The length distribution of class I-restricted T cell epitopes is determined by both peptide supply and MHC allele-specific binding preference

Journal of Immunology

Volumn 196, Issue 4, 2016, Pages 1480-1487

  Trolle, Thomas ^a   McMurtrey, Curtis P ^b   Sidney, John ^c   Bardet, Wilfried ^b   Osborn, Sean C ^b   Kaever, Thomas ^b   Sette, Alessandro ^b   Hildebrand, William H ^b   Nielsen, Morten ^a,d   Peters, Bjoern ^c  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^d INSTITUTO DE INVESTIGACIONES BIOTECNOLÓGICAS   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; HLA A ANTIGEN; HLA B ANTIGEN; LIGAND; PEPTIDE; PROTEIN BINDING;

ALLELE; ANIMAL; CD8+ T LYMPHOCYTE; CHEMISTRY; EPITOPE MAPPING; GENE; GENETICS; HELA CELL LINE; HUMAN; IMMUNOLOGY; METABOLISM; PROCEDURES;

ALLELES; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; EPITOPE MAPPING; EPITOPES, T-LYMPHOCYTE; GENES, MHC CLASS I; HELA CELLS; HLA-A ANTIGENS; HLA-B ANTIGENS; HUMANS; IMMUNODOMINANT EPITOPES; LIGANDS; PEPTIDES; PROTEIN BINDING;

EID: 84958568837     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501721     Document Type: Article

References (46)

1. Peters, B., H.-H. Bui, S. Frankild, M. Nielson, C. Lundegaard, E. Kostem, D. Basch, K. Lamberth, M. Harndahl, W. Fleri, et al. 2006. A community resource benchmarking predictions of peptide binding to MHC-I molecules. PLOS Comput. Biol. 2: e65.
2. Lin, H. H., S. Ray, S. Tongchusak, E. L. Reinherz, and V. Brusic. 2008. Evaluation of MHC class I peptide binding prediction servers: applications for vaccine research. BMC Immunol. 9: 8.
3. Zhang, G. L., H. R. Ansari, P. Bradley, G. C. Cawley, T. Hertz, X. Hu, N. Jojic, Y. Kim, O. Kohlbacher, O. Lund, et al. 2011. Machine learning competition in immunology-Prediction of HLA class I binding peptides. J. Immunol. Methods 374: 1-4.
4. Trolle, T., I. G. Metushi, J. A. Greenbaum, Y. Kim, J. Sidney, O. Lund, A. Sette, B. Peters, and M. Nielsen. 2015. Automated benchmarking of peptide-MHC class I binding predictions. Bioinformatics 31: 2174-2181.
5. Erup Larsen, M., H. Kloverpris, A. Stryhn, C. K. Koofhethile, S. Sims, T. Ndung'u, P. Goulder, S. Buus, and M. Nielsen. 2011. HLArestrictor-A tool for patient-specific predictions of HLA restriction elements and optimal epitopes within peptides. Immunogenetics 63: 43-55.
6. Paul, S., D. Weiskopf, M. A. Angelo, J. Sidney, B. Peters, and A. Sette. 2013. HLA class I alleles are associated with peptide-binding repertoires of different size, affinity, and immunogenicity. J. Immunol. 191: 5831-5839.
7. Wang, M., K. Lamberth, M. Harndahl, G. Røder, A. Stryhn, M. V. Larsen, M. Nielsen, C. Lundegaard, S. T. Tang, M. H. Dziegiel, et al. 2007. CTL epitopes for influenza A including the H5N1 bird flu; genome-, pathogen-, and HLA-wide screening. Vaccine 25: 2823-2831.
8. Sedegah, M., Y. Kim, H. Ganeshan, J. Huang, M. Belmonte, E. Abot, J. G. Banania, F. Farooq, S. McGrath, B. Peters, et al. 2013. Identification of minimal human MHC-restricted CD8+ T-cell epitopes within the Plasmodium falciparum circumsporozoite protein (CSP). Malar. J. 12: 185.
9. Chiu, C., M. McCausland, J. Sidney, F. M. Duh, N. Rouphael, A. Mehta, M. Mulligan, M. Carrington, A. Wieland, N. L. Sullivan, et al. 2014. Broadly reactive human CD8 T cells that recognize an epitope conserved between VZV, HSV and EBV. PLoS Pathog. 10: e1004008.
10. Rajasagi, M., S. A. Shukla, E. F. Fritsch, D. B. Keskin, D. DeLuca, E. Carmona, W. Zhang, C. Sougnez, K. Cibulskis, J. Sidney, et al. 2014. Systematic identification of personal tumor-specific neoantigens in chronic lymphocytic leukemia. Blood 124: 453-462.
11. Robbins, P. F., Y.-C. Lu, M. El-Gamil, Y. F. Li, C. Gross, J. Gartner, J. C. Lin, J. K. Teer, P. Cliften, E. Tycksen, et al. 2013. Mining exomic sequencing data to identify mutated antigens recognized by adoptively transferred tumor-reactive T cells. Nat. Med. 19: 747-752.
12. Rizvi, N. A., M. D. Hellmann, A. Snyder, P. Kvistborg, V. Makarov, J. J. Havel, W. Lee, J. Yuan, P. Wong, T. S. Ho, et al. 2015. Caner immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348: 124-128.
13. Chen, Y., J. Sidney, S. Southwood, A. L. Cox, K. Sakaguchi, R. A. Henderson, E. Appella, D. F. Hunt, A. Sette, and V. H. Engelhard. 1994. Naturally processed peptides longer than nine amino acid residues bind to the class I MHC molecule HLA-A2.1 with high affinity and in different conformations. J. Immunol. 152: 2874-2881.
14. Weiskopf, D., M. A. Angelo, E. L. de Azeredo, J. Sidney, J. A. Greenbaum, A. N. Fernando, A. Broadwater, R. V. Kolla, A. D. De Silva, A. M. de Silva, et al. 2013. Comprehensive analysis of dengue virus-specific responses supports an HLA-linked protective role for CD8+ T cells. Proc. Natl. Acad. Sci. USA 110: E2046-E2053.
15. Lidehall, A. K., F. Sund, T. Lundberg, B. M. Eriksson, T. H. Tötterman, and O. Korsgren. 2005. T cell control of primary and latent cytomegalovirus infections in healthy subjects. J. Clin. Immunol. 25: 473-481.
16. Motozono, C., N. Kuse, X. Sun, P. J. Rizkallah, A. Fuller, S. Oka, D. K. Cole, A. K. Sewell, and M. Takiguchi. 2014. Molecular basis of a dominant T cell response to an HIV reverse transcriptase 8-mer epitope presented by the protective allele HLA-B∗51:01. J. Immunol. 192: 3428-3434.
17. Rist, M. J., A. Theodossis, N. P. Croft, M. A. Neller, A. Welland, Z. Chen, L. C. Sullivan, J. M. Burrows, J. J. Miles, R. M. Brennan, et al. 2013. HLA peptide length preferences control CD8+ T cell responses. J. Immunol. 191: 561-571.
18. Tey, S. K., F. Goodrum, and R. Khanna. 2010. CD8+ T-cell recognition of human cytomegalovirus latency-associated determinant pUL138. J. Gen. Virol. 91: 2040-2048.
19. Hassan, C., E. Chabrol, L. Jahn, M. G. Kester, A. H. de Ru, J. W. Drijfhout, J. Rossjohn, J. H. Falkenburg, M. H. Heemskerk, S. Gras, and P. A. van Veelen. 2015. Naturally processed non-canonical HLA-A∗02:01 presented peptides. J. Biol. Chem. 290: 2593-2603.
20. Lundegaard, C., O. Lund, and M. Nielsen. 2008. Accurate approximation method for prediction of class I MHC affinities for peptides of length 8, 10 and 11 using prediction tools trained on 9mers. Bioinformatics 24: 1397-1398.
21. Blum, J. S., P. A. Wearsch, and P. Cresswell. 2013. Pathways of antigen processing. Annu. Rev. Immunol. 31: 443-473.
22. Sidney, J., S. Southwood, C. Moore, C. Oseroff, C. Pinilla, H. M. Grey, and A. Sette. 2013. Measurement of MHC/peptide interactions by gel filtration or monoclonal antibody capture. Curr. Protoc. Immunol. Chapter 18: Unit 18.3.
23. Cheng, Y., andW. H. Prusoff. 1973. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem. Pharmacol. 22: 3099-3108.
24. Gulukota, K., J. Sidney, A. Sette, and C. DeLisi. 1997. Two complementary methods for predicting peptides binding major histocompatibility complex molecules. J. Mol. Biol. 267: 1258-1267.
25. Yaciuk, J. C., M. Skaley, W. Bardet, F. Schafer, D. Mojsilovic, S. Cate, C. J. Stewart, C. McMurtrey, K. W. Jackson, R. Buchli, et al. 2014. Direct interrogation of viral peptides presented by the class I HLA of HIV-infected T cells. J. Virol. 88: 12992-13004.
26. Carreno, B. M., V. Magrini, M. Becker-Hapak, S. Kaabinejadian, J. Hundal, A. A. Petti, A. Ly, W. R. Lie, W. H. Hildebrand, E. R. Mardis, and G. P. Linette. 2015. Cancer immunotherapy. A dendritic cell vaccine increases the breadth and diversity of melanoma neoantigen-specific T cells. Science 348: 803-808.
27. Zhang, J., L. Xin, B. Shan, W. Chen, M. Xie, D. Yuen, W. Zhang, Z. Zhang, G. a. Lajoie, and B. Ma. 2012. PEAKS DB: de novo sequencing assisted database search for sensitive and accurate peptide identification. Mol. Cell. Proteomics 11: M111.010587.
28. Nielsen, M., C. Lundegaard, T. Blicher, K. Lamberth, M. Harndahl, S. Justesen, G. Røder, B. Peters, A. Sette, O. Lund, and S. Buus. 2007. NetMHCpan, a method for quantitative predictions of peptide binding to any HLA-A and-B locus protein of known sequence. PLoS One 2: e796.
29. Hoof, I., B. Peters, J. Sidney, L. E. Pedersen, A. Sette, O. Lund, S. Buus, and M. Nielsen. 2009. NetMHCpan, a method for MHC class I binding prediction beyond humans. Immunogenetics 61: 1-13.
30. Jørgensen, K. W., M. Rasmussen, S. Buus, and M. Nielsen. 2014. NetMHCstab-predicting stability of peptide-MHC-I complexes; impacts for cytotoxic T lymphocyte epitope discovery. Immunology 141: 18-26.
31. Vita, R., J. A. Overton, J. A. Greenbaum, J. Ponomarenko, J. D. Clark, J. R. Cantrell, D. K. Wheeler, J. L. Gabbard, D. Hix, A. Sette, and B. Peters. 2015. The immune epitope database (IEDB) 3.0. Nucleic Acids Res. 43: D405-D412.
32. Granados, D. P., D. Sriranganadane, T. Daouda, A. Zieger, C. M. Laumont, O. Caron-Lizotte, G. Boucher, M.-P. Hardy, P. Gendron, C. Côté, et al. 2014. Impact of genomic polymorphisms on the repertoire of human MHC class Iassociated peptides. Nat. Commun. 5: 3600.
33. Marcilla, M., A. Alpízar, M. Lombardía, A. Ramos-Fernandez, M. Ramos, and J. P. Albar. 2014. Increased diversity of the HLA-B40 ligandome by the presentation of peptides phosphorylated at their main anchor residue. Mol. Cell. Proteomics 13: 462-474.
34. Thommen, D. S., H. Schuster, M. Keller, S. Kapoor, A. O. Weinzierl, C. S. Chennakesava, X. Wang, L. Rohrer, A. von Eckardstein, S. Stevanovic, and B. C. Biedermann. 2012. Two preferentially expressed proteins protect vascular endothelial cells from an attack by peptide-specific CTL. J. Immunol. 188: 5283-5292.
35. Kotturi, M. F., B. Peters, F. Buendia-Laysa, Jr., J. Sidney, C. Oseroff, J. Botten, H. Grey, M. J. Buchmeier, and A. Sette. 2007. The CD8+ T-cell response to lymphocytic choriomeningitis virus involves the L antigen: uncovering new tricks for an old virus. J. Virol. 81: 4928-4940.
36. Wenzel, T., C. Eckerskorn, F. Lottspeich, and W. Baumeister. 1994. Existence of a molecular ruler in proteasomes suggested by analysis of degradation products. FEBS Lett. 349: 205-209.
37. Nussbaum, A. K., T. P. Dick, W. Keilholz, M. Schirle, S. Stevanović, K. Dietz, W. Heinemeyer, M. Groll, D. H. Wolf, R. Huber, et al. 1998. Cleavage motifs of the yeast 20S proteasome beta subunits deduced from digests of enolase 1. Proc. Natl. Acad. Sci. USA 95: 12504-12509.
38. Kisselev, A. F., T. N. Akopian, K. M. Woo, and A. L. Goldberg. 1999. The sizes of peptides generated from protein by mammalian 26 and 20 S proteasomes. Implications for understanding the degradative mechanism and antigen presentation. J. Biol. Chem. 274: 3363-3371.
39. van Endert, P. M., R. Tampé, T. H. Meyer, R. Tisch, J. F. Bach, and H. O. McDevitt. 1994. A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity 1: 491-500.
40. Schumacher, T. N., D. V. Kantesaria, M. T. Heemels, P. G. Ashton-Rickardt, J. C. Shepherd, K. Fruh, Y. Yang, P. A. Peterson, S. Tonegawa, and H. L. Ploegh. 1994. Peptide length and sequence specificity of the mouse TAP1/TAP2 translocator. J. Exp. Med. 179: 533-540.
41. Chang, S.-C., F. Momburg, N. Bhutani, and A. L. Goldberg. 2005. The ER aminopeptidase, ERAP1, trims precursors to lengths of MHC class I peptides by a "molecular ruler" mechanism. Proc. Natl. Acad. Sci. USA 102: 17107-17112.
42. Tynan, F. E., N. A. Borg, J. J. Miles, T. Beddoe, D. El-Hassen, S. L. Silins, W. J. van Zuylen, A. W. Purcell, L. Kjer-Nielsen, J. McCluskey, et al. 2005. High resolution structures of highly bulged viral epitopes bound to major histocompatibility complex class I. Implications for T-cell receptor engagement and T-cell immunodominance. J. Biol. Chem. 280: 23900-23909.
43. Burrows, S. R., J. Rossjohn, and J. McCluskey. 2006. Have we cut ourselves too short in mapping CTL epitopes? Trends Immunol. 27: 11-16.
44. Samino, Y., D. López, S. Guil, L. Saveanu, P. M. van Endert, and M. Del Val. 2006. A long N-terminal-extended nested set of abundant and antigenic major histocompatibility complex class I natural ligands from HIV envelope protein. J. Biol. Chem. 281: 6358-6365.
45. Hörig, H., A. C. Young, N. J. Papadopoulos, T. P. DiLorenzo, and S. G. Nathenson. 1999. Binding of longer peptides to the H-2Kb heterodimer is restricted to peptides extended at their C terminus: refinement of the inherent MHC class I peptide binding criteria. J. Immunol. 163: 4434-4441.
46. Collins, E. J., D. N. Garboczi, and D. C. Wiley. 1994. Three-dimensional structure of a peptide extending from one end of a class I MHC binding site. Nature 371: 626-629.