ERAP1 genetic variations associated with HLA-B27 interaction and disease severity of syndesmophytes formation in Taiwanese ankylosing spondylitis

Arthritis Research and Therapy

Volumn 14, Issue 3, 2012, Pages

  Wang, Chin Man ^a   Ho, Huei Huang ^a   Chang, Su Wei ^b   Wu, Yeong Jian Jan ^a   Lin, Jing Chi ^a   Chang, Pi Yueh ^b   Wu, Jianming ^c   Chen, Ji Yih ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HLA B27 ANTIGEN; AMINOPEPTIDASE; ERAP1 PROTEIN, HUMAN;

ADOLESCENT; ADULT; ANKYLOSING SPONDYLITIS; ARTICLE; CHILD; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE SEVERITY; ERAP1 GENE; FEMALE; GENE EXPRESSION; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC RISK; GENETIC VARIATION; GENOTYPE; HAPLOTYPE; HUMAN; MAJOR CLINICAL STUDY; MALE; OSTEOPHYTE; PATHOGENESIS; SINGLE NUCLEOTIDE POLYMORPHISM; SYNDESMOPHYTE; TAIWANESE; ASIAN; GENETIC PREDISPOSITION; GENETICS; MIDDLE AGED; ONSET AGE; PATHOLOGY; TAIWAN;

ADOLESCENT; ADULT; AGE OF ONSET; AMINOPEPTIDASES; ASIAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HLA-B27 ANTIGEN; HUMANS; MALE; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; SPONDYLITIS, ANKYLOSING; TAIWAN; YOUNG ADULT;

EID: 84861403821     PISSN: 14786354     EISSN: 14786362     Source Type: Journal    
DOI: 10.1186/ar3855     Document Type: Article

References (55)

1. van der Linden SM, van der Heijde D, Maksymowych WP: Ankylosing spondylitis. In Kelley's Textbook of Rheumatology. Volume II. 8 edition. Edited by: Firestein GS, Budd RC, Harris ED Jr, McInnes IB, Ruddy S, Sergent JS. Philadelphia: Saunders-Elsevier; 2008:1169-1190
2. Braun J, Sieper J: Ankylosing spondylitis. Lancet 2007, 369:1379-1390
3. Lories RJ, Luyten FP, de Vlam K: Progress in spondylarthritis. Mechanisms of new bone formation in spondyloarthritis. Arthritis Res Ther 2009, 11:221
4. Tam LS, Gu J, Yu D: Pathogenesis of ankylosing spondylitis. Nat Rev Rheumatol 2010, 6:399-405
5. Brown MA: Genetics and the pathogenesis of ankylosing spondylitis. Curr Opin Rheumatol 2009, 21:318-323
6. Said-Nahal R, Miceli-Richard C, Berthelot JM, Duché A, Dernis-Labous E, Le Blévec G, Saraux A, Perdriger A, Guis S, Claudepierre P, Sibilia J, Amor B, Dougados M, Breban M: The familial form of spondylarthropathy: a clinical study of 115 multiplex families. Arthritis Rheum 2000, 43:1356-1365
7. Brown MA, Kennedy LG, MacGregor AJ, Darke C, Duncan E, Shatford JL, Taylor A, Calin A, Wordsworth P: Susceptibility to ankylosing spondylitis in twins: the role of genes, HLA, and the environment. Arthritis Rheum 1997, 40:1823-1828
8. Reveille JD: The genetic basis of spondyloarthritis. Ann Rheum Dis 2011, 70(Suppl 1):44-50
9. Wellcome Trust CaseControl Consortium; Australo-Anglo-American Spondylitis Consortium (TASC), Burton PR, Clayton DG, Cardon LR, Craddock N, Deloukas P, Duncanson A, Kwiatkowski DP, McCarthy MI, Ouwehand WH, Samani NJ, Todd JA, Donnelly P, Barrett JC, Davison D, Easton D, Evans DM, Leung HT, Marchini JL, Morris AP, Spencer CC, Tobin MD, Attwood AP, Boorman JP, Cant B, Everson U, Hussey JM, Jolley JD, Knight AS, Koch K, et al: Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat Genet 2007, 39:1329-1337
10. Australo-Anglo-American Spondyloarthritis Consortium(TASC), Reveille JD, Sims AM, Danoy P, Evans DM, Leo P, Pointon JJ, Jin R, Zhou X, Bradbury LA, Appleton LH, Davis JC, Diekman L, Doan T, Dowling A, Duan R, Duncan EL, Farrar C, Hadler J, Harvey D, Karaderi T, Mogg R, Pomeroy E, Pryce K, Taylor J, Savage L, Deloukas P, Kumanduri V, Peltonen L, Ring SM, Whittaker P, et al: Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci. Nat Genet 2010, 42:123-127
11. Harvey D, Pointon JJ, Evans DM, Karaderi T, Farrar C, Appleton LH, Sturrock RD, Stone MA, Oppermann U, Brown MA, Wordsworth BP: Investigating the genetic association between ERAP1 and ankylosing spondylitis. Hum Mol Genet 2009, 18:4204-4212
12. Davidson SI, Wu X, Liu Y, Wei M, Danoy PA, Thomas G, Cai Q, Sun L, Duncan E, Wang N, Yu Q, Xu A, Fu Y, Brown MA, Xu H: Association of ERAP1, but not IL23R, with ankylosing spondylitis in a Han Chinese population. Arthritis Rheum 2009, 60:3263-3268
13. Saric T, Chang SC, Hattori AI, York IA, Markant SK, Rock KL, Tsujimoto M, Goldberg AL: An IFN gamma induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nat Immunol 2002, 3:1169-1176
14. York IA, Chang SC, Saric t, Keys A, Favreau JM, Goldberg AL, Rock KL: The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat Immunol 2002, 3:1177-1184
15. Hilton C, Kisselev AF, Rock KL, Goldberg AL: 26S proteasomes and immunoproteasomes produce mainly N-extended versions of an antigenic peptide. EMBO J 2001, 20:2357-2366
16. Rock KL, York IA, Goldberg AL: Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nat Immunol 2004, 5:670-677
17. Serwold T, Gonzalez F, Kim J, Jacob R, Shastri N: ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 2002, 419:480-483
18. Cui X, Hawari F, Alsaaty S, Lawrence M, Combs CA, Geng W, Rouhani FN, Miskinis D, Levine SJ: Identification of ARTS-1 as a novel TNFR1-binding protein that promotes TNFR1 ectodomain shedding. J Clin Invest 2002, 110:515-526
19. Cui X, Rouhani FN, Hawari F, Levine SJ: An aminopeptidase, ARTS-1, is required for interleukin-6 receptor shedding. J Biol Chem 2003, 278:28677-28685
20. Cui X, Rouhani FN, Hawari F, Levine SJ: Shedding of the type II IL-1 decoy receptor requires a multifunctional aminopeptidase, aminopeptidase regulator of TNF receptor type 1 shedding. J Immunol 2003, 171:6814-6819
21. Tsui FW, Haroon N, Reveille JD, Rahman P, Chiu B, Tsui HW, Inman RD: Association of an ERAP1 ERAP2 haplotype with familial ankylosing spondylitis. Ann Rheum Dis 2010, 69:733-736
22. Choi CB, Kim TH, Jun JB, Lee HS, Shim SC, Lee B, Pope A, Uddin M, Rahman P, Inman RD: ARTS1 polymorphisms are associated with ankylosing spondylitis in Koreans. Ann Rheum Dis 2010, 69:582-584
23. Davidson SI, Liu Y, Danoy PA, Wu X, Thomas GP, Jiang L, Sun L, Wang N, Han J, Han H, Australo-Anglo-American Spondyloarthritis Consortium, Visscher PM, Brown MA, Xu H: Association of STAT3 and TNFRSF1A with ankylosing spondylitis in Han Chinese. Ann Rheum Dis 2011, 70:289-292
24. Li C, Lin Z, Xie Y, Guo Z, Huang J, Wei Q, Li QX, Wang X, Cao S, Liao Z, Xu M, Shen Y, Gu J: ERAP1 is associated with ankylosing spondylitis in Han Chinese. J Rheumatol 2011, 38:317-321
25. Bang SY, Kim TH, Lee B, Kwon E, Choi SH, Lee KS, Shim SC, Pope A, Rahman P, Reveille JD, Inman RD: Genetic studies of ankylosing spondylitis in Koreans confirm associations with ERAP1 and 2p15 reported in white patients. J Rheumatol 2011, 38:322-324
26. Pazár B, Sáfrány E, Gergely P, Szántó S, Szekanecz Z, Poór G: Association of ARTS1 gene polymorphisms with ankylosing spondylitis in the Hungarian population: the rs27044 variant is associated with HLAB* 2705 subtype in Hungarian patients with ankylosing spondylitis. J Rheumatol 2010, 37:379-384
27. van der Linden S, Valkenburg HA, Cats A: Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 1984, 27:361-368
28. Chen JY, Wang CM, Ma CC, Luo SF, Edberg JC, Kimberly RP, Wu J: Association of a transmembrane polymorphism of Fcgamma receptor IIb (FCGR2B) with systemic lupus erythematosus in Taiwanese patients. Arthritis Rheum 2006, 54:3908-3917
29. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC: PLINK: a toolset for wholegenome association and population-based linkage analysis. Am J Hum Genet 2007, 81:559-575
30. Chang SC, Momburg F, Bhutani N, Goldberg AL: The ER aminopeptidase, ERAP1, trims precursors to lengths of MHC class I peptides by a "molecular ruler" mechanism. Proc Natl Acad Sci USA 2005, 102:17107-17112
31. York IA, Brehm MA, Zendzian S, Towne CF, Rock KL: Endoplasmic reticulum aminopeptidase 1 (ERAP1) trims MHC class I-presented peptides in vivo and plays an important role in immunodominance. Proc Natl Acad Sci USA 2006, 103:9202-9207
32. Blanchard N, Kanaseki T, Escobar H, Delebecque F, Nagarajan NA, Reyes-Vargas E, Crockett DK, Raulet DH, Delgado JC, Shastri N: Endoplasmic reticulum aminopeptidase associated with antigen processing defines the composition and structure of MHC class I peptide repertoire in normal and virus-infected cells. J Immunol 2010, 184:3033-3042
33. Hammer GE, Gonzalez F, Champsaur M, Cado D, Shastri N: The aminopeptidase ERAAP shapes the peptide repertoire displayed by major histocompatibility complex class I molecules. Nat Immunol 2006, 7:103-112
34. Hammer GE, Gonzalez F, James E, Nolla H, Shastri N: In the absence of aminopeptidase ERAAP, MHC class I molecules present many unstable and highly immunogenic peptides. Nat Immunol 2006, 8:101-108
35. Yan J, Parekh VV, Mendez-Fernandez Y, Olivares-Villagomez D, Dragovic S, Hill T, Roopenian DC, Joyce S, Van Kaer L: In vivo role of ER-associated peptidase activity in tailoring peptides for presentation by MHC class Ia and class Ib molecules. J Exp Med 2006, 203:647-665
36. Firat E, Saveanu L, Aichele P, Staeheli P, Huai J, Gaedicke S, Nil A, Besin G, Kanzler B, van Endert P, Niedermann G: The role of endoplasmic reticulum-associated aminopeptidase 1 in immunity to infection and in cross-presentation. J Immunol 2007, 178:2241-2248
37. Campbell EC, Fettke F, Bhat S, Morley KD, Powis SJ: Expression of MHC class I dimers and ERAP1 in an ankylosing spondylitis patient cohort. Immunology 2011, 133:379-385
38. Goto Y, Ogawa K, Hattori A, Tsujimoto M: Secretion of endoplasmic reticulum aminopeptidase 1 is involved in the activation of macrophages induced by lipopolysaccharide and interferon gamma. J Biol Chem 2011, 286:21906-21914
39. Colbert RA, DeLay ML, Klenk EI, Layh-Schmitt G: From HLA-B27 to spondyloarthritis: a journey through the ER. Immunol Rev 2010, 233:181-202
40. Haroon N, Inman RD: Endoplasmic reticulum aminopeptidases: biology and pathogenic potential. Nat Rev Rheumatol 2010, 6:461-467
41. Kanaseki T, Blanchard N, Hammer GE, Gonzalez F Shastri N: ERAAP synergizes with MHC class I molecules to make the final cut in the antigenic peptide precursors in the endoplasmic reticulum. Immunity 2006, 25:795-806
42. Evans DM, Spencer CC, Pointon JJ, Su Z, Harvey D, Kochan G, Oppermann U, Dilthey A, Pirinen M, Stone MA, Appleton L, Moutsianas L, Leslie S, Wordsworth T, Kenna TJ, Karaderi T, Thomas GP, Ward MM, Weisman MH, Farrar C, Bradbury LA, Danoy P, Inman RD, Maksymowych W, Gladman D, Rahman P, Spondyloarthritis Research Consortium of Canada (SPARCC), Morgan A, Marzo-Ortega H, Bowness P, 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, 43:761-767
43. Baraliakos X, Listing J, Rudwaleit M, Haibel H, Brandt J, Sieper J, Braun J: Progression of radiographic damage in patients with ankylosing spondylitis: defining the central role of syndesmophytes. Ann Rheum Dis 2007, 66:910-915
44. Baraliakos X, Listing J, Rudwaleit M, Sieper J, Braun J: The relationship between inflammation and new bone formation in patients with ankylosing spondylitis. Arthritis Res Ther 2008, 10:R104
45. Schett G: Joint remodelling in inflammatory disease. Ann Rheum Dis 2007, 66(Suppl 3):42-44
46. Haroon N, Tsui FW, Chiu B, Tsui HW, Inman RD: Serum cytokine receptors in ankylosing spondylitis: relationship to inflammatory markers and endoplasmic reticulum aminopeptidase polymorphisms. J Rheumatol 2010, 37:1907-1910
47. Lories RJ, Derese I, Luyten FP: Inhibition of osteoclasts does not prevent joint ankylosis in a mouse model of spondyloarthritis. Rheumatology 2008, 47:605-608
48. Lories RJ, Derese I, de Bari C, Luyten FP: Evidence for uncoupling of inflammation and joint remodeling in a mouse model of spondylarthritis. Arthritis Rheum 2007, 56:489-497
49. van der Heijde D, Salonen D, Weissman BN, Landewé R, Maksymowych WP, Kupper H, Ballal S, Gibson E, Wong R: Assessment of radiographic progression in the spines of patients with ankylosing spondylitis treated with adalimumab for up to 2 years. Arthritis Res Ther 2009, 11:R127
50. van der Heijde D, Landewé R, Einstein S, Ory P, Vosse D, Ni L, Lin SL, Tsuji W, Davis JC Jr: Radiographic progression of ankylosing spondylitis after up to two years of treatment with etanercept. Arthritis Rheum 2008, 58:1324-1331
51. van der Heijde D, Landewé R, Baraliakos X, Houben H, van Tubergen A, Williamson P, Xu W, Baker D, Goldstein N, Braun J: Radiographic findings following two years of infliximab therapy in patients with ankylosing spondylitis. Ankylosing Spondylitis Study for the Evaluation of Recombinant Infliximab Therapy Study Group. Arthritis Rheum 2008, 58:3063-3070
52. Evnouchidou I, Kamal RP, Seregin SS, Goto Y, Tsujimoto M, Hattori A, Voulgari PV, Drosos AA, Amalfitano A, York IA, Stratikos E: Coding single nucleotide polymorphisms of endoplasmic reticulum aminopeptidase 1 can affect antigenic peptide generation in vitro by influencing basic enzymatic properties of the enzyme. J Immunol 2011, 186:1909-1913
53. Kochan G, Krojer T, Harvey D, Fischer R, Chen L, Vollmar M, von Delft F, Kavanagh KL, Brown MA, Bowness P, Wordsworth P, Kessler BM, Oppermann U: Crystal structures of the endoplasmic reticulum aminopeptidase-1 (ERAP1) reveal the molecular basis for N-terminal peptide trimming. Proc Natl Acad Sci USA 2011, 108:7745-7750
54. Haroon N, Maksymowych W, Rahman P, Tsui F, O'Shea F, Inman R: Radiographic severity in ankylosing spondylitis is associated with polymorphism in large multifunctional peptidase 2 (LMP2) in the Spondyloarthritis Research Consortium of Canada cohort. Arthritis Rheum 2012, 64:1119-1126
55. Haroon N, Tsui FW, Uchanska-Ziegler B, Ziegler A, Inman RD: Endoplasmic reticulum aminopeptidase 1 (ERAP1) exhibits functionally significant interaction with HLA-B27 and relates to subtype specificity in ankylosing spondylitis. Ann Rheum Dis 2012, 71:589-595