Role of HLA-B27 in the pathogenesis of ankylosing spondylitis (Review)
- Authors:
- Bin Chen
- Jia Li
- Chongru He
- Dahe Li
- Wenwen Tong
- Yuming Zou
- Weidong Xu
-
Affiliations: Department of Joint Surgery and Sports Medicine, Changhai Hospital, The Second Military Medical University, Shanghai 200433, P.R. China - Published online on: February 24, 2017 https://doi.org/10.3892/mmr.2017.6248
- Pages: 1943-1951
-
Copyright: © Chen et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Dougados M and Baeten D: Spondyloarthritis. Lancet. 377:2127–2137. 2011. View Article : Google Scholar : PubMed/NCBI | |
Cho H, Kim T, Kim TH, Lee S and Lee KH: Spinal mobility, vertebral squaring, pulmonary function, pain, fatigue, and quality of life in patients with ankylosing spondylitis. Ann Rehabil Med. 37:675–682. 2013. View Article : Google Scholar : PubMed/NCBI | |
Braun J and Sieper J: Ankylosing spondylitis. Lancet. 369:1379–1390. 2007. View Article : Google Scholar : PubMed/NCBI | |
Végvári A, Szabó Z, Szántó S, Glant TT, Mikecz K and Szekanecz Z: The genetic background of ankylosing spondylitis. Joint Bone Spine. 76:623–628. 2009. View Article : Google Scholar : PubMed/NCBI | |
Brewerton DA, Hart FD, Nicholls A, Caffrey M, James DC and Sturrock RD: Ankylosing spondylitis and HL-A 27. Lancet. 1:904–907. 1973. View Article : Google Scholar : PubMed/NCBI | |
Chatzikyriakidou A, Voulgari PV and Drosos AA: What is the role of HLA-B27 in spondyloarthropathies? Autoimmun Rev. 10:464–468. 2011. View Article : Google Scholar : PubMed/NCBI | |
International Genetics of Ankylosing Spondylitis Consortium (IGAS), ; Cortes A, Hadler J, Pointon JP, Robinson PC, Karaderi T, Leo P, Cremin K, Pryce K, Harris J, et al: Identification of multiple risk variants for ankylosing spondylitis through high-density genotyping of immune-related loci. Nat Genet. 45:730–738. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sheehan NJ: HLA-B27: What's new? Rheumatology (Oxford). 49:621–631. 2010. View Article : Google Scholar : PubMed/NCBI | |
Khan MA: Polymorphism of HLA-B27: 105 subtypes currently known. Curr Rheumatol Rep. 15:3622013. View Article : Google Scholar : PubMed/NCBI | |
Brown MA: Progress in the genetics of ankylosing spondylitis. Brief Funct Genomics. 10:249–257. 2011. View Article : Google Scholar : PubMed/NCBI | |
Warde N: Spondyloarthropathies: HLA-B27 and ERAP1 contribute to ankylosing spondylitis via aberrant peptide processing and presentation. Nat Rev Rheumatol. 7:4982011. View Article : Google Scholar : PubMed/NCBI | |
Evans DM, Spencer CC, Pointon JJ, Su Z, Harvey D, Kochan G, Oppermann U, Dilthey A, Pirinen M, Stone MA, 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. 43:761–767. 2011. View Article : Google Scholar : PubMed/NCBI | |
Nguyen TT, Chang SC, Evnouchidou I, York IA, Zikos C, Rock KL, Goldberg AL, Stratikos E and Stern LJ: Structural basis for antigenic peptide precursor processing by the endoplasmic reticulum aminopeptidase ERAP1. Nat Struct Mol Biol. 18:604–613. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yewdell JW: DRiPs solidify: Progress in understanding endogenous MHC class I antigen processing. Trends Immunol. 32:548–558. 2011. View Article : Google Scholar : PubMed/NCBI | |
Madden DR: The three-dimensional structure of peptide-MHC complexes. Annu Rev Immunol. 13:587–622. 1995. View Article : Google Scholar : PubMed/NCBI | |
Colbert RA, Tran TM and Layh-Schmitt G: HLA-B27 misfolding and ankylosing spondylitis. Mol Immunol. 57:44–51. 2014. View Article : Google Scholar : PubMed/NCBI | |
Lenart I, Guiliano DB, Burn G, Campbell EC, Morley KD, Fussell H, Powis SJ and Antoniou AN: The MHC Class I heavy chain structurally conserved cysteines 101 and 164 participate in HLA-B27 dimer formation. Antioxid Redox Signal. 16:33–43. 2012. View Article : Google Scholar : PubMed/NCBI | |
Alvarez-Navarro C and López de Castro JA: ERAP1 structure, function and pathogenetic role in ankylosing spondylitis and other MHC-associated diseases. Mol Immunol. 57:12–21. 2014. View Article : Google Scholar : PubMed/NCBI | |
Colbert RA: The immunobiology of HLA-B27: Variations on a theme. Curr Mol Med. 4:21–30. 2004. View Article : Google Scholar : PubMed/NCBI | |
Raposo G and Stoorvogel W: Extracellular vesicles: Exosomes, microvesicles, and friends. J Cell Biol. 200:373–383. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lynch S, Santos SG, Campbell EC, Nimmo AM, Botting C, Prescott A, Antoniou AN and Powis SJ: Novel MHC class I structures on exosomes. J Immunol. 183:1884–1891. 2009. View Article : Google Scholar : PubMed/NCBI | |
Lorente E, Infantes S, Abia D, Barnea E, Beer I, García R, Lasala F, Jiménez M, Mir C, Morreale A, et al: A viral, transporter associated with antigen processing (TAP)-independent, high affinity ligand with alternative interactions endogenously presented by the nonclassical human leukocyte antigen E class I molecule. J Biol Chem. 287:34895–34903. 2012. View Article : Google Scholar : PubMed/NCBI | |
Chen B, Li D and Xu W: Association of ankylosing spondylitis with HLA-B27 and ERAP1: Pathogenic role of antigenic peptide. Med Hypotheses. 80:36–38. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lévy F, Burri L, Morel S, Peitrequin AL, Lévy N, Bachi A, Hellman U, Van den Eynde BJ and Servis C: The final N-terminal trimming of a subaminoterminal proline-containing HLA class I-restricted antigenic peptide in the cytosol is mediated by two peptidases. J Immunol. 169:4161–4171. 2002. View Article : Google Scholar : PubMed/NCBI | |
Antoniou AN, Lenart I and Guiliano DB: Pathogenicity of misfolded and dimeric HLA-B27 molecules. Int J Rheumatol. 2011:4868562011. View Article : Google Scholar : PubMed/NCBI | |
Dakwar E, Reddy J, Vale FL and Uribe JS: A review of the pathogenesis of ankylosing spondylitis. Neurosurg Focus. 24:E22008. View Article : Google Scholar : PubMed/NCBI | |
Taurog JD, Dorris ML, Satumtira N, Tran TM, Sharma R, Dressel R, van den Brandt J and Reichardt HM: Spondylarthritis in HLA-B27/human beta2-microglobulin-transgenic rats is not prevented by lack of CD8. Arthritis Rheum. 60:1977–1984. 2009. View Article : Google Scholar : PubMed/NCBI | |
Collins EJ, Garboczi DN and Wiley DC: Three-dimensional structure of a peptide extending from one end of a class I MHC binding site. Nature. 371:626–629. 1994. View Article : Google Scholar : PubMed/NCBI | |
Probst-Kepper M, Hecht HJ, Herrmann H, Janke V, Ocklenburg F, Klempnauer J, van den Eynde BJ and Weiss S: Conformational restraints and flexibility of 14-meric peptides in complex with HLA-B*3501. J Immunol. 173:5610–5616. 2004. View Article : Google Scholar : PubMed/NCBI | |
Green KJ, Miles JJ, Tellam J, van Zuylen WJ, Connolly G and Burrows SR: Potent T cell response to a class I-binding 13-mer viral epitope and the influence of HLA micropolymorphism in controlling epitope length. Eur J Immunol. 34:2510–2519. 2004. View Article : Google Scholar : PubMed/NCBI | |
York IA, Brehm MA, Zendzian S, Towne CF and Rock KL: Endoplasmic reticulum aminopeptidase 1 (ERAP1) trims MHC class I-present edpeptides in vivo and plays an important role in immunodominance. Proc Natl Acad Sci USA. 103:9202–9207. 2006. View Article : Google Scholar : PubMed/NCBI | |
Hammer GE, Gonzalez F, James E, Nolla H and Shastri N: In the absence of aminopeptidase ERAAP, MHC class I molecules present many unstable and highly immunogenic peptides. Nat Immunol. 8:101–108. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lorente E, García R, Mir C, Barriga A, Lemonnier FA, Ramos M and López D: Role of metalloproteases in vaccinia virus epitope processing for transporter associated with antigen processing (TAP)-independent human leukocyte antigen (HLA)-B7 class I antigen presentation. J Biol Chem. 287:9990–10000. 2012. View Article : Google Scholar : PubMed/NCBI | |
Schwarz K, De Giuli R, Schmidtke G, Kostka S, van den Broek M, Kim KB, Crews CM, Kraft R and Groettrup M: The selective proteasome inhibitors lactacystin and epoxomicin can be used to either up- or down-regulate antigen presentation at nontoxic doses. J Immunol. 164:6147–6157. 2000. View Article : Google Scholar : PubMed/NCBI | |
Allen RL and Trowsdale J: Recognition of classical and heavy chain forms of HLA-B27 by leukocyte receptors. Curr Mol Med. 4:59–65. 2004. View Article : Google Scholar : PubMed/NCBI | |
Kollnberger S, Chan A, Sun MY, Chen LY, Wright C, di Gleria K, McMichael A and Bowness P: Interaction of HLA-B27 homodimers with KIR3DL1 and KIR3DL2, unlike HLA-B27 heterotrimers, is independent of the sequence of bound peptide. Eur J Immunol. 37:1313–1322. 2007. View Article : Google Scholar : PubMed/NCBI | |
Allen RL, Raine T, Haude A, Trowsdale J and Wilson MJ: Leukocyte receptor complex-encoded immunomodulatory receptors show differing specificity for alternative HLA-B27 structures. J Immunol. 167:5543–5547. 2001. View Article : Google Scholar : PubMed/NCBI | |
Chan AT, Kollnberger SD, Wedderburn LR and Bowness P: Expansion and enhanced survival of natural killer cells expressing the killer immunoglobulin-like receptor KIR3DL2 in spondylarthritis. Arthritis Rheum. 52:3586–3595. 2005. View Article : Google Scholar : PubMed/NCBI | |
Bowness P, Ridley A, Shaw J, Chan AT, Wong-Baeza I, Fleming M, Cummings F, McMichael A and Kollnberger S: Th17 cells expressing KIR3DL2+ and responsive to HLA-B27 homodimers are increased in ankylosing spondylitis. J Immunol. 186:2672–2680. 2011. View Article : Google Scholar : PubMed/NCBI | |
Giles J, Shaw J, Piper C, Wong-Baeza I, McHugh K, Ridley A, Li D, Lenart I, Antoniou AN, DiGleria K, et al: HLA-B27 homodimers and free H chains are stronger ligands for leukocyte Ig-like receptor B2 than classical HLA class I. J Immunol. 188:6184–6193. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wong-Baeza I, Ridley A, Shaw J, Hatano H, Rysnik O, McHugh K, Piper C, Brackenbridge S, Fernandes R, Chan A, et al: KIR3DL2 binds to HLA-B27 dimers and free H chains more strongly than other HLA class I and promotes the expansion of T cells in ankylosing spondylitis. J Immunol. 190:3216–3224. 2013. View Article : Google Scholar : PubMed/NCBI | |
Dangoria NS, DeLay ML, Kingsbury DJ, Mear JP, Uchanska-Ziegler B, Ziegler A and Colbert RA: HLA-B27 misfolding is associated with aberrant intermolecular disulfide bond formation (dimerization) in the endoplasmic reticulum. J Biol Chem. 277:23459–23468. 2002. View Article : Google Scholar : PubMed/NCBI | |
Campbell EC, Antoniou AN and Powis SJ: The multi-faceted nature of HLA class I dimer molecules. Immunology. 136:380–384. 2012. View Article : Google Scholar : PubMed/NCBI | |
Cauli A, Shaw J, Giles J, Hatano H, Rysnik O, Payeli S, McHugh K, Dessole G, Porru G, Desogus E, et al: The arthritis-associated HLA-B*27:05 allele forms more cell surface B27 dimer and free heavy chain ligands for KIR3DL2 than HLA-B*27:09. Rheumatology (Oxford). 52:1952–1962. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kuśnierczyk P and Majorczyk E: Pas de quatre: An interaction of HLA-B*27:05 and KIR3DL2 homodimers in spondyloarthropathies. Rheumatology (Oxford). 52:1931–1912. 2013. View Article : Google Scholar : PubMed/NCBI | |
Rajagopalan S and Long EO: KIR2DL4 (CD158d): An activation receptor for HLA-G. Front Immunol. 3:2582012. View Article : Google Scholar : PubMed/NCBI | |
Antoniou AN, Ford S, Taurog JD, Butcher GW and Powis SJ: Formation of HLA-B27 homodimers and their relationship to assembly kinetics. J Biol Chem. 279:8895–8902. 2004. View Article : Google Scholar : PubMed/NCBI | |
Colbert RA, DeLay ML, Layh-Schmitt G and Sowders DP: HLA-B27 misfolding and spondyloarthropathies. Prion. 3:15–26. 2009. View Article : Google Scholar : PubMed/NCBI | |
Turner MJ, Sowders DP, DeLay ML, Mohapatra R, Bai S, Smith JA, Brandewie JR, Taurog JD and Colbert RA: HLA-B27 misfolding in transgenic rats is associated with activation of the unfolded protein response. J Immunol. 175:2438–2348. 2005. View Article : Google Scholar : PubMed/NCBI | |
DeLay ML, Turner MJ, Klenk EI, Smith JA, Sowders DP and Colbert RA: HLA-B27 misfolding and the unfolded protein response augment interleukin-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum. 60:2633–2643. 2009. View Article : Google Scholar : PubMed/NCBI | |
Zeng L, Lindstrom MJ and Smith JA: Ankylosing spondylitis macrophage production of higher levels of interleukin-23 in response to lipopolysaccharide without induction of a significant unfolded protein response. Arthritis Rheum. 63:3807–3817. 2011. View Article : Google Scholar : PubMed/NCBI | |
Ciccia F, Accardo-Palumbo A, Rizzo A, Guggino G, Raimondo S, Giardina A, Cannizzaro A, Colbert RA, Alessandro R and Triolo G: 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. 73:1566–1574. 2014. View Article : Google Scholar : PubMed/NCBI | |
Neerinckx B, Carter S and 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. Ann Rheum Dis. 73:e682014. View Article : Google Scholar : PubMed/NCBI | |
Ciccia F, Bombardieri M, Principato A, Giardina A, Tripodo C, Porcasi R, Peralta S, Franco V, Giardina E, Craxi A, et al: Overexpression of interleukin-23, but not interleukin-17, as an immunologic signature of subclinical intestinal inflammation in ankylosing spondylitis. Arthritis Rheum. 60:955–965. 2009. View Article : Google Scholar : PubMed/NCBI | |
Appel H, Maier R, Bleil J, Hempfing A, Loddenkemper C, Schlichting U, Syrbe U and Sieper J: In situ analysis of interleukin-23- and interleukin-12-positive cells in the spine of patients with ankylosing spondylitis. Arthritis Rheum. 65:1522–1529. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kenna TJ, Lau MC, Keith P, Ciccia F, Costello ME, Bradbury L, Low PL, Agrawal N, Triolo G, Alessandro R, et al: Disease-associated polymorphisms in ERAP1 do not alter endoplasmic reticulum stress in patients with ankylosing spondylitis. Genes Immun. 16:35–42. 2015. View Article : Google Scholar : PubMed/NCBI | |
Shaw J, Hatano H and Kollnberger S: The biochemistry and immunology of non-canonical forms of HLA-B27. Mol Immunol. 57:52–58. 2014. View Article : Google Scholar : PubMed/NCBI | |
Luthra-Guptasarma M and Singh B: HLA-B27 lacking associated beta2-microglobulin rearranges to auto-display or cross-display residues 169–181: A novel molecular mechanism for spondyloarthropathies. FEBS Lett. 575:1–8. 2004. View Article : Google Scholar : PubMed/NCBI | |
Uchanska-Ziegler B and Ziegler A: Ankylosing spondylitis: A beta2m-deposition disease? Trends Immunol. 24:73–76. 2003. View Article : Google Scholar : PubMed/NCBI | |
Tran TM, Dorris ML, Satumtira N, Richardson JA, Hammer RE, Shang J and Taurog JD: Additional human beta2-microglobulin curbs HLA-B27 misfolding and promotes arthritis and spondylitis without colitis in male HLA-B27-transgenic rats. Arthritis Rheum. 54:1317–1327. 2006. View Article : Google Scholar : PubMed/NCBI | |
Yeremenko N, Paramarta JE and Baeten D: The interleukin-23/interleukin-17 immune axis as a promising new target in the treatment of spondyloarthritis. Curr Opin Rheumatol. 26:361–370. 2014. View Article : Google Scholar : PubMed/NCBI | |
Jethwa H and Bowness P: The interleukin (IL)-23/IL-17 axis in ankylosing spondylitis: New advances and potentials for treatment. Clin Exp Immunol. 183:30–36. 2016. View Article : Google Scholar : PubMed/NCBI |