasco L. Enhanced intracellular calcium concentration during poliovirus infection. J Virol. 1995 Aug;69(8):5142–5146. [Europe PMC free article] [Abstract] [Google Scholar]
  • Irurzun A, Perez L, Carrasco L. Involvement of membrane traffic in the replication of poliovirus genomes: effects of brefeldin A. Virology. 1992 Nov;191(1):166–175. [Abstract] [Google Scholar]
  • Jézéquel AM, Steiner JW. Some ultrastructural and histochemical aspects of Coxsackie virus-cell interactions. Lab Invest. 1966 Jun;15(6):1055–1083. [Abstract] [Google Scholar]
  • Krijnse-Locker J, Ericsson M, Rottier PJ, Griffiths G. 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. [Europe PMC free article] [Abstract] [Google Scholar]
  • Bishop WW, Dickson JH. Radiocarbon dates related to the Scottish Late-Glacial Sea in the Firth of Clyde. Nature. 1970 Aug 1;227(5257):480–482. [Abstract] [Google Scholar]
  • Lawrence BP, Brown WJ. Autophagic vacuoles rapidly fuse with pre-existing lysosomes in cultured hepatocytes. J Cell Sci. 1992 Jul;102(Pt 3):515–526. [Abstract] [Google Scholar]
  • Lawrence BP, Brown WJ. Inhibition of protein synthesis separates autophagic sequestration from the delivery of lysosomal enzymes. J Cell Sci. 1993 Jun;105(Pt 2):473–480. [Abstract] [Google Scholar]
  • Maynell LA, Kirkegaard K, Klymkowsky MW. Inhibition of poliovirus RNA synthesis by brefeldin A. J Virol. 1992 Apr;66(4):1985–1994. [Europe PMC free article] [Abstract] [Google Scholar]
  • Pasamontes L, Egger D, Bienz K. Production of monoclonal and monospecific antibodies against non-capsid proteins of poliovirus. J Gen Virol. 1986 Nov;67(Pt 11):2415–2422. [Abstract] [Google Scholar]
  • Pata JD, Schultz SC, Kirkegaard K. Functional oligomerization of poliovirus RNA-dependent RNA polymerase. RNA. 1995 Jul;1(5):466–477. [Europe PMC free article] [Abstract] [Google Scholar]
  • Pfister T, Egger D, Bienz K. Poliovirus subviral particles associated with progeny RNA in the replication complex. J Gen Virol. 1995 Jan;76(Pt 1):63–71. [Abstract] [Google Scholar]
  • Pfister T, Pasamontes L, Troxler M, Egger D, Bienz K. Immunocytochemical localization of capsid-related particles in subcellular fractions of poliovirus-infected cells. Virology. 1992 Jun;188(2):676–684. [Abstract] [Google Scholar]
  • Punnonen EL, Autio S, Kaija H, Reunanen H. Autophagic vacuoles fuse with the prelysosomal compartment in cultured rat fibroblasts. Eur J Cell Biol. 1993 Jun;61(1):54–66. [Abstract] [Google Scholar]
  • Rabouille C, Hui N, Hunte F, Kieckbusch R, Berger EG, Warren G, Nilsson T. Mapping the distribution of Golgi enzymes involved in the construction of complex oligosaccharides. J Cell Sci. 1995 Apr;108(Pt 4):1617–1627. [Abstract] [Google Scholar]
  • Rothman JE. Mechanisms of intracellular protein transport. Nature. 1994 Nov 3;372(6501):55–63. [Abstract] [Google Scholar]
  • Schweizer A, Ericsson M, Bächi T, Griffiths G, Hauri HP. 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):671–683. [Abstract] [Google Scholar]
  • Schweizer A, Rohrer J, Slot JW, Geuze HJ, Kornfeld S. Reassessment of the subcellular localization of p63. J Cell Sci. 1995 Jun;108(Pt 6):2477–2485. [Abstract] [Google Scholar]
  • Skinner MS, Halperen S, Harkin JC. Cytoplasmic membrane-bound vesicles in echovirus 12-infected cells. Virology. 1968 Oct;36(2):241–253. [Abstract] [Google Scholar]
  • Strous GJ, Van Kerkhof P, Willemsen R, Geuze HJ, Berger EG. Transport and topology of galactosyltransferase in endomembranes of HeLa cells. J Cell Biol. 1983 Sep;97(3):723–727. [Europe PMC free article] [Abstract] [Google Scholar]
  • Takeda N, Kuhn RJ, Yang CF, Takegami T, Wimmer E. Initiation of poliovirus plus-strand RNA synthesis in a membrane complex of infected HeLa cells. J Virol. 1986 Oct;60(1):43–53. [Europe PMC free article] [Abstract] [Google Scholar]
  • Takegami T, Semler BL, Anderson CW, Wimmer E. Membrane fractions active in poliovirus RNA replication contain VPg precursor polypeptides. Virology. 1983 Jul 15;128(1):33–47. [Abstract] [Google Scholar]
  • Tershak DR. Association of poliovirus proteins with the endoplasmic reticulum. J Virol. 1984 Dec;52(3):777–783. [Europe PMC free article] [Abstract] [Google Scholar]
  • Towbin H, Staehelin T, Gordon J. 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):4350–4354. [Europe PMC free article] [Abstract] [Google Scholar]
  • Toyoda H, Yang CF, Takeda N, Nomoto A, Wimmer E. Analysis of RNA synthesis of type 1 poliovirus by using an in vitro molecular genetic approach. J Virol. 1987 Sep;61(9):2816–2822. [Europe PMC free article] [Abstract] [Google Scholar]
  • Troxler M, Egger D, Pfister T, Bienz K. Intracellular localization of poliovirus RNA by in situ hybridization at the ultrastructural level using single-stranded riboprobes. Virology. 1992 Dec;191(2):687–697. [Abstract] [Google Scholar]
  • Trugnan G, Ogier-Denis E, Sapin C, Darmoul D, Bauvy C, Aubery M, Codogno P. 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):20849–20855. [Abstract] [Google Scholar]
  • Watzele G, Bachofner R, Berger EG. Immunocytochemical localization of the Golgi apparatus using protein-specific antibodies to galactosyltransferase. Eur J Cell Biol. 1991 Dec;56(2):451–458. [Abstract] [Google Scholar]
  • Wu SX, Ahlquist P, Kaesberg P. Active complete in vitro replication of nodavirus RNA requires glycerophospholipid. Proc Natl Acad Sci U S A. 1992 Dec 1;89(23):11136–11140. [Europe PMC free article] [Abstract] [Google Scholar]
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