Home LiteratureArticle Details
PMID: 11483778 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

In vivo generation and characterization of a soluble form of the Semliki forest virus fusion protein.

Journal of virology ·Vol. 75 ·No. 17 ·2001-09-00 ·Pages 8329-39

Lu YE, Eng CH, Shome SG, Kielian M

Abstract

During infection of host cells, a number of enveloped animal viruses are known to produce soluble forms of viral membrane glycoproteins lacking the transmembrane domain. The roles of such soluble glycoproteins in viral life cycles are incompletely understood, but in several cases they are believed to modulate host immune response and viral pathogenesis. Semliki Forest virus (SFV) is an enveloped alphavirus that infects cells through low-pH-dependent fusion and buds from the plasma membrane. Fusion is mediated by the E1 subunit of the SFV spike protein. Previous studies described the in vivo generation of E1s, a truncated soluble form of E1, under conditions in which budding is inhibited in mammalian host cells. We have here examined the properties of E1s generation and the biological activity of E1s. E1s cleavage required spike protein transport out of the endoplasmic reticulum and was independent of virus infection. Cell surface E1 efficiently acted as a precursor for E1s. E1s generation was strongly pH dependent in BHK cells, with optimal cleavage at a pH of < or =7.0, conditions that inhibited the budding of SFV but not the budding of the rhabdovirus vesicular stomatitis virus. The pH dependence of E1s production and SFV budding was unaffected by the stability of the spike protein dimer but was a function of the host cell. Similar to the intact virus and in vitro-generated E1 ectodomain, treatment of E1s at low pH in the presence of target membranes triggered specific acid-dependent conformational changes. Thus, under a variety of conditions, SFV-infected cells can produce a soluble form of E1 that is biologically active.

MeSH Terms
Animals Cell Line Dimerization Hydrogen-Ion Concentration Membrane Fusion Membrane Glycoproteins/chemistry,metabolism Semliki forest virus/pathogenicity,physiology Solubility Spodoptera Transfection Viral Envelope Proteins/chemistry,metabolism Viral Fusion Proteins/chemistry,metabolism
Chemicals
Membrane Glycoproteins Viral Envelope Proteins Viral Fusion Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Lu Y E
Department of Cell Biology, Albert Einstein College of Medicine, Bronx, New York 10461, USA.
Eng C H
Shome S G
Kielian M
References (72)
72 references, click to expand
  1. Spike protein-nucleocapsid interactions drive the budding of alphaviruses.
    J Virol. 1992 Aug;66(8):4737-47 PMID: 1629953
  2. Role of cell surface spikes in alphavirus budding.
    J Virol. 1992 Dec;66(12):7089-95 PMID: 1331511
  3. Membrane fusion of Semliki Forest virus involves homotrimers of the fusion protein.
    J Virol. 1992 Dec;66(12):7309-18 PMID: 1433520
  4. Shedding of Gs protein (a soluble form of the viral glycoprotein) by the rabies virus-infected BHK-21 cells.
    Virology. 1993 Aug;195(2):541-9 PMID: 8337829
  5. Cholesterol is required in the exit pathway of Semliki Forest virus.
    J Cell Biol. 1993 Oct;123(1):57-65 PMID: 8408205
  6. Three-dimensional structure of a membrane-containing virus.
    Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9095-9 PMID: 8415660
  7. Role of spike protein conformational changes in fusion of Semliki Forest virus.
    J Virol. 1993 Dec;67(12):7597-607 PMID: 8230478
  8. Membrane protein lateral interactions control Semliki Forest virus budding.
    EMBO J. 1994 Mar 1;13(5):1058-64 PMID: 8131740
  9. fus-1, a pH shift mutant of Semliki Forest virus, acts by altering spike subunit interactions via a mutation in the E2 subunit.
    J Virol. 1998 May;72(5):4281-7 PMID: 9557718
  10. Biochemical analysis of the secreted and virion glycoproteins of Ebola virus.
    J Virol. 1998 Aug;72(8):6442-7 PMID: 9658086
  11. Virus maturation by budding.
    Microbiol Mol Biol Rev. 1998 Dec;62(4):1171-90 PMID: 9841669
  12. The cholesterol requirement for sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence.
    J Virol. 1999 May;73(5):4272-8 PMID: 10196324
  13. Brefeldin A: the advantage of being uncompetitive.
    Cell. 1999 Apr 16;97(2):153-5 PMID: 10219235
  14. Retrograde protein translocation: ERADication of secretory proteins in health and disease.
    Trends Biochem Sci. 1999 Jul;24(7):266-70 PMID: 10390615
  15. The glycoproteins of Marburg and Ebola virus and their potential roles in pathogenesis.
    Arch Virol Suppl. 1999;15:159-69 PMID: 10470276
  16. Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses.
    J Virol. 1994 Mar;68(3):1316-23 PMID: 7508993
  17. The membrane-associated and secreted forms of the respiratory syncytial virus attachment glycoprotein G are synthesized from alternative initiation codons.
    J Virol. 1994 Jul;68(7):4538-46 PMID: 8207828
  18. Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane.
    EMBO J. 1994 Jun 15;13(12):2797-804 PMID: 8026464
  19. Assembly and entry mechanisms of Semliki Forest virus.
    Arch Virol Suppl. 1994;9:329-38 PMID: 8032265
  20. A tyrosine-based motif in the cytoplasmic domain of the alphavirus envelope protein is essential for budding.
    EMBO J. 1994 Sep 15;13(18):4204-11 PMID: 7925266
  21. Membrane and protein interactions of a soluble form of the Semliki Forest virus fusion protein.
    J Virol. 1994 Nov;68(11):6940-6 PMID: 7933075
  22. The alphaviruses: gene expression, replication, and evolution.
    Microbiol Rev. 1994 Sep;58(3):491-562 PMID: 7968923
  23. The 6-kilodalton membrane protein of Semliki Forest virus is involved in the budding process.
    J Virol. 1995 Jan;69(1):469-75 PMID: 7983743
  24. Cytomegalovirus plasmid vectors for permanent lines of polarized epithelial cells.
    Methods Cell Biol. 1994;43 Pt A:233-45 PMID: 7823864
  25. Nucleocapsid and glycoprotein organization in an enveloped virus.
    Cell. 1995 Feb 24;80(4):621-30 PMID: 7867069
  26. Mutations in the putative fusion peptide of Semliki Forest virus affect spike protein oligomerization and virus assembly.
    J Virol. 1995 Apr;69(4):2471-9 PMID: 7884895
  27. Fusion of Semliki Forest virus with cholesterol-containing liposomes at low pH: a specific requirement for sphingolipids.
    Mol Membr Biol. 1995 Jan-Mar;12(1):143-9 PMID: 7767374
  28. Low pH induces swiveling of the glycoprotein heterodimers in the Semliki Forest virus spike complex.
    Cell. 1995 Jun 2;81(5):715-25 PMID: 7774013
  29. Membrane fusion and the alphavirus life cycle.
    Adv Virus Res. 1995;45:113-51 PMID: 7793323
  30. GP mRNA of Ebola virus is edited by the Ebola virus polymerase and by T7 and vaccinia virus polymerases.
    Virology. 1995 Dec 20;214(2):421-30 PMID: 8553543
  31. Budding of rabies virus particles in the absence of the spike glycoprotein.
    Cell. 1996 Mar 22;84(6):941-51 PMID: 8601317
  32. The virion glycoproteins of Ebola viruses are encoded in two reading frames and are expressed through transcriptional editing.
    Proc Natl Acad Sci U S A. 1996 Apr 16;93(8):3602-7 PMID: 8622982
  33. Aromatic interactions define the binding of the alphavirus spike to its nucleocapsid.
    Structure. 1996 May 15;4(5):519-29 PMID: 8736551
  34. Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly.
    Structure. 1996 May 15;4(5):531-41 PMID: 8736552
  35. Mechanisms of mutations inhibiting fusion and infection by Semliki Forest virus.
    J Cell Biol. 1996 Aug;134(4):863-72 PMID: 8769412
  36. A single point mutation controls the cholesterol dependence of Semliki Forest virus entry and exit.
    J Cell Biol. 1998 Jan 12;140(1):91-9 PMID: 9425157
  37. Molecular genetic study of the interaction of Sindbis virus E2 with Ross River virus E1 for virus budding.
    J Virol. 1998 Feb;72(2):1418-23 PMID: 9445043
  38. Distinct cellular interactions of secreted and transmembrane Ebola virus glycoproteins.
    Science. 1998 Feb 13;279(5353):1034-7 PMID: 9461435
  39. Priming with secreted glycoprotein G of respiratory syncytial virus (RSV) augments interleukin-5 production and tissue eosinophilia after RSV challenge.
    J Virol. 1998 Apr;72(4):2871-80 PMID: 9525607
  40. Characterization of the soluble glycoprotein released from vesicular stomatitis virus-infected cells.
    J Virol. 1983 Jan;45(1):80-90 PMID: 6296461
  41. Regulation of asparagine-linked oligosaccharide processing. Oligosaccharide processing in Aedes albopictus mosquito cells.
    J Biol Chem. 1984 Feb 25;259(4):2375-82 PMID: 6698972
  42. Intracellular appearance of a glycoprotein in VSV-infected BHK cells lacking the membrane-anchoring oligopeptide of the viral G-protein.
    EMBO J. 1984 Jul;3(7):1469-76 PMID: 6086325
  43. Role of cholesterol in fusion of Semliki Forest virus with membranes.
    J Virol. 1984 Oct;52(1):281-3 PMID: 6481854
  44. pH-induced alterations in the fusogenic spike protein of Semliki Forest virus.
    J Cell Biol. 1985 Dec;101(6):2284-91 PMID: 3905823
  45. The soluble glycoprotein of vesicular stomatitis virus is formed during or shortly after the translation process.
    J Virol. 1986 Mar;57(3):968-75 PMID: 3005639
  46. Fusion of Semliki Forest virus infected Aedes albopictus cells at low pH is a fusion from within.
    Arch Virol. 1986;89(1-4):145-59 PMID: 3521544
  47. Temperature and energy dependence of secretory protein transport in the exocrine pancreas.
    EMBO J. 1986 Jul;5(7):1477-82 PMID: 3743549
  48. An epitope of the Semliki Forest virus fusion protein exposed during virus-membrane fusion.
    J Virol. 1999 Dec;73(12):10029-39 PMID: 10559317
  49. Biochemical consequences of a mutation that controls the cholesterol dependence of Semliki Forest virus fusion.
    J Virol. 2000 Feb;74(4):1623-31 PMID: 10644331
  50. Specific roles for lipids in virus fusion and exit. Examples from the alphaviruses.
    Subcell Biochem. 2000;34:409-55 PMID: 10808340
  51. Cryo-electron microscopy reveals the functional organization of an enveloped virus, Semliki Forest virus.
    Mol Cell. 2000 Feb;5(2):255-66 PMID: 10882067
  52. Semliki forest virus budding: assay, mechanisms, and cholesterol requirement.
    J Virol. 2000 Sep;74(17):7708-19 PMID: 10933676
  53. Formation and characterization of the trimeric form of the fusion protein of Semliki Forest Virus.
    J Virol. 2000 Sep;74(17):7772-80 PMID: 10933683
  54. Differential roles of two conserved glycine residues in the fusion peptide of Semliki Forest virus.
    Virology. 2001 Jan 5;279(1):146-60 PMID: 11145898
  55. Proteins of vesicular stomatitis virus. II. Immunological comparisons of viral antigens.
    J Virol. 1970 Jul;6(1):20-7 PMID: 4319479
  56. Activation of influenza A viruses by trypsin treatment.
    Virology. 1975 Dec;68(2):426-39 PMID: 173078
  57. Isolation of a Singh's Aedes albopictus cell clone sensitive to Dengue and Chikungunya viruses.
    J Gen Virol. 1978 Sep;40(3):531-44 PMID: 690610
  58. Shedding of the glycoprotein from vesicular stomatitis virus-infected cells.
    J Virol. 1978 Aug;27(2):330-9 PMID: 211264
  59. Phase separation of integral membrane proteins in Triton X-114 solution.
    J Biol Chem. 1981 Feb 25;256(4):1604-7 PMID: 6257680
  60. Production of spikeless particles of the rabies virus under conditions of low pH.
    Virology. 1981 Jan 30;108(2):267-76 PMID: 7008336
  61. Cell fusion by Semliki Forest, influenza, and vesicular stomatitis viruses.
    J Cell Biol. 1981 Jun;89(3):674-9 PMID: 6265470
  62. Shedding of vesicular stomatitis virus soluble glycoprotein by removal of carboxy-terminal peptide.
    J Virol. 1982 Apr;42(1):322-5 PMID: 6283151
  63. Dissection of Semliki Forest virus glycoprotein delivery from the trans-Golgi network to the cell surface in permeabilized BHK cells.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8052-6 PMID: 3186706
  64. The heterodimeric association between the membrane proteins of Semliki Forest virus changes its sensitivity to low pH during virus maturation.
    J Virol. 1989 Dec;63(12):4991-7 PMID: 2479769
  65. Intracellular maturation and transport of the SV5 type II glycoprotein hemagglutinin-neuraminidase: specific and transient association with GRP78-BiP in the endoplasmic reticulum and extensive internalization from the cell surface.
    J Cell Biol. 1989 Dec;109(6 Pt 2):3273-89 PMID: 2557352
  66. Biosynthesis, maturation, and acid activation of the Semliki Forest virus fusion protein.
    J Virol. 1990 Oct;64(10):4614-24 PMID: 2118964
  67. Cholesterol is required for infection by Semliki Forest virus.
    J Cell Biol. 1991 Feb;112(4):615-23 PMID: 1671572
  68. In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000-molecular-weight membrane protein modulates virus release.
    J Virol. 1991 Aug;65(8):4107-13 PMID: 2072446
  69. Mutagenesis of the putative fusion domain of the Semliki Forest virus spike protein.
    J Virol. 1991 Aug;65(8):4292-300 PMID: 2072453
  70. Fate of the 6K membrane protein of Semliki Forest virus during virus assembly.
    Virology. 1991 Dec;185(2):843-6 PMID: 1962454
  71. Membrane fusion process of Semliki Forest virus. II: Cleavage-dependent reorganization of the spike protein complex controls virus entry.
    J Cell Biol. 1992 Jan;116(2):349-57 PMID: 1730759
  72. Formation of heterotrimers between the membrane-integrated and the soluble glycoproteins of vesicular stomatitis virus leads to their intracellular cotransport.
    J Virol. 1992 May;66(5):2792-7 PMID: 1313903
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2001-09-00
Pages
8329-39
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC115077
Subset
IM
Grants
NCI NIH HHS · P30 CA013330 · United States
NIGMS NIH HHS · R01 GM057454 · United States
NCI NIH HHS · P30-CA13330 · United States
NIGMS NIH HHS · R01 GM57454 · 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: product@genelibs.com