HLA-B27 and the pathogenesis of spondyloarthropathies

Immunology Letters

Volumn 108, Issue 1, 2007, Pages 27-33

  López de Castro, José A ^a  

^a CSIC   (Spain)

Author keywords

HLA B27; Human; MHC; Spondyloarthropathies

Indexed keywords

CELL RECEPTOR; HLA B27 ANTIGEN; HOMODIMER; MAJOR HISTOCOMPATIBILITY ANTIGEN;

ADAPTIVE IMMUNITY; ANKYLOSING SPONDYLITIS; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; AUTOIMMUNITY; CROSS REACTION; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; HEAVY CHAIN; HUMAN; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; LIGAND BINDING; MOLECULAR GENETICS; MOLECULAR RECOGNITION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FOLDING; REVIEW; SPONDYLOARTHROPATHY;

ANIMALS; DIMERIZATION; HLA-B27 ANTIGEN; HUMANS; PROTEIN FOLDING; SIGNAL TRANSDUCTION; SPONDYLARTHROPATHIES;

EID: 33845643625     PISSN: 01652478     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.imlet.2006.10.004     Document Type: Review

References (71)

1. Brewerton D.A., Hart F.D., Nicholls A., Caffrey M., James D.C., and Sturrock R.D. Ankylosing spondylitis and HL-A 27. Lancet 1 (1973) 904-907
2. Schlosstein L., Terasaki P.I., Bluestone R., and Pearson C.M. High association of an HL-A antigen, W27, with ankylosing spondylitis. N Engl J Med 288 (1973) 704-706
3. Brewerton D.A., Caffrey M., Nicholls A., Walters D., Oates J.K., and James D.C. Reiter's disease and HL-A 27. Lancet 2 (1973) 996-998
4. Benjamin R., and Parham P. Guilt by association: HLA-B27 and ankylosing spondylitis. Immunol Today 11 (1990) 137-142
5. Hermann E., Yu D.T., Meyer zum Buschenfelde K.H., and Fleischer B. HLA-B27-restricted CD8 T cells derived from synovial fluids of patients with reactive arthritis and ankylosing spondylitis. Lancet 342 (1993) 646-650
6. May E., Dulphy N., Frauendorf E., Duchmann R., Bowness P., López de Castro J.A., et al. Conserved TCR β chain usage in reactive arthritis; evidence for selection by a putative HLA-B27-associated autoantigen. Tissue Antigens 60 (2002) 299-308
7. Atagunduz P., Appel H., Kuon W., Wu P., Thiel A., Kloetzel P.M., et al. HLA-B27-restricted CD8+ T cell response to cartilage-derived self peptides in ankylosing spondylitis. Arthritis Rheum 52 (2005) 892-901
8. Jardetzky T.S., Lane W.S., Robinson R.A., Madden D.R., and Wiley D.C. Identification of self peptides bound to purified HLA-B27. Nature 353 (1991) 326-329
9. Madden D.R., Gorga J.C., Strominger J.L., and Wiley D.C. The structure of HLA-B27 reveals nonamer self-peptides bound in an extended conformation. Nature 353 (1991) 321-325
10. Madden D.R., Gorga J.C., Strominger J.L., and Wiley D.C. The three-dimensional structure of HLA-B27 at 2.1. A resolution suggests a general mechanism for tight peptide binding to MHC. Cell 70 (1992) 1035-1048
11. Garrett T.P., Saper M.A., Bjorkman P.J., Strominger J.L., and Wiley D.C. Specificity pockets for the side chains of peptide antigens in HLA-Aw68. Nature 342 (1989) 692-696
12. Lopez-Larrea C., Sujirachato K., Mehra N.K., Chiewsilp P., Isarangkura D., Kanga U., et al. HLA-B27 subtypes in Asian patients with ankylosing spondylitis. Evidence for new associations. Tissue Antigens 45 (1995) 169-176
13. Ren E.C., Koh W.H., Sim D., Boey M.L., Wee G.B., and Chan S.H. Possible protective role of HLA-B*2706 for ankylosing spondylitis. Tissue Antigens 49 (1997) 67-69
14. Nasution A.R., Mardjuadi A., Kunmartini S., Suryadhana N.G., Setyohadi B., Sudarsono D., et al. HLA-B27 subtypes positively and negatively associated with spondyloarthropathy. J Rheumatol 24 (1997) 1111-1114
15. D'Amato M., Fiorillo M.T., Carcassi C., Mathieu A., Zuccarelli A., Bitti P.P., et al. Relevance of residue 116 of HLA-B27 in determining susceptibility to ankylosing spondylitis. Eur J Immunol 25 (1995) 3199-3201
16. Paladini F., Taccari E., Fiorillo M.T., Cauli A., Passiu G., Mathieu A., et al. Distribution of HLA-B27 subtypes in Sardinia and continental Italy and their association with spondylarthropathies. Arthritis Rheum 52 (2005) 3319-3321
17. Del Porto P., D'Amato M., Fiorillo M.T., Tuosto L., Piccolella E., and Sorrentino R. Identification of a novel HLA-B27 subtype by restriction analysis of a cytotoxic γδ T cell clone. J Immunol 153 (1994) 3093-3100
18. Fiorillo M.T., Meadows L., D'Amato M., Shabanowitz J., Hunt D.F., Apella E., et al. Susceptibility to ankylosing spondylitis correlates with the C-terminal residue of peptides presented by various HLA-B27 subtypes. Eur J Immunol 27 (1997) 368-373
19. Garcia F., Marina A., and López de Castro J.A. Lack of carboxyl-terminal tyrosine distinguishes the B*2706-bound peptide repertoire from those of B*2704 and other HLA-B27 subtypes associated to ankylosing spondylitis. Tissue Antigens 49 (1997) 215-221
20. Ramos M., Paradela A., Vazquez M., Marina A., Vazquez J., and López de Castro J.A. Differential association of HLA-B*2705 and B*2709 to ankylosing spondylitis correlates with limited peptide subsets but not with altered cell surface stability. J Biol Chem 277 (2002) 28749-28756
21. Sesma L., Montserrat V., Lamas J.R., Marina A., Vazquez J., and López de Castro J.A. The peptide repertoires of HLA-B27 subtypes differentially associated to spondyloarthropathy (B*2704 and B*2706) differ by specific changes at three anchor positions. J Biol Chem 277 (2002) 16744-16749
22. Tieng V., Dulphy N., Boisgérault F., Tamouza R., Charron D., and Toubert A. HLA-B*2707 peptide motif: Tyr C-terminal anchor is not shared by all disease-associated subtypes. Immunogenetics 47 (1997) 103-105
23. Varnavidou-Nicolaidou A., Karpasitou K., Georgiou D., Stylianou G., Kokkofitou A., Michalis C., et al. HLA-B27 in the Greek Cypriot population: Distribution of subtypes in patients with ankylosing spondylitis and other HLA-B27-related diseases. The possible protective role of B*2707. Hum Immunol 65 (2004) 1451-1454
24. Gomez P., Montserrat V., Marcilla M., Paradela A., and de Castro J.A. B*2707 differs in peptide specificity from B*2705 and B*2704 as much as from HLA-B27 subtypes not associated to spondyloarthritis. Eur J Immunol 36 (2006) 1867-1881
25. Lopez-Larrea C., Mijiyawa M., Gonzalez S., Fernandez-Morera J.L., Blanco-Gelaz M.A., Martinez-Borra J., et al. Ankylosing spondylitis is associated with HLA-B*1403 in a West African population. Arthritis Rheum 46 (2002) 2968-2971
26. Merino E., Montserrat V., Paradela A., and López de Castro J.A. Two HLA-B14 subtypes (B*1402 and B*1403) differentially associated with ankylosing spondylitis differ substantially in peptide specificity, but have limited peptide and T-cell epitope sharing with HLA-B27. J Biol Chem 280 (2005) 35868-35880
27. Scofield R.H., Warren W.L., Koelsch G., and Harley J.B. A hypothesis for the HLA-B27 immune dysregulation in spondyloarthropathy: contributions from enteric organisms, B27 structure, peptides bound by B27, and convergent evolution. Proc Natl Acad Sci USA 90 (1993) 9330-9334
28. Scofield R.H., Kurien B., Gross T., Warren W.L., and Harley J.B. HLA-B27 binding of peptide from its own sequence and similar peptides from bacteria: implications for spondyloarthropathies. Lancet 345 (1995) 1542-1544
29. Frauendorf E., von Goessel H., May E., and Marker-Hermann E. HLA-B27-restricted T cells from patients with ankylosing spondylitis recognize peptides from B*2705 that are similar to bacteria-derived peptides. Clin Exp Immunol 134 (2003) 351-359
30. Alvarez I., Sesma L., Marcilla M., Ramos M., Marti M., Camafeita E., et al. Identification of novel HLA-B27 ligands derived from polymorphic regions of its own or other class I molecules based on direct generation by 20S proteasome. J Biol Chem 276 (2001) 32729-32737
31. Ramos M., Alvarez I., Sesma L., Logean A., Rognan D., and López de Castro J.A. Molecular mimicry of an HLA-B27-derived ligand of arthritis-linked subtypes with chlamydial proteins. J Biol Chem 277 (2002) 37573-37581
32. + T-cell autoreactivity to an HLA-B27-restricted self-epitope correlates with ankylosing spondylitis. J Clin Invest 106 (2000) 47-53
33. Hülsmeyer M., Fiorillo M.T., Bettosini F., Sorrentino R., Saenger W., Ziegler A., et al. Dual, HLA-B27 subtype-dependent conformation of a self-peptide. J Exp Med 199 (2004) 271-281
34. Ruckert C., Fiorillo M.T., Loll B., Moretti R., Biesiadka J., Saenger W., et al. Conformational dimorphism of self-peptides and molecular mimicry in a disease-associated HLA-B27 subtype. J Biol Chem 281 (2005) 2306-2316
35. Fiorillo M.T., Ruckert C., Hulsmeyer M., Sorrentino R., Saenger W., Ziegler A., et al. Allele-dependent similarity between viral and self-peptide presentation by HLA-B27 subtypes. J Biol Chem 280 (2005) 2962-2971
36. Kuon W., Holzhutter H.G., Appel H., Grolms M., Kollnberger S., Traeder A., et al. Identification of HLA-B27-restricted peptides from the Chlamydia trachomatis proteome with possible relevance to HLA-B27-associated diseases. J Immunol 167 (2001) 4738-4746
37. Hammer R.E., Maika S.D., Richardson J.A., Tang J.P., and Taurog J.D. Spontaneous inflammatory disease in transgenic rats expressing HLA-B27 and human β2m: an animal model of HLA-B27-associated human disorders. Cell 63 (1990) 1099-1112
38. Breban M., Fernandez-Sueiro J.L., Richardson J.A., Hadavand R.R., Maika S.D., Hammer R.E., et al. T cells, but not thymic exposure to HLA-B27, are required for the inflammatory disease of HLA-B27 transgenic rats. J Immunol 156 (1996) 794-803
39. May E., Dorris M.L., Satumtira N., Iqbal I., Rehman M.I., Lightfoot E., et al. CD8αβ T cells are not essential to the pathogenesis of arthritis or colitis in HLA-B27 transgenic rats. J Immunol 170 (2003) 1099-1105
40. Mear J.P., Schreiber K.L., Münz C., Zhu X., Stevanovic S., Rammensee H.G., et al. Misfolding of HLA-B27 as a result of its B pocket suggests a novel mechanism for its role in susceptibility to spondyloarthropathies. J Immunol 163 (1999) 6665-6670
41. Allen R.L., O'Callaghan C.A., McMichael A.J., and Bowness P. Cutting edge: HLA-B27 can form a novel β2-microglobulin-free heavy chain homodimer structure. J Immunol 162 (1999) 5045-5048
42. Edwards J.C., Bowness P., and Archer J.R. Jekyll and Hyde: the transformation of HLA-B27. Immunol Today 21 (2000) 256-260
43. Dangoria N.S., DeLay M.L., Kingsbury D.J., Mear J.P., Uchanska-Ziegler B., Ziegler A., et al. HLA-B27 misfolding is associated with aberrant intermolecular disulfide bond formation (dimerization) in the endoplasmic reticulum. J Biol Chem 277 (2002) 23459-23468
44. Antoniou A.N., Ford S., Taurog J.D., Butcher G.W., and Powis S.J. Formation of HLA-B27 homodimers and their relationship to assembly kinetics. J Biol Chem 279 (2004) 8895-8902
45. Bird L.A., Peh C.A., Kollnberger S., Elliott T., McMichael A.J., and Bowness P. Lymphoblastoid cells express HLA-B27 homodimers both intracellularly and at the cell surface following endosomal recycling. Eur J Immunol 33 (2003) 748-759
46. Allen R.L., Raine T., Haude A., Trowsdale J., and Wilson M.J. Leukocyte receptor complex-encoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J Immunol 167 (2001) 5543-5547
47. Kollnberger S., Bird L., Sun M.Y., Retiere C., Braud V.M., McMichael A., et al. Cell-surface expression and immune receptor recognition of HLA-B27 homodimers. Arthritis Rheum 46 (2002) 2972-2982
48. Colbert R.A. HLA-B27 misfolding: a solution to the spondyloarthropathy conundrum?. Mol Med Today 6 (2000) 224-230
49. Schroder M., and Kaufman R.J. ER stress and the unfolded protein response. Mutat Res 569 (2005) 29-63
50. Pahl H.L., and Baeuerle P.A. The ER-overload response: activation of NF-κB. Trends Biochem Sci 22 (1997) 63-67
51. Turner M.J., Sowders D.P., DeLay M.L., Mohapatra R., Bai S., Smith J.A., et al. HLA-B27 misfolding in transgenic rats is associated with activation of the unfolded protein response. J Immunol 175 (2005) 2438-2448
52. Tran T.M., Dorris M.L., Satumtira N., Richardson J.A., Hammer R.E., Shang J., et al. Additional human β2-microglobulin curbs HLA-B27 misfolding and promotes arthrits and spondylitis without colitis in male HLA-B27 transgenic rats. Arthritis Rheum 54 (2006) 1317-1327
53. Bowness P. HLA B27 in health and disease: a double-edged sword?. Rheumatology (Oxford) 41 (2002) 857-868
54. Chan A.T., Kollnberger S.D., Wedderburn L.R., and Bowness P. Expansion and enhanced survival of natural killer cells expressing the killer immunoglobulin-like receptor KIR3DL2 in spondylarthritis. Arthritis Rheum 52 (2005) 3586-3595
55. Allen R.L., and Trowsdale J. Recognition of classical and heavy chain forms of HLA-B27 by leukocyte receptors. Curr Mol Med 4 (2004) 59-65
56. Lopez-Larrea C., Blanco-Gelaz M.A., Torre-Alonso J.C., Armas J.B., Suarez-Alvarez B., Pruneda L., et al. Contribution of KIR3DL1/3DS1 to ankylosing spondylitis in human leukocyte antigen-B27 Caucasian populations. Arthritis Res Ther 8 (2006) R101
57. Raine T., Brown D., Bowness P., Hill Gaston J.S., Moffett A., Trowsdale J., et al. 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 (Oxford) (2006)
58. Boyle L.H., Goodall J.C., and Gaston J.S. The recognition of abnormal forms of HLA-B27 by CD4+ T cells. Curr Mol Med 4 (2004) 51-58
59. + T cell responses in TCR transgenic mice. J Immunol 172 (2004) 155-161
60. + T lymphocytes. J Immunol 167 (2001) 2619-2624
61. + T cells. Immunology 12 (2004) 54-63
62. Momburg F., and Tan P. Tapasin-the keystone of the loading complex optimizing peptide binding by MHC class I molecules in the endoplasmic reticulum. Mol Immunol 39 (2002) 217-233
63. Williams A.P., Peh C.A., Purcell A.W., McCluskey J., and Elliott T. Optimization of the MHC class I peptide cargo is dependent on tapasin. Immunity 16 (2002) 509-520
64. Peh C.A., Burrows S.R., Barnden M., Khanna R., Cresswell P., Moss D.J., et al. HLA-B27-restricted antigen presentation in the absence of tapasin reveals polymorphism in mechanisms of HLA class I peptide loading. Immunity 8 (1998) 531-542
65. Purcell A.W., Gorman J.J., Garcia-Peydro M., Paradela A., Burrows S.R., Talbo G.H., et al. Quantitative and qualitative influences of tapasin on the class I peptide repertoire. J Immunol 166 (2001) 1016-1027
66. Goodall J.C., Ellis L., and Hill Gaston J.S. Spondylarthritis-associated and non-spondylarthritis-associated B27 subtypes differ in their dependence upon tapasin for surface expression and their incorporation into the peptide loading complex. Arthritis Rheum 54 (2006) 138-147
67. Montserrat V., Galocha B., Marcilla M., Vázquez M., and López de Castro J. HLA-B*2704, an allotype associated with ankylosing spondylitis, is critically dependent on TAP and relatively independent of tapasin and immunoproteasome for maturation, surface expression and T-cell recognition: relationship to B*2705 and B*2706. J Immunol 177 (2006) 7015-7023
68. Laitio P., Virtala M., Salmi M., Pelliniemi L.J., Yu D.T., and Granfors K. HLA-B27 modulates intracellular survival of Salmonella enteritidis in human monocytic cells. Eur J Immunol 27 (1997) 1331-1338
69. Virtala M., Kirveskari J., and Granfors K. HLA-B27 modulates the survival of Salmonella enteritidis in transfected L cells, possibly by impaired nitric oxide production. Infect Immun 10 (1997) 4236-4242
70. Penttinen M.A., Heiskanen K.M., Mohapatra R., DeLay M.L., Colbert R.A., Sistonen L., et al. Enhanced intracellular replication of Salmonella enteritidis in HLA-B27-expressing human monocytic cells: dependency on glutamic acid at position 45 in the B pocket of HLA-B27. Arthritis Rheum 50 (2004) 2255-2263
71. Penttinen M.A., Ekman P., and Granfors K. Non-antigen presenting effects of HLA-B27. Curr Mol Med 4 (2004) 41-49