KIR3DL2 binds to HLA-B27 dimers and free H chains more strongly than other HLA class I and promotes the expansion of T cells in ankylosing spondylitis

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3216-3224

  Wong Baeza, Isabel ^a   Ridley, Anna ^a   Shaw, Jackie ^a   Hatano, Hiroko ^a   Rysnik, Oliwia ^a   McHugh, Kirsty ^a   Piper, Christopher ^a   Brackenbridge, Simon ^b   Fernandes, Ricardo ^b   Chan, Anthoni ^c   Bowness, Paul ^d   Kollnberger, Simon ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c ROYAL BERKSHIRE HOSPITAL   (United Kingdom)

^d NIHR OXFORD BIOMEDICAL RESEARCH CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DIMER; GAMMA INTERFERON; HLA A3 ANTIGEN; HLA ANTIGEN CLASS 1; HLA B27 ANTIGEN; INTERLEUKIN 2; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 3DL2;

ANKYLOSING SPONDYLITIS; ANTIGEN EXPRESSION; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISULFIDE BOND; HEAVY CHAIN; HUMAN; HUMAN CELL; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

ANTIGENS; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; HISTOCOMPATIBILITY ANTIGENS CLASS I; HLA-A3 ANTIGEN; HLA-B27 ANTIGEN; HLA-B35 ANTIGEN; HLA-B7 ANTIGEN; HUMANS; INTERFERON-GAMMA; KILLER CELLS, NATURAL; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RECEPTORS, KIR3DL2; SPONDYLITIS, ANKYLOSING; T-LYMPHOCYTE SUBSETS;

EID: 84875448412     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202926     Document Type: Article

References (35)

1. Brown, M. A., K. D. Pile, L. G. Kennedy, A. Calin, C. Darke, J. Bell, B. P. Wordsworth, and F. Cornélis. 1996. HLA class I associations of ankylosing spondylitis in the white population in the United Kingdom. Ann. Rheum. Dis. 55: 268-270.
2. Colbert, R. A., M. L. DeLay, G. Layh-Schmitt, and D. P. Sowders. 2009. HLAB27 misfolding and spondyloarthropathies. Adv. Exp. Med. Biol. 649: 217-234.
3. Fiorillo, M. T., and R. Sorrentino. 2009. T-cell responses against viral and selfepitopes and HLA-B27 subtypes differentially associated with ankylosing spondylitis. Adv. Exp. Med. Biol. 649: 255-262.
4. López de Castro, J. A. 2007. HLA-B27 and the pathogenesis of spondyloarthropathies. Immunol. Lett. 108: 27-33.
5. Kollnberger, S., L. Bird, M. Y. Sun, C. Retiere, V. M. Braud, A. McMichael, and P. Bowness. 2002. Cell-surface expression and immune receptor recognition of HLA-B27 homodimers. Arthritis Rheum. 46: 2972-2982.
6. Kollnberger, S., L. A. Bird, M. Roddis, C. Hacquard-Bouder, H. Kubagawa, H. C. Bodmer, M. Breban, A. J. McMichael, and P. Bowness. 2004. HLA-B27 heavy chain homodimers are expressed in HLA-B27 transgenic rodent models of spondyloarthritis and are ligands for paired Ig-like receptors. J. Immunol. 173: 1699-1710.
7. Payeli, S. K., S. Kollnberger, O. Marroquin Belaunzaran, M. Thiel, K. McHugh, J. Giles, J. Shaw, S. Kleber, A. Ridley, I. Wong-Baeza, et al. 2012. Inhibiting HLA-B27 homodimer-driven immune cell inflammation in spondylarthritis. Arthritis Rheum. 64: 3139-3149.
8. Lanier, L. L. 1998. Follow the leader: NK cell receptors for classical and nonclassical MHC class I. Cell 92: 705-707.
9. Allen, R. L., T. Raine, A. Haude, J. Trowsdale, and M. J. Wilson. 2001. Leukocyte receptor complex-encoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J. Immunol. 167: 5543-5547.
10. Kollnberger, S., and P. Bowness. 2009. The role of B27 heavy chain dimer immune receptor interactions in spondyloarthritis. Adv. Exp. Med. Biol. 649: 277-285.
11. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274.
12. Chwae, Y. J., M. J. Chang, S. M. Park, H. Yoon, H. J. Park, S. J. Kim, and J. Kim. 2002. Molecular mechanism of the activation-induced cell death inhibition mediated by a p70 inhibitory killer cell Ig-like receptor in Jurkat T cells. J. Immunol. 169: 3726-3735.
13. Döhring, C., D. Scheidegger, J. Samaridis, M. Cella, and M. Colonna. 1996. A human killer inhibitory receptor specific for HLA-A1,2. J. Immunol. 156: 3098-3101.
14. Hansasuta, P., T. Dong, H. Thananchai, M. Weekes, C. Willberg, H. Aldemir, S. Rowland-Jones, and V. M. Braud. 2004. Recognition of HLA-A3 and HLAA11 by KIR3DL2 is peptide-specific. Eur. J. Immunol. 34: 1673-1679.
15. Stewart-Jones, G. B., K. di Gleria, S. Kollnberger, A. J. McMichael, E. Y. Jones, and P. Bowness. 2005. Crystal structures and KIR3DL1 recognition of three immunodominant viral peptides complexed to HLA-B&z.ast;2705. Eur. J. Immunol. 35: 341-351.
16. Kollnberger, S., A. Chan, M. Y. Sun, L. Y. Chen, C. Wright, K. di Gleria, A. McMichael, and P. Bowness. 2007. Interaction of HLA-B27 homodimers with KIR3DL1 and KIR3DL2, unlike HLA-B27 heterotrimers, is independent of the sequence of bound peptide. Eur. J. Immunol. 37: 1313-1322.
17. Chan, A. T., S. D. Kollnberger, L. R. Wedderburn, and P. Bowness. 2005. Expansion and enhanced survival of natural killer cells expressing the killer immunoglobulin-like receptor KIR3DL2 in spondylarthritis. Arthritis Rheum. 52: 3586-3595.
18. Bowness, P., A. Ridley, J. Shaw, A. T. Chan, I. Wong-Baeza, M. Fleming, F. Cummings, A. McMichael, and S. Kollnberger. 2011. Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J. Immunol. 186: 2672-2680.
19. Fernandes, R. A., C. Yu, A. M. Carmo, E. J. Evans, P. A. van der Merwe, and S. J. Davis. 2010. What controls T cell receptor phosphorylation? Cell 142: 668-669.
20. Giles, J., J. Shaw, C. Piper, I. Wong-Baeza, K. McHugh, A. Ridley, D. Li, I. Lenart, A. N. Antoniou, K. DiGleria, et al. 2012. HLA-B27 homodimers and free H chains are stronger ligands for leukocyte Ig-like receptor B2 than classical HLA class I. J. Immunol. 188: 6184-6193.
21. Peh, C. A., S. R. Burrows, M. Barnden, R. Khanna, P. Cresswell, D. J. Moss, and J. McCluskey. 1998. HLA-B27-restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I peptide loading. Immunity 8: 531-542.
22. Bird, L. A., C. A. Peh, S. Kollnberger, T. Elliott, A. J. McMichael, and P. Bowness. 2003. Lymphoblastoid cells express HLA-B27 homodimers both intracellularly and at the cell surface following endosomal recycling. Eur. J. Immunol. 33: 748-759.
23. Perosa, F., G. Luccarelli, M. Prete, E. Favoino, S. Ferrone, and F. Dammacco. 2003. Beta 2-microglobulin-free HLA class I heavy chain epitope mimicry by monoclonal antibody HC-10-specific peptide. J. Immunol. 171: 1918-1926.
24. Seitz, C., B. Uchanska-Ziegler, A. Zank, and A. Ziegler. 1998. The monoclonal antibody HCA2 recognises a broadly shared epitope on selected classical as well as several non-classical HLA class I molecules. Mol. Immunol. 35: 819-827.
25. Vivian, J. P., R. C. Duncan, R. Berry, G. M. O'Connor, H. H. Reid, T. Beddoe, S. Gras, P. M. Saunders, M. A. Olshina, J. M. Widjaja, et al. 2011. Killer cell immunoglobulin-like receptor 3DL1-mediated recognition of human leukocyte antigen B. Nature 479: 401-405.
26. Ugolini, S., C. Arpin, N. Anfossi, T. Walzer, A. Cambiaggi, R. Forster, M. Lipp, R. E. Toes, C. J. Melief, J. Marvel, et al. 2001. Involvement of inhibitory NKRs in the survival of a subset of memory-phenotype CD81 T cells. Nat. Immunol. 2: 430-435.
27. Fauriat, C., S. Andersson, A. T. Björklund, M. Carlsten, M. Schaffer, N. K. Björkström, B. C. Baumann, J. Michaëlsson, H. G. Ljunggren, and K. J. Malmberg. 2008. Estimation of the size of the alloreactive NK cell repertoire: studies in individuals homozygous for the group A KIR haplotype. J. Immunol. 181: 6010-6019.
28. Tsai, W. C., C. J. Chen, J. H. Yen, T. T. Ou, J. J. Tsai, C. S. Liu, and H. W. Liu. 2002. Free HLA class I heavy chain-carrying monocytes - a potential role in the pathogenesis of spondyloarthropathies. J. Rheumatol. 29: 966-972.
29. Raine, T., D. Brown, P. Bowness, J. S. Hill Gaston, A. Moffett, J. Trowsdale, and R. L. Allen. 2006. Consistent patterns of expression of HLA class I free heavy chains in healthy individuals and raised expression in spondyloarthropathy patients point to physiological and pathological roles. Rheumatology 45: 1338-1344.
30. Tanabe, M., M. Sekimata, S. Ferrone, and M. Takiguchi. 1992. Structural and functional analysis of monomorphic determinants recognized by monoclonal antibodies reacting with the HLA class I alpha 3 domain. J. Immunol. 148: 3202-3209.
31. McCutcheon, J. A., K. D. Smith, A. Valenzuela, K. Aalbers, and C. T. Lutz. 1993. HLA-B&z.ast;0702 antibody epitopes are affected indirectly by distant antigen residues. Hum. Immunol. 36: 69-75.
32. Martayan, A., L. Sibilio, E. Tremante, E. Lo Monaco, A. Mulder, D. Fruci, A. Cova, L. Rivoltini, and P. Giacomini. 2009. Class I HLA folding and antigen presentation in beta 2-microglobulin-defective Daudi cells. J. Immunol. 182: 3609-3617.
33. Dangoria, N. S., M. L. DeLay, D. J. Kingsbury, J. P. Mear, B. Uchanska-Ziegler, A. Ziegler, and R. A. Colbert. 2002. HLA-B27 misfolding is associated with aberrant intermolecular disulfide bond formation (dimerization) in the endoplasmic reticulum. J. Biol. Chem. 277: 23459-23468.
34. Lan, C. C., W. C. Tsai, C. S. Wu, C. L. Yu, and H. S. Yu. 2004. Psoriatic patients with arthropathy show significant expression of free HLA class I heavy chains on circulating monocytes: a potential role in the pathogenesis of psoriatic arthropathy. Br. J. Dermatol. 151: 24-31.
35. Fu, L., B. Hazes, and D. N. Burshtyn. 2011. The first Ig domain of KIR3DL1 contacts MHC class I at a secondary site. J. Immunol. 187: 1816-1825.