Home LiteratureArticle Details
PMID: 17804515 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Signal peptide requirements for lymphocytic choriomeningitis virus glycoprotein C maturation and virus infectivity.

Journal of virology ·Vol. 81 ·No. 22 ·2007-11-00 ·Pages 12515-24

Schrempf S, Froeschke M, Giroglou T, von Laer D, Dobberstein B

Abstract

Insertion of the lymphocytic choriomeningitis virus (LCMV) precursor glycoprotein C (GP-C) into the membrane of the endoplasmic reticulum is mediated by an unusual signal peptide (SP(GP-C)). It is comprised of 58 amino acid residues and contains an extended hydrophilic N-terminal region, two hydrophobic regions, and a short C-terminal region. After cleavage by signal peptidase, SP(GP-C) accumulates in cells and virus particles. In the present study, we identified the LCMV SP(GP-C) as being an essential component of the GP complex and show that the different regions of SP(GP-C) are required for distinct steps in GP maturation and virus infectivity. More specifically, we show that one hydrophobic region of SP(GP-C) is sufficient for the membrane insertion of GP-C, while both hydrophobic regions are required for the processing and cell surface expression of the GPs. The N-terminal region of SP(GP-C), on the other hand, is essential for pseudoviral infection of target cells. Furthermore, we show that unmyristoylated SP(GP-C) exposes its N-terminal region to the exoplasmic side. This SP(GP-C) can promote GP-C maturation but is defective in pseudoviral infection. Myristoylation and topology of SP(GP-C) in the membrane may thus hold the key to an understanding of the role of SP(GP-C) in GP-C complex maturation and LCMV infectivity.

MeSH Terms
Amino Acid Sequence Cell Line Cell Membrane/chemistry,metabolism,virology Glycoproteins/genetics,metabolism Humans Lymphocytic choriomeningitis virus/genetics,physiology Molecular Sequence Data Myristic Acid/metabolism Protein Sorting Signals/genetics Viral Envelope Proteins/genetics,metabolism Virus Internalization
Chemicals
Glycoproteins Protein Sorting Signals Viral Envelope Proteins glycoprotein C, lymphocytic choriomeningitis virus Myristic Acid
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Schrempf Sabrina
Zentrum für Molekulare Biologie der Universität Heidelberg, Im Neuenheimer Feld 282, 69120, Heidelberg, Germany.
Froeschke Marc
Giroglou Tsanan
von Laer Dorothee
Dobberstein Bernhard
References (40)
40 references, click to expand
  1. Mechanism of lymphocytic choriomeningitis virus entry into cells.
    Virology. 1994 Jan;198(1):1-9 PMID: 8259643
  2. Identification of signal peptide peptidase, a presenilin-type aspartic protease.
    Science. 2002 Jun 21;296(5576):2215-8 PMID: 12077416
  3. Long-lived signal peptide of lymphocytic choriomeningitis virus glycoprotein pGP-C.
    J Biol Chem. 2003 Oct 24;278(43):41914-20 PMID: 12917426
  4. Reptilian reovirus utilizes a small type III protein with an external myristylated amino terminus to mediate cell-cell fusion.
    J Virol. 2004 Apr;78(8):4342-51 PMID: 15047847
  5. The signal peptide.
    J Membr Biol. 1990 May;115(3):195-201 PMID: 2197415
  6. Arenaviruses: protein structure and function.
    Curr Top Microbiol Immunol. 2002;262:159-73 PMID: 11987805
  7. The signal peptide of the Junín arenavirus envelope glycoprotein is myristoylated and forms an essential subunit of the mature G1-G2 complex.
    J Virol. 2004 Oct;78(19):10783-92 PMID: 15367645
  8. Protein targeting signals.
    Curr Opin Cell Biol. 1990 Aug;2(4):604-8 PMID: 2252586
  9. Signal peptide of Lassa virus glycoprotein GP-C exhibits an unusual length.
    FEBS Lett. 2003 Mar 13;538(1-3):203-6 PMID: 12633879
  10. Signal sequences. The limits of variation.
    J Mol Biol. 1985 Jul 5;184(1):99-105 PMID: 4032478
  11. Conformational control through translocational regulation: a new view of secretory and membrane protein folding.
    Bioessays. 2002 Aug;24(8):741-8 PMID: 12210535
  12. Fatty acylation of proteins: new insights into membrane targeting of myristoylated and palmitoylated proteins.
    Biochim Biophys Acta. 1999 Aug 12;1451(1):1-16 PMID: 10446384
  13. Dual topology of the hepatitis B virus large envelope protein: determinants influencing post-translational pre-S translocation.
    J Biol Chem. 2001 Jun 22;276(25):22265-72 PMID: 11301328
  14. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa.
    Anal Biochem. 1987 Nov 1;166(2):368-79 PMID: 2449095
  15. Myristylation of the hepatitis B virus large surface protein is essential for viral infectivity.
    Virology. 1995 Nov 10;213(2):292-9 PMID: 7491754
  16. A new class of fusion-associated small transmembrane (FAST) proteins encoded by the non-enveloped fusogenic reoviruses.
    EMBO J. 2000 Mar 1;19(5):902-12 PMID: 10698932
  17. Identification of Lassa virus glycoprotein signal peptide as a trans-acting maturation factor.
    EMBO Rep. 2003 Nov;4(11):1084-8 PMID: 14555961
  18. Intracellular protein topogenesis.
    Proc Natl Acad Sci U S A. 1980 Mar;77(3):1496-500 PMID: 6929499
  19. Snapshots of membrane-translocating proteins.
    Trends Cell Biol. 1996 Apr;6(4):142-7 PMID: 15157477
  20. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies.
    Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12978-83 PMID: 14563923
  21. Protein translocation across the endoplasmic reticulum.
    Cell. 1984 Aug;38(1):5-8 PMID: 6088076
  22. A general method for the generation of high-titer, pantropic retroviral vectors: highly efficient infection of primary hepatocytes.
    Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9564-8 PMID: 7937806
  23. The N-terminus of B96Bom, a Bombyx mori G-protein-coupled receptor, is N-myristoylated and translocated across the membrane.
    FEBS J. 2005 Jan;272(2):472-81 PMID: 15654885
  24. High-level transient expression of influenza virus proteins from a series of SV40 late and early replacement vectors.
    Gene. 1988 Jun 30;66(2):163-81 PMID: 2844629
  25. Protein insertion into the membrane of the endoplasmic reticulum: the architecture of the translocation site.
    Cold Spring Harb Symp Quant Biol. 1995;60:41-5 PMID: 8824376
  26. Role of the stable signal peptide and cytoplasmic domain of G2 in regulating intracellular transport of the Junín virus envelope glycoprotein complex.
    J Virol. 2006 Jun;80(11):5189-98 PMID: 16698999
  27. Acidic pH triggers LCMV membrane fusion activity and conformational change in the glycoprotein spike.
    Virology. 1994 Feb;198(2):455-65 PMID: 8291229
  28. Recombinant expression of lymphocytic choriomeningitis virus strain WE glycoproteins: a single amino acid makes the difference.
    J Virol. 2001 Jan;75(2):1061-4 PMID: 11134321
  29. Oncoretrovirus and lentivirus vectors pseudotyped with lymphocytic choriomeningitis virus glycoprotein: generation, concentration, and broad host range.
    J Virol. 2002 Feb;76(3):1488-95 PMID: 11773421
  30. Mapping the landscape of the lymphocytic choriomeningitis virus stable signal peptide reveals novel functional domains.
    J Virol. 2007 Jun;81(11):5649-57 PMID: 17376927
  31. Lymphocytic choriomeningitis virus. VI. Isolation of a glycoprotein mediating neutralization.
    Virology. 1983 Oct 15;130(1):247-51 PMID: 6636539
  32. Signal sequences: more than just greasy peptides.
    Trends Cell Biol. 1998 Oct;8(10):410-5 PMID: 9789330
  33. Bitopic membrane topology of the stable signal peptide in the tripartite Junín virus GP-C envelope glycoprotein complex.
    J Virol. 2007 Apr;81(8):4331-7 PMID: 17267481
  34. Glycosylation efficiency of Asn-Xaa-Thr sequons depends both on the distance from the C terminus and on the presence of a downstream transmembrane segment.
    J Biol Chem. 2000 Jun 9;275(23):17338-43 PMID: 10748070
  35. Complete sequence of the S RNA of lymphocytic choriomeningitis virus (WE strain) compared to that of Pichinde arenavirus.
    Virus Res. 1985 Sep;3(2):101-14 PMID: 4060885
  36. Lassa virus glycoprotein signal peptide displays a novel topology with an extended endoplasmic reticulum luminal region.
    J Biol Chem. 2004 Mar 26;279(13):12293-9 PMID: 14709548
  37. Predicting the topology of eukaryotic membrane proteins.
    Eur J Biochem. 1993 May 1;213(3):1333-40 PMID: 8099327
  38. Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus.
    Science. 1998 Dec 11;282(5396):2079-81 PMID: 9851928
  39. Biochemistry, molecular biology, and genetics of the oligosaccharyltransferase.
    FASEB J. 1996 Jun;10(8):849-58 PMID: 8666161
  40. Endoproteolytic processing of the lymphocytic choriomeningitis virus glycoprotein by the subtilase SKI-1/S1P.
    J Virol. 2003 Mar;77(5):2866-72 PMID: 12584310
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
2007-11-00
Epub
2007-00-05
Pages
12515-24
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC2168972
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