HLA-B27 and psoriatic disease: A modern view of an old relationship

Rheumatology (United Kingdom)

Volumn 55, Issue 2, 2015, Pages 221-229

  Queiro, Rubén ^a   Morante, Isla ^a   Cabezas, Iván ^a   Acasuso, Belén ^a  

^a HOSPITAL UNIVERSITARIO CENTRAL DE ASTURIAS   (Spain)

Author keywords

Genetic epidemiology; HLA B27; HLA Cw6; Psoriasis; Psoriatic arthritis; Psoriatic disease aetiology

Indexed keywords

BIOLOGICAL MARKER; HLA B27 ANTIGEN;

DISEASE COURSE; HUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PSORIASIS; PSORIATIC ARTHRITIS; REVIEW;

EID: 84961912393     PISSN: 14620324     EISSN: 14620332     Source Type: Journal    
DOI: 10.1093/rheumatology/kev296     Document Type: Review

References (79)

1. Nestle FO, Kaplan DH, Barker J. Psoriasis. N Engl J Med 2009;361:496-509.
2. Lowes MA, Bowcock AM, Krueger JG. Pathogenesis and therapy of psoriasis. Nature 2007;445:866-73.
3. Nograles KE, Brasington RD, Bowcock AM. New insights into the pathogenesis and genetics of psoriatic arthritis. Nat Clin Pract Rheumatol 2009;5:83-91.
4. Hüffmeier U, Lascorz J, Becker T et al. Characterisation of psoriasis susceptibility locus 6 (PSORS6) in patients with early onset psoriasis and evidence for interaction with PSORS1. J Med Genet 2009;46:736-44.
5. Nair RP, Duffin KC, Helms C et al. Genome-wide scan reveals association of psoriasis with IL-23 and NF-kB pathways. Nat Genet 2009;41:199-204.
6. Elder JT. Genome-wide association scan yields new insights into the immunopathogenesis of psoriasis. Genes Immun 2009;10:201-9.
7. Feng BJ, Sun LD, Soltani-Arabshahi R et al. Multiple loci within the major histocompatibility complex confer risk of psoriasis. PLoS Genet 2009;5:e1000606.
8. Henseler T, Christophers E. Psoriasis of early and late onset: characterization of two types of psoriasis vulgaris. J Am Acad Dermatol 1985;13:450-6.
9. Nair RP, Stuart PE, Nistor I et al. Sequence and haplotype analysis supports HLA-C as the psoriasis susceptibility 1 gene. Am J Hum Genet 2006;78:827-51.
10. Castelino M, Barton A. Genetic susceptibility factors for psoriatic arthritis. Curr Opin Rheumatol 2010;22:152-6.
11. Enerbäck C, Martinsson T, Inerot A et al. Evidence that HLA-Cw6 determines early onset of psoriasis, obtained using sequence-specific primers (PCR-SSP). Acta Derm Venereol 1997;77:273-6.
12. Juliá A, Tortosa R, Hernanz JM et al. Risk variants for psoriasis vulgaris in a large case-control collection and association with clinical subphenotypes. Hum Mol Genet 2012;21:4549-57.
13. Moll JM, Wright V. Familial occurrence of psoriatic arthritis. Ann Rheum Dis 1973;32:181-201.
14. Gladman DD, Farewell VT, Pellett F, Schentag C, Rahman P. HLA is a candidate region for psoriatic arthritis: evidence for excessive HLA sharing in sibling pairs. Hum Immunol 2003;64:887-9.
15. Armstrong RD, Panayi GS, Welsh KI. Histocompatibility antigens in psoriasis, psoriatic arthropathy, and ankylosing spondylitis. Ann Rheum Dis 1983;42:142-6.
16. Gladman DD, Cheung C, Ng CM, Wade JA. HLA-C locus alleles in patients with psoriatic arthritis (PsA). Hum Immunol 1999;60:259-61.
17. Queiro R, Torre JC, González S, López-Larrea C, Tinturé T, López-Lagunas I. HLA antigens may influence the age of onset of psoriasis and psoriatic arthritis. J Rheumatol 2003;30:505-7.
18. McHugh NJ, Laurent MR, Treadwell BL, Tweed JM, Dagger J. Psoriatic arthritis: clinical subgroups and histocompatibility antigens. Ann Rheum Dis 1987;46:184-8.
19. López-Larrea C, Torre Alonso JC, Rodriguez Perez A, Coto E. HLA antigens in psoriatic arthritis subtypes of a Spanish population. Ann Rheum Dis 1990;49:318-9.
20. Gladman DD, Anhorn KA, Schachter RK, Mervart H. HLA antigens in psoriatic arthritis. J Rheumatol 1986;13:586-92.
21. Jenisch S, Westphal E, Nair RP et al. Linkage disequilibrium analysis of familial psoriasis: identification of multiple disease-associated MHC haplotypes. Tissue Antigens 1999;53:135-46.
22. Marsal S, Armadans-Gil L, Martínez M, Gallardo D, Ribera A, Lience E. Clinical, radiographic and HLA associations as markers for different patterns of psoriatic arthritis. Rheumatology 1999;38:332-7.
23. Rahman P, Elder JT. Genetic epidemiology of psoriasis and psoriatic arthritis. Ann Rheum Dis 2005;64(Suppl 2):ii37-9.
24. Salvarani C, Macchioni PL, Zizzi F et al. Clinical subgroups and HLA antigens in Italian patients with psoriatic arthritis. Clin Exp Rheumatol 1989;7:391-6.
25. Korendowych E, Dixey J, Cox B, Jones S, McHugh N. The Influence of the HLA-DRB1 rheumatoid arthritis shared epitope on the clinical characteristics and radiological outcome of psoriatic arthritis. J Rheumatol 2003;30:96-101.
26. Queiro-Silva R, Torre-Alonso JC, Tinturé-Eguren T, López-Lagunas I. The effect of HLA-DR antigens on the susceptibility to, and clinical expression of psoriatic arthritis. Scand J Rheumatol 2004;33:318-22.
27. Gonzalez S, Martinez-Borra J, Torre-Alonso JC et al. The MICA-A9 triplet repeat polymorphism in the transmembrane region confers additional susceptibility to the development of psoriatic arthritis and is independent of the association of Cw*0602 in psoriasis. Arthritis Rheum 1999;42:1010-6.
28. Gonzalez S, Martinez-Borra J, Lopez-Vazquez A et al. MICA rather than MICB, TNFA, or HLA-DRB1 is associated with susceptibility to psoriatic arthritis. J Rheumatol 2002;29:973-8.
29. Pollock R, Chandran V, Barrett J et al. Differential major histocompatibility complex class I chain-related A allele associations with skin and joint manifestations of psoriatic disease. Tissue Antigens 2011;77:554-61.
30. Alenius GM, Jidell E, Nordmark L, RantapääDahlqvist S. Disease manifestations and HLA antigens in psoriatic arthritis in northern Sweden. Clin Rheumatol 2002;21:357-62.
31. Chandran V, Tolusso DC, Cook RJ, Gladman DD. Risk factors for axial inflammatory arthritis in patients with psoriatic arthritis. J Rheumatol 2010;37:809-15.
32. Elkayam O, Segal R, Caspi D. Human leukocyte antigen distribution in Israeli patients with psoriatic arthritis. Rheumatol Int 2004;24:93-7.
33. Liao HT, Lin KC, Chang YT et al. Human leukocyte antigen and clinical and demographic characteristics in psoriatic arthritis and psoriasis in Chinese patients. J Rheumatol 2008;35:891-5.
34. Eastmond CJ. Psoriatic arthritis. Genetics and HLA antigens. Baillieres Clin Rheumatol 1994;8:263-76.
35. Queiro R, Tejón P, Alonso S, Coto P. Age at disease onset:a key factor for understanding psoriatic disease. Rheumatology 2014;53:1178-85.
36. McHugh K, Bowness P. The link between HLA-B27 and SpA-new ideas on an old problem. Rheumatology 2012;51:1529-39.
37. Robinson PC, Brown MA. The genetics of ankylosing spondylitis and axial spondyloarthritis. Rheum Dis Clin N Am 2012;38:539-53.
38. Colbert RA, Tran TM, Layh-Schmitt G. HLA-B27 misfolding and ankylosing spondylitis. Mol Immunol 2014;57:44-51.
39. Hermann E, Yu DT, Meyerzum Buschenfelde KH, Fleischer B. HLA-B27-restricted CD8 T cells derived from synovial fluids of patients with reactive arthritis and ankylosing spondylitis. Lancet 1993;342:646-50.
40. May E, Dorris ML, Satumtira N et al. CD8ab T cells are not essential to the pathogenesis of arthritis or colitis in HLAB27 transgenic rats. J Immunol 2003;170:1099-105.
41. Khare SD, Hansen J, Luthra HS, David CS. HLA-B27 heavy chains contribute to spontaneous inflammatory disease in B27/human b2-microglobulin (b2m) double transgenic mice with disrupted mouse b2m. J Clin Invest 1996;98:2746-55.
42. Tran TM, Dorris ML, Satumtira N et al. Additional human b2-microglobulin curbs HLA-B27 misfolding and promotes arthritis and spondylitis without colitis in male HLA-B27-transgenic rats. Arthritis Rheum 2006;54:1317-27.
43. Appel H, Maier R, Bleil J et al. In situ analysis of interleukin-23 and interleukin-12 positive cells in the spine of patients with ankylosing spondylitis. Arthritis Rheum 2013;65:1522-9.
44. Sherlock J, Joyce-Shaikh B, Turner SP et al. IL-23 induces spondylarthropathy by acting on ROR-gt+ CD3+CD4_CD8_ entheseal resident T cells. Nat Med 2012;18:1069-76.
45. Ciccia F, Accardo-Palumbo A, Rizzo A et al. Evidence that autophagy, but not the unfolded protein response, regulates the expression of IL-23 in the gut of patients with ankylosing spondylitis and subclinical gut inflammation. Ann Rheum Dis 2014;73:1566-74.
46. Neerinckx B, Carter S, Lories R. IL-23 expression and activation of autophagy in synovium and PBMCs of HLA-B27 positive patients with ankylosing spondylitis. Response to: 'Evidence that autophagy, but not the unfolded protein response, regulates the expression of IL-23 in the gut of patients with ankylosing spondylitis and subclinical gut inflammation' by Ciccia et al. Ann Rheum Dis 2014;73:e68.
47. Schatteman L, Mielants H, Veys EM et al. Gut inflammation in psoriatic arthritis: a prospective ileocolonoscopic study. J Rheumatol 1995;22:680-3.
48. Díaz-Peña R, Vidal-Castiñeira JR, Mulero J et al. Activating killer immunoglobulin-like receptors genes are associated with increased susceptibility to ankylosing spondylitis. Clin Exp Immunol 2015;180:201-6.
49. Bird LA, Peh CA, Kollnberger S et al. Lymphoblastoid cells express HLA-B27 homodimers both intracellularly and at the cell surface following endosomal recycling. Eur J Immunol 2003;33:748-59.
50. Lanier LL. Follow the leader: NK cell receptors for classical and non classical MHC class I. Cell 1998;92:705-7.
51. Chan AT, Kollnberger SD, Wedderburn LR, Bowness P. Expansion and enhanced survival of natural killer cells expressing the killer immunoglobulin-like receptor KIR3DL2 in spondylarthritis. Arthritis Rheum 2005;52:3586-95.
52. Bowness P, Ridley A, Shaw J et al. Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J Immunol 2011;186:2672-80.
53. York IA, Chang SC, Saric T et al. The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8_9 residues. Nat Immunol 2002;3:1177-84.
54. Evans DM, Spencer CC, Pointon JJ et al. Interaction between ERAP1 and HLA-B27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility. Nat Genet 2011;43:761-7.
55. Strange A, Capon F, Spencer CC et al. A genome-wide association study identifies new psoriasis susceptibility loci and an interaction between HLA-C and ERAP1. Nat Genet 2010;42:985-90.
56. Jadon D, Tillet W, Wallis D et al. Exploring ankylosing spondylitis-associated ERAP1, IL23R and IL12B gene polymorphisms in subphenotypes of psoriatic arthritis. Rheumatology 2013;52:261-6.
57. Brewerton DA, Hart FD, Nicholls A et al. Ankylosing spondylitis and HL-A 27. Lancet 1973;1:904-7.
58. Schlosstein L, Terasaki PI, Bluestone R, Pearson CM. High association of an HL-A antigen, W27, with ankylosing spondylitis. N Engl J Med 1973;288:704-6.
59. Brewerton DA, Caffrey M, Nicholls A, Walters D, James DC. HL-A 27 and arthropathies associated with ulcerative colitis and psoriasis. Lancet 1974;1:956-8.
60. Haroon M, Fitzgerald O, Winchester R. Epidemiology, genetics and management of psoriatic arthritis 2013:focus on developments of who develops the disease, its clinical features, and emerging treatment options. Psoriasis Targets Therapy 2013;3:11-23.
61. Chandran V, Bull SB, Pellett FJ et al. Human leukocyte antigen alleles and susceptibility to psoriatic arthritis. Hum Immunol 2013;74:1333-8.
62. Eder L, Chandran V, Pellet F et al. Human leucocyte antigen risk alleles for psoriatic arthritis among patients with psoriasis. Ann Rheum Dis 2012;71:50-5.
63. Eder L, Chandran V, Pellett F et al. Differential human leucocyte allele association between psoriasis and psoriatic arthritis: a family-based association study. Ann Rheum Dis 2012;71:1361-5.
64. Winchester R, Minevich G, Steshenko V et al. HLA associations reveal genetic heterogeneity in psoriatic arthritis and in the psoriasis phenotype. Arthritis Rheum 2012;64:1134-44.
65. Chandran V. Genetic determinants of psoriatic arthritis. PhD thesis, Institute of Medical Sciences, University of Toronto, Toronto, ON, Canada, 2013.
66. Gladman DD, Farewell VT. The role of HLA antigens as indicators of disease progression in psoriatic arthritis. Multivariate relative risk model. Arthritis Rheum 1995;38:845-50.
67. Queiro R, Sarasqueta C, Belzunegui J et al. Psoriatic spondyloarthropathy: a comparative study between HLAB27 positive and HLA-B27 negative disease. Semin Arthritis Rheum 2002;31:413-8.
68. Haroon M, Winchester R, Giles JT, Heffernan E, FitzGerald O. Certain class I HLA alleles and haplotypes implicated in susceptibility play a role in determining specific features of the psoriatic arthritis phenotype. Ann Rheum Dis 2014 Sep 26. pii: annrheumdis-2014-205461. doi: 10.1136/ annrheumdis-2014-205461 [Epub ahead of print].
69. Queiro R, Sarasqueta C, Torre JC, Tinturé T, López-Lagunas I. Spectrum of psoriatic spondyloarthropathy in a cohort of 100 Spanish patients. Ann Rheum Dis 2002;61:857-8.
70. Queiro R, Gonzalez S, Lopez-Larrea C et al. HLA-C locus alleles may modulate the clinical expression of psoriatic arthritis. Arthritis Res Ther 2006;8:R185.
71. Queiro R, Alperi M, Lopez A et al. Clinical expression, but not disease outcome, may vary according to age at disease onset in psoriatic spondylitis. Joint Bone Spine 2008;75:544-7.
72. Queiro R, Tejón P, Alonso S et al. The region centromeric to HLA-C is a key region for understanding the phenotypic variability of psoriatic arthritis. ISRN Dermatol 2014;2014:570178.
73. Marzo-Ortega H, McGonagle D, O'Connor P et al. Baseline and 1-year magnetic resonance imaging of the sacroiliac joint and lumbar spine in very early inflammatory back pain. Relationship between symptoms, HLA-B27 and disease extent and persistence. Ann Rheum Dis 2009;68:1721-7.
74. Bennett AN, McGonagle D, O'Connor P et al. Severity of baseline magnetic resonance imaging-evident sacroiliitis and HLA-B27 status in early inflammatory back pain predict radiographically evident ankylosing spondylitis at eight years. Arthritis Rheum 2008;58:3413-8.
75. Castillo-Gallego C, Aydin SZ, Emery P, McGonagle DG, Marzo-Ortega H. Magnetic resonance imaging assessment of axial psoriatic arthritis: extent of disease relates to HLA-B27. Arthritis Rheum 2013;65:2274-8.
76. Wilson FC, Icen M, Crowson CS et al. Time trends in epidemiology and characteristics of psoriatic arthritis over 3 decades: a population-based study. J Rheumatol 2009;36:361-7.
77. Queiro R, Tejón P, Coto P et al. Clinical differences between men and women with psoriatic arthritis: relevance of the analysis of genes and polymorphisms in the major histocompatibility complex region and of the age at onset of psoriasis. Clin Dev Immunol 2013;2013:482691.
78. Queiro R, Sarasqueta C, Torre JC, Tinturé T, López-Lagunas I. Comparative analysis of psoriatic spondyloarthropathy between men and women. Rheumatol Int 2001;21:66-8.
79. Queiro R, Alonso S, Alperi M et al. Stratification by age of onset with 30 years as age limit is an effective means of identifying PSORS1-associated psoriasis in patients with psoriatic arthritis. Joint Bone Spine 2011;78:581-3.