Home LiteratureArticle Details
PMID: 9254646 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Introduction of a glycosylation site into a secreted protein provides evidence for an alternative antigen processing pathway: transport of precursors of major histocompatibility complex class I-restricted peptides from the endoplasmic reticulum to the cytosol.

The Journal of experimental medicine ·Vol. 186 ·No. 4 ·1997-08-18 ·Pages 479-87

Bacik I, Snyder HL, Antón LC, Russ G, Chen W, Bennink JR, Urge L, Otvos L, Dudkowska B, Eisenlohr L, Yewdell JW

Abstract

We found that the presentation of a H-2Kd-restricted determinant from influenza virus nucleoprotein (NP) to T cells is strictly dependent on expression of the transporter associated with antigen presentation (TAP), regardless of whether NP is expressed as a cytosolic or secreted NP (SNP). Introducing an N-linked glycosylation site into the determinant selectively reduced presentation of SNP. This indicates that glycosylation does not interfere with TAP-transported peptides, and therefore that cytosolic peptides derived from SNP must have been exposed to the glycosylation machinery of the endoplasmic reticulum (ER) before their existence in the cytosol. Based on these findings, we propose that TAP-dependent processing of at least some ER-targeted proteins entails the reimportation of protein from the secretory pathway to the cytosol, where the protein is processed via the classical pathway.

MeSH Terms
Animals Antigen Presentation Biological Transport Cytosol/metabolism Endoplasmic Reticulum/metabolism Glycosylation Histocompatibility Antigens Class I/physiology Mice Mice, Inbred BALB C Mice, Inbred CBA Nucleocapsid Proteins Nucleoproteins/metabolism Peptide Fragments/metabolism RNA-Binding Proteins Viral Core Proteins/metabolism
Chemicals
Histocompatibility Antigens Class I NP protein, Influenza A virus Nucleocapsid Proteins Nucleoproteins Peptide Fragments RNA-Binding Proteins Viral Core Proteins
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Bacik I
Laboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, Bethesda, Maryland 20892-0440, USA.
Snyder H L
Antón L C
Russ G
Chen W
Bennink J R
Urge L
Otvos L
Dudkowska B
Eisenlohr L
Yewdell J W
References (42)
42 references, click to expand
  1. RMA/S cells present endogenously synthesized cytosolic proteins to class I-restricted cytotoxic T lymphocytes.
    J Exp Med. 1992 Jan 1;175(1):163-8 PMID: 1309852
  2. The role of the endoplasmic reticulum in antigen processing. N-glycosylation of influenza hemagglutinin abrogates CD4+ cytotoxic T cell recognition of endogenously processed antigen.
    J Immunol. 1990 Apr 1;144(7):2789-94 PMID: 1690778
  3. Expression of a membrane protease enhances presentation of endogenous antigens to MHC class I-restricted T lymphocytes.
    Cell. 1992 Dec 11;71(6):963-72 PMID: 1333889
  4. Class I molecules retained in the endoplasmic reticulum bind antigenic peptides.
    J Exp Med. 1993 Jun 1;177(6):1633-41 PMID: 8496682
  5. Peptides shorter than a minimal CTL epitope may have a higher binding affinity than the epitope for the class I Kk molecule.
    Virology. 1993 Aug;195(2):851-4 PMID: 7687804
  6. Selective and ATP-dependent translocation of peptides by the MHC-encoded transporter.
    Science. 1993 Aug 6;261(5122):769-71 PMID: 8342042
  7. Peptide length and sequence specificity of the mouse TAP1/TAP2 translocator.
    J Exp Med. 1994 Feb 1;179(2):533-40 PMID: 8294864
  8. Glycosylation of a synthetic peptide representing a T-cell determinant of influenza virus hemagglutinin results in loss of recognition by CD4+ T-cell clones.
    Virology. 1994 Mar;199(2):422-30 PMID: 7907197
  9. Vaccination with the immediate-early protein ICP47 of herpes simplex virus-type 1 (HSV-1) induces virus-specific lymphoproliferation, but fails to protect against lethal challenge.
    Virology. 1994 Apr;200(1):236-45 PMID: 8128625
  10. MHC class I/beta 2-microglobulin complexes associate with TAP transporters before peptide binding.
    Nature. 1994 Apr 28;368(6474):864-7 PMID: 8159247
  11. A cytosolic herpes simplex virus protein inhibits antigen presentation to CD8+ T lymphocytes.
    Cell. 1994 May 20;77(4):525-35 PMID: 8187174
  12. Interaction of MHC class I molecules with the transporter associated with antigen processing.
    Science. 1994 May 27;264(5163):1322-6 PMID: 8191286
  13. Purification and enzymatic properties of peptide:N-glycanase from C3H mouse-derived L-929 fibroblast cells. Possible widespread occurrence of post-translational remodification of proteins by N-deglycosylation.
    J Biol Chem. 1994 Jul 1;269(26):17611-8 PMID: 8021270
  14. Recognition of carbohydrate by major histocompatibility complex class I-restricted, glycopeptide-specific cytotoxic T lymphocytes.
    J Exp Med. 1994 Aug 1;180(2):739-44 PMID: 8046349
  15. Trimming of TAP-translocated peptides in the endoplasmic reticulum and in the cytosol during recycling.
    J Exp Med. 1994 Nov 1;180(5):1591-7 PMID: 7964447
  16. Trimming of antigenic peptides in an early secretory compartment.
    J Exp Med. 1994 Dec 1;180(6):2389-94 PMID: 7964513
  17. Human transporters associated with antigen processing possess a promiscuous peptide-binding site.
    Immunity. 1994 Apr;1(1):7-14 PMID: 7889401
  18. A sequential model for peptide binding and transport by the transporters associated with antigen processing.
    Immunity. 1994 Sep;1(6):491-500 PMID: 7895159
  19. Effect of TAP on the generation and intracellular trafficking of peptide-receptive major histocompatibility complex class I molecules.
    Immunity. 1995 Feb;2(2):137-47 PMID: 7895170
  20. An epitope-selective, transporter associated with antigen presentation (TAP)-1/2-independent pathway and a more general TAP-1/2-dependent antigen-processing pathway allow recognition of the HIV-1 envelope glycoprotein by CD8+ CTL.
    J Immunol. 1995 Jun 1;154(11):6140-56 PMID: 7538543
  21. Herpes simplex virus turns off the TAP to evade host immunity.
    Nature. 1995 Jun 1;375(6530):411-5 PMID: 7760935
  22. A viral inhibitor of peptide transporters for antigen presentation.
    Nature. 1995 Jun 1;375(6530):415-8 PMID: 7760936
  23. Antigen presentation to cytotoxic T lymphocytes in vivo.
    J Exp Med. 1995 Sep 1;182(3):639-41 PMID: 7650475
  24. Assembly, intracellular localization, and nucleotide binding properties of the human peptide transporters TAP1 and TAP2 expressed by recombinant vaccinia viruses.
    J Biol Chem. 1995 Sep 8;270(36):21312-8 PMID: 7673167
  25. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol.
    Cell. 1996 Mar 8;84(5):769-79 PMID: 8625414
  26. An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins.
    J Exp Med. 1996 Feb 1;183(2):527-34 PMID: 8627164
  27. Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP.
    J Cell Biol. 1996 Feb;132(3):291-8 PMID: 8636208
  28. Molecular mechanism and species specificity of TAP inhibition by herpes simplex virus ICP47.
    EMBO J. 1996 Jul 1;15(13):3247-55 PMID: 8670825
  29. Stable binding of the herpes simplex virus ICP47 protein to the peptide binding site of TAP.
    EMBO J. 1996 Jul 1;15(13):3256-66 PMID: 8670826
  30. Antigen processing and presentation by the class I major histocompatibility complex.
    Annu Rev Immunol. 1996;14:369-96 PMID: 8717519
  31. Defective ribosomal products (DRiPs): a major source of antigenic peptides for MHC class I molecules?
    J Immunol. 1996 Sep 1;157(5):1823-6 PMID: 8757297
  32. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction.
    Nature. 1996 Dec 5;384(6608):432-8 PMID: 8945469
  33. Generation, translocation, and presentation of MHC class I-restricted peptides.
    Annu Rev Biochem. 1995;64:463-91 PMID: 7574490
  34. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  35. Isolation and structure of a human fibroblast interferon gene.
    Nature. 1980 Jun 19;285(5766):542-7 PMID: 6157094
  36. Assembly of asparagine-linked oligosaccharides.
    Annu Rev Biochem. 1985;54:631-64 PMID: 3896128
  37. Impaired assembly and transport of HLA-A and -B antigens in a mutant TxB cell hybrid.
    EMBO J. 1986 May;5(5):943-9 PMID: 3522223
  38. Vaccinia virus expression vector: coexpression of beta-galactosidase provides visual screening of recombinant virus plaques.
    Mol Cell Biol. 1985 Dec;5(12):3403-9 PMID: 3939316
  39. Cytotoxic T lymphocytes recognize influenza haemagglutinin that lacks a signal sequence.
    Nature. 1986 Dec 11-17;324(6097):575-7 PMID: 3491325
  40. Defective presentation to class I-restricted cytotoxic T lymphocytes in vaccinia-infected cells is overcome by enhanced degradation of antigen.
    J Exp Med. 1988 Oct 1;168(4):1211-24 PMID: 2459295
  41. Brefeldin A specifically inhibits presentation of protein antigens to cytotoxic T lymphocytes.
    Science. 1989 Jun 2;244(4908):1072-5 PMID: 2471266
  42. MHC interaction and T cell recognition of carbohydrates and glycopeptides.
    J Immunol. 1992 Apr 15;148(8):2446-51 PMID: 1560200
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
1997-08-18
Pages
479-87
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2199039
Subset
IM
Grants
NIAID NIH HHS · AI-36331 · 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