HLA micropolymorphisms strongly affect peptide-MHC multimer-based monitoring of antigen-specific CD8+ T cell responses

Journal of Immunology

Volumn 192, Issue 2, 2014, Pages 641-648

  Van Buuren, Marit M ^a   Dijkgraaf, Feline E ^a   Linnemann, Carsten ^a   Toebes, Mireille ^a   Chang, Cynthia X L ^b   Mok, Juk Yee ^c   Nguyen, Melanie ^c   Van Esch, Wim J E ^c   Kvistborg, Pia ^a   Grotenbreg, Gijsbert M ^b   Schumacher, Ton N M ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c Reagents Division   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HLA A2 ANTIGEN; MELANOMA ANTIGEN;

ARTICLE; CD8+ T LYMPHOCYTE; CELL CLONE; CELLULAR IMMUNITY; CONTROLLED STUDY; HLA SYSTEM; HUMAN; HUMAN CELL; IMMUNOLOGICAL MONITORING; MAJOR HISTOCOMPATIBILITY COMPLEX; MELANOMA; PERSONALIZED MEDICINE; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; TUMOR ASSOCIATED LEUKOCYTE;

ALLELES; AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CLONE CELLS; HLA-A2 ANTIGEN; HUMANS; LYMPHOCYTES, TUMOR-INFILTRATING; MAJOR HISTOCOMPATIBILITY COMPLEX; MELANOMA; MOLECULAR SEQUENCE DATA; NEOPLASM PROTEINS; PEPTIDES; POLYMORPHISM, GENETIC; SEQUENCE ALIGNMENT;

EID: 84892771793     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301770     Document Type: Article

References (40)

1. 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. (Pubitemid 26332731)
2. Davis, M. M., J. D. Altman, and E.W. Newell. 2011. Interrogating the repertoire: broadening the scope of peptide-MHC multimer analysis. Nat. Rev. Immunol. 11: 551-558.
3. Cobbold, M., N. Khan, B. Pourgheysari, S. Tauro, D. McDonald, H. Osman, M. Assenmacher, L. Billingham, C. Steward, C. Crawley, et al. 2005. Adoptive transfer of cytomegalovirus-specific CTL to stem cell transplant patients after selection by HLA-peptide tetramers. J. Exp. Med. 202: 379-386. (Pubitemid 41126955)
4. Moon, J. J., H. H. Chu, M. Pepper, S. J. McSorley, S. C. Jameson, R. M. Kedl, and M. K. Jenkins. 2007. Naive CD4+ T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27: 203-213. (Pubitemid 47284919)
5. + T cells reveals conserved precursor frequencies. Blood 115: 3718-3725.
6. Andersen, R. S., C. A. Thrue, N. Junker, R. Lyngaa, M. Donia, E. Ellebæk, I. M. Svane, T. N. Schumacher, P. Thor Straten, and S. R. Hadrup. 2012. Dissection of T-cell antigen specificity in human melanoma. Cancer Res. 72: 1642-1650.
7. + T-cell responses in acute and chronic viral diseases. Eur. J. Immunol. 43: 1109-1120.
8. Rohren, E. M., L. R. Pease, H. L. Ploegh, and T. N. Schumacher. 1993. Polymorphisms in pockets of major histocompatibility complex class I molecules influence peptide preference. J. Exp. Med. 177: 1713-1721. (Pubitemid 23146138)
9. Robinson, J., J. A. Halliwell, H. McWilliam, R. Lopez, P. Parham, and S. G. Marsh. 2013. The IMGT/HLA database. Nucleic Acids Res. 41(Database issue): D1222-D1227.
10. Gras, S., X. Saulquin, J. B. Reiser, E. Debeaupuis, K. Echasserieau, A. Kissenpfennig, F. Legoux, A. Chouquet, M. Le Gorrec, P. Machillot, et al. 2009. Structural bases for the affinity-driven selection of a public TCR against a dominant human cytomegalovirus epitope. J. Immunol. 183: 430-437.
11. Rodenko, B., M. Toebes, S. R. Hadrup, W. J. van Esch, A. M. Molenaar, T. N. Schumacher, and H. Ovaa. 2006. Generation of peptide-MHC class I complexes through UV-mediated ligand exchange. Nat. Protoc. 1: 1120-1132.
12. 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.
13. Toebes, M., B. Rodenko, H. Ovaa, and T. N. Schumacher. 2009. Generation of peptide MHC class I monomers and multimers through ligand exchange. Curr. Protoc. Immunol. Chapter 18: Unit 18.16. doi:10.1002/0471142735.im1816s87
14. Garboczi, D. N., D. T. Hung, and D. C. Wiley. 1992. HLA-A2-peptide complexes: refolding and crystallization of molecules expressed in Escherichia coli and complexed with single antigenic peptides. Proc. Natl. Acad. Sci. USA 89: 3429-3433.
15. Andersen, R. S., P. Kvistborg, T. M. Frøsig, N. W. Pedersen, R. Lyngaa, A. H. Bakker, C. J. Shu, Pt. Straten, T. N. Schumacher, and S. R. Hadrup. 2012. Parallel detection of antigen-specific T cell responses by combinatorial encoding of MHC multimers. Nat. Protoc. 7: 891-902.
16. + T cell compartment in melanoma patients. OncoImmunology 1: 409-418.
17. Hadrup, S. R., A. H. Bakker, C. J. Shu, R. S. Andersen, J. van Veluw, P. Hombrink, E. Castermans, P. Thor Straten, C. Blank, J. B. Haanen, et al. 2009. Parallel detection of antigen-specific T-cell responses by multidimensional encoding of MHC multimers. Nat. Methods 6: 520-526.
18. Linnemann, C., B. Heemskerk, P. Kvistborg, R. J. Kluin, D. A. Bolotin, X. Chen, K. Bresser, M. Nieuwland, R. Schotte, S. Michels, et al. 2013. High-throughput identification of antigen-specific TCRs by TCR gene capture. Nat. Med. 19: 1534-1541.
19. Dudley, M. E., J. R. Wunderlich, T. E. Shelton, J. Even, and S. A. Rosenberg. 2003. Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J. Immunother. 26: 332-342. (Pubitemid 36858717)
20. Saper, M. A., P. J. Bjorkman, and D. C. Wiley. 1991. Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 A resolution. J. Mol. Biol. 219: 277-319.
21. Matsumura, M., D. H. Fremont, P. A. Peterson, and I. A. Wilson. 1992. Emerging principles for the recognition of peptide antigens by MHC class I molecules. Science 257: 927-934.
22. Sidney, J., B. Peters, N. Frahm, C. Brander, and A. Sette. 2008. HLA class I supertypes: a revised and updated classification. BMC Immunol. 9: 1.
23. Rapin, N., I. Hoof, O. Lund, and M. Nielsen. 2008. MHC motif viewer. Immunogenetics 60: 759-765.
24. 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. (Pubitemid 43214754)
25. Guilloux, Y., S. Lucas, V. G. Brichard, A. Van Pel, C. Viret, E. De Plaen, F. Brasseur, B. Lethé, F. Jotereau, and T. Boon. 1996. A peptide recognized by human cytolytic T lymphocytes on HLA-A2 melanomas is encoded by an intron sequence of the N-acetylglucosaminyltransferase V gene. J. Exp. Med. 183: 1173-1183. (Pubitemid 26113980)
26. Yu, X. G., M. Lichterfeld, S. Chetty, K. L. Williams, S. K. Mui, T. Miura, N. Frahm, M. E. Feeney, Y. Tang, F. Pereyra, et al. 2007. Mutually exclusive T-cell receptor induction and differential susceptibility to human immunodeficiency virus type 1 mutational escape associated with a two-amino-acid difference between HLA class I subtypes. J. Virol. 81: 1619-1631. (Pubitemid 46214437)
27. Archbold, J. K., W. A. Macdonald, S. Gras, L. K. Ely, J. J. Miles, M. J. Bell, R. M. Brennan, T. Beddoe, M. C. Wilce, C. S. Clements, et al. 2009. Natural micropolymorphism in human leukocyte antigens provides a basis for genetic control of antigen recognition. J. Exp. Med. 206: 209-219.
28. Stewart-Jones, G. B., P. Simpson, P. A. van der Merwe, P. Easterbrook, A. J. McMichael, S. L. Rowland-Jones, E. Y. Jones, and G. M. Gillespie. 2012. Structural features underlying T-cell receptor sensitivity to concealed MHC class I micropolymorphisms. Proc. Natl. Acad. Sci. USA 109: E3483-E3492.
29. Macdonald, W. A., A. W. Purcell, N. A. Mifsud, L. K. Ely, D. S. Williams, L. Chang, J. J. Gorman, C. S. Clements, L. Kjer-Nielsen, D. M. Koelle, et al. 2003. A naturally selected dimorphism within the HLA-B44 supertype alters class I structure, peptide repertoire, and T cell recognition. J. Exp. Med. 198: 679-691. (Pubitemid 37087768)
30. Park, I., and P. Terasaki. 2000. Origins of the first HLA specificities. Hum. Immunol. 61: 185-189. (Pubitemid 30117785)
31. Sauce, D., M. Bodinier, M. Garin, B. Petracca, N. Tonnelier, A. Duperrier, J. V. Melo, J. F. Apperley, C. Ferrand, P. Hervé, et al. 2002. Retrovirus-mediated gene transfer in primary T lymphocytes impairs their anti-Epstein-Barr virus potential through both culture-dependent and selection process-dependent mechanisms. Blood 99: 1165-1173. (Pubitemid 37258302)
32. + T cells in chronic human immunodeficiency virus infection. Blood 96: 3094-3101.
33. Lambert, M., M. Gannagé, A. Karras, M. Abel, C. Legendre, D. Kerob, F. Agbalika, P. M. Girard, C. Lebbe, and S. Caillat-Zucman. 2006. Differences in the frequency and function of HHV8-specific CD8 T cells between asymptomatic HHV8 infection and Kaposi sarcoma. Blood 108: 3871-3880. (Pubitemid 44864571)
34. Warren, R. L., G. Choe, D. J. Freeman, M. Castellarin, S. Munro, R. Moore, and R. A. Holt. 2012. Derivation of HLA types from shotgun sequence datasets. Genome Med. 4: 95.
35. Boegel, S., M. Lower, M. Schafer, T. Bukur, J. de Graaf, V. Boisguerin, O. Tureci, M. Diken, J. C. Castle, and U. Sahin. 2013. HLA typing from RNASeq sequence reads. Genome Med. 4: 102.
36. Liu, C., X. Yang, B. Duffy, T. Mohanakumar, R. D. Mitra, M. C. Zody, and J. D. Pfeifer. 2013. ATHLATES: accurate typing of human leukocyte antigen through exome sequencing. Nucleic Acids Res. 41: e142.
37. Kvistborg, P., M. M. van Buuren, and T. N. Schumacher. 2013. Human cancer regression antigens. Curr. Opin. Immunol. 25: 284-290.
38. 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.
39. van Rooij, N., M. M. van Buuren, D. Philips, A. Velds, M. Toebes, B. Heemskerk, L. van Dijk, S. Behjati, H. Hilkmann, D. el Atmioui, et al. 2013. Tumor exome analysis reveals neoantigen-specific T-cell reactivity in an ipilimumab-responsive melanoma. J. Clin. Oncol. 31: e439-e442.
40. Newell, E. W., N. Sigal, N. Nair, B. A. Kidd, H. B. Greenberg, and M. M. Davis. 2013. Combinatorial tetramer staining and mass cytometry analysis facilitate T-cell epitope mapping and characterization. Nat. Biotechnol. 31: 623-629.