• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of jvirolPermissionsJournals.ASM.orgJournalJV ArticleJournal InfoAuthorsReviewers
J Virol. Dec 1997; 71(12): 9278–9284.
PMCID: PMC230230

Protein interactions during coronavirus assembly.

Abstract

Coronaviruses assemble and obtain their envelope at membranes of the intermediate compartment between the endoplasmic reticulum and Golgi complex. Like other enveloped viruses, coronavirus assembly is presumably dependent on protein localization and protein-protein as well as protein-RNA interactions. We have used the bovine coronavirus (BCV) as a model to study interactions between the viral proteins in virus-infected cells that are important for coronavirus assembly. BCV is a prototype for the coronaviruses that express an additional major structural protein, the hemagglutinin esterase (HE), in addition to the spike (S) glycoprotein, membrane (M) glycoprotein, and nucleocapsid (N) protein. Complexes consisting of the M, S, and HE proteins were detected in virus-infected cells by coimmunoprecipitations. Kinetic analyses demonstrated that S protein and HE each quickly formed a complex with M protein after synthesis, whereas heterocomplexes consisting of all three proteins formed more slowly. The kinetics of HE biosynthesis revealed that the half-life of oligomerization was approximately 30 min, which correlated with the appearance of complexes consisting of M, HE, and S proteins, suggesting that oligomerization and/or conformational changes may be important for the S-M-HE protein complexes to form. Only HE dimers were found associated with the heterocomplexes consisting of all three proteins. S-M-HE protein complexes were detected prior to processing of the oligosaccharide chains on HE, indicating that these protein complexes formed in a premedial Golgi compartment before trimming of sugar chains. Transient coexpressions and double-labeling immunofluorescence demonstrated that HE and S proteins colocalized with M protein. This was further supported by coimmunoprecipitation of specific HE-M and S-M protein complexes from transfected cells, indicating that these proteins can form complexes in the absence of other viral proteins.

Full Text

The Full Text of this article is available as a PDF (3.1M).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bos EC, Luytjes W, van der Meulen HV, Koerten HK, Spaan WJ. The production of recombinant infectious DI-particles of a murine coronavirus in the absence of helper virus. Virology. 1996 Apr 1;218(1):52–60. [PubMed]
  • Copeland CS, Zimmer KP, Wagner KR, Healey GA, Mellman I, Helenius A. Folding, trimerization, and transport are sequential events in the biogenesis of influenza virus hemagglutinin. Cell. 1988 Apr 22;53(2):197–209. [PubMed]
  • Deregt D, Babiuk LA. Monoclonal antibodies to bovine coronavirus: characteristics and topographical mapping of neutralizing epitopes on the E2 and E3 glycoproteins. Virology. 1987 Dec;161(2):410–420. [PubMed]
  • Deregt D, Sabara M, Babiuk LA. Structural proteins of bovine coronavirus and their intracellular processing. J Gen Virol. 1987 Nov;68(Pt 11):2863–2877. [PubMed]
  • Fuerst TR, Niles EG, Studier FW, Moss B. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8122–8126. [PMC free article] [PubMed]
  • Godet M, L'Haridon R, Vautherot JF, Laude H. TGEV corona virus ORF4 encodes a membrane protein that is incorporated into virions. Virology. 1992 Jun;188(2):666–675. [PubMed]
  • Griffiths G, Rottier P. Cell biology of viruses that assemble along the biosynthetic pathway. Semin Cell Biol. 1992 Oct;3(5):367–381. [PubMed]
  • Hogue BG, King B, Brian DA. Antigenic relationships among proteins of bovine coronavirus, human respiratory coronavirus OC43, and mouse hepatitis coronavirus A59. J Virol. 1984 Aug;51(2):384–388. [PMC free article] [PubMed]
  • Hogue BG, Kienzle TE, Brian DA. Synthesis and processing of the bovine enteric coronavirus haemagglutinin protein. J Gen Virol. 1989 Feb;70(Pt 2):345–352. [PubMed]
  • Hogue BG, Nayak DP. Synthesis and processing of the influenza virus neuraminidase, a type II transmembrane glycoprotein. Virology. 1992 Jun;188(2):510–517. [PubMed]
  • Hogue BG, Nayak DP. Deletion mutation in the signal anchor domain activates cleavage of the influenza virus neuraminidase, a type II transmembrane protein. J Gen Virol. 1994 May;75(Pt 5):1015–1022. [PubMed]
  • Hurtley SM, Helenius A. Protein oligomerization in the endoplasmic reticulum. Annu Rev Cell Biol. 1989;5:277–307. [PubMed]
  • Kienzle TE, Abraham S, Hogue BG, Brian DA. Structure and orientation of expressed bovine coronavirus hemagglutinin-esterase protein. J Virol. 1990 Apr;64(4):1834–1838. [PMC free article] [PubMed]
  • Kim KH, Narayanan K, Makino S. Assembled coronavirus from complementation of two defective interfering RNAs. J Virol. 1997 May;71(5):3922–3931. [PMC free article] [PubMed]
  • King B, Brian DA. Bovine coronavirus structural proteins. J Virol. 1982 May;42(2):700–707. [PMC free article] [PubMed]
  • Klumperman J, Locker JK, Meijer A, Horzinek MC, Geuze HJ, Rottier PJ. Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding. J Virol. 1994 Oct;68(10):6523–6534. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Locker JK, Opstelten DJ, Ericsson M, Horzinek MC, Rottier PJ. Oligomerization of a trans-Golgi/trans-Golgi network retained protein occurs in the Golgi complex and may be part of its retention. J Biol Chem. 1995 Apr 14;270(15):8815–8821. [PubMed]
  • Lapps W, Hogue BG, Brian DA. Sequence analysis of the bovine coronavirus nucleocapsid and matrix protein genes. Virology. 1987 Mar;157(1):47–57. [PubMed]
  • Liao CL, Zhang X, Lai MM. Coronavirus defective-interfering RNA as an expression vector: the generation of a pseudorecombinant mouse hepatitis virus expressing hemagglutinin-esterase. Virology. 1995 Apr 1;208(1):319–327. [PubMed]
  • Liu DX, Inglis SC. Association of the infectious bronchitis virus 3c protein with the virion envelope. Virology. 1991 Dec;185(2):911–917. [PubMed]
  • Macneughton MR, Davies HA. Ribonucleoprotein-like structures from coronavirus particles. J Gen Virol. 1978 Jun;39(3):545–549. [PubMed]
  • Opstelten DJ, Raamsman MJ, Wolfs K, Horzinek MC, Rottier PJ. Envelope glycoprotein interactions in coronavirus assembly. J Cell Biol. 1995 Oct;131(2):339–349. [PMC free article] [PubMed]
  • Parker MD, Yoo D, Cox GJ, Babiuk LA. Primary structure of the S peplomer gene of bovine coronavirus and surface expression in insect cells. J Gen Virol. 1990 Feb;71(Pt 2):263–270. [PubMed]
  • Pettersson RF. Protein localization and virus assembly at intracellular membranes. Curr Top Microbiol Immunol. 1991;170:67–106. [PubMed]
  • Risco C, Antón IM, Enjuanes L, Carrascosa JL. The transmissible gastroenteritis coronavirus contains a spherical core shell consisting of M and N proteins. J Virol. 1996 Jul;70(7):4773–4777. [PMC free article] [PubMed]
  • Rose JK, Doms RW. Regulation of protein export from the endoplasmic reticulum. Annu Rev Cell Biol. 1988;4:257–288. [PubMed]
  • Stephens EB, Compans RW. Assembly of animal viruses at cellular membranes. Annu Rev Microbiol. 1988;42:489–516. [PubMed]
  • Tooze J, Tooze S, Warren G. 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):281–293. [PubMed]
  • Tooze SA, Tooze J, Warren G. Site of addition of N-acetyl-galactosamine to the E1 glycoprotein of mouse hepatitis virus-A59. J Cell Biol. 1988 May;106(5):1475–1487. [PMC free article] [PubMed]
  • Vennema H, Godeke GJ, Rossen JW, Voorhout WF, Horzinek MC, Opstelten DJ, Rottier PJ. Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J. 1996 Apr 15;15(8):2020–2028. [PMC free article] [PubMed]
  • Yu X, Bi W, Weiss SR, Leibowitz JL. Mouse hepatitis virus gene 5b protein is a new virion envelope protein. Virology. 1994 Aug 1;202(2):1018–1023. [PubMed]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...