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Class I major histocompatibility complexes loaded by a periodate trigger.

Rodenko B, Toebes M, Celie PH, Perrakis A, Schumacher TN, Ovaa H
J Am Chem Soc 131 12305-13 (2009)
Related entries: 2x4n, 2x4o, 2x4q, 2x4r, 2x4s, 2x4t, 2x4u, 2x70

Cited: 21 times
EuropePMC logo PMID: 19655751

Abstract

Class I major histocompatibility complexes (MHCs) present peptide ligands on the cell surface for recognition by appropriate cytotoxic T cells. The unstable nature of unliganded MHC necessitates the production of recombinant class I complexes through in vitro refolding reactions in the presence of an added excess of peptides. This strategy is not amenable to high-throughput production of vast collections of class I complexes. To address this issue, we recently designed photocaged MHC ligands that can be cleaved by a UV light trigger in the MHC bound state under conditions that do not affect the integrity of the MHC structure. The results obtained with photocaged MHC ligands demonstrate that conditional MHC ligands can form a generally applicable concept for the creation of defined peptide-MHCs. However, the use of UV exposure to mediate ligand exchange is unsuited for a number of applications, due to the lack of UV penetration through cell culture systems and due to the transfer of heat upon UV irradiation, which can induce evaporation. To overcome these limitations, here, we provide proof-of-concept for the generation of defined peptide-MHCs by chemical trigger-induced ligand exchange. The crystal structure of the MHC with the novel chemosensitive ligand showcases that the ligand occupies the expected binding site, in a conformation where the hydroxyl groups should be reactive to periodate. We proceed to validate this technology by producing peptide-MHCs that can be used for T cell detection. The methodology that we describe here should allow loading of MHCs with defined peptides in cell culture devices, thereby permitting antigen-specific T cell expansion and purification for cell therapy. In addition, this technology will be useful to develop miniaturized assay systems for performing high-throughput screens for natural and unnatural MHC ligands.

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  1. Broad TCR repertoire and diverse structural solutions for recognition of an immunodominant CD8+ T cell epitope. Song I, Gil A, Mishra R, Ghersi D, Selin LK, Stern LJ. Nat Struct Mol Biol 24 395-406 (2017)


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  1. Chemical biology of antigen presentation by MHC molecules. van Kasteren SI, Overkleeft H, Ovaa H, Neefjes J. Curr Opin Immunol 26 21-31 (2014)
  2. Photochemical approaches to T-cell activation. Huse M. Immunology 130 151-157 (2010)
  3. Antigen-specific and cross-reactive T cells in protection and disease. Jiang N, Malone M, Chizari S. Immunol Rev 316 120-135 (2023)

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  1. Catalytic and molecular beacons for amplified detection of metal ions and organic molecules with high sensitivity. Zhang XB, Wang Z, Xing H, Xiang Y, Lu Y. Anal Chem 82 5005-5011 (2010)
  2. A ligation-triggered DNAzyme cascade for amplified fluorescence detection of biological small molecules with zero-background signal. Lu LM, Zhang XB, Kong RM, Yang B, Tan W. J Am Chem Soc 133 11686-11691 (2011)
  3. Definition of Proteasomal Peptide Splicing Rules for High-Efficiency Spliced Peptide Presentation by MHC Class I Molecules. Berkers CR, de Jong A, Schuurman KG, Linnemann C, Meiring HD, Janssen L, Neefjes JJ, Schumacher TN, Rodenko B, Ovaa H. J Immunol 195 4085-4095 (2015)
  4. Altered peptide ligands revisited: vaccine design through chemically modified HLA-A2-restricted T cell epitopes. Hoppes R, Oostvogels R, Luimstra JJ, Wals K, Toebes M, Bies L, Ekkebus R, Rijal P, Celie PH, Huang JH, Emmelot ME, Spaapen RM, Lokhorst H, Schumacher TN, Mutis T, Rodenko B, Ovaa H. J Immunol 193 4803-4813 (2014)
  5. Dipeptides catalyze rapid peptide exchange on MHC class I molecules. Saini SK, Schuster H, Ramnarayan VR, Rammensee HG, Stevanović S, Springer S. Proc Natl Acad Sci U S A 112 202-207 (2015)
  6. In-solution enrichment identifies peptide inhibitors of protein-protein interactions. Touti F, Gates ZP, Bandyopadhyay A, Lautrette G, Pentelute BL. Nat Chem Biol 15 410-418 (2019)
  7. A simple and effective cleavable linker for chemical proteomics applications. Yang Y, Hahne H, Kuster B, Verhelst SH. Mol Cell Proteomics 12 237-244 (2013)
  8. A flexible MHC class I multimer loading system for large-scale detection of antigen-specific T cells. Luimstra JJ, Garstka MA, Roex MCJ, Redeker A, Janssen GMC, van Veelen PA, Arens R, Falkenburg JHF, Neefjes J, Ovaa H. J Exp Med 215 1493-1504 (2018)
  9. Peptide Splicing in the Proteasome Creates a Novel Type of Antigen with an Isopeptide Linkage. Berkers CR, de Jong A, Schuurman KG, Linnemann C, Geenevasen JA, Schumacher TN, Rodenko B, Ovaa H. J Immunol 195 4075-4084 (2015)
  10. Bioorthogonal cleavage and exchange of major histocompatibility complex ligands by employing azobenzene-containing peptides. Choo JA, Thong SY, Yap J, van Esch WJ, Raida M, Meijers R, Lescar J, Verhelst SH, Grotenbreg GM. Angew Chem Int Ed Engl 53 13390-13394 (2014)
  11. Development of a hypersensitive periodate-cleavable amino acid that is methionine- and disulfide-compatible and its application in MHC exchange reagents for T cell characterisation. Amore A, Wals K, Koekoek E, Hoppes R, Toebes M, Schumacher TN, Rodenko B, Ovaa H. Chembiochem 14 123-131 (2013)
  12. Chemical Modification of Influenza CD8+ T-Cell Epitopes Enhances Their Immunogenicity Regardless of Immunodominance. Rosendahl Huber SK, Luimstra JJ, van Beek J, Hoppes R, Jacobi RH, Hendriks M, Kapteijn K, Ouwerkerk C, Rodenko B, Ovaa H, de Jonge J. PLoS One 11 e0156462 (2016)
  13. Stability screening of arrays of major histocompatibility complexes on combinatorially encoded flow cytometry beads. Chew SL, Or MY, Chang CX, Gehring AJ, Bertoletti A, Grotenbreg GM. J Biol Chem 286 28466-28475 (2011)
  14. MHC-I peptide binding activity assessed by exchange after cleavage of peptide covalently linked to β2-microglobulin. Jurewicz MM, Willis RA, Ramachandiran V, Altman JD, Stern LJ. Anal Biochem 584 113328 (2019)
  15. Production and Thermal Exchange of Conditional Peptide-MHC I Multimers. Luimstra JJ, Franken KLMC, Garstka MA, Drijfhout JW, Neefjes J, Ovaa H. Curr Protoc Immunol 126 e85 (2019)
  16. Xeno interactions between MHC-I proteins and molecular chaperones enable ligand exchange on a broad repertoire of HLA allotypes. Sun Y, Papadaki GF, Devlin CA, Danon JN, Young MC, Winters TJ, Burslem GM, Procko E, Sgourakis NG. Sci Adv 9 eade7151 (2023)
  17. Fast peptide exchange on major histocompatibility complex class I molecules by acidic stabilization of a peptide-empty intermediate. Saikia A, Hadeler A, Prasad P, Zacharias M, Springer S. Protein Sci 31 e4478 (2022)


Related citations provided by authors (1)

  1. UV-induced ligand exchange in MHC class I protein crystals.. Celie PH, Toebes M, Rodenko B, Ovaa H, Perrakis A, Schumacher TN J Am Chem Soc 131 12298-304 (2009)

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