Functionally distinct ERAP1 allotype combinations distinguish individuals with ankylosing spondylitis

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 49, 2014, Pages 17594-17599

  Reeves, Emma ^a   Colebatch Bourn, Alexandra ^a   Elliott, Tim ^a,b   Edwards, Christopher J ^a,b   James, Edward ^a,b  

^a UNIVERSITY HOSPITAL SOUTHAMPTON NHS FOUNDATION TRUST   (United Kingdom)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Ankylosing spondylitis; Antigen presentation; Antigen processing; ERAP1; HLA B27

Indexed keywords

AMINOPEPTIDASE; ENDOPLASMIC RETICULUM AMINOPEPTIDASE 1; HLA B27 ANTIGEN; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; EPITOPE; ERAP1 PROTEIN, HUMAN; HLA-B*27:05 ANTIGEN;

ALLOTYPE; ANKYLOSING SPONDYLITIS; ANTIGEN PRESENTATION; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENZYME SPECIFICITY; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; PHENOTYPE; PHYLOGENY; PROTEIN EXPRESSION; PROTEIN FUNCTION; SINGLE NUCLEOTIDE POLYMORPHISM; T LYMPHOCYTE; ADULT; AGED; CELL MEMBRANE; COHORT ANALYSIS; FEMALE; GENETIC POLYMORPHISM; GENETICS; HEK293 CELL LINE; IMMUNOLOGY; INFLAMMATION; MALE; METABOLISM; MIDDLE AGED; MOLECULAR GENETICS;

MURINAE;

ADULT; AGED; AMINOPEPTIDASES; ANTIGEN PRESENTATION; BIOMARKERS; CELL MEMBRANE; COHORT STUDIES; EPITOPES; FEMALE; HEK293 CELLS; HLA-B27 ANTIGEN; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; POLYMORPHISM, SINGLE NUCLEOTIDE; SPONDYLITIS, ANKYLOSING;

EID: 84916890237     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1408882111     Document Type: Article

References (31)

1. Burton PR, et al.; Wellcome Trust Case Control Consortium; Australo-Anglo-American Spondylitis Consortium (TASC); Biologics in RA Genetics and Genomics Study Syndicate (BRAGGS) Steering Committee; Breast Cancer Susceptibility Collaboration (UK) (2007) Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat Genet 39(11):1329-1337.
2. Evans DM, et al.; Spondyloarthritis Research Consortium of Canada (SPARCC); Australo-Anglo-American Spondyloarthritis Consortium (TASC); Wellcome Trust Case Control Consortium 2 (WTCCC2) (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(8):761-767.
3. Harvey D, et al. (2009) Investigating the genetic association between ERAP1 and ankylosing spondylitis. Hum Mol Genet 18(21):4204-4212.
4. Serwold T, Gonzalez F, Kim J, Jacob R, Shastri N (2002) ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 419(6906):480-483.
5. York IA, et al. (2002) The ER aminopeptidase ERAP1 enhances or limits antigen presentation by trimming epitopes to 8-9 residues. Nat Immunol 3(12):1177-1184.
6. Hammer GE, Gonzalez F, Champsaur M, Cado D, Shastri N (2006) The aminopeptidase ERAAP shapes the peptide repertoire displayed by major histocompatibility complex class I molecules. Nat Immunol 7(1):103-112.
7. Yan J, et al. (2006) In vivo role of ER-associated peptidase activity in tailoring peptides for presentation by MHC class Ia and class Ib molecules. J Exp Med 203(3):647-659.
8. York IA, Brehm MA, Zendzian S, Towne CF, Rock KL (2006) 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 103(24):9202-9207.
9. Keidel S, Chen L, Pointon J, Wordsworth P (2013) ERAP1 and ankylosing spondylitis. Curr Opin Immunol 25(1):97-102.
10. Choi CB, et al. (2010) ARTS1 polymorphisms are associated with ankylosing spondylitis in Koreans. Ann Rheum Dis 69(3):582-584.
11. Kadi A, et al. (2013) Investigating the genetic association between ERAP1 and spondyloarthritis. Ann Rheum Dis 72(4):608-613.
12. Maksymowych WP, et al. (2009) Association of a specific ERAP1/ARTS1 haplotype with disease susceptibility in ankylosing spondylitis. Arthritis Rheum 60(5):1317-1323.
13. Evnouchidou I, et al. (2011) Cutting Edge: 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(4):1909-1913.
14. Kochan G, 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 USA 108(19):7745-7750.
15. Reeves E, Edwards CJ, Elliott T, James E (2013) Naturally occurring ERAP1 haplotypes encode functionally distinct alleles with fine substrate specificity. J Immunol 191(1):35-43.
16. García-Medel N, et al. (2012) Functional interaction of the ankylosing spondylitis-associated endoplasmic reticulum aminopeptidase 1 polymorphism and HLA-B27 in vivo. Mol Cell Proteomics 11(11):1416-1429.
17. Martín-Esteban A, Gómez-Molina P, Sanz-Bravo A, López de Castro JA (2014) Combined effects of ankylosing spondylitis-associated ERAP1 polymorphisms outside the catalytic and peptide-binding sites on the processing of natural HLA-B27 ligands. J Biol Chem 289(7):3978-3990.
18. Cong L, et al. (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339(6121):819-823.
19. Saveanu L, et al. (2005) Concerted peptide trimming by human ERAP1 and ERAP2 aminopeptidase complexes in the endoplasmic reticulum. Nat Immunol 6(7):689-697.
20. Nguyen TT, et al. (2011) Structural basis for antigenic peptide precursor processing by the endoplasmic reticulum aminopeptidase ERAP1. Nat Struct Mol Biol 18(5):604-613.
21. Alvarez-Navarro C, López de Castro JA (2014) ERAP1 structure, function and pathogenetic role in ankylosing spondylitis and other MHC-associated diseases. Mol Immunol 57(1):12-21.
22. Draenert R, et al. (2004) Immune selection for altered antigen processing leads to cytotoxic T lymphocyte escape in chronic HIV-1 infection. J Exp Med 199(7):905-915.
23. Kim S, et al. (2011) Human cytomegalovirus microRNA miR-US4-1 inhibits CD8(+) T cell responses by targeting the aminopeptidase ERAP1. Nat Immunol 12(10):984-991.
24. Kirino Y, et al. (2013) Genome-wide association analysis identifies new susceptibility loci for Behc¸et's disease and epistasis between HLA-B∗51 and ERAP1. Nat Genet 45(2):202-207.
25. Bird LA, et al. (2003) Lymphoblastoid cells express HLA-B27 homodimers both intracellularly and at the cell surface following endosomal recycling. Eur J Immunol 33(3):748-759.
26. McHugh K, et al. (2014) Expression of aberrant HLA-B27 molecules is dependent on B27 dosage and peptide supply. Ann Rheum Dis 73(4):763-770.
27. Turner MJ, et al. (2005) HLA-B27 misfolding in transgenic rats is associated with activation of the unfolded protein response. J Immunol 175(4):2438-2448.
28. Bowness P, et al. (2011) Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J Immunol 186(4):2672-2680.
29. Chen L, et al. (2014) Critical role of endoplasmic reticulum aminopeptidase 1 in determining the length and sequence of peptides bound and presented by HLA-B27. Arthritis Rheum (Munch) 66(2):284-294.
30. Evnouchidou I, et al. (2012) A common single nucleotide polymorphism in endoplasmic reticulum aminopeptidase 2 induces a specificity switch that leads to altered antigen processing. J Immunol 189(5):2383-2392.
31. Tsui FW, et al. (2010) Association of an ERAP1 ERAP2 haplotype with familial ankylosing spondylitis. Ann Rheum Dis 69(4):733-736.