Home LiteratureArticle Details
PMID: 7625126 Published · ppublish English Journal Article

The membrane glycoprotein G1 of Uukuniemi virus contains a signal for localization to the Golgi complex.

Virus research ·Vol. 36 ·No. 1 ·1995-04-00 ·Pages 49-66

Melin L, Persson R, Andersson A, Bergström A, Rönnholm R, Pettersson RF

Abstract

Members of the Bunyaviridae family acquire their envelopes by budding into the Golgi complex (GC). The accumulation of the membrane glycoproteins G1 and G2 in the GC probably determines the site of maturation. Here we have studied the intracellular transport and targeting to the GC of G1 and G2 of Uukuniemi virus, a member of the Phlebovirus genus, and report on their expression from cloned cDNAs either together or separately by using a T7 RNA polymerase-driven vaccinia virus expression system. When G1 and G2 were expressed together from a full-length cDNA as the p110 precursor, both proteins were localized to the Golgi complex, as evidenced by colocalization with the Golgi marker enzyme mannosidase II. Immunofluorescent staining indicated that G1 expressed alone also localized to the GC. However, pulse-chase experiments showed that G1 remained endoglycosidase H sensitive. G2 expressed alone remained associated with the endoplasmic reticulum (ER). G2 could be rescued from the ER and transported to the GC by coexpression with G1 from separate mRNAs. Coexpression also increased the efficiency of G1 transport to the GC. With none of the constructs could the glycoproteins be observed on the cell surface. These results show that efficient export of G1 and G2 from the ER requires coexpression of both proteins, in conformity with our previous results showing that G1 and G2 form heterodimeric complexes in the ER. Since G1 expressed alone is retained in the GC, we conclude that G1 contains a retention signal for localization to the GC. G2 might thus become associated with the GC indirectly via its interaction with G1.

MeSH Terms
Biological Transport Cell Line Golgi Apparatus/metabolism,virology HeLa Cells Humans Plasmids Protein Sorting Signals/metabolism Recombination, Genetic Uukuniemi virus/metabolism Viral Envelope Proteins/metabolism
Chemicals
Protein Sorting Signals Viral Envelope Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Melin L
Ludwig Institute for Cancer Research, Stockholm, Sweden.
Persson R
Andersson A
Bergström A
Rönnholm R
Pettersson R F
References (37)
37 references, click to expand
  1. Golgi apparatus in chick skeletal muscle: changes in its distribution during end plate development and after denervation.
    Proc Natl Acad Sci U S A. 1989 Sep;86(18):7218-22 PMID: 2674951
  2. 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):8122-6 PMID: 3095828
  3. Posttranslational processing of Uukuniemi virus glycoproteins G1 and G2.
    J Virol. 1984 Sep;51(3):806-12 PMID: 6471168
  4. Coexpression of the membrane glycoproteins G1 and G2 of Hantaan virus is required for targeting to the Golgi complex.
    Virology. 1992 Jan;186(1):53-64 PMID: 1727611
  5. Uukuniemi virus glycoproteins accumulate in and cause morphological changes of the Golgi complex in the absence of virus maturation.
    J Virol. 1986 Mar;57(3):899-906 PMID: 3512854
  6. The 17-residue transmembrane domain of beta-galactoside alpha 2,6-sialyltransferase is sufficient for Golgi retention.
    J Cell Biol. 1992 Apr;117(2):245-58 PMID: 1560026
  7. Monosaccharide sequence of protein-bound glycans of Uukuniemi virus.
    J Virol. 1982 Feb;41(2):390-400 PMID: 7077748
  8. Formation and intracellular transport of a heterodimeric viral spike protein complex.
    J Cell Biol. 1991 Jan;112(2):257-66 PMID: 1988460
  9. Bunyavirus protein transport and assembly.
    Curr Top Microbiol Immunol. 1991;169:161-79 PMID: 1935227
  10. Oligomerization, transport, and Golgi retention of Punta Toro virus glycoproteins.
    J Virol. 1991 Nov;65(11):5902-9 PMID: 1920619
  11. Regulation of protein export from the endoplasmic reticulum.
    Annu Rev Cell Biol. 1988;4:257-88 PMID: 3058161
  12. Intracellular accumulation of Punta Toro virus glycoproteins expressed from cloned cDNA.
    Virology. 1988 Nov;167(1):251-60 PMID: 3142146
  13. Novel purification of the catalytic domain of Golgi alpha-mannosidase II. Characterization and comparison with the intact enzyme.
    J Biol Chem. 1991 Sep 5;266(25):16876-85 PMID: 1885615
  14. The Golgi sorting domain of coronavirus E1 protein.
    J Cell Sci. 1991 Apr;98 ( Pt 4):567-75 PMID: 1860903
  15. Expression of the Bunyamwera virus M genome segment and intracellular localization of NSm.
    Virology. 1993 Aug;195(2):511-20 PMID: 8337827
  16. In vitro translation of Uukuniemi virus-specific RNAs: identification of a nonstructural protein and a precursor to the membrane glycoproteins.
    J Virol. 1981 Jan;37(1):72-79 PMID: 7194383
  17. Protein oligomerization in the endoplasmic reticulum.
    Annu Rev Cell Biol. 1989;5:277-307 PMID: 2688707
  18. Uukuniemi virus maturation: immunofluorescence microscopy with monoclonal glycoprotein-specific antibodies.
    J Virol. 1984 Jul;51(1):137-46 PMID: 6374166
  19. The Hantaan virus M-segment glycoproteins G1 and G2 can be expressed independently.
    J Virol. 1992 Apr;66(4):1907-14 PMID: 1548747
  20. The signal for Golgi retention of bovine beta 1,4-galactosyltransferase is in the transmembrane domain.
    J Biol Chem. 1992 Feb 25;267(6):4084-96 PMID: 1637374
  21. Localization of Bunyamwera bunyavirus G1 glycoprotein to the Golgi requires association with G2 but not with NSm.
    J Gen Virol. 1994 Dec;75 ( Pt 12):3441-51 PMID: 7996137
  22. Efficient transport of Semliki Forest virus glycoproteins through a Golgi complex morphologically altered by Uukuniemi virus glycoproteins.
    EMBO J. 1986 Dec 1;5(12):3111-8 PMID: 3545812
  23. Sequences within and adjacent to the transmembrane segment of alpha-2,6-sialyltransferase specify Golgi retention.
    EMBO J. 1991 Dec;10(12):3577-88 PMID: 1935890
  24. Targeting of viral glycoproteins to the Golgi complex.
    Trends Microbiol. 1993 Jul;1(4):124-30 PMID: 8143127
  25. The membrane spanning domain of beta-1,4-galactosyltransferase specifies trans Golgi localization.
    EMBO J. 1991 Dec;10(12):3567-75 PMID: 1935889
  26. Protein localization and virus assembly at intracellular membranes.
    Curr Top Microbiol Immunol. 1991;170:67-106 PMID: 1760931
  27. Cap-independent translation of mRNA conferred by encephalomyocarditis virus 5' sequence improves the performance of the vaccinia virus/bacteriophage T7 hybrid expression system.
    Proc Natl Acad Sci U S A. 1989 Aug;86(16):6126-30 PMID: 2548200
  28. Golgi complex localization of the Punta Toro virus G2 protein requires its association with the G1 protein.
    Virology. 1991 Jul;183(1):351-65 PMID: 1905078
  29. Complete nucleotide sequence of the M RNA segment of Uukuniemi virus encoding the membrane glycoproteins G1 and G2.
    Virology. 1987 Sep;160(1):191-202 PMID: 3629974
  30. Nucleotide sequence and coding strategy of the Uukuniemi virus L RNA segment.
    J Gen Virol. 1992 Jul;73 ( Pt 7):1745-52 PMID: 1629699
  31. A Golgi retention signal in a membrane-spanning domain of coronavirus E1 protein.
    J Cell Biol. 1991 Oct;115(1):19-30 PMID: 1655802
  32. A signal for Golgi retention in the bunyavirus G1 glycoprotein.
    J Biol Chem. 1994 Sep 9;269(36):22565-73 PMID: 8077205
  33. Posttranslational oligomerization and cooperative acid activation of mixed influenza hemagglutinin trimers.
    J Cell Biol. 1988 Mar;106(3):629-39 PMID: 3279048
  34. Uukuniemi virus S RNA segment: ambisense coding strategy, packaging of complementary strands into virions, and homology to members of the genus Phlebovirus.
    J Virol. 1990 Jan;64(1):247-55 PMID: 2136709
  35. Bunyaviridae genome structure and gene expression.
    Curr Top Microbiol Immunol. 1991;169:91-141 PMID: 1935231
  36. Localization to the Golgi complex of Uukuniemi virus glycoproteins G1 and G2 expressed from cloned cDNAs.
    J Virol. 1992 Jul;66(7):4525-31 PMID: 1602557
  37. Cell biology of viruses that assemble along the biosynthetic pathway.
    Semin Cell Biol. 1992 Oct;3(5):367-81 PMID: 1333835
Article Info
Journal
Virus research
Abbr.
Virus Res
ISSN
0168-1702
Published
1995-04-00
Pages
49-66
Language
English
Region
Netherlands
NLM ID
8410979
PMCID
PMC7133855
Subset
IM
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