Skip to main content
Erschienen in: Clinical Rheumatology 5/2019

05.12.2018 | Review Article

Dendritic cells in the pathogenesis of ankylosing spondylitis and axial spondyloarthritis

verfasst von: Gleb Slobodin, Itzhak Rosner, Aharon Kessel

Erschienen in: Clinical Rheumatology | Ausgabe 5/2019

Einloggen, um Zugang zu erhalten

Abstract

The interaction of dendritic cells (DCs) with the human microbiome, with distorted handling of the microbiota or its products via the direct effect of HLA B27, probably represents the initial element in the chain of events leading to the development of clinical axial spondyloarthritis. The mechanism of disease extension onto the skeleton and other tissues involved, such as uvea, may also involve migratory DCs. Finally, the role of DCs in the initiation of the inflammatory tissue response with activation of the IL-17 axis has been demonstrated. Further, some initial data suggests the possible connection of DCs with disease-related new bone formation.
Literatur
1.
Zurück zum Zitat Taurog JD, Chhabra A, Colbert RA (2016) Ankylosing spondylitis and axial spondyloarthritis. N Engl J Med Jun 374(26):2563–2574CrossRef Taurog JD, Chhabra A, Colbert RA (2016) Ankylosing spondylitis and axial spondyloarthritis. N Engl J Med Jun 374(26):2563–2574CrossRef
2.
Zurück zum Zitat Robinson PC, Brown MA (2014) Genetics of ankylosing spondylitis. Mol Immunol Jan 57(1):2–11CrossRef Robinson PC, Brown MA (2014) Genetics of ankylosing spondylitis. Mol Immunol Jan 57(1):2–11CrossRef
3.
Zurück zum Zitat Powis SJ, Colbert RA (2016) Editorial: HLA-B27: the story continues to unfold. Arthritis Rheumatol. 68(5):1057–1059PubMedPubMedCentral Powis SJ, Colbert RA (2016) Editorial: HLA-B27: the story continues to unfold. Arthritis Rheumatol. 68(5):1057–1059PubMedPubMedCentral
4.
Zurück zum Zitat Breban M, Tap J, Leboime A, Said-Nahal R, Langella P, Chiocchia G, Furet JP, Sokol H (2017) Faecal microbiota study reveals specific dysbiosis in spondyloarthritis. Ann Rheum Dis 76(9):1614–1622CrossRefPubMed Breban M, Tap J, Leboime A, Said-Nahal R, Langella P, Chiocchia G, Furet JP, Sokol H (2017) Faecal microbiota study reveals specific dysbiosis in spondyloarthritis. Ann Rheum Dis 76(9):1614–1622CrossRefPubMed
5.
Zurück zum Zitat Wen C, Zheng Z, Shao T, Liu L, Xie Z, Le Chatelier E, He Z, Zhong W, Fan Y, Zhang L, Li H, Wu C, Hu C, Xu Q, Zhou J, Cai S, Wang D, Huang Y, Breban M, Qin N, Ehrlich SD (2017) Quantitative metagenomics reveals unique gut microbiome biomarkers in ankylosing spondylitis. Genome Biol 18(1):142CrossRefPubMedPubMedCentral Wen C, Zheng Z, Shao T, Liu L, Xie Z, Le Chatelier E, He Z, Zhong W, Fan Y, Zhang L, Li H, Wu C, Hu C, Xu Q, Zhou J, Cai S, Wang D, Huang Y, Breban M, Qin N, Ehrlich SD (2017) Quantitative metagenomics reveals unique gut microbiome biomarkers in ankylosing spondylitis. Genome Biol 18(1):142CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Asquith M, Davin S, Stauffer P, Michell C, Janowitz C, Lin P, Ensign-Lewis J, Kinchen JM, Koop DR, Rosenbaum JT (2017) Intestinal metabolites are profoundly altered in the context of HLA-B27 expression and functionally modulate disease in a rat model of spondyloarthritis. Arthritis Rheumatol 69(10):1984–1995CrossRefPubMedPubMedCentral Asquith M, Davin S, Stauffer P, Michell C, Janowitz C, Lin P, Ensign-Lewis J, Kinchen JM, Koop DR, Rosenbaum JT (2017) Intestinal metabolites are profoundly altered in the context of HLA-B27 expression and functionally modulate disease in a rat model of spondyloarthritis. Arthritis Rheumatol 69(10):1984–1995CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Smolinska S, Groeger D, O'Mahony L (2017) Biology of the microbiome 1: interactions with the host immune response. Gastroenterol Clin N Am 46(1):19–35CrossRef Smolinska S, Groeger D, O'Mahony L (2017) Biology of the microbiome 1: interactions with the host immune response. Gastroenterol Clin N Am 46(1):19–35CrossRef
9.
Zurück zum Zitat Krajewska-Wlodarczyk M, Owczarczyk-Saczonek A, Placek W, Osowski A, Engelgardt P, Wojtkiewicz J (2017) Role of stem cells in pathophysiology and therapy of spondyloarthropathies-new therapeutic possibilities? Int J Mol Sci 28(19):1 Krajewska-Wlodarczyk M, Owczarczyk-Saczonek A, Placek W, Osowski A, Engelgardt P, Wojtkiewicz J (2017) Role of stem cells in pathophysiology and therapy of spondyloarthropathies-new therapeutic possibilities? Int J Mol Sci 28(19):1
10.
Zurück zum Zitat Pepelyayeva Y, Rastall DPW, Aldhamen YA, O’Connell P, Raehtz S, Alyaqoub Blake MK, Raedy AM, Angarita AM, Abbas AM, Pereira-Hicks CN, Roosa SG, McCabe L, Amalfitano A (2018) ERAP1 deficient mice have reduced type 1 regulatory T cells and develop skeletal and intestinal features of ankylosing spondylitis. Sci Rep 8(1):12464CrossRefPubMedPubMedCentral Pepelyayeva Y, Rastall DPW, Aldhamen YA, O’Connell P, Raehtz S, Alyaqoub Blake MK, Raedy AM, Angarita AM, Abbas AM, Pereira-Hicks CN, Roosa SG, McCabe L, Amalfitano A (2018) ERAP1 deficient mice have reduced type 1 regulatory T cells and develop skeletal and intestinal features of ankylosing spondylitis. Sci Rep 8(1):12464CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Berthelot JM, Claudepierre P (2016) Trafficking of antigens from gut to sacroiliac joints and spine in reactive arthritis and spondyloarthropathies: mainly through lymphatics? Joint Bone Spine 83(5):485–490CrossRefPubMed Berthelot JM, Claudepierre P (2016) Trafficking of antigens from gut to sacroiliac joints and spine in reactive arthritis and spondyloarthropathies: mainly through lymphatics? Joint Bone Spine 83(5):485–490CrossRefPubMed
12.
Zurück zum Zitat Hacquard-Bouder C, Falgarone G, Bosquet A, Smaoui F, Monnet D, Ittah M, Breban M (2004) Defective costimulatory function is a striking feature of antigen-presenting cells in an HLA-B27-transgenic rat model of spondyloarthropathy. Arthritis Rheum 50(5):1624–1635CrossRefPubMed Hacquard-Bouder C, Falgarone G, Bosquet A, Smaoui F, Monnet D, Ittah M, Breban M (2004) Defective costimulatory function is a striking feature of antigen-presenting cells in an HLA-B27-transgenic rat model of spondyloarthropathy. Arthritis Rheum 50(5):1624–1635CrossRefPubMed
13.
Zurück zum Zitat Hacquard-Bouder C, Chimenti MS, Giquel B, Donnadieu E, Fert I, Schmitt A, André C, Breban M (2007) Alteration of antigen-independent immunologic synapse formation between dendritic cells from HLA-B27-transgenic rats and CD4+ T cells: selective impairment of costimulatory molecule engagement by mature HLA- B27. Arthritis Rheum 56(5):1478–1489CrossRefPubMed Hacquard-Bouder C, Chimenti MS, Giquel B, Donnadieu E, Fert I, Schmitt A, André C, Breban M (2007) Alteration of antigen-independent immunologic synapse formation between dendritic cells from HLA-B27-transgenic rats and CD4+ T cells: selective impairment of costimulatory molecule engagement by mature HLA- B27. Arthritis Rheum 56(5):1478–1489CrossRefPubMed
14.
Zurück zum Zitat Dhaenens M, Fert I, Glatigny S, Haerinck S, Poulain C, Donnadieu E, Hacquard-Bouder C, Andre C, Elewaut D, Deforce D, Breban M (2009) Dendritic cells from spondyloarthritis-prone HLA-B27-transgenic rats display altered cytoskeletal dynamics, class II major histocompatibility complex expression, and viability. Arthritis Rheum 60(9):2622–2632CrossRefPubMed Dhaenens M, Fert I, Glatigny S, Haerinck S, Poulain C, Donnadieu E, Hacquard-Bouder C, Andre C, Elewaut D, Deforce D, Breban M (2009) Dendritic cells from spondyloarthritis-prone HLA-B27-transgenic rats display altered cytoskeletal dynamics, class II major histocompatibility complex expression, and viability. Arthritis Rheum 60(9):2622–2632CrossRefPubMed
15.
Zurück zum Zitat Slobodin G, Kessel A, Kofman N, Toubi E, Rosner I, Odeh M (2012) Phenotype of resting and activated monocyte-derived dendritic cells grown from peripheral blood of patients with ankylosing spondylitis. Inflammation 35(2):772–775CrossRefPubMed Slobodin G, Kessel A, Kofman N, Toubi E, Rosner I, Odeh M (2012) Phenotype of resting and activated monocyte-derived dendritic cells grown from peripheral blood of patients with ankylosing spondylitis. Inflammation 35(2):772–775CrossRefPubMed
16.
Zurück zum Zitat Fert I, Glatigny S, Poulain C, Satumtira N, Dorris ML, Taurog JD, Breban M (2008) Correlation between dendritic cell functional defect and spondyloarthritis phenotypes in HLA-B27/HUMAN beta2-microglobulin-transgenic rat lines. Arthritis Rheum 58(11):3425–3429CrossRefPubMed Fert I, Glatigny S, Poulain C, Satumtira N, Dorris ML, Taurog JD, Breban M (2008) Correlation between dendritic cell functional defect and spondyloarthritis phenotypes in HLA-B27/HUMAN beta2-microglobulin-transgenic rat lines. Arthritis Rheum 58(11):3425–3429CrossRefPubMed
17.
Zurück zum Zitat Talpin A, Costantino F, Bonilla N, Leboime A, Letourneur F, Jacques S, Dumont F, Amraoui S, Dutertre CA, Garchon HJ, Breban M, Chiocchia G (2014) Monocyte- derived dendritic cells from HLA-B27+ axial spondyloarthritis (SpA) patients display altered functional capacity and deregulated gene expression. Arthritis Res Ther. 16(4):417CrossRefPubMedPubMedCentral Talpin A, Costantino F, Bonilla N, Leboime A, Letourneur F, Jacques S, Dumont F, Amraoui S, Dutertre CA, Garchon HJ, Breban M, Chiocchia G (2014) Monocyte- derived dendritic cells from HLA-B27+ axial spondyloarthritis (SpA) patients display altered functional capacity and deregulated gene expression. Arthritis Res Ther. 16(4):417CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Utriainen L, Firmin D, Wright P, Cerovic V, Breban M, McInnes I, Milling S (2012) Expression of HLA-B27 causes loss of migratory dendritic cells in a rat model of spondyloarthritis. Arthritis Rheum 64(10):3199–3209CrossRefPubMedPubMedCentral Utriainen L, Firmin D, Wright P, Cerovic V, Breban M, McInnes I, Milling S (2012) Expression of HLA-B27 causes loss of migratory dendritic cells in a rat model of spondyloarthritis. Arthritis Rheum 64(10):3199–3209CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Fert I, Cagnard N, Glatigny S, Letourneur F, Jacques S, Smith JA, Colbert RA, Taurog JD, Chiocchia G, Araujo LM, Breban M (2014) Reverse interferon signature is characteristic of antigen-presenting cells in human and rat spondyloarthritis. Arthritis Rheumatol. 66(4):841–851CrossRefPubMedPubMedCentral Fert I, Cagnard N, Glatigny S, Letourneur F, Jacques S, Smith JA, Colbert RA, Taurog JD, Chiocchia G, Araujo LM, Breban M (2014) Reverse interferon signature is characteristic of antigen-presenting cells in human and rat spondyloarthritis. Arthritis Rheumatol. 66(4):841–851CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Santos SG, Lynch S, Campbell EC, Antoniou AN, Powis SJ (2008) Induction of HLA- B27 heavy chain homodimer formation after activation in dendritic cells. Arthritis Res Ther 10(4):R100CrossRefPubMedPubMedCentral Santos SG, Lynch S, Campbell EC, Antoniou AN, Powis SJ (2008) Induction of HLA- B27 heavy chain homodimer formation after activation in dendritic cells. Arthritis Res Ther 10(4):R100CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Raine T, Brown D, Bowness P, Hill Gaston JS, Moffett A, Trowsdale J, Allen RL (2006) Consistent patterns of expression of HLA class I free heavy chains in healthy individuals and raised expression in spondyloarthropathy patients point to physiological and pathological roles. Rheumatology (Oxford) 45(11):1338–1344CrossRef Raine T, Brown D, Bowness P, Hill Gaston JS, Moffett A, Trowsdale J, Allen RL (2006) Consistent patterns of expression of HLA class I free heavy chains in healthy individuals and raised expression in spondyloarthropathy patients point to physiological and pathological roles. Rheumatology (Oxford) 45(11):1338–1344CrossRef
22.
Zurück zum Zitat Wong-Baeza I, Ridley A, Shaw J, Hatano H, Rysnik O, McHugh K, Piper C, Brackenbridge S, Fernandes R, Chan A, Bowness P, Kollnberger S (2013) 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(7):3216–3224CrossRefPubMed Wong-Baeza I, Ridley A, Shaw J, Hatano H, Rysnik O, McHugh K, Piper C, Brackenbridge S, Fernandes R, Chan A, Bowness P, Kollnberger S (2013) 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(7):3216–3224CrossRefPubMed
23.
Zurück zum Zitat Wright PB, McEntegart A, McCarey D, McInnes IB, Siebert S, Milling SW (2016) Ankylosing spondylitis patients display altered dendritic cell and T cell populations that implicate pathogenic roles for the IL-23 cytokine axis and intestinal inflammation. Rheumatology (Oxford) 55(1):120–132CrossRef Wright PB, McEntegart A, McCarey D, McInnes IB, Siebert S, Milling SW (2016) Ankylosing spondylitis patients display altered dendritic cell and T cell populations that implicate pathogenic roles for the IL-23 cytokine axis and intestinal inflammation. Rheumatology (Oxford) 55(1):120–132CrossRef
24.
Zurück zum Zitat Pang L, Wang L, Suo T, Hao H, Fang X, Jia J, Huang F, Tang J (2008) Tumor necrosis factor-alpha blockade leads to decreased peripheral T cell reactivity and increased dendritic cell number in peripheral blood of patients with ankylosing spondylitis. J Rheumatol 35(11):2220–2228CrossRefPubMed Pang L, Wang L, Suo T, Hao H, Fang X, Jia J, Huang F, Tang J (2008) Tumor necrosis factor-alpha blockade leads to decreased peripheral T cell reactivity and increased dendritic cell number in peripheral blood of patients with ankylosing spondylitis. J Rheumatol 35(11):2220–2228CrossRefPubMed
25.
Zurück zum Zitat Hallett RM, Chew T (2014) Immune cell transcript modules reveal leukocyte heterogeneity in synovial biopsies of seronegative spondyloarthropathy patients. BMC Musculoskelet Disord 15:446CrossRefPubMedPubMedCentral Hallett RM, Chew T (2014) Immune cell transcript modules reveal leukocyte heterogeneity in synovial biopsies of seronegative spondyloarthropathy patients. BMC Musculoskelet Disord 15:446CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Appel H, Maier R, Bleil J, Hempfing A, Loddenkemper C, Schlichting U, Syrbe U, Sieper J (2013) In situ analysis of interleukin-23- and interleukin-12-positive cells in the spine of patients with ankylosing spondylitis. Arthritis Rheum 65(6):1522–1529CrossRefPubMed Appel H, Maier R, Bleil J, Hempfing A, Loddenkemper C, Schlichting U, Syrbe U, Sieper J (2013) In situ analysis of interleukin-23- and interleukin-12-positive cells in the spine of patients with ankylosing spondylitis. Arthritis Rheum 65(6):1522–1529CrossRefPubMed
27.
Zurück zum Zitat Glatigny S, Fert I, Blaton MA, Lories RJ, Araujo LM, Chiocchia G, Breban M (2012) Proinflammatory Th17 cells are expanded and induced by dendritic cells in spondyloarthritis-prone HLA-B27-transgenic rats. Arthritis Rheum 64(1):110–120CrossRefPubMed Glatigny S, Fert I, Blaton MA, Lories RJ, Araujo LM, Chiocchia G, Breban M (2012) Proinflammatory Th17 cells are expanded and induced by dendritic cells in spondyloarthritis-prone HLA-B27-transgenic rats. Arthritis Rheum 64(1):110–120CrossRefPubMed
28.
Zurück zum Zitat Smith JA, Barnes MD, Hong D, DeLay ML, Inman RD, Colbert RA (2008) Gene expression analysis of macrophages derived from ankylosing spondylitis patients reveals interferon-gamma dysregulation. Arthritis Rheum 58(6):1640–1649CrossRefPubMedPubMedCentral Smith JA, Barnes MD, Hong D, DeLay ML, Inman RD, Colbert RA (2008) Gene expression analysis of macrophages derived from ankylosing spondylitis patients reveals interferon-gamma dysregulation. Arthritis Rheum 58(6):1640–1649CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Cortes A, Maksymowych WP, Wordsworth BP, Inman RD, Danoy P, Rahman P, Stone MA, Corr M, Gensler LS, Gladman D, Morgan A, Marzo-Ortega H, Ward MM, SPARCC (Spondyloarthritis Research Consortium of Canada); TASC (Australo-Anglo-American Spondyloarthritis Consortium), Learch TJ, Reveille JD, Brown MA, Weisman MH (2015) Association study of genes related to bone formation and resorption and the extent of radiographic change in ankylosing spondylitis. Ann Rheum Dis 74(7):1387–1393CrossRefPubMed Cortes A, Maksymowych WP, Wordsworth BP, Inman RD, Danoy P, Rahman P, Stone MA, Corr M, Gensler LS, Gladman D, Morgan A, Marzo-Ortega H, Ward MM, SPARCC (Spondyloarthritis Research Consortium of Canada); TASC (Australo-Anglo-American Spondyloarthritis Consortium), Learch TJ, Reveille JD, Brown MA, Weisman MH (2015) Association study of genes related to bone formation and resorption and the extent of radiographic change in ankylosing spondylitis. Ann Rheum Dis 74(7):1387–1393CrossRefPubMed
32.
Zurück zum Zitat Clark GJ, Silveira PA, Hogarth PM, Hart DNJ (2018) The cell surface phenotype of human dendritic cells. Semin Cell Dev Biol pii S1084-9521(17):30494–30499 Clark GJ, Silveira PA, Hogarth PM, Hart DNJ (2018) The cell surface phenotype of human dendritic cells. Semin Cell Dev Biol pii S1084-9521(17):30494–30499
33.
Zurück zum Zitat Domogalla MP, Rostan PV, Raker VK, Steinbrink K (2017) Tolerance through education: how tolerogenic dendritic cells shape immunity. Front Immunol 8:1764CrossRefPubMedPubMedCentral Domogalla MP, Rostan PV, Raker VK, Steinbrink K (2017) Tolerance through education: how tolerogenic dendritic cells shape immunity. Front Immunol 8:1764CrossRefPubMedPubMedCentral
Metadaten
Titel
Dendritic cells in the pathogenesis of ankylosing spondylitis and axial spondyloarthritis
verfasst von
Gleb Slobodin
Itzhak Rosner
Aharon Kessel
Publikationsdatum
05.12.2018
Verlag
Springer London
Erschienen in
Clinical Rheumatology / Ausgabe 5/2019
Print ISSN: 0770-3198
Elektronische ISSN: 1434-9949
DOI
https://doi.org/10.1007/s10067-018-4388-4

Weitere Artikel der Ausgabe 5/2019

Clinical Rheumatology 5/2019 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.