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PMID: 7559769 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Virus-mediated release of endosomal content in vitro: different behavior of adenovirus and rhinovirus serotype 2.

The Journal of cell biology ·Vol. 131 ·No. 1 ·1995-10-00 ·Pages 111-23

Prchla E, Plank C, Wagner E, Blaas D, Fuchs R

Abstract

Endosomal penetration by nonenveloped viruses might be accomplished by either local breakdown of the endosomal membrane (e.g., adenovirus) or formation of a membrane-spanning pore by capsid proteins. Uncoating of the nonenveloped virus human rhinovirus serotype 2 (HRV2) has been shown to occur from late endosomes and to be entirely dependent on the acidic pH in this compartment (Prchla, E., E. Kuechler, D. Blaas, and R. Fuchs. 1994. J. Virol. 68: 3713-3723). To investigate further the mechanism of uncoating of HRV2, an in vitro assay was established to test viruses or virus-derived peptides for their capacity to release cointernalized biotin-dextran of different molecular mass (10 and 70 kD) from isolated endosomes. The suitability of the assay was demonstrated by use of a fusogenic peptide derived from influenza virus hemagglutinin (GALA-INF3). Whereas adenovirus induced a low pH-dependent release of up to 46% of the internalized biotin-dextran and did not show any significant size selectivity (as expected for endosome disruption), HRV2 mediated release of 27% of the 10 kD dextran and only traces of the 70-kD dextran. Similarly, GALA-INF3-induced release of biotin-dextran was also size dependent. The potential role of the capsid protein VP1 in HRV2 uncoating in vivo was also substantiated in our in vitro system using an amphipathic, NH2-terminal peptide of VP1. Taken together, these data favor the model of a specific pore-forming mechanism for HRV2 uncoating which is in contrast to the membrane-disrupting mechanism of adenovirus.

MeSH Terms
Adenoviridae/metabolism Amino Acid Sequence Antigens, Viral/metabolism Biomarkers Biotin Capsid/metabolism Capsid Proteins Cell-Free System/metabolism,virology Dextrans Endosomes/metabolism,virology HeLa Cells/metabolism,virology Humans Molecular Sequence Data Molecular Weight Peptides/pharmacology Porins/metabolism Rhinovirus/classification,metabolism Serotyping
Chemicals
Antigens, Viral Biomarkers Capsid Proteins Dextrans Peptides Porins Biotin
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Prchla E
Department of General and Experimental Pathology, University of Vienna, Austria.
Plank C
Wagner E
Blaas D
Fuchs R
References (62)
62 references, click to expand
  1. Proteins are cointernalized with virion particles during early infection.
    Virology. 1987 Sep;160(1):75-80 PMID: 2820142
  2. Cytoplasmic dynein-dependent vesicular transport from early to late endosomes.
    J Cell Biol. 1993 Dec;123(6 Pt 1):1373-87 PMID: 8253838
  3. Stabilization of human rhinovirus serotype 2 against pH-induced conformational change by antiviral compounds.
    J Gen Virol. 1991 Feb;72 ( Pt 2):431-3 PMID: 1847178
  4. Influenza virus hemagglutinin HA-2 N-terminal fusogenic peptides augment gene transfer by transferrin-polylysine-DNA complexes: toward a synthetic virus-like gene-transfer vehicle.
    Proc Natl Acad Sci U S A. 1992 Sep 1;89(17):7934-8 PMID: 1518816
  5. Adenovirus-mediated augmentation of cell transfection with unmodified plasmid vectors.
    J Biol Chem. 1993 Feb 5;268(4):2300-3 PMID: 8428904
  6. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):7972-6 PMID: 2973058
  7. Adenovirus-dependent changes in cell membrane permeability: role of Na+, K+-ATPase.
    J Virol. 1987 Mar;61(3):883-8 PMID: 2879942
  8. Virus-receptor interaction in an adenovirus system.
    J Virol. 1968 Oct;2(10):1064-75 PMID: 5723709
  9. The structure and function of the hemagglutinin membrane glycoprotein of influenza virus.
    Annu Rev Biochem. 1987;56:365-94 PMID: 3304138
  10. Mutations in VP1 of poliovirus specifically affect both encapsidation and release of viral RNA.
    J Virol. 1990 Jan;64(1):195-206 PMID: 2152812
  11. Inhibitors of poliovirus uncoating efficiently block the early membrane permeabilization induced by virus particles.
    J Virol. 1991 May;65(5):2572-7 PMID: 1850030
  12. Internalization of intact poliovirus by HeLa cells as shown by subcellular fractionation in isoosmotic Nycodenz gradients.
    J Gen Virol. 1992 Mar;73 ( Pt 3):597-605 PMID: 1312119
  13. Characterization of protein transport between successive compartments of the Golgi apparatus: asymmetric properties of donor and acceptor activities in a cell-free system.
    Arch Biochem Biophys. 1985 Jul;240(1):413-25 PMID: 2990347
  14. Adenovirus-dependent release of choline from plasma membrane vesicles at an acidic pH is mediated by the penton base protein.
    J Virol. 1994 Feb;68(2):1204-6 PMID: 8289352
  15. Mechanism of entry of human rhinovirus 2 into HeLa cells.
    Virology. 1987 May;158(1):255-8 PMID: 3033893
  16. Cell-induced conformational change in poliovirus: externalization of the amino terminus of VP1 is responsible for liposome binding.
    J Virol. 1990 May;64(5):1934-45 PMID: 2157861
  17. Kinetics of poliovirus uncoating in HeLa cells in a nonacidic environment.
    J Virol. 1990 Aug;64(8):3590-7 PMID: 2164587
  18. Kinetic study of the cytotoxic effect of alpha-sarcin, a ribosome inactivating protein from Aspergillus giganteus, on tumour cell lines: protein biosynthesis inhibition and cell binding.
    Mol Cell Biochem. 1993 May 12;122(1):39-47 PMID: 8350862
  19. Lipid-anchored influenza hemagglutinin promotes hemifusion, not complete fusion.
    Cell. 1994 Jan 28;76(2):383-91 PMID: 8293471
  20. Adenovirus enhancement of transferrin-polylysine-mediated gene delivery.
    Proc Natl Acad Sci U S A. 1991 Oct 1;88(19):8850-4 PMID: 1681545
  21. Membrane fusion by peptide analogues of influenza virus haemagglutinin.
    J Gen Virol. 1988 Aug;69 ( Pt 8):1847-57 PMID: 3404116
  22. Poliovirus mutants resistant to neutralization with soluble cell receptors.
    Science. 1990 Dec 14;250(4987):1596-9 PMID: 2177226
  23. Ion channels induced in lipid bilayers by subvirion particles of the nonenveloped mammalian reoviruses.
    Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10549-52 PMID: 7504268
  24. Early interaction of rhinoviruses with host cells.
    J Virol. 1972 Jan;9(1):29-40 PMID: 4333543
  25. Virus entry into animal cells.
    Adv Virus Res. 1989;36:107-51 PMID: 2500008
  26. Coupling of adenovirus to transferrin-polylysine/DNA complexes greatly enhances receptor-mediated gene delivery and expression of transfected genes.
    Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6099-103 PMID: 1631096
  27. Anti-peptide antibodies detect steps in a protein conformational change: low-pH activation of the influenza virus hemagglutinin.
    J Cell Biol. 1987 Dec;105(6 Pt 2):2887-96 PMID: 2447101
  28. Structure of influenza haemagglutinin at the pH of membrane fusion.
    Nature. 1994 Sep 1;371(6492):37-43 PMID: 8072525
  29. The influence of endosome-disruptive peptides on gene transfer using synthetic virus-like gene transfer systems.
    J Biol Chem. 1994 Apr 29;269(17):12918-24 PMID: 8175709
  30. A possible role for Na+,K+-ATPase in regulating ATP-dependent endosome acidification.
    Proc Natl Acad Sci U S A. 1989 Jan;86(2):539-43 PMID: 2536167
  31. Adenovirus-dependent increase in cell membrane permeability.
    J Biol Chem. 1985 Aug 15;260(17):9598-602 PMID: 4019489
  32. Entry of poliovirus into cells does not require a low-pH step.
    J Virol. 1993 Aug;67(8):4543-8 PMID: 8392597
  33. Uncoating of human rhinovirus serotype 2 from late endosomes.
    J Virol. 1994 Jun;68(6):3713-23 PMID: 8189509
  34. Adenovirus-dependent release of 51Cr from KB cells at an acidic pH.
    J Biol Chem. 1984 Dec 10;259(23):14350-3 PMID: 6334083
  35. A mutation in VP4 defines a new step in the late stages of cell entry by poliovirus.
    J Virol. 1993 Aug;67(8):5075-8 PMID: 8392631
  36. Membrane fusion.
    Science. 1992 Nov 6;258(5084):917-24 PMID: 1439803
  37. Vacuolar ATPase activity is required for endosomal carrier vesicle formation.
    J Biol Chem. 1994 Jan 7;269(1):21-4 PMID: 8276796
  38. The arguments for pre-existing early and late endosomes.
    Trends Cell Biol. 1991 Jul;1(1):5-9 PMID: 14731803
  39. Adenovirus-induced release of epidermal growth factor and pseudomonas toxin into the cytosol of KB cells during receptor-mediated endocytosis.
    Cell. 1983 Feb;32(2):607-17 PMID: 6130853
  40. The major human rhinovirus receptor is ICAM-1.
    Cell. 1989 Mar 10;56(5):839-47 PMID: 2538243
  41. Rapid analytical and preparative isolation of functional endosomes by free flow electrophoresis.
    J Cell Biol. 1987 Apr;104(4):875-86 PMID: 3031085
  42. Human adenovirus type 2 protein IIIa. I. Purification and characterization.
    Virology. 1980 Feb;101(1):131-43 PMID: 7355574
  43. Stepwise dismantling of adenovirus 2 during entry into cells.
    Cell. 1993 Nov 5;75(3):477-86 PMID: 8221887
  44. Naturally occurring and artificially produced components of three rhinoviruses.
    Virology. 1972 Apr;48(1):71-86 PMID: 4335940
  45. A quantitative analysis of the endocytic pathway in baby hamster kidney cells.
    J Cell Biol. 1989 Dec;109(6 Pt 1):2703-20 PMID: 2592402
  46. A cell adhesion molecule, ICAM-1, is the major surface receptor for rhinoviruses.
    Cell. 1989 Mar 10;56(5):849-53 PMID: 2538244
  47. The first milliseconds of the pore formed by a fusogenic viral envelope protein during membrane fusion.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3623-7 PMID: 2023911
  48. Human adenovirus-host cell interactions: comparative study with members of subgroups B and C.
    J Virol. 1990 Aug;64(8):3661-73 PMID: 2196380
  49. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
    Anal Biochem. 1976 May 7;72:248-54 PMID: 942051
  50. Members of the low density lipoprotein receptor family mediate cell entry of a minor-group common cold virus.
    Proc Natl Acad Sci U S A. 1994 Mar 1;91(5):1839-42 PMID: 8127891
  51. cDNA cloning reveals that the major group rhinovirus receptor on HeLa cells is intercellular adhesion molecule 1.
    Proc Natl Acad Sci U S A. 1989 Jul;86(13):4907-11 PMID: 2544880
  52. Cellular receptor for poliovirus: molecular cloning, nucleotide sequence, and expression of a new member of the immunoglobulin superfamily.
    Cell. 1989 Mar 10;56(5):855-65 PMID: 2538245
  53. pH-dependent lysis of liposomes by adenovirus.
    Biochemistry. 1986 Apr 22;25(8):2231-7 PMID: 3754765
  54. Rhinovirus-mediated endosomal release of transfection complexes.
    J Virol. 1995 Feb;69(2):1085-92 PMID: 7815487
  55. Receptor-mediated endocytosis in semiintact cells.
    Methods Enzymol. 1992;219:223-34 PMID: 1487996
  56. Mechanism of leakage of phospholipid vesicle contents induced by the peptide GALA.
    Biochemistry. 1990 Sep 18;29(37):8720-8 PMID: 2271552
  57. An adenovirus type 5 early gene function regulates expression of other early viral genes.
    Proc Natl Acad Sci U S A. 1979 Aug;76(8):3665-9 PMID: 291030
  58. Characteristics of a human cell line transformed by DNA from human adenovirus type 5.
    J Gen Virol. 1977 Jul;36(1):59-74 PMID: 886304
  59. Membrane destabilization by N-terminal peptides of viral envelope proteins.
    J Membr Biol. 1992 May;128(1):71-80 PMID: 1323686
  60. Viral infection permeabilizes mammalian cells to protein toxins.
    Cell. 1980 Jul;20(3):769-75 PMID: 6251972
  61. Protein-mediated membrane fusion.
    Annu Rev Biophys Biophys Chem. 1989;18:187-211 PMID: 2660823
  62. Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment.
    Cell. 1993 Apr 23;73(2):309-19 PMID: 8477447
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
DOI
10.1083/jcb.131.1.111
Published
1995-10-00
Pages
111-23
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120603
Subset
IM
External Links
PubMed source DOI: 10.1083/jcb.131.1.111 PMC Full Text View journal details
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