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The production of a new MAGE-3 peptide presented to cytolytic T lymphocytes by HLA-B40 requires the immunoproteasome

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Schultz, Erwin S. [UCL] Chapiro, Jacques [UCL] Lurquin, Christophe [UCL] Claverol, Stéphane Burlet-Schiltz, Odile Warnier, Guy [UCL] Morel, Sandra [UCL] Boon-Falleur, Thierry [UCL] Van den Eynde, Benoît [UCL] van der Bruggen, Pierre [UCL]

By stimulating human CD8(+) T lymphocytes with autologous dendritic cells infected with an adenovirus encoding MAGE-3, we obtained a cytotoxic T lymphocyte (CTL) clone that recognized a new MAGE-3 antigenic peptide, AELVHFLLL, which is presented by HLA-B40. This peptide is also encoded by MAGE-12. The CTL clone recognized MAGE-3--expressing tumor cells only when they were first treated with IFN-gamma. Since this treatment is known to induce the exchange of the three catalytic subunits of the proteasome to form the immunoproteasome, this result suggested that the processing of this MAGE-3 peptide required the immunoproteasome. Transfection experiments showed that the substitution of beta5i (LMP7) for beta5 is necessary and sufficient for producing the peptide, whereas a mutated form of beta5i (LMP7) lacking the catalytically active site was ineffective. Mass spectrometric analyses of in vitro digestions of a long precursor peptide with either proteasome type showed that the immunoproteasome produced the antigenic peptide more efficiently, whereas the standard proteasome more efficiently introduced cleavages destroying the antigenic peptide. This is the first example of a tumor-specific antigen exclusively presented by tumor cells expressing the immunoproteasome.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2002
Language Anglais
Journal information "The Journal of Experimental Medicine" - Vol. 195, no. 4, p. 391-399 (2002)
Peer reviewed yes
Publisher Rockefeller University Press (New York)
issn 0022-1007
e-issn 1540-9538
Publication status Publié
Affiliation UCL - MD/MIGE - Département de microbiologie, d'immunologie et de génétique
MESH Subject Adenoviridae - genetics ; Amino Acid Sequence ; Animals ; Antigen Presentation ; Antigens, Neoplasm - chemistry - genetics - immunology - metabolism ; COS Cells ; Clone Cells - enzymology - immunology - metabolism ; Cysteine Endopeptidases - chemistry - metabolism ; Cytokines - immunology ; Cytotoxicity, Immunologic ; Dendritic Cells - immunology ; HLA-B Antigens - immunology ; Humans ; Molecular Sequence Data ; Multienzyme Complexes - chemistry - metabolism ; Neoplasm Proteins - chemistry - genetics - immunology - metabolism ; Peptide Fragments - chemistry - genetics - immunology - metabolism ; Proteasome Endopeptidase Complex ; Protein Processing, Post-Translational ; Protein Subunits ; T-Lymphocytes, Cytotoxic - enzymology - immunology - metabolism ; Transfection ; Tumor Cells, Cultured
Keywords Beta5i ; Proteasome ; Mass spectrometry ; Tumor ; HLA-B40
Links
  1. Marchand Marie, Brichard Vincent, van Baren Nicolas, Coulie Pierre G, Biological and clinical developments in melanoma vaccines, 10.1517/14712598.1.3.497
  2. van Hall Thorbald, Sijts Alice, Camps Marcel, Offringa Rienk, Melief Cornelis, Kloetzel Peter-M., Ossendorp Ferry, Differential Influence on Cytotoxic T Lymphocyte Epitope Presentation by Controlled Expression of Either Proteasome Immunosubunits or Pa28, 10.1084/jem.192.4.483
  3. Sijts A. J. A. M., Standera S., Toes R. E. M., Ruppert T., Beekman N. J. C. M., van Veelen P. A., Ossendorp F. A., Melief C. J. M., Kloetzel P. M., MHC Class I Antigen Processing of an Adenovirus CTL Epitope Is Linked to the Levels of Immunoproteasomes in Infected Cells, 10.4049/jimmunol.164.9.4500
  4. Van den Eynde, B., and P. van der Bruggen. 2001. Peptide database of T-cell defined tumor antigens. Cancer Immunity. www.cancerimmunity.org/peptidedatabase/Tcellepitopes.htm.
  5. Van Snick J., Interleukin-HP1, a T cell-derived hybridoma growth factor that supports the in vitro growth of murine plasmacytomas, 10.1084/jem.165.3.641
  6. Stratford-Perricaudet L D, Makeh I, Perricaudet M, Briand P, Widespread long-term gene transfer to mouse skeletal muscles and heart., 10.1172/jci115902
  7. J. Immunol., 163, 2928 (1999)
  8. Seed B., Aruffo A., Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure., 10.1073/pnas.84.10.3365
  9. Takebe Y, Seiki M, Fujisawa J, Hoy P, Yokota K, Arai K, Yoshida M, Arai N, SR alpha promoter: an efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of human T-cell leukemia virus type 1 long terminal repeat., 10.1128/mcb.8.1.466
  10. Espevik Terje, Nissen-Meyer Jon, A highly sensitive cell line, WEHI 164 clone 13, for measuring cytotoxic factor/tumor necrosis factor from human monocytes, 10.1016/0022-1759(86)90322-4
  11. Hansen Morten Bagge, Nielsen Svend Erik, Berg Kurt, Re-examination and further development of a precise and rapid dye method for measuring cell growth/cell kill, 10.1016/0022-1759(89)90397-9
  12. Rock Kenneth L., Goldberg Alfred L., DEGRADATION OF CELL PROTEINS AND THE GENERATION OF MHC CLASS I-PRESENTED PEPTIDES, 10.1146/annurev.immunol.17.1.739
  13. Traversari Catia, van der Bruggen Pierre, Van den Eynde Benoît, Hainaut Philippe, Lemoine Carine, Ohta Nobuyoshi, Old Lloyd, Boon Thierry, Transfection and expression of a gene coding for a human melanoma antigen recognized by autologous cytolytic T lymphocytes, 10.1007/bf00185107
  14. J. Immunol., 163, 6045 (1999)
  15. Sijts A. J.A.M., Efficient Generation of a Hepatitis B Virus Cytotoxic T Lymphocyte Epitope Requires the Structural Features of Immunoproteasomes, 10.1084/jem.191.3.503
  16. Mizushima Seiichi, Nagata Shigekazu, pEF-BOS, a powerful mammalian expression vector, 10.1093/nar/18.17.5322
  17. Hendil Klavs B., Uerkvitz Wolfgang, The human multicatalytic proteinase: affinity purification using a monoclonal antibody, 10.1016/0165-022x(91)90028-u
  18. De Plaen Etienne, Traversari Catia, Gaforio José J., Szikora Jean-Pierre, De Smet Charles, Brasseur Francis, van der Bruggen Pierre, Lethé Bernard, Lurquin Christophe, Chomez Patrick, De Backer Olivier, Boon Thierry, Arden Karen, Cavenee Webster, Brasseur Robert, Structure, chromosomal localization, and expression of 12 genes of the MAGE family, 10.1007/bf01246677
  19. Rammensee Hans-Georg, Bachmann Jutta, Stevanović Stefan, History and Overview, MHC Ligands and Peptide Motifs (1997) ISBN:9783662221648 p.1-16, 10.1007/978-3-662-22162-4_1
  20. Chen J.-L., Dunbar P. R., Gileadi U., Jager E., Gnjatic S., Nagata Y., Stockert E., Panicali D. L., Chen Y.-T., Knuth A., Old L. J., Cerundolo V., Identification of NY-ESO-1 Peptide Analogues Capable of Improved Stimulation of Tumor-Reactive CTL, 10.4049/jimmunol.165.2.948
  21. J. Immunol., 162, 7075 (1999)
  22. Kingsbury Daniel J., Griffin Thomas A., Colbert Robert A., Novel Propeptide Function in 20 S Proteasome Assembly Influences β Subunit Composition, 10.1074/jbc.m001742200
  23. Macagno Annalisa, Gilliet Michel, Sallusto Federica, Lanzavecchia Antonio, Nestle Frank O., Groettrup Marcus, Dendritic cells up-regulate immunoproteasomes and the proteasome regulator PA28 during maturation, 10.1002/(sici)1521-4141(199912)29:12<4037::aid-immu4037>3.0.co;2-t
  24. Dahlmann Burkhardt, Ruppert Thomas, Kuehn Lothar, Merforth Simone, Kloetzel Peter-M, Different proteasome subtypes in a single tissue exhibit different enzymatic properties 1 1Edited by R. Huber, 10.1006/jmbi.2000.4185
  25. Foss Grethe S, Larsen Frank, Solheim Jorun, Prydz Hans, Constitutive and interferon-γ-induced expression of the human proteasome subunit multicatalytic endopeptidase complex-like 11EMBL accession number for MECL1 cDNA: Y13640.1, 10.1016/s0167-4889(97)00152-3
  26. Loukissa Anna, Cardozo Christopher, Altschuller-Felberg Claudia, Nelson Judith E, CONTROL OF LMP7 EXPRESSION IN HUMAN ENDOTHELIAL CELLS BY CYTOKINES REGULATING CELLULAR AND HUMORAL IMMUNITY, 10.1006/cyto.2000.0717
  27. Stoltze Lars, Schirle Markus, Schwarz Gerold, Schröter Christian, Thompson Michael W., Hersh Louis B., Kalbacher Hubert, Stevanovic Stefan, Rammensee Hans-Georg, Schild Hansjörg, 10.1038/80852
  28. Fruci Doriana, Niedermann Gabriele, Butler Richard H, van Endert Peter M, Efficient MHC Class I-Independent Amino-Terminal Trimming of Epitope Precursor Peptides in the Endoplasmic Reticulum, 10.1016/s1074-7613(01)00203-5
  29. Klein, J. 1986. Natural History of the Major Histocompatibility Complex. Wiley-Interscience, New York. pp. 1–775.
  30. Morel Sandra, Lévy Frédéric, Burlet-Schiltz Odile, Brasseur Francis, Probst-Kepper Michaël, Peitrequin Anne-Lise, Monsarrat Bernard, Van Velthoven Robert, Cerottini Jean-Charles, Boon Thierry, Gairin Jean Edouard, Van den Eynde Benoît J., Processing of Some Antigens by the Standard Proteasome but Not by the Immunoproteasome Results in Poor Presentation by Dendritic Cells, 10.1016/s1074-7613(00)80163-6
  31. Toes R.E.M., Nussbaum A.K., Degermann S., Schirle M., Emmerich N.P.N., Kraft M., Laplace C., Zwinderman A., Dick T.P., Müller J., Schönfisch B., Schmid C., Fehling H.-J., Stevanovic S., Rammensee H.G., Schild H., Discrete Cleavage Motifs of Constitutive and Immunoproteasomes Revealed by Quantitative Analysis of Cleavage Products, 10.1084/jem.194.1.1
  32. Driscoll James, Brown Michael G., Finley Daniel, Monaco John J., MHC-linked LMP gene products specifically alter peptidase activities of the proteasome, 10.1038/365262a0
  33. Kuckelkorn Ulrike, Frentzel Stefan, Kraft Regine, Kostka Susanne, Groettrup Marcus, Kloetzel Peter-M., Incorporation of major histocompatibility complex – encoded subunits LMP2 and LMP7 changes the quality of the 20S proteasome polypeptide processing products independent of interferon-γ, 10.1002/eji.1830250930
  34. Van den Eynde Benoı̂t J, Morel Sandra, Differential processing of class-I-restricted epitopes by the standard proteasome and the immunoproteasome, 10.1016/s0952-7915(00)00197-7
  35. Schwarz K., van den Broek M., Kostka S., Kraft R., Soza A., Schmidtke G., Kloetzel P.-M., Groettrup M., Overexpression of the Proteasome Subunits LMP2, LMP7, and MECL-1, But Not PA28 / , Enhances the Presentation of an Immunodominant Lymphocytic Choriomeningitis Virus T Cell Epitope, 10.4049/jimmunol.165.2.768
Bibliographic reference Schultz, Erwin S. ; Chapiro, Jacques ; Lurquin, Christophe ; Claverol, Stéphane ; Burlet-Schiltz, Odile ; et. al. The production of a new MAGE-3 peptide presented to cytolytic T lymphocytes by HLA-B40 requires the immunoproteasome. In: The Journal of Experimental Medicine, Vol. 195, no. 4, p. 391-399 (2002)
Permanent URL http://hdl.handle.net/2078.1/29533