Definition of proteasomal peptide splicing rules for high-efficiency spliced peptide presentation by MHC class I molecules

Journal of Immunology

Volumn 195, Issue 9, 2015, Pages 4085-4095

  Berkers, Celia R ^a,c,d   De Jong, Annemieke ^a   Schuurman, Karianne G ^a   Linnemann, Carsten ^a   Meiring, Hugo D ^b   Janssen, Lennert ^a   Neefjes, Jacques J ^a,c   Schumacher, Ton N M ^a,c   Rodenko, Boris ^a,e   Ovaa, Huib ^a,c  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b Institute for Translational Vaccinology (Intravacc)   (Netherlands)

^c Institute for Chemical Immunology   (Netherlands)

^d UTRECHT UNIVERSITY   (Netherlands)

^e UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; HLA ANTIGEN CLASS 1; PEPTIDE; PROTEASOME;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; PEPTIDE LIBRARY; PREDICTION; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROCESSING; REACTION ANALYSIS; RNA SPLICING; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; TRANSPEPTIDATION; VALIDATION PROCESS; ANTIGEN PRESENTATION; CHEMISTRY; IMMUNOLOGY; MOLECULAR GENETICS; PROTEIN SPLICING;

AMINO ACID SEQUENCE; ANTIGEN PRESENTATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SPLICING;

EID: 84945125570     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1402455     Document Type: Article

References (35)

1. Neefjes, J., M. L. Jongsma, P. Paul, and O. Bakke. 2011. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat. Rev. Immunol. 11: 823-836.
2. Sijts, E. J., and P. M. Kloetzel. 2011. The role of the proteasome in the generation of MHC class I ligands and immune responses. Cell. Mol. Life Sci. 68: 1491-1502.
3. Vigneron, N., and B. J. Van den Eynde. 2012. Proteasome subtypes and the processing of tumor antigens: increasing antigenic diversity. Curr. Opin. Immunol. 24: 84-91.
4. Basler, M., C. J. Kirk, and M. Groettrup. 2013. The immunoproteasome in antigen processing and other immunological functions. Curr. Opin. Immunol. 25: 74-80.
5. Vigneron, N., V. Stroobant, J. Chapiro, A. Ooms, G. Degiovanni, S. Morel, P. van der Bruggen, T. Boon, and B. J. Van den Eynde. 2004. An antigenic peptide produced by peptide splicing in the proteasome. Science 304: 587-590.
6. Hanada, K., J. W. Yewdell, and J. C. Yang. 2004. Immune recognition of a human renal cancer antigen through post-translational protein splicing. Nature 427: 252-256.
7. Warren, E. H., N. J. Vigneron, M. A. Gavin, P. G. Coulie, V. Stroobant, A. Dalet, S. S. Tykodi, S. M. Xuereb, J. K. Mito, S. R. Riddell, and B. J. Van den Eynde. 2006. An antigen produced by splicing of noncontiguous peptides in the reverse order. Science 313: 1444-1447.
8. Dalet, A., P. F. Robbins, V. Stroobant, N. Vigneron, Y. F. Li, M. El-Gamil, K. Hanada, J. C. Yang, S. A. Rosenberg, and B. J. Van den Eynde. 2011. An antigenic peptide produced by reverse splicing and double asparagine deamidation. Proc. Natl. Acad. Sci. USA 108: E323-E331.
9. Michaux, A., P. Larrieu, V. Stroobant, J. F. Fonteneau, F. Jotereau, B. J. Van den Eynde, A. Moreau-Aubry, and N. Vigneron. 2014. A spliced antigenic peptide comprising a single spliced amino acid is produced in the proteasome by reverse splicing of a longer peptide fragment followed by trimming. J. Immunol. 192: 1962-1971.
10. Dalet, A., N. Vigneron, V. Stroobant, K. Hanada, and B. J. Van den Eynde. 2010. Splicing of distant peptide fragments occurs in the proteasome by transpeptidation and produces the spliced antigenic peptide derived from fibroblast growth factor-5. J. Immunol. 184: 3016-3024.
11. Mishto, M., A. Goede, K. T. Taube, C. Keller, K. Janek, P. Henklein, A. Niewienda, A. Kloss, S. Gohlke, B. Dahlmann, et al. 2012. Driving forces of proteasome-catalyzed peptide splicing in yeast and humans. Mol. Cell. Proteomics 11: 1008-1023.
12. Berkers, C. R., A. de Jong, H. Ovaa, and B. Rodenko. 2009. Transpeptidation and reverse proteolysis and their consequences for immunity. Int. J. Biochem. Cell Biol. 41: 66-71.
13. Shastri, N. 2006. Cell biology: peptides, scrambled and stitched. Science 313: 1398-1399.
14. Borissenko, L., and M. Groll. 2007. Diversity of proteasomal missions: fine tuning of the immune response. Biol. Chem. 388: 947-955.
15. Liepe, J., M. Mishto, K. Textoris-Taube, K. Janek, C. Keller, P. Henklein, P. M. Kloetzel, and A. Zaikin. 2010. The 20S proteasome splicing activity discovered by SpliceMet. PLOS Comput. Biol. 6: e1000830.
16. Henderson, R. A., H. Michel, K. Sakaguchi, J. Shabanowitz, E. Appella, D. F. Hunt, and V. H. Engelhard. 1992. HLA-A2.1-associated peptides from a mutant cell line: a second pathway of antigen presentation. Science 255: 1264-1266.
17. Hunt, D. F., R. A. Henderson, J. Shabanowitz, K. Sakaguchi, H. Michel, N. Sevilir, A. L. Cox, E. Appella, and V. H. Engelhard. 1992. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science 255: 1261-1263.
18. Rammensee, H., J. Bachmann, N. P. Emmerich, O. A. Bachor, and S. Stevanović. 1999. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50: 213-219.
19. Nielsen, M., C. Lundegaard, P. Worning, S. L. Lauemøller, K. Lamberth, S. Buus, S. Brunak, and O. Lund. 2003. Reliable prediction of T-cell epitopes using neural networks with novel sequence representations. Protein Sci. 12: 1007-1017.
20. Toebes, M., M. Coccoris, A. Bins, B. Rodenko, R. Gomez, N. J. Nieuwkoop, W. van de Kasteele, G. F. Rimmelzwaan, J. B. Haanen, H. Ovaa, and T. N. Schumacher. 2006. Design and use of conditional MHC class I ligands. Nat. Med. 12: 246-251.
21. Altman, J. D., P. A. Moss, P. J. Goulder, D. H. Barouch, M. G. McHeyzer-Williams, J. I. Bell, A. J. McMichael, and M. M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science 274: 94-96.
22. Grommé, M., F. G. Uytdehaag, H. Janssen, J. Calafat, R. S. van Binnendijk, M. J. Kenter, A. Tulp, D. Verwoerd, and J. Neefjes. 1999. Recycling MHC class I molecules and endosomal peptide loading. Proc. Natl. Acad. Sci. USA 96: 10326-10331.
23. Raijmakers, R., C. R. Berkers, A. de Jong, H. Ovaa, A. J. Heck, and S. Mohammed. 2008. Automated online sequential isotope labeling for protein quantitation applied to proteasome tissue-specific diversity. Mol. Cell. Proteomics 7: 1755-1762.
24. Berkers, C. R., F. W. van Leeuwen, T. A. Groothuis, V. Peperzak, E. W. van Tilburg, J. Borst, J. J. Neefjes, and H. Ovaa. 2007. Profiling proteasome activity in tissue with fluorescent probes. Mol. Pharm. 4: 739-748.
25. de Jong, A., K. G. Schuurman, B. Rodenko, H. Ovaa, and C. R. Berkers. 2012. Fluorescence-based proteasome activity profiling. Methods Mol. Biol. 803: 183-204.
26. Rodenko, B., M. Toebes, P. H. Celie, A. Perrakis, T. N. Schumacher, and H. Ovaa. 2009. Class I major histocompatibility complexes loaded by a periodate trigger. J. Am. Chem. Soc. 131: 12305-12313.
27. Bakker, A. H., R. Hoppes, C. Linnemann, M. Toebes, B. Rodenko, C. R. Berkers, S. R. Hadrup, W. J. van Esch, M. H. Heemskerk, H. Ovaa, and T. N. Schumacher. 2008. Conditional MHC class I ligands and peptide exchange technology for the human MHC gene products HLA-A1, -A3, -A11, and -B7. Proc. Natl. Acad. Sci. USA 105: 3825-3830.
28. Bendle, G. M., C. Linnemann, A. I. Hooijkaas, L. Bies, M. A. de Witte, A. Jorritsma, A. D. Kaiser, N. Pouw, R. Debets, E. Kieback, et al. 2010. Lethal graft-versus-host disease in mouse models of T cell receptor gene therapy. Nat. Med. 16: 565-570.
29. Meiring, H. D., E. C. Soethout, A. P. de Jong, and C. A. van Els. 2007. Targeted identification of infection-related HLA class I-presented epitopes by stable isotope tagging of epitopes (SITE). Curr. Protoc. Immunol. Chapter 16: Unit 16.13.
30. Meiring, H., E. van der Heeft, G. ten Hove, and A. de Jong. 2002. Nanoscale LC-MS(n): technical design and applications to peptide and protein analysis. J. Sep. Sci. 25: 557-568.
31. Hoppes, R., R. Oostvogels, J. J. Luimstra, K. Wals, M. Toebes, L. Bies, R. Ekkebus, P. Rijal, P. H. Celie, J. H. Huang, et al. 2014. Altered peptide ligands revisited: vaccine design through chemically modified HLA-A2-restricted T cell epitopes. J. Immunol. 193: 4803-4813.
32. Reits, E., A. Griekspoor, J. Neijssen, T. Groothuis, K. Jalink, P. van Veelen, H. Janssen, J. Calafat, J. W. Drijfhout, and J. Neefjes. 2003. Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 18: 97-108.
33. Groll, M., R. Huber, and B. C. Potts. 2006. Crystal structures of Salinosporamide A (NPI-0052) and B (NPI-0047) in complex with the 20S proteasome reveal important consequences of β-lactone ring opening and a mechanism for irreversible binding. J. Am. Chem. Soc. 128: 5136-5141.
34. Groll, M., M. Götz, M. Kaiser, E. Weyher, and L. Moroder. 2006. TMC-95-based inhibitor design provides evidence for the catalytic versatility of the proteasome. Chem. Biol. 13: 607-614.
35. Berkers, C. R., A. de Jong, K. G. Schuurman, C. Linnemann, J. A. J. Geenevasen, T. N. M. Schumacher, B. Rodenko, and H. Ovaa. 2015. Peptide splicing in the proteasome creates a novel type of antigen with an isopeptide linkage. J. Immunol. 195: 4075-4084.