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PMID: 2844793 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Membrane integration and intracellular transport of the coronavirus glycoprotein E1, a class III membrane glycoprotein.

The Journal of biological chemistry ·Vol. 263 ·No. 29 ·1988-10-15 ·Pages 14956-63

Mayer T, Tamura T, Falk M, Niemann H

Abstract

The E1-glycoprotein (Mr = 26,014; 228 amino acids) of mouse hepatitis virus A59 is a class III membrane glycoprotein which has been used in this study as a model system in the study of membrane integration and protein transport. The protein lacks an NH2-terminal cleavable signal sequence and spans the viral membrane three times. Hydrophobic domains I and III could serve as signal sequences for cotranslational membrane integration. Domain I alone was sufficient to translocate the hydrophilic NH2 terminus of E1 across the membranes as evidenced by glycosylation of a newly introduced N-glycosylation site. The COOH-terminal part of E1 involving amino acids Leu124 to Thr228 was found to associate tightly with membranes at the post-translational level, although this part of the molecule lacks pronounced hydrophobic sequences. Membrane protection assays with proteinase K showed that a 2-kDa hydrophilic fragment was removed from the COOH terminus of E1 indicating that the protein is largely embedded into the membrane. Microinjection of in vitro transcribed capped and polyadenylated mRNA into CV-1 cells or into secretory AtT20 pituitary tumor cells showed that the E1-protein accumulated in the Golgi but was not detectable at the plasma membrane or in secretory granules. The 28 NH2-terminal hydrophilic amino acid residues play no role in membrane assembly or in intracellular targeting. Various NH2-terminal portions of E1 were fused to Ile145 of the cytoplasmic N-protein of mouse hepatitis virus. The resulting hybrid proteins were shown to assemble into membranes in vitro and were detected either in the rough endoplasmic reticulum or transient vesicles of microinjected cells.

MeSH Terms
Amino Acid Sequence Animals Cell Line Genetic Vectors Golgi Apparatus/metabolism Intracellular Membranes/metabolism Membrane Glycoproteins/metabolism Microsomes/metabolism Molecular Sequence Data Murine hepatitis virus/genetics,metabolism Mutation Protein Biosynthesis Protein Processing, Post-Translational Recombinant Fusion Proteins/metabolism Transcription, Genetic Viral Envelope Proteins/genetics,metabolism
Chemicals
Membrane Glycoproteins Recombinant Fusion Proteins Viral Envelope Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Mayer T
Institut für Medizinische Virologie, Justus-Liebig-Universität, Giessen, Federal Republic of Germany.
Tamura T
Falk M
Niemann H
References (46)
46 references, click to expand
  1. Foreign transmembrane peptides replacing the internal signal sequence of transferrin receptor allow its translocation and membrane binding.
    Cell. 1987 Jan 16;48(1):147-55 PMID: 3791411
  2. Rapid and efficient site-specific mutagenesis without phenotypic selection.
    Proc Natl Acad Sci U S A. 1985 Jan;82(2):488-92 PMID: 3881765
  3. Coronavirus E1 glycoprotein expressed from cloned cDNA localizes in the Golgi region.
    J Virol. 1987 Jun;61(6):2042-5 PMID: 3033331
  4. Coronavirus JHM: nucleotide sequence of the mRNA that encodes nucleocapsid protein.
    Nucleic Acids Res. 1983 Aug 11;11(15):5045-54 PMID: 6308569
  5. A simple method for displaying the hydropathic character of a protein.
    J Mol Biol. 1982 May 5;157(1):105-32 PMID: 7108955
  6. The carbohydrates of mouse hepatitis virus (MHV) A59: structures of the O-glycosidically linked oligosaccharides of glycoprotein E1.
    EMBO J. 1984 Mar;3(3):665-70 PMID: 6325180
  7. Using recombinant DNA techniques to study protein targeting in the eucaryotic cell.
    Annu Rev Cell Biol. 1985;1:403-45 PMID: 3916319
  8. Sequence analysis of the bovine coronavirus nucleocapsid and matrix protein genes.
    Virology. 1987 Mar;157(1):47-57 PMID: 3029965
  9. Sequence of the membrane protein gene from avian coronavirus IBV.
    Virus Res. 1984;1(4):303-13 PMID: 6099661
  10. Signal recognition particle-dependent insertion of coronavirus E1, an intracellular membrane glycoprotein.
    J Biol Chem. 1985 Apr 25;260(8):4648-52 PMID: 2985561
  11. Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs.
    Nucleic Acids Res. 1984 Sep 25;12(18):7057-70 PMID: 6207484
  12. Translational stability of native and deadenylylated rabbit globin mRNA injected into HeLa cells.
    Proc Natl Acad Sci U S A. 1981 Feb;78(2):908-11 PMID: 6940155
  13. Analysis of the functions of coronavirus glycoproteins by differential inhibition of synthesis with tunicamycin.
    Adv Exp Med Biol. 1981;142:133-42 PMID: 6278876
  14. An internal signal sequence: the asialoglycoprotein receptor membrane anchor.
    Cell. 1986 Jan 17;44(1):177-85 PMID: 3753585
  15. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  16. Primary structure and transmembrane orientation of the murine anion exchange protein.
    Nature. 1985 Jul 18-24;316(6025):234-8 PMID: 2410791
  17. Expression of the E1 gene of mouse hepatitis virus (MHV A59) in vivo and in vitro.
    Adv Exp Med Biol. 1987;218:83-97 PMID: 2829574
  18. Glycoprotein E1 of MHV-A59: structure of the O-linked carbohydrates and construction of full length recombinant cDNA clones.
    Adv Exp Med Biol. 1984;173:201-13 PMID: 6331111
  19. Sorting of progeny coronavirus from condensed secretory proteins at the exit from the trans-Golgi network of AtT20 cells.
    J Cell Biol. 1987 Sep;105(3):1215-26 PMID: 2821011
  20. The effect of capping and polyadenylation on the stability, movement and translation of synthetic messenger RNAs in Xenopus oocytes.
    Nucleic Acids Res. 1985 Oct 25;13(20):7375-94 PMID: 3932972
  21. Translocation of secretory proteins across the microsomal membrane occurs through an environment accessible to aqueous perturbants.
    Cell. 1985 Sep;42(2):497-505 PMID: 2992801
  22. Hybridoma antibodies to the murine coronavirus JHM: characterization of epitopes on the peplomer protein (E2).
    J Gen Virol. 1984 Nov;65 ( Pt 11):1931-42 PMID: 6209363
  23. The human glucose transporter can insert posttranslationally into microsomes.
    Cell. 1986 Feb 28;44(4):629-37 PMID: 3004742
  24. Bovine opsin has more than one signal sequence.
    Nature. 1985 Nov 28-Dec 4;318(6044):338-43 PMID: 2999609
  25. Enteric coronavirus TGEV: partial sequence of the genomic RNA, its organization and expression.
    Biochimie. 1987 Jun-Jul;69(6-7):591-600 PMID: 2825819
  26. Post-translational glycosylation of coronavirus glycoprotein E1: inhibition by monensin.
    EMBO J. 1982;1(12):1499-504 PMID: 6327272
  27. Predicted membrane topology of the coronavirus protein E1.
    Biochemistry. 1986 Mar 25;25(6):1335-9 PMID: 3008826
  28. Improved system for capillary microinjection into living cells.
    Exp Cell Res. 1982 Jul;140(1):31-7 PMID: 6286332
  29. The transmembrane segment of the human transferrin receptor functions as a signal peptide.
    EMBO J. 1986 Jul;5(7):1543-50 PMID: 3017701
  30. A specific transmembrane domain of a coronavirus E1 glycoprotein is required for its retention in the Golgi region.
    J Cell Biol. 1987 Sep;105(3):1205-14 PMID: 2821010
  31. The effects of processing inhibitors of N-linked oligosaccharides on the intracellular migration of glycoprotein E2 of mouse hepatitis virus and the maturation of coronavirus particles.
    J Biol Chem. 1985 Dec 15;260(29):15873-9 PMID: 2999142
  32. Complete structure of the hemagglutinin gene from the human influenza A/Victoria/3/75 (H3N2) strain as determined from cloned DNA.
    Cell. 1980 Mar;19(3):683-96 PMID: 6153930
  33. Antibodies against synthetic peptides as a tool for functional analysis of the transforming protein pp60src.
    Cell. 1983 Sep;34(2):587-96 PMID: 6193891
  34. Affinity purification of antibodies from diazotized paper blots of heterogeneous protein samples.
    J Biol Chem. 1981 Dec 10;256(23):11955-7 PMID: 7028745
  35. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface.
    Cell. 1985 Mar;40(3):627-33 PMID: 3882238
  36. Analysis of membrane and surface protein sequences with the hydrophobic moment plot.
    J Mol Biol. 1984 Oct 15;179(1):125-42 PMID: 6502707
  37. Preparation and use of nuclease-treated rabbit reticulocyte lysates for the translation of eukaryotic messenger RNA.
    Methods Enzymol. 1983;96:50-74 PMID: 6656641
  38. Morphogenesis of avian infectious bronchitis virus and a related human virus (strain 229E).
    J Virol. 1967 Oct;1(5):1019-27 PMID: 5630226
  39. Sequence and N-terminal processing of the transmembrane protein E1 of the coronavirus transmissible gastroenteritis virus.
    J Gen Virol. 1987 Jun;68 ( Pt 6):1687-93 PMID: 3035066
  40. Replication of coronavirus MHV-A59 in sac- cells: determination of the first site of budding of progeny virions.
    Eur J Cell Biol. 1984 Mar;33(2):281-93 PMID: 6325194
  41. Multiple mechanisms of protein insertion into and across membranes.
    Science. 1985 Oct 25;230(4724):400-7 PMID: 4048938
  42. Sequence and topology of a model intracellular membrane protein, E1 glycoprotein, from a coronavirus.
    Nature. 1984 Apr 19-25;308(5961):751-2 PMID: 6325918
  43. Coronavirus glycoprotein E1, a new type of viral glycoprotein.
    J Mol Biol. 1981 Dec 25;153(4):993-1010 PMID: 7343686
  44. A monoclonal antibody against a 135-K Golgi membrane protein.
    EMBO J. 1982;1(12):1621-8 PMID: 7188254
  45. Structural requirements of N-glycosylation of proteins. Studies with proline peptides as conformational probes.
    Biochem J. 1983 Feb 1;209(2):331-6 PMID: 6847620
  46. Isolation of coronavirus envelope glycoproteins and interaction with the viral nucleocapsid.
    J Virol. 1980 Jan;33(1):449-62 PMID: 6245243
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
Published
1988-10-15
Pages
14956-63
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC7960488
Subset
IM
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