Home LiteratureArticle Details
PMID: 7679413 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Binding of myelin basic protein peptides to human histocompatibility leukocyte antigen class II molecules and their recognition by T cells from multiple sclerosis patients.

The Journal of clinical investigation ·Vol. 91 ·No. 2 ·1993-02-00 ·Pages 616-28

Valli A, Sette A, Kappos L, Oseroff C, Sidney J, Miescher G, Hochberger M, Albert ED, Adorini L

Abstract

Multiple sclerosis (MS) is an autoimmune disease in which myelin proteins have been implicated as autoantigens recognized by pathogenic autoreactive T cells. To study the relationship between human myelin basic protein (hMBP) and HLA alleles associated to MS susceptibility, such as DRB1*1501, the binding of synthetic peptides spanning the entire hMBP sequence to 10 purified HLA-DR molecules was determined. All the hMBP peptides tested showed binding affinity for at least one of the DR molecules analyzed, but three hMBP peptides, included in sequences 13-32, 84-103, and 144-163 were found capable of binding to three or more DR molecules. The hMBP peptide 84-103 was the most degenerate in binding, in that it bound to 9 out of 10 DR molecules tested. Interestingly, it bound with highest affinity to DRB1*1501 molecules. To correlate the binding pattern of hMBP peptides to HLA class II molecules with their recognition by T cells, 61 hMBP-specific T cell lines (TCL) were established from the peripheral blood of 20 MS patients, who were homozygous, heterozygous, or negative for DRB1*1501. Analysis of hMBP epitopes recognized by these TCL and their HLA restriction demonstrated a very good correlation between binding data and T cell proliferation to hMBP peptides. Although virtually all hMBP peptides tested could be recognized by at least one TCL from MS patients, three immunodominant T cell epitopes were apparent among the TCL examined, corresponding exactly to the hMBP peptides capable of binding to several DR molecules. No major difference could be detected in the recognition of immunodominant hMBP peptides by TCL from DRB1*1501 positive or negative MS patients. These results have implications for the role of hMBP as relevant autoantigen, and of DRB1*1501 as susceptibility allele in MS.

MeSH Terms
Adult Aged Alleles Amino Acid Sequence Cell Line Female HLA-DQ Antigens/genetics HLA-DR Antigens/genetics Histocompatibility Antigens Class II/immunology Humans Immunodominant Epitopes Male Middle Aged Molecular Sequence Data Multiple Sclerosis/etiology,immunology Myelin Basic Protein/immunology Peptide Fragments/immunology T-Lymphocytes/immunology
Chemicals
HLA-DQ Antigens HLA-DR Antigens Histocompatibility Antigens Class II Immunodominant Epitopes Myelin Basic Protein Peptide Fragments
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Valli A
Preclinical Research, Sandoz Pharma Ltd., Basel, Switzerland.
Sette A
Kappos L
Oseroff C
Sidney J
Miescher G
Hochberger M
Albert E D
Adorini L
References (58)
58 references, click to expand
  1. The rapid isolation of clonable antigen-specific T lymphocyte lines capable of mediating autoimmune encephalomyelitis.
    Eur J Immunol. 1981 Mar;11(3):195-9 PMID: 6165588
  2. HLA and Japanese MS.
    Tissue Antigens. 1978 Jul;12(1):19-24 PMID: 80838
  3. Adoptive transfer of experimental allergic encephalomyelitis in SJL/J mice after in vitro activation of lymph node cells by myelin basic protein: requirement for Lyt 1+ 2- T lymphocytes.
    J Immunol. 1981 Oct;127(4):1420-3 PMID: 6168690
  4. Distinct forms of both alpha and beta subunits are present in the human Ia molecular pool.
    Proc Natl Acad Sci U S A. 1981 Jul;78(7):4549-51 PMID: 6945597
  5. Detection of a novel human class II HLA antigen.
    Nature. 1983 Jul 28-Aug 3;304(5924):358-61 PMID: 6192342
  6. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS).
    Neurology. 1983 Nov;33(11):1444-52 PMID: 6685237
  7. T-cell clones specific for myelin basic protein induce chronic relapsing paralysis and demyelination.
    Nature. 1985 Sep 26-Oct 2;317(6035):355-8 PMID: 2413363
  8. Immunogenetic profile of multiple sclerosis in Mexicans.
    Hum Immunol. 1986 Aug;16(4):364-74 PMID: 3093412
  9. A population-based study of multiple sclerosis in twins.
    N Engl J Med. 1986 Dec 25;315(26):1638-42 PMID: 3785335
  10. T-cell epitope of the autoantigen myelin basic protein that induces encephalomyelitis.
    Nature. 1986 Nov 20-26;324(6094):258-60 PMID: 2431317
  11. Multiple sclerosis: gadolinium enhancement in MR imaging.
    Radiology. 1986 Dec;161(3):721-5 PMID: 3786722
  12. Immunochemically purified DR antigens in liposomes stimulate xenogeneic cytolytic T cells in secondary in vitro cultures.
    Cell Immunol. 1986 Nov;103(1):160-73 PMID: 3492282
  13. 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
  14. Multiple sclerosis in Saudi Arabia.
    Neurology. 1988 Apr;38(4):621-3 PMID: 3352920
  15. Peptide specificities of myelin basic protein-reactive human T-cell clones.
    Neurology. 1988 May;38(5):739-42 PMID: 2452382
  16. Mechanisms influencing the immunodominance of T cell determinants.
    J Exp Med. 1988 Dec 1;168(6):2091-104 PMID: 2462005
  17. A malaria T-cell epitope recognized in association with most mouse and human MHC class II molecules.
    Nature. 1988 Dec 22-29;336(6201):778-80 PMID: 2462673
  18. Peptides of myelin basic protein stimulate T lymphocytes from patients with multiple sclerosis.
    J Neuroimmunol. 1989 Mar;22(1):23-30 PMID: 2465311
  19. Identification of an encephalitogenic determinant of myelin proteolipid protein for SJL mice.
    J Immunol. 1989 Mar 1;142(5):1523-7 PMID: 2465343
  20. T cell receptors in murine autoimmune diseases.
    Annu Rev Immunol. 1989;7:371-405 PMID: 2653372
  21. Response of human T lymphocyte lines to myelin basic protein: association of dominant epitopes with HLA class II restriction molecules.
    J Neurosci Res. 1989 Jun;23(2):207-16 PMID: 2474079
  22. Molecular mimicry as a mechanism for the cause and a probe uncovering etiologic agent(s) of autoimmune disease.
    Curr Top Microbiol Immunol. 1989;145:127-35 PMID: 2805785
  23. How some T cells escape tolerance induction.
    Nature. 1989 Nov 9;342(6246):183-5 PMID: 2478888
  24. Lessons from magnetic resonance imaging in multiple sclerosis.
    Trends Neurosci. 1989 Oct;12(10):376-9 PMID: 2479134
  25. Universally immunogenic T cell epitopes: promiscuous binding to human MHC class II and promiscuous recognition by T cells.
    Eur J Immunol. 1989 Dec;19(12):2237-42 PMID: 2481588
  26. T cells responsive to myelin basic protein in patients with multiple sclerosis.
    Science. 1990 Feb 9;247(4943):718-21 PMID: 1689076
  27. Limited heterogeneity of rearranged T-cell receptor V alpha transcripts in brains of multiple sclerosis patients.
    Nature. 1990 May 24;345(6273):344-6 PMID: 1971424
  28. Shared human T cell receptor V beta usage to immunodominant regions of myelin basic protein.
    Science. 1990 May 25;248(4958):1016-9 PMID: 1693015
  29. Autoimmune diseases: the failure of self tolerance.
    Science. 1990 Jun 15;248(4961):1380-8 PMID: 1972595
  30. Fine specificity and HLA restriction of myelin basic protein-specific cytotoxic T cell lines from multiple sclerosis patients and healthy individuals.
    J Immunol. 1990 Jul 15;145(2):540-8 PMID: 1694881
  31. T-cell recognition of an immunodominant myelin basic protein epitope in multiple sclerosis.
    Nature. 1990 Jul 12;346(6280):183-7 PMID: 1694970
  32. Characterization of the specificity of peptide binding to four DR haplotypes.
    J Immunol. 1990 Sep 15;145(6):1799-808 PMID: 2167910
  33. A novel approach to the generation of high affinity class II-binding peptides.
    J Immunol. 1990 Sep 15;145(6):1809-13 PMID: 1975260
  34. HLA-DR2a is the dominant restriction molecule for the cytotoxic T cell response to myelin basic protein in DR2Dw2 individuals.
    J Immunol. 1990 Nov 1;145(9):2880-5 PMID: 1698864
  35. Myelin autoreactivity in multiple sclerosis: recognition of myelin basic protein in the context of HLA-DR2 products by T lymphocytes of multiple-sclerosis patients and healthy donors.
    Proc Natl Acad Sci U S A. 1990 Oct;87(20):7968-72 PMID: 1700423
  36. A myelin basic protein peptide is recognized by cytotoxic T cells in the context of four HLA-DR types associated with multiple sclerosis.
    J Exp Med. 1991 Jan 1;173(1):19-24 PMID: 1702137
  37. Truncation analysis of several DR binding epitopes.
    J Immunol. 1991 Feb 15;146(4):1240-6 PMID: 1704034
  38. Single amino acid changes in DR and antigen define residues critical for peptide-MHC binding and T cell recognition.
    J Immunol. 1991 Apr 1;146(7):2331-40 PMID: 1706393
  39. Restricted T-cell receptor V beta gene usage by myelin basic protein-specific T-cell clones in multiple sclerosis: predominant genes vary in individuals.
    Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2466-70 PMID: 1706524
  40. T cell response to myelin basic protein epitopes in multiple sclerosis patients and healthy subjects.
    Eur J Immunol. 1991 Jun;21(6):1391-5 PMID: 1710565
  41. Nomenclature for factors of the HLA system, 1990.
    Hum Immunol. 1991 Jul;31(3):186-94 PMID: 1890020
  42. T-cell recognition of myelin basic protein.
    Immunol Today. 1991 Aug;12(8):277-82 PMID: 1716903
  43. MHC class-II molecules and autoimmunity.
    Annu Rev Immunol. 1991;9:493-525 PMID: 1910687
  44. On the interaction of promiscuous antigenic peptides with different DR alleles. Identification of common structural motifs.
    J Immunol. 1991 Oct 15;147(8):2663-9 PMID: 1717570
  45. Preferential T-cell receptor beta-chain variable gene use in myelin basic protein-reactive T-cell clones from patients with multiple sclerosis.
    Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9161-5 PMID: 1717998
  46. Multiple sclerosis and HLA: is the susceptibility gene really HLA-DR or -DQ?
    Hum Immunol. 1991 Oct;32(2):119-24 PMID: 1683865
  47. Effect of pH on MHC class II-peptide interactions.
    J Immunol. 1992 Feb 1;148(3):844-51 PMID: 1730877
  48. Non-radioactive oligotyping for HLA-DR1-DRw10 using polymerase chain reaction, digoxigenin-labelled oligonucleotides and chemiluminescence detection.
    Eur J Immunogenet. 1991 Oct-Dec;18(5-6):323-32 PMID: 1772877
  49. T-cell receptor alpha chain germline gene polymorphisms in multiple sclerosis.
    Neurology. 1992 Jan;42(1):80-4 PMID: 1346471
  50. Diversity in fine specificity and T cell receptor usage of the human CD4+ cytotoxic T cell response specific for the immunodominant myelin basic protein peptide 87-106.
    J Immunol. 1992 Mar 1;148(5):1359-66 PMID: 1371525
  51. Diversity of T cell receptor alpha and beta chain genes expressed by human T cells specific for similar myelin basic protein peptide/major histocompatibility complexes.
    Eur J Immunol. 1992 Mar;22(3):753-8 PMID: 1372258
  52. Influence of HLA-DR2, HLA-DPw4, and T cell receptor alpha chain genes on the susceptibility to multiple sclerosis.
    Int Immunol. 1992 Feb;4(2):177-81 PMID: 1352460
  53. A molecular model of MHC class-I-restricted antigen processing.
    Immunol Today. 1992 May;13(5):173-9 PMID: 1386516
  54. High affinity for class II molecules as a necessary but not sufficient characteristic of encephalitogenic determinants.
    Int Immunol. 1992 Jul;4(7):773-7 PMID: 1379827
  55. PROBLEMS OF EXPERIMENTAL TRIALS OF THERAPY IN MULTIPLE SCLEROSIS: REPORT BY THE PANEL ON THE EVALUATION OF EXPERIMENTAL TRIALS OF THERAPY IN MULTIPLE SCLEROSIS.
    Ann N Y Acad Sci. 1965 Mar 31;122:552-68 PMID: 14313512
  56. Sardinian multiple sclerosis is associated with HLA-DR4: a serologic and molecular analysis.
    Neurology. 1988 Nov;38(11):1749-53 PMID: 2903464
  57. Experimental allergic encephalomyelitis in the rat: response to encephalitogenic proteins and peptides.
    Science. 1973 Feb 2;179(4072):478-80 PMID: 4122324
  58. Human Ia molecules carrying DC1 determinants differ in both alpha- and beta-subunits from Ia molecules carrying DR determinants.
    Nature. 1981 Jul 23;292(5821):357-60 PMID: 6166865
Article Info
Journal
The Journal of clinical investigation
Abbr.
J Clin Invest
ISSN
0021-9738
Published
1993-02-00
Pages
616-28
Language
English
Region
United States
NLM ID
7802877
PMCID
PMC287995
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: [email protected]