Home LiteratureArticle Details
PMID: 8758895 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Identification of an H2-M3-restricted Listeria epitope: implications for antigen presentation by M3.

Immunity ·Vol. 5 ·No. 1 ·1996-07-00 ·Pages 63-72

Lenz LL, Dere B, Bevan MJ

Abstract

Using expression cloning, we have identified an H2-M3-restricted epitope of the intracellular bacterial pathogen Listeria monocytogenes. Picomolar concentrations of an amino-terminal N-formylated hexapeptide, fMIGWII, targeted cells for lysis by CD8+ cytotoxic T cells, while the nonformylated peptide was approximately 100-fold less active. The sequence of the 185 aa protein source of this epitope predicts a transmembrane protein that retains its N terminus and assumes an N(out)-C(in) topology. This membrane orientation offers an explanation for the protection of the epitope from deformylases present in the bacterial cell and suggests an explanation for the ability of phagocytes to present H2-M3-restricted bacterial epitopes via a vacuolar TAP-independent mechanism.

MeSH Terms
Alleles Amino Acid Sequence Animals Antigen Presentation/genetics Antigens, Bacterial/genetics,immunology,isolation & purification Bacterial Proteins/genetics,immunology,isolation & purification Base Sequence Cytotoxicity, Immunologic/genetics Epitopes/genetics,immunology,isolation & purification Gene Library H-2 Antigens/genetics,immunology Listeria monocytogenes/genetics,immunology Membrane Proteins/genetics,immunology,isolation & purification Mice Mice, Inbred C57BL Molecular Sequence Data T-Lymphocytes, Cytotoxic/immunology Transformation, Bacterial/immunology
Chemicals
Antigens, Bacterial Bacterial Proteins Epitopes H-2 Antigens LemA protein, Listeria Membrane Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Lenz L L
Department of Immunology, University of Washington, Seattle, 98195, USA.
Dere B
Bevan M J
References (50)
50 references, click to expand
  1. Cloned Listeria monocytogenes specific non-MHC-restricted Lyt-2+ T cells with cytolytic and protective activity.
    J Immunol. 1988 May 1;140(9):3173-9 PMID: 3129513
  2. Maternally transmitted antigen of mice: a model transplantation antigen.
    Annu Rev Immunol. 1991;9:351-72 PMID: 1910682
  3. Metabolic requirements for macrophage presentation of Listeria monocytogenes to immune CD8 cells.
    J Immunol. 1992 Jan 15;148(2):555-61 PMID: 1729372
  4. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein.
    Cell. 1992 Feb 7;68(3):521-31 PMID: 1739966
  5. CD1-restricted T cell recognition of microbial lipoglycan antigens.
    Science. 1995 Jul 14;269(5221):227-30 PMID: 7542404
  6. Recognition of a lipid antigen by CD1-restricted alpha beta+ T cells.
    Nature. 1994 Dec 15;372(6507):691-4 PMID: 7527500
  7. The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology.
    EMBO J. 1986 Nov;5(11):3021-7 PMID: 16453726
  8. Ham-2 corrects the class I antigen-processing defect in RMA-S cells.
    Nature. 1992 Feb 13;355(6361):647-9 PMID: 1538753
  9. CD8+ T cells specific for a single nonamer epitope of Listeria monocytogenes are protective in vivo.
    J Exp Med. 1992 Jun 1;175(6):1531-8 PMID: 1375265
  10. Introduction of pAM beta 1 into Listeria monocytogenes by conjugation and homology between native L. monocytogenes plasmids.
    Infect Immun. 1984 Apr;44(1):157-61 PMID: 6323313
  11. A pair of mobilizable shuttle vectors conferring resistance to spectinomycin for molecular cloning in Escherichia coli and in gram-positive bacteria.
    Nucleic Acids Res. 1990 Jul 25;18(14):4296 PMID: 2143017
  12. Direct sequence identification and kinetic analysis of an MHC class I-restricted Listeria monocytogenes CTL epitope.
    J Immunol. 1994 Jan 15;152(2):686-94 PMID: 7506732
  13. CD1b restricts the response of human CD4-8- T lymphocytes to a microbial antigen.
    Nature. 1992 Dec 10;360(6404):593-7 PMID: 1281285
  14. H2-M3wt-restricted, Listeria monocytogenes-specific CD8 T cells recognize a novel, hydrophobic, protease-resistant, periodate-sensitive antigen.
    Int Immunol. 1996 Mar;8(3):367-78 PMID: 8671623
  15. Biochemical specificity of H-2M3a. Stereospecificity and space-filling requirements at position 1 maintain N-formyl peptide binding.
    J Immunol. 1992 Dec 1;149(11):3605-11 PMID: 1431130
  16. IgG or IgM monoclonal antibodies reactive with different determinants on the molecular complex bearing Lyt 2 antigen block T cell-mediated cytolysis in the absence of complement.
    J Immunol. 1980 Dec;125(6):2665-72 PMID: 6159417
  17. Nonclassical binding of formylated peptide in crystal structure of the MHC class Ib molecule H2-M3.
    Cell. 1995 Aug 25;82(4):655-64 PMID: 7664344
  18. Specialized functions of major histocompatibility complex class I molecules. II. Hmt binds N-formylated peptides of mitochondrial and prokaryotic origin.
    J Exp Med. 1991 Oct 1;174(4):941-4 PMID: 1919442
  19. Physical map of the Listeria monocytogenes chromosome.
    J Bacteriol. 1992 Nov;174(22):7098-103 PMID: 1385384
  20. MHC-unrestricted transfer of antilisterial immunity by freshly isolated immune CD8 spleen cells.
    J Immunol. 1989 Dec 1;143(11):3731-6 PMID: 2479688
  21. Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues.
    Nature. 1989 Oct 5;341(6241):456-8 PMID: 2677744
  22. CD8 T lymphocytes specific for the secreted p60 antigen protect against Listeria monocytogenes infection.
    J Immunol. 1995 May 1;154(9):4642-50 PMID: 7722316
  23. Protein secretion in Bacillus species.
    Microbiol Rev. 1993 Mar;57(1):109-37 PMID: 8464403
  24. Phagocyte-induced antigen-specific activation of unprimed CD8+ T cells in vitro.
    Eur J Immunol. 1995 May;25(5):1274-85 PMID: 7539754
  25. Introduction of soluble protein into the class I pathway of antigen processing and presentation.
    Cell. 1988 Sep 9;54(6):777-85 PMID: 3261634
  26. The complete general secretory pathway in gram-negative bacteria.
    Microbiol Rev. 1993 Mar;57(1):50-108 PMID: 8096622
  27. Peptide presentation by the MHC class Ib molecule, H2-M3.
    Int Immunol. 1994 Dec;6(12):1917-26 PMID: 7696209
  28. H2-M3 restricted presentation of Listeria monocytogenes antigens.
    Immunol Rev. 1996 Jun;151:107-21 PMID: 8872487
  29. Antigen presentation by major histocompatibility complex class I-B molecules.
    Annu Rev Immunol. 1994;12:839-80 PMID: 8011299
  30. 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
  31. Nucleotide sequence of the lecithinase operon of Listeria monocytogenes and possible role of lecithinase in cell-to-cell spread.
    Infect Immun. 1992 Jan;60(1):219-30 PMID: 1309513
  32. Membrane topology and mutational analysis of the TolQ protein of Escherichia coli required for the uptake of macromolecules and cell envelope integrity.
    J Bacteriol. 1994 Feb;176(3):822-9 PMID: 8300535
  33. The biochemistry and cell biology of antigen processing and presentation.
    Annu Rev Immunol. 1993;11:403-50 PMID: 8476568
  34. Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, Listeria monocytogenes.
    J Cell Biol. 1989 Oct;109(4 Pt 1):1597-608 PMID: 2507553
  35. Precise prediction of a dominant class I MHC-restricted epitope of Listeria monocytogenes.
    Nature. 1991 Oct 31;353(6347):852-5 PMID: 1719425
  36. Do nonclassical, class Ib MHC molecules present bacterial antigens to T cells?
    Trends Microbiol. 1993 Apr;1(1):35-8 PMID: 8143114
  37. TAP1-independent loading of class I molecules by exogenous viral proteins.
    Eur J Immunol. 1995 Jun;25(6):1739-43 PMID: 7615001
  38. Efficiency of MHC class I antigen processing: a quantitative analysis.
    Immunity. 1994 Sep;1(6):479-89 PMID: 7534616
  39. Presentation of Listeria monocytogenes to CD8+ T cells requires secretion of hemolysin and intracellular bacterial growth.
    J Immunol. 1990 Dec 1;145(11):3540-6 PMID: 2147195
  40. Methionine as translation start signal: a review of the enzymes of the pathway in Escherichia coli.
    Biochimie. 1993;75(12):1061-75 PMID: 8199241
  41. H-2M3 encodes the MHC class I molecule presenting the maternally transmitted antigen of the mouse.
    Cell. 1991 Jul 26;66(2):335-45 PMID: 1855254
  42. Antigen-specific Lyt-2+ cytolytic T lymphocytes from mice infected with the intracellular bacterium Listeria monocytogenes.
    J Immunol. 1986 Oct 15;137(8):2688-94 PMID: 3489772
  43. Specialized role for a murine class I-b MHC molecule in prokaryotic host defenses.
    Science. 1992 Jul 31;257(5070):678-9 PMID: 1496381
  44. How MHC class II molecules acquire peptide cargo: biosynthesis and trafficking through the endocytic pathway.
    Annu Rev Cell Dev Biol. 1995;11:267-306 PMID: 8689559
  45. Maternally transmitted histocompatibility antigen of mice: a hydrophobic peptide of a mitochondrially encoded protein.
    Cell. 1990 Mar 23;60(6):971-80 PMID: 2317868
  46. H-2M3a violates the paradigm for major histocompatibility complex class I peptide binding.
    J Exp Med. 1995 May 1;181(5):1817-25 PMID: 7722457
  47. Two Listeria monocytogenes CTL epitopes are processed from the same antigen with different efficiencies.
    J Immunol. 1996 Jan 15;156(2):683-92 PMID: 8543821
  48. Sequence of the leader peptidase gene of Escherichia coli and the orientation of leader peptidase in the bacterial envelope.
    J Biol Chem. 1983 Oct 10;258(19):12073-80 PMID: 6311837
  49. H-2M3 presents a Listeria monocytogenes peptide to cytotoxic T lymphocytes.
    Cell. 1992 Jul 24;70(2):215-23 PMID: 1353418
  50. Specialized functions of MHC class I molecules. I. An N-formyl peptide receptor is required for construction of the class I antigen Mta.
    J Exp Med. 1990 Mar 1;171(3):897-912 PMID: 2307936
Article Info
Journal
Immunity
Abbr.
Immunity
ISSN
1074-7613
Published
1996-07-00
Pages
63-72
Language
English
Region
United States
NLM ID
9432918
PMCID
PMC2778046
Subset
IM
Grants
NCI NIH HHS · CA-09537 · United States
NIAID NIH HHS · R01 AI019335 · United States
NCI NIH HHS · T32 CA009537-13 · United States
NIAID NIH HHS · R01 AI019335-19 · United States
Howard Hughes Medical Institute · United States
NCI NIH HHS · T32 CA009537 · United States
NIAID NIH HHS · AI-19335 · United States
Databases
GENBANK
U66186
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: [email protected]