Endoplasmic reticulum aminopeptidase-1 alleles associated with increased risk of ankylosing spondylitis reduce HLA-B27 mediated presentation of multiple antigens

References

• Brown, M. A. 2008. Breakthroughs in genetic studies of ankylosing spondylitis. Rheumatology (Oxford). 47:132–137
   PubMedGoogle Scholar
• Evans, D. M., C. C. Spencer, J. J. Pointon, et al. 2011. Interaction between ERAP1 and HLA-B27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility. Nat. Genet. 43:761–767
   PubMed Web of Science ®Google Scholar
• Reveille, J. D., A. M. Sims, P. Danoy, et al. 2010. Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci. Nat. Genet. 42:123–127
   PubMed Web of Science ®Google Scholar
• Lin, Z., J. X. Bei, M. Shen, et al. 2012. A genome-wide association study in Han Chinese identifies new susceptibility loci for ankylosing spondylitis. Nat. Genet. 44:73–77
   Web of Science ®Google Scholar
• Burton, P. R., D. G. Clayton, L. R. Cardon, et al. ( Wellcome Trust Case Control Consortium). 2007. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature. 447:661–678
   PubMed Web of Science ®Google Scholar
• Tsui, F. W., N. Haroon, J. D. Reveille, et al. 2010. Association of an ERAP1 ERAP2 haplotype with familial ankylosing spondylitis. Ann. Rheum. Dis. 69:733–736
   PubMed Web of Science ®Google Scholar
• Haroon, N., F. W. Tsui, B. Uchanska-Ziegler, et al. 2012. Endoplasmic reticulum aminopeptidase 1 (ERAP1) exhibits functionally significant interaction with HLA-B27 and relates to subtype specificity in ankylosing spondylitis. Ann. Rheum Dis. 71:589–595
   PubMed Web of Science ®Google Scholar
• Rock, K. L., C. Gramm, L. Rothstein, et al. 1994. Inhibitors of the proteasome block the degradation of most cell proteins and the generation of peptides presented on MHC class I molecules. Cell 78:761–771
   PubMed Web of Science ®Google Scholar
• Rock, K. L., I. A. York, A. L. Goldberg. 2004. Post-proteasomal antigen processing for major histocompatibility complex class I presentation. Nature Immunol. 5:670–677
   PubMedGoogle Scholar
• Chang, S. C., F. Momburg, N. Bhutani, A. L. Goldberg. 2005. The ER aminopeptidase, ERAP1, trims precursors to lengths of MHC class I peptides by a “molecular ruler” mechanism. Proc. Natl. Acad. Sci. U. S. A. 102:17107–17112
   PubMed Web of Science ®Google Scholar
• Evnouchidou, I., F. Momburg, A. Papakyriakou, et al. 2008. The internal sequence of the peptide-substrate determines its N-terminus trimming by ERAP1. PLoS One. 3:e3658
   PubMedGoogle Scholar
• Nguyen, T. T., S. C. Chang, I. Evnouchidou, et al. 2011. Structural basis for antigenic peptide precursor processing by the endoplasmic reticulum aminopeptidase ERAP1. Nat. Struct. Mol. Biol. 18:604–613
   PubMed Web of Science ®Google Scholar
• van Endert, P. M., R. Tampe, T. H. Meyer, et al. 1994. A sequential model for peptide binding and transport by the transporters associated with antigen processing. Immunity. 1:491–500
   PubMed Web of Science ®Google Scholar
• Blanchard, N., F. Gonzalez, M. Schaeffer, et al. 2008. Immunodominant, protective response to the parasite Toxoplasma gondii requires antigen processing in the endoplasmic reticulum. Nature Immunol. 9:937–944
   PubMed Web of Science ®Google Scholar
• Mehta, A. M., E. S. Jordanova, W. E. Corver, et al. 2009. Single nucleotide polymorphisms in antigen processing machinery component ERAP1 significantly associate with clinical outcome in cervical carcinoma. Genes Chromosomes Cancer. 48:410–418
   PubMed Web of Science ®Google Scholar
• Khare, S. D., H. S. Luthra, C. S. David. 1995. Spontaneous inflammatory arthritis in HLA-B27 transgenic mice lacking beta 2-microglobulin: a model of human spondyloarthropathies. J. Exp. Med. 182:1153–1158
   PubMed Web of Science ®Google Scholar
• Breban, M., J. L. Fernandez-Sueiro, J. A. Richardson, et al. 1996. T cells, but not thymic exposure to HLA-B27, are required for the inflammatory disease of HLA-B27 transgenic rats. J. Immunol. 156:794–803
   Google Scholar
• May, E., M. L. Dorris, N. Satumtira, et al. 2003. CD8 alpha beta T cells are not essential to the pathogenesis of arthritis or colitis in HLA-B27 transgenic rats. J. Immunol. 170:1099–1105
   PubMed Web of Science ®Google Scholar
• Bowness, P., A. Ridley, J. Shaw, et al. 2011. Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J. Immunol. 186:2672–2680
   Google Scholar
• Evnouchidou, I., R. P. Kamal, S. S. Seregin, et al. 2011. 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. 186:1909–1913
   PubMed Web of Science ®Google Scholar
• Kochan, G., T. Krojer, D. Harvey, et al. 2011. Crystal structures of the endoplasmic reticulum aminopeptidase-1 (ERAP1) reveal the molecular basis for N-terminal peptide trimming. Proc. Natl. Acad. Sci. U. S. A. 108:7745–7750
   PubMed Web of Science ®Google Scholar
• Reeves, E., C. J. Edwards, T. Elliott, E. James. 2013. Naturally Occurring ERAP1 haplotypes encode functionally distinct alleles with fine substrate specificity. J. Immunol. 191:35–43
   PubMed Web of Science ®Google Scholar
• Stratikos, E., L. J. Stern. 2013. Antigenic peptide trimming by ER aminopeptidases – Insights from structural studies. Mol. Immunol. 55:212–219
   PubMedGoogle Scholar
• Saric, T., S. C. Chang, A. Hattori, et al. 2002. An IFN-gamma-induced aminopeptidase in the ER, ERAP1, trims precursors to MHC class I-presented peptides. Nature Immunol. 3:1169–1176
   PubMed Web of Science ®Google Scholar
• York, I. A., S. C. Chang, T. Saric, et al. 2002. The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8–9 residues. Nature Immunol. 3:1177–1184
   PubMed Web of Science ®Google Scholar
• Boyle, L. H., J. C. Goodall, S. S. Opat, J. S. Gaston. 2001. The recognition of HLA-B27 by human CD4(+) T lymphocytes. J. Immunol. 167:2619–2624
   Google Scholar
• Perosa, F., G. Luccarelli, M. Prete, et al. 2003. Beta 2-microglobulin-free HLA class I heavy chain epitope mimicry by monoclonal antibody HC-10-specific peptide. J. Immunol. 171:1918–1926
   PubMed Web of Science ®Google Scholar
• Georgiadou, D., A. Hearn, I. Evnouchidou, et al. 2010. Placental leucine aminopeptidase efficiently generates mature antigenic peptides in vitro but in patterns distinct from endoplasmic reticulum aminopeptidase 1. J. Immunol. 185:1584–1592
   Google Scholar
• Zervoudi, E., A. Papakyriakou, D. Georgiadou, et al. 2011. Probing the S1 specificity pocket of the aminopeptidases that generate antigenic peptides. Biochem. J. 435:411–420
   PubMedGoogle Scholar
• Seregin, S. S., Y. A. Aldhamen, D. M. Appledorn, et al. 2011. TRIF Is a critical negative regulator of TLR agonist mediated activation of dendritic cells in vivo. PLoS One. 6:e22064
   Google Scholar
• Parameswaran, N., C. S. Pao, K. S. Leonhard, et al. 2006. Arrestin-2 and G protein-coupled receptor kinase 5 interact with NFkappaB1 p105 and negatively regulate lipopolysaccharide-stimulated ERK1/2 activation in macrophages. J. Biol. Chem. 281:34159–34170
   PubMed Web of Science ®Google Scholar
• Seregin, S. S., D. M. Appledorn, A. J. McBride, et al. 2009. Transient pretreatment with glucocorticoid ablates innate toxicity of systemically delivered adenoviral vectors without reducing efficacy. Mol. Ther. 17:685–696
   PubMed Web of Science ®Google Scholar
• Burton, P. R., D. G. Clayton, L. R. Cardon, et al. 2007. Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat. Genet. 39:1329–1337
   PubMed Web of Science ®Google Scholar
• Choi, C. B., T. H. Kim, J. B. Jun, et al. 2010. ARTS1 polymorphisms are associated with ankylosing spondylitis in Koreans. Ann. Rheum. Dis. 69:582–584
   PubMed Web of Science ®Google Scholar
• Harvey, D., J. J. Pointon, D. M. Evans, et al. 2009. Investigating the genetic association between ERAP1 and ankylosing spondylitis. Hum. Mol. Genet. 18:4204–4212
   PubMed Web of Science ®Google Scholar
• Maksymowych, W. P., R. D. Inman, D. D. Gladman, et al. 2009. Association of a specific ERAP1/ARTS1 haplotype with disease susceptibility in ankylosing spondylitis. Arthritis Rheum. 60:1317–1323
   PubMed Web of Science ®Google Scholar
• Chen, R., L. Yao, T. Meng, W. Xu. 2012. The association between seven ERAP1 polymorphisms and ankylosing spondylitis susceptibility: a meta-analysis involving 8,530 cases and 12,449 controls. Rheumatol Int. 32:909–914
   PubMed Web of Science ®Google Scholar
• Lee, Y. H., S. J. Choi, J. D. Ji, G. G. Song. 2011. Associations between ERAP1 polymorphisms and ankylosing spondylitis susceptibility: a meta-analysis. Inflamm Res. 60:999–1003
   PubMed Web of Science ®Google Scholar
• York, I. A., E. P. Grant, A. M. Dahl, K. L. Rock. 2005. A mutant cell with a novel defect in MHC class I quality control. J. Immunol. 174:6839–6846
   Google Scholar
• Hill, A., P. Jugovic, I. York, et al. 1995. Herpes simplex virus turns off the TAP to evade host immunity. Nature. 375:411–415
   PubMed Web of Science ®Google Scholar
• Atagunduz, P., H. Appel, W. Kuon, et al. 2005. HLA-B27-restricted CD8+ T cell response to cartilage-derived self peptides in ankylosing spondylitis. Arthritis Rheum. 52:892–901
   PubMed Web of Science ®Google Scholar
• Fiorillo, M. T., M. Maragno, R. Butler, et al. 2000. CD8(+) T-cell autoreactivity to an HLA-B27-restricted self-epitope correlates with ankylosing spondylitis. J. Clin. Invest. 106:47–53
   PubMedGoogle Scholar
• Liu, Y., L. Jiang, Q. Cai, et al. 2010. Predominant association of HLA-B*2704 with ankylosing spondylitis in Chinese Han patients. Tissue Antigens. 75:61–64
   Google Scholar
• Lopez de Castro, J. A., I. Alvarez, M. Marcilla, et al. 2004. HLA-B27: a registry of constitutive peptide ligands. Tissue Antigens. 63:424–445
   Google Scholar
• Scofield, R. H., B. Kurien, T. Gross, et al. 1995. HLA-B27 binding of peptide from its own sequence and similar peptides from bacteria: implications for spondyloarthropathies. Lancet. 345:1542–1544
   PubMed Web of Science ®Google Scholar
• Appel, H., W. Kuon, M. Kuhne, et al. 2004. Use of HLA-B27 tetramers to identify low-frequency antigen-specific T cells in Chlamydia-triggered reactive arthritis. Arthritis Res. Ther. 6:R521–534
   Google Scholar
• Brooks, J. M., R. J. Murray, W. A. Thomas, et al. 1993. Different HLA-B27 subtypes present the same immunodominant Epstein–Barr virus peptide. J. Exp Med. 178:879–887
   Google Scholar
• Cheuk, E., J. W. Chamberlain. 2005. Strong memory CD8+ T cell responses against immunodominant and three new subdominant HLA-B27-restricted influenza A CTL epitopes following secondary infection of HLA-B27 transgenic mice. Cell Immunol. 234:110–123
   PubMed Web of Science ®Google Scholar
• Kuon, W., H. G. Holzhutter, H. Appel, et al. 2001. Identification of HLA-B27-restricted peptides from the Chlamydia trachomatis proteome with possible relevance to HLA-B27-associated diseases. J. Immunol. 167:4738–4746
   PubMed Web of Science ®Google Scholar
• Kuon, W., M. Kuhne, D. H. Busch, et al. 2004. Identification of novel human aggrecan T cell epitopes in HLA-B27 transgenic mice associated with spondyloarthropathy. J. Immunol. 173:4859–4866
   PubMed Web of Science ®Google Scholar
• Liu, J., P. Zhu, J. Peng, et al. 2007. Identification of disease-associated proteins by proteomic approach in ankylosing spondylitis. Biochem. Biophys. Res. Commun. 357:531–536
   Google Scholar
• Ugrinovic, S., A. Mertz, P. Wu, et al. 1997. A single nonamer from the Yersinia 60-kDa heat shock protein is the target of HLA-B27-restricted CTL response in Yersinia-induced reactive arthritis. J. Immunol. 159:5715–5723
   PubMed Web of Science ®Google Scholar
• Garcia-Medel, N., A. Sanz-Bravo, D. Van Nguyen, et al. 2012. Functional interaction of the ankylosing spondylitis associated endoplasmic reticulum aminopeptidase 1 polymorphism and HLA-B27 in vivo. Mol. Cell. Proteomics. 11:1416–1429
   PubMed Web of Science ®Google Scholar
• Cui, X., F. Hawari, S. Alsaaty, et al. 2002. Identification of ARTS-1 as a novel TNFR1-binding protein that promotes TNFR1 ectodomain shedding. J. Clin. Invest. 110:515–526
   PubMed Web of Science ®Google Scholar
• Jensen, P. E. 2007. Recent advances in antigen processing and presentation. Nature Immunol. 8:1041–1048
   PubMed Web of Science ®Google Scholar
• Saveanu, L., O. Carroll, V. Lindo, et al. 2005. Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nature Immunol. 6:689–697
   PubMed Web of Science ®Google Scholar
• Rufer, E., R. M. Leonhardt, M. R. Knittler. 2007. Molecular architecture of the TAP-associated MHC class I peptide-loading complex. J. Immunol. 179:5717–5727
   Google Scholar