Home LiteratureArticle Details
PMID: 10562307 Published · ppublish English Journal Article

Naturally processed and presented epitopes of the islet cell autoantigen IA-2 eluted from HLA-DR4.

The Journal of clinical investigation ·Vol. 104 ·No. 10 ·1999-11-00 ·Pages 1449-57

Peakman M, Stevens EJ, Lohmann T, Narendran P, Dromey J, Alexander A, Tomlinson AJ, Trucco M, Gorga JC, Chicz RM

Abstract

During immune responses, antigen-presenting cells (APCs) process antigens and present peptide epitopes complexed with human leukocyte antigen (HLA) molecules. CD4 cells recognize these naturally processed and presented epitopes (NPPEs) bound to HLA class II molecules. Epitope identification is important for developing diagnostic and therapeutic tools for immune-mediated diseases and providing insight into their etiology, but current approaches overlook effects of natural processing on epitope selection. We have developed a technique to identify NPPEs using mass spectrometry (MS) after antigen is targeted onto APCs using a lectin-based antigen delivery system (ADS). We applied the technique to identify NPPEs of the intracellular domain of the type 1 diabetes mellitus-associated (type 1 DM-associated) autoantigen insulinoma-associated-2 (IA-2ic), presented by HLA-DR4 (0401). IA-2ic-derived NPPEs eluted from HLA-DR4 constitute 6 sets of peptides nested around distinct core regions. Synthetic peptides based on these regions bind HLA-DR4 and elicit primary T-cell proliferation frequently in HLA-DR4-positive type 1 DM patients, but rarely in non-HLA-DR4 patients, and in none of the HLA-DR4 nondiabetic controls we tested. This flexible, direct approach identifies an HLA allele-specific map of NPPEs for any antigen, presented by any HLA class II molecule. This method should enable a greater understanding of epitope selection and lead to the generation of sensitive and specific reagents for detecting autoreactive T cells.

MeSH Terms
Adolescent Adult Aged Amino Acid Sequence Antigen-Presenting Cells/immunology Arthritis, Rheumatoid/genetics,immunology Autoantibodies/analysis Autoantigens/immunology B-Lymphocytes Cell Line Cell Membrane/immunology Child Diabetes Mellitus, Type 1/genetics,immunology Epitopes/chemistry,immunology,isolation & purification Europe Genotype HLA-DR4 Antigen/immunology Humans Islets of Langerhans/immunology Lymphocyte Activation Membrane Proteins/chemistry,immunology Middle Aged Molecular Sequence Data Peptide Fragments/chemistry,immunology Protein Tyrosine Phosphatase, Non-Receptor Type 1 Protein Tyrosine Phosphatases/chemistry,immunology Receptor-Like Protein Tyrosine Phosphatases, Class 8 T-Lymphocytes/immunology United States Whites
Chemicals
Autoantibodies Autoantigens Epitopes HLA-DR4 Antigen Membrane Proteins Peptide Fragments PTPRN protein, human Protein Tyrosine Phosphatase, Non-Receptor Type 1 Protein Tyrosine Phosphatases Receptor-Like Protein Tyrosine Phosphatases, Class 8
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Peakman M
Department of Immunology, Guy's, King's and St. Thomas' School of Medicine, King's College London, Denmark Hill Campus, London SE5 9PJ, United Kingdom. mark.peakman@kcl.ac.uk
Stevens E J
Lohmann T
Narendran P
Dromey J
Alexander A
Tomlinson A J
Trucco M
Gorga J C
Chicz R M
References (49)
49 references, click to expand
  1. Type-I diabetes: a chronic autoimmune disease of human, mouse, and rat.
    Annu Rev Immunol. 1990;8:647-79 PMID: 2188676
  2. HLA class II region sequences, 1998.
    Tissue Antigens. 1998 Apr;51(4 Pt 2):467-507 PMID: 9583802
  3. Predominant naturally processed peptides bound to HLA-DR1 are derived from MHC-related molecules and are heterogeneous in size.
    Nature. 1992 Aug 27;358(6389):764-8 PMID: 1380674
  4. Autoreactive epitopes defined by diabetes-associated human monoclonal antibodies are localized in the middle and C-terminal domains of the smaller form of glutamate decarboxylase.
    Proc Natl Acad Sci U S A. 1993 Apr 1;90(7):2832-6 PMID: 7681990
  5. Inverse relation between humoral and cellular immunity to glutamic acid decarboxylase in subjects at risk of insulin-dependent diabetes.
    Lancet. 1993 May 29;341(8857):1365-9 PMID: 8098789
  6. Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles.
    J Exp Med. 1993 Jul 1;178(1):27-47 PMID: 8315383
  7. HLA DR4 is associated with the development of multiple basal cell carcinomas and malignant melanoma.
    Dermatology. 1993;187(1):16-8 PMID: 8324271
  8. Minute quantities of a single immunodominant foreign epitope are presented as large nested sets by major histocompatibility complex class II molecules.
    Eur J Immunol. 1993 Jul;23(7):1602-7 PMID: 7686856
  9. Comparison of peptides bound to spleen and thymus class II.
    J Exp Med. 1993 Dec 1;178(6):2173-83 PMID: 8245790
  10. T-cell epitopes in type 1 diabetes autoantigen tyrosine phosphatase IA-2: potential for mimicry with rotavirus and other environmental agents.
    Mol Med. 1998 Apr;4(4):231-9 PMID: 9606176
  11. Detection of antigen-specific T cells with multivalent soluble class II MHC covalent peptide complexes.
    Immunity. 1998 Jun;8(6):675-82 PMID: 9655481
  12. Altered peptide ligand design: altering immune responses to class I MHC/peptide complexes.
    Immunol Rev. 1998 Jun;163:151-60 PMID: 9700508
  13. Association between HLA class II genotype and spontaneous clearance of hepatitis C viraemia.
    J Hepatol. 1998 Aug;29(2):207-13 PMID: 9722201
  14. Enhanced T cell proliferation and increased responder frequency following delivery of antigen to the antigen-presenting cell; B cell dependency and use in detection of autoreactive T cells.
    J Immunol Methods. 1998 Jun 1;215(1-2):59-70 PMID: 9744748
  15. Neural network-based prediction of candidate T-cell epitopes.
    Nat Biotechnol. 1998 Oct;16(10):966-9 PMID: 9788355
  16. The role of CD4+ T cell responses in antitumor immunity.
    Curr Opin Immunol. 1998 Oct;10(5):588-94 PMID: 9794842
  17. Immunoregulation of Th cells by naturally processed peptide antagonists.
    J Immunol. 1999 Jan 1;162(1):1-4 PMID: 9886362
  18. N-terminal elongation of a peptide determinant beyond the first primary anchor improves binding to H-2 I-Ad and HLA-DR1 by backbone-dependent and aromatic side chain-dependent interactions, respectively.
    Eur J Immunol. 1999 Jan;29(1):189-95 PMID: 9933100
  19. Autoantigens IA-2 and GAD in Type I (insulin-dependent) diabetes.
    Diabetologia. 1999 Jan;42(1):3-14 PMID: 10027571
  20. Scanning a DRB3*0101 (DR52a)-restricted epitope cross-presented by DR3: overlapping natural and artificial determinants in the human acetylcholine receptor.
    J Immunol. 1999 Apr 1;162(7):4079-87 PMID: 10201931
  21. Spontaneous T-cell proliferation in the non-obese diabetic mouse to a peptide from the unique class II MHC molecule, I-Ag7, which is also protective against the development of autoimmune diabetes.
    Diabetologia. 1999 May;42(5):560-5 PMID: 10333048
  22. T cell reactivity to DR*0401- and DQ*0302-binding peptides of the putative autoantigen IA-2 in type 1 diabetes.
    Exp Clin Endocrinol Diabetes. 1999;107(3):166-71 PMID: 10376440
  23. Sequence analysis of peptides bound to MHC class II molecules.
    Nature. 1991 Oct 17;353(6345):622-7 PMID: 1656276
  24. Purification and characterization of class II histocompatibility antigens from a homozygous human B cell line.
    J Biol Chem. 1987 Nov 25;262(33):16087-94 PMID: 2824477
  25. Mitogenic lectins bind to the antigen receptor on human lymphocytes.
    Eur J Immunol. 1989 Feb;19(2):389-96 PMID: 2703017
  26. Characterization of a naturally processed MHC class II-restricted T-cell determinant of hen egg lysozyme.
    Nature. 1989 Dec 7;342(6250):682-4 PMID: 2480524
  27. MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation.
    Cell. 1994 Jan 28;76(2):287-99 PMID: 8293464
  28. Characterization of specific T cells in myasthenia gravis.
    Immunol Today. 1994 Jan;15(1):41-2 PMID: 8136013
  29. Immunodominant epitopes of glutamic acid decarboxylase 65 and 67 in insulin-dependent diabetes mellitus.
    Lancet. 1994 Jun 25;343(8913):1607-8 PMID: 7911924
  30. T cell clones generated from patients with type 1 diabetes using interleukin-2 proliferate to human islet antigens.
    Autoimmunity. 1994;17(1):31-9 PMID: 8025212
  31. Antibodies to islet 37k antigen, but not to glutamate decarboxylase, discriminate rapid progression to IDDM in endocrine autoimmunity.
    Diabetes. 1994 Oct;43(10):1254-9 PMID: 7926297
  32. Cellular immunity to a determinant common to glutamate decarboxylase and coxsackie virus in insulin-dependent diabetes.
    J Clin Invest. 1994 Nov;94(5):2125-9 PMID: 7962558
  33. Precise prediction of major histocompatibility complex class II-peptide interaction based on peptide side chain scanning.
    J Exp Med. 1994 Dec 1;180(6):2353-8 PMID: 7964508
  34. Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein.
    Cell. 1995 Mar 10;80(5):695-705 PMID: 7534214
  35. Relationship of the 37,000- and 40,000-M(r) tryptic fragments of islet antigens in insulin-dependent diabetes to the protein tyrosine phosphatase-like molecule IA-2 (ICA512).
    J Clin Invest. 1995 Sep;96(3):1506-11 PMID: 7657822
  36. Low avidity recognition of self-antigen by T cells permits escape from central tolerance.
    Immunity. 1995 Oct;3(4):407-15 PMID: 7584132
  37. Arginine at positions 13 or 70-71 in pocket 4 of HLA-DRB1 alleles is associated with susceptibility to tuberculoid leprosy.
    J Exp Med. 1996 Mar 1;183(3):829-36 PMID: 8642287
  38. HLA-associated inverse correlation between T cell and antibody responsiveness to islet autoantigen in recent-onset insulin-dependent diabetes mellitus.
    Eur J Immunol. 1996 Jun;26(6):1285-9 PMID: 8647206
  39. Susceptibility to type I diabetes: HLA-DQ and DR revisited.
    Immunol Today. 1996 Jul;17(7):323-9 PMID: 8763818
  40. Direct identification of naturally processed autoantigen-derived peptides bound to HLA-DR15.
    J Biol Chem. 1996 Aug 2;271(31):18549-53 PMID: 8702503
  41. Reverse immunogenetics: from HLA-disease associations to vaccine candidates.
    Mol Med Today. 1996 Jan;2(1):38-45 PMID: 8796850
  42. Sequence-specific priming and exonuclease-released fluorescence detection of HLA-DQB1 alleles.
    Tissue Antigens. 1996 Aug;48(2):97-112 PMID: 8883299
  43. Evaluation of islet cell antigen (ICA) 512/IA-2 autoantibody radioassays using overlapping ICA512/IA-2 constructs.
    J Clin Endocrinol Metab. 1997 Feb;82(2):375-80 PMID: 9024221
  44. Capture and processing of exogenous antigens for presentation on MHC molecules.
    Annu Rev Immunol. 1997;15:821-50 PMID: 9143708
  45. Identification of naturally processed T cell epitopes from glutamic acid decarboxylase presented in the context of HLA-DR alleles by T lymphocytes of recent onset IDDM patients.
    J Clin Invest. 1997 May 15;99(10):2405-15 PMID: 9153283
  46. Human B cells secreting immunoglobulin G to glutamic acid decarboxylase-65 from a nondiabetic patient with multiple autoantibodies and Graves' disease: a comparison with those present in type 1 diabetes.
    J Clin Endocrinol Metab. 1997 Aug;82(8):2664-70 PMID: 9253351
  47. T cell receptor recognition of MHC class II-bound peptide flanking residues enhances immunogenicity and results in altered TCR V region usage.
    Immunity. 1997 Sep;7(3):387-99 PMID: 9324359
  48. HLA class II peptide binding specificity and autoimmunity.
    Adv Immunol. 1997;66:67-100 PMID: 9328640
  49. HLA-DP2: self peptide sequences and binding properties.
    J Immunol. 1997 Nov 15;159(10):4935-42 PMID: 9366419
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1999-11-00
Pages
1449-57
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC409844
Subset
IM
Corrections
CommentIn
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