Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Arthritis Research & Therapy
Published in: Arthritis Research & Therapy 1/2011

Open Access 01-02-2011 | Research article

RETRACTED ARTICLE: Reduced immunomodulation potential of bone marrow-derived mesenchymal stem cells induced CCR4+CCR6+Th/Treg cell subset imbalance in ankylosing spondylitis

Authors: Yanfeng Wu, Mingliang Ren, Rui Yang, Xinjun Liang, Yuanchen Ma, Yong Tang, Lin Huang, Jichao Ye, Keng Chen, Peng Wang, Huiyong Shen

Published in: Arthritis Research & Therapy | Issue 1/2011

Login to get access

Abstract

Introduction

Ankylosing spondylitis (AS) is a chronic autoimmune disease, and the precise pathogenesis is largely unknown at present. Bone marrow-derived mesenchymal stem cells (BMSCs) with immunosuppressive and anti-inflammatory potential and Th17/Treg cells with a reciprocal relationship regulated by BMSCs have been reported to be involved in some autoimmune disorders. Here we studied the biological and immunological characteristics of BMSCs, the frequency and phenotype of CCR4+CCR6+ Th/Treg cells and their interaction in vitro in AS.

Methods

The biological and immunomodulation characteristics of BMSCs were examined by induced multiple-differentiation and two-way mixed peripheral blood mononuclear cell (PBMC) reactions or after stimulation with phytohemagglutinin, respectively. The interactions of BMSCs and PBMCs were detected with a direct-contact co-culturing system. CCR4+CCR6+ Th/Treg cells and surface markers of BMSCs were assayed using flow cytometry.

Results

The AS-BMSCs at active stage showed normal proliferation, cell viability, surface markers and multiple differentiation characteristics, but significantly reduced immunomodulation potential (decreased 68 ± 14%); the frequencies of Treg and Fox-P3+ cells in AS-PBMCs decreased, while CCR4+CCR6+ Th cells increased, compared with healthy donors. Moreover, the AS-BMSCs induced imbalance in the ratio of CCR4+CCR6+ Th/Treg cells by reducing Treg/PBMCs and increasing CCR4+CCR6+ Th/PBMCs, and also reduced Fox-P3+ cells when co-cultured with PBMCs. Correlation analysis showed that the immunomodulation potential of BMSCs has significant negative correlations with the ratio of CCR4+CCR6+ Th to Treg cells in peripheral blood.

Conclusions

The immunomodulation potential of BMSCs is reduced and the ratio of CCR4+CCR6+ Th/Treg cells is imbalanced in AS. The BMSCs with reduced immunomodulation potential may play a novel role in AS pathogenesis by inducing CCR4+CCR6+ Th/Treg cell imbalance.
Appendix
Available only for authorised users
Literature
1.
Braun J, Sieper J: Ankylosing spondylitis. Lancet. 2007, 369: 1379-1390. 10.1016/S0140-6736(07)60635-7.
2.
Penttinen MA, Heiskanen KM, Mohapatra R, DeLay ML, Colbert RA, Sistonen L, Granfors K: Enhanced intracellular replication of Salmonella enteritidis in HLA-B27-expressing human monocytic cells: dependency on glutamic acid at position 45 in the B pocket of HLA-B27. Arthritis Rheum. 2004, 50: 2255-2263. 10.1002/art.20336.
3.
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. 10.1002/art.1780401015.
4.
Brewerton DA, Hart FD, Nicholls A, Caffrey M, James DC, Sturrock RD: Ankylosing spondylitis and HL-A 27. Lancet. 1973, 1: 904-907. 10.1016/S0140-6736(73)91360-3.
5.
Paladini F, Belfiore F, Cocco E, Carcassi C, Cauli A, Vacca A, Fiorillo MT, Mathieu A, Cascino I, Sorrentino R: HLA-E gene polymorphism associates with ankylosing spondylitis in Sardinia. Arthritis Res Ther. 2009, 11: R171-10.1186/ar2860.
6.
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. 10.1038/ng.513.
7.
Braun J, Tuszewski M, Ehlers S, Haberle J, Bollow M, Eggens U, Distler A, Sieper J: Nested polymerase chain reaction strategy simultaneously targeting DNA sequences of multiple bacterial species in inflammatory joint diseases. II. Examination of sacroiliac and knee joint biopsies of patients with spondyloarthropathies and other arthritides. J Rheumatol. 1997, 24: 1101-1105.
8.
Aggarwal S, Pittenger MF: Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood. 2005, 105: 1815-1822. 10.1182/blood-2004-04-1559.
9.
Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM: Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood. 2002, 99: 3838-3843. 10.1182/blood.V99.10.3838.
10.
Bartholomew A, Sturgeon C, Siatskas M, Ferrer K, McIntosh K, Patil S, Hardy W, Devine S, Ucker D, Deans R, Moseley A, Hoffman R: Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo. Exp Hematol. 2002, 30: 42-48. 10.1016/S0301-472X(01)00769-X.
11.
Dazzi F, Marelli-Berg FM: Mesenchymal stem cells for graft-versus-host disease: close encounters with T cells. Eur J Immunol. 2008, 38: 1479-1482. 10.1002/eji.200838433.
12.
Uccelli A, Moretta L, Pistoia V: Immunoregulatory function of mesenchymal stem cells. Eur J Immunol. 2006, 36: 2566-2573. 10.1002/eji.200636416.
13.
Zappia E, Casazza S, Pedemonte E, Benvenuto F, Bonanni I, Gerdoni E, Giunti D, Ceravolo A, Cazzanti F, Frassoni F, Mancardi G, Uccelli A: Mesenchymal stem cells ameliorate experimental autoimmune encephalomyelitis inducing T-cell anergy. Blood. 2005, 106: 1755-1761. 10.1182/blood-2005-04-1496.
14.
Bacigalupo A, Valle M, Podesta M, Pitto A, Zocchi E, De Flora A, Pozzi S, Luchetti S, Frassoni F, Van Lint MT, Piaggio G: T-cell suppression mediated by mesenchymal stem cells is deficient in patients with severe aplastic anemia. Exp Hematol. 2005, 33: 819-827. 10.1016/j.exphem.2005.05.006.
15.
Bernardo ME, Avanzini MA, Ciccocioppo R, Perotti C, Cometa AM, Moretta A, Marconi M, Valli M, Novara F, Bonetti F, Zuffardi O, Maccario R, Corazza GR, Locatelli F: Phenotypical/functional characterization of in vitro-expanded mesenchymal stromal cells from patients with Crohn's disease. Cytotherapy. 2009, 11: 825-836. 10.3109/14653240903121260.
16.
Costantino CM, Baecher-Allan CM, Hafler DA: Human regulatory T cells and autoimmunity. Eur J Immunol. 2008, 38: 921-924. 10.1002/eji.200738104.
17.
Ouyang W, Kolls JK, Zheng Y: The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity. 2008, 28: 454-467. 10.1016/j.immuni.2008.03.004.
18.
Mills KH: Induction, function and regulation of IL-17-producing T cells. Eur J Immunol. 2008, 38: 2636-2649. 10.1002/eji.200838535.
19.
Romagnani S: Human Th17 cells. Arthritis Res Ther. 2008, 10: 206-10.1186/ar2392.
20.
Vila J, Isaacs JD, Anderson AE: Regulatory T cells and autoimmunity. Curr Opin Hematol. 2009, 16: 274-279. 10.1097/MOH.0b013e32832a9a01.
21.
Banica L, Besliu A, Pistol G, Stavaru C, Ionescu R, Forsea AM, Tanaseanu C, Dumitrache S, Otelea D, Tamsulea I, Tanaseanu S, Chitonu C, Paraschiv S, Balteanu M, Stefanescu M, Matache C: Quantification and molecular characterization of regulatory T cells in connective tissue diseases. Autoimmunity. 2009, 42: 41-49. 10.1080/08916930802282651.
22.
Abdulahad WH, Stegeman CA, van der Geld YM, Doornbos-van der Meer B, Limburg PC, Kallenberg CG: Functional defect of circulating regulatory CD4+ T cells in patients with Wegener's granulomatosis in remission. Arthritis Rheum. 2007, 56: 2080-2091. 10.1002/art.22692.
23.
Okumura A, Ishikawa T, Sato S, Yamauchi T, Oshima H, Ohashi T, Sato K, Ayada M, Hotta N, Kakumu S: Deficiency of forkhead box P3 and cytotoxic T-lymphocyte-associated antigen-4 gene expressions and impaired suppressor function of CD4(+)CD25(+) T cells in patients with autoimmune hepatitis. Hepatol Res. 2008, 38: 896-903. 10.1111/j.1872-034X.2008.00349.x.
24.
Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA, Cua DJ: IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med. 2005, 201: 233-240. 10.1084/jem.20041257.
25.
Murphy CA, Langrish CL, Chen Y, Blumenschein W, McClanahan T, Kastelein RA, Sedgwick JD, Cua DJ: Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med. 2003, 198: 1951-1957. 10.1084/jem.20030896.
26.
Chen X, Vodanovic-Jankovic S, Johnson B, Keller M, Komorowski R, Drobyski WR: Absence of regulatory T-cell control of TH1 and TH17 cells is responsible for the autoimmune-mediated pathology in chronic graft-versus-host disease. Blood. 2007, 110: 3804-3813. 10.1182/blood-2007-05-091074.
27.
Weaver CT, Hatton RD, Mangan PR, Harrington LE: IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol. 2007, 25: 821-852. 10.1146/annurev.immunol.25.022106.141557.
28.
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, Meech E, et al: Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat Genet. 2007, 39: 1329-1337. 10.1038/ng.2007.17.
29.
Rahman P, Inman RD, Gladman DD, Reeve JP, Peddle L, Maksymowych WP: Association of interleukin-23 receptor variants with ankylosing spondylitis. Arthritis Rheum. 2008, 58: 1020-1025. 10.1002/art.23389.
30.
Rueda B, Orozco G, Raya E, Fernandez-Sueiro JL, Mulero J, Blanco FJ, Vilches C, Gonzalez-Gay MA, Martin J: The IL23R Arg381Gln non-synonymous polymorphism confers susceptibility to ankylosing spondylitis. Ann Rheum Dis. 2008, 67: 1451-1454. 10.1136/ard.2007.080283.
31.
Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B, Lucian L, To W, Kwan S, Churakova T, Zurawski S, Wiekowski M, Lira SA, Gorman D, Kastelein RA, Sedgwick JD: Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 2003, 421: 744-748. 10.1038/nature01355.
32.
Acosta-Rodriguez EV, Rivino L, Geginat J, Jarrossay D, Gattorno M, Lanzavecchia A, Sallusto F, Napolitani G: Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol. 2007, 8: 639-646. 10.1038/ni1467.
33.
Shen H, Goodall JC, Hill Gaston JS: Frequency and phenotype of peripheral blood Th17 cells in ankylosing spondylitis and rheumatoid arthritis. Arthritis Rheum. 2009, 60: 1647-1656. 10.1002/art.24568.
34.
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. 10.1002/art.1780270401.
35.
Betz MW, Modi PC, Caccamese JF, Coletti DP, Sauk JJ, Fisher JP: Cyclic acetal hydrogel system for bone marrow stromal cell encapsulation and osteodifferentiation. J Biomed Mater Res A. 2008, 86: 662-670.
36.
Jung JW, Cho SD, Ahn NS, Yang SR, Park JS, Jo EH, Hwang JW, Jung JY, Kim SH, Kang KS, Lee YS: Ras/MAP kinase pathways are involved in Ras specific apoptosis induced by sodium butyrate. Cancer Lett. 2005, 225: 199-206. 10.1016/j.canlet.2004.11.029.
37.
Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E: Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy. 2006, 8: 315-317. 10.1080/14653240600855905.
38.
Ehrenstein MR, Evans JG, Singh A, Moore S, Warnes G, Isenberg DA, Mauri C: Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFα therapy. J Exp Med. 2004, 200: 277-285. 10.1084/jem.20040165.
39.
Boissier MC, Assier E, Falgarone G, Bessis N: Shifting the imbalance from Th1/Th2 to Th17/treg: the changing rheumatoid arthritis paradigm. Joint Bone Spine. 2008, 75: 373-375. 10.1016/j.jbspin.2008.04.005.
40.
Wanders A, Landewe R, Dougados M, Mielants H, van der Linden S, van der Heijde D: Association between radiographic damage of the spine and spinal mobility for individual patients with ankylosing spondylitis: can assessment of spinal mobility be a proxy for radiographic evaluation?. Ann Rheum Dis. 2005, 64: 988-994. 10.1136/ard.2004.029728.
41.
El Tamer MK, Reis RL: Progenitor and stem cells for bone and cartilage regeneration. J Tissue Eng Regen Med. 2009, 3: 327-337. 10.1002/term.173.
42.
Yang Y: Skeletal morphogenesis during embryonic development. Crit Rev Eukaryot Gene Expr. 2009, 19: 197-218.
43.
Braun J, Bollow M, Neure L, Seipelt E, Seyrekbasan F, Herbst H, Eggens U, Distler A, Sieper J: Use of immunohistologic and in situ hybridization techniques in the examination of sacroiliac joint biopsy specimens from patients with ankylosing spondylitis. Arthritis Rheum. 1995, 38: 499-505. 10.1002/art.1780380407.
44.
Rifas L: T-cell cytokine induction of BMP-2 regulates human mesenchymal stromal cell differentiation and mineralization. J Cell Biochem. 2006, 98: 706-714. 10.1002/jcb.20933.
45.
Kim J, Lahl K, Hori S, Loddenkemper C, Chaudhry A, deRoos P, Rudensky A, Sparwasser T: Cutting edge: depletion of Foxp3+ cells leads to induction of autoimmunity by specific ablation of regulatory T cells in genetically targeted mice. J Immunol. 2009, 183: 7631-7634. 10.4049/jimmunol.0804308.
46.
Kimura A, Kishimoto T: IL-6: regulator of Treg/Th17 balance. Eur J Immunol. 2010, 40: 1830-1835. 10.1002/eji.201040391.
47.
Nistala K, Wedderburn LR: Th17 and regulatory T cells: rebalancing pro- and anti-inflammatory forces in autoimmune arthritis. Rheumatology (Oxford). 2009, 48: 602-606. 10.1093/rheumatology/kep028.
48.
Zhou L, Lopes JE, Chong MM, Ivanov II, Min R, Victora GD, Shen Y, Du J, Rubtsov YP, Rudensky AY, Ziegler SF, Littman DR: TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature. 2008, 453: 236-240. 10.1038/nature06878.
49.
Rivino L, Gruarin P, Haringer B, Steinfelder S, Lozza L, Steckel B, Weick A, Sugliano E, Jarrossay D, Kuhl AA, Loddenkemper C, Abrignani S, Sallusto F, Lanzavecchia A, Geginat J: CCR6 is expressed on an IL-10-producing, autoreactive memory T cell population with context-dependent regulatory function. J Exp Med. 2010, 207: 565-577. 10.1084/jem.20091021.
50.
Campbell JJ, Haraldsen G, Pan J, Rottman J, Qin S, Ponath P, Andrew DP, Warnke R, Ruffing N, Kassam N, Wu L, Butcher EC: The chemokine receptor CCR4 in vascular recognition by cutaneous but not intestinal memory T cells. Nature. 1999, 400: 776-780. 10.1038/23495.
51.
Baekkevold ES, Wurbel MA, Kivisakk P, Wain CM, Power CA, Haraldsen G, Campbell JJ: A role for CCR4 in development of mature circulating cutaneous T helper memory cell populations. J Exp Med. 2005, 201: 1045-1051. 10.1084/jem.20041059.
52.
Yang PT, Kasai H, Zhao LJ, Xiao WG, Tanabe F, Ito M: Increased CCR4 expression on circulating CD4(+) T cells in ankylosing spondylitis, rheumatoid arthritis and systemic lupus erythematosus. Clin Exp Immunol. 2004, 138: 342-347. 10.1111/j.1365-2249.2004.02617.x.
53.
Ruth JH, Shahrara S, Park CC, Morel JC, Kumar P, Qin S, Koch AE: Role of macrophage inflammatory protein-3α and its ligand CCR6 in rheumatoid arthritis. Lab Invest. 2003, 83: 579-588.
54.
Kohler RE, Caon AC, Willenborg DO, Clark-Lewis I, McColl SR: A role for macrophage inflammatory protein-3 alpha/CC chemokine ligand 20 in immune priming during T cell-mediated inflammation of the central nervous system. J Immunol. 2003, 170: 6298-6306.
55.
Homey B, Dieu-Nosjean MC, Wiesenborn A, Massacrier C, Pin JJ, Oldham E, Catron D, Buchanan ME, Muller A, deWaal Malefyt R, Deng G, Orozco R, Ruzicka T, Lehmann P, Lebecque S, Caux C, Zlotnik A: Up-regulation of macrophage inflammatory protein-3 alpha/CCL20 and CC chemokine receptor 6 in psoriasis. J Immunol. 2000, 164: 6621-6632.
56.
Schaerli P, Britschgi M, Keller M, Steiner UC, Steinmann LS, Moser B, Pichler WJ: Characterization of human T cells that regulate neutrophilic skin inflammation. J Immunol. 2004, 173: 2151-2158.
57.
Kikly K, Liu L, Na S, Sedgwick JD: The IL-23/Th(17) axis: therapeutic targets for autoimmune inflammation. Curr Opin Immunol. 2006, 18: 670-675. 10.1016/j.coi.2006.09.008.
58.
Nakae S, Nambu A, Sudo K, Iwakura Y: Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol. 2003, 171: 6173-6177.
59.
Nakae S, Saijo S, Horai R, Sudo K, Mori S, Iwakura Y: IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc Natl Acad Sci USA. 2003, 100: 5986-5990. 10.1073/pnas.1035999100.
60.
Cook DN, Prosser DM, Forster R, Zhang J, Kuklin NA, Abbondanzo SJ, Niu XD, Chen SC, Manfra DJ, Wiekowski MT, Sullivan LM, Smith SR, Greenberg HB, Narula SK, Lipp M, Lira SA: CCR6 mediates dendritic cell localization, lymphocyte homeostasis, and immune responses in mucosal tissue. Immunity. 2000, 12: 495-503. 10.1016/S1074-7613(00)80201-0.
61.
Keller M, Spanou Z, Schaerli P, Britschgi M, Yawalkar N, Seitz M, Villiger PM, Pichler WJ: T cell-regulated neutrophilic inflammation in autoinflammatory diseases. J Immunol. 2005, 175: 7678-7686.
62.
Liao F, Rabin RL, Smith CS, Sharma G, Nutman TB, Farber JM: CC-chemokine receptor 6 is expressed on diverse memory subsets of T cells and determines responsiveness to macrophage inflammatory protein 3 alpha. J Immunol. 1999, 162: 186-194.
63.
van Amelsfort JM, Jacobs KM, Bijlsma JW, Lafeber FP, Taams LS: CD4(+)CD25(+) regulatory T cells in rheumatoid arthritis: differences in the presence, phenotype, and function between peripheral blood and synovial fluid. Arthritis Rheum. 2004, 50: 2775-2785. 10.1002/art.20499.
64.
Jandus C, Bioley G, Rivals JP, Dudler J, Speiser D, Romero P: Increased numbers of circulating polyfunctional Th17 memory cells in patients with seronegative spondylarthritides. Arthritis Rheum. 2008, 58: 2307-2317. 10.1002/art.23655.
65.
Flores-Borja F, Jury EC, Mauri C, Ehrenstein MR: Defects in CTLA-4 are associated with abnormal regulatory T cell function in rheumatoid arthritis. Proc Natl Acad Sci USA. 2008, 105: 19396-19401. 10.1073/pnas.0806855105.
66.
Valencia X, Stephens G, Goldbach-Mansky R, Wilson M, Shevach EM, Lipsky PE: TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood. 2006, 108: 253-261. 10.1182/blood-2005-11-4567.
67.
Kong QF, Sun B, Bai SS, Zhai DX, Wang GY, Liu YM, Zhang SJ, Li R, Zhao W, Sun YY, Li N, Wang Q, Peng HS, Jin LH, Li HL: Administration of bone marrow stromal cells ameliorates experimental autoimmune myasthenia gravis by altering the balance of Th1/Th2/Th17/Treg cell subsets through the secretion of TGF-β. J Neuroimmunol. 2009, 207: 83-91. 10.1016/j.jneuroim.2008.12.005.
68.
Maccario R, Podesta M, Moretta A, Cometa A, Comoli P, Montagna D, Daudt L, Ibatici A, Piaggio G, Pozzi S, Frassoni F, Locatelli F: Interaction of human mesenchymal stem cells with cells involved in alloantigen-specific immune response favors the differentiation of CD4+ T-cell subsets expressing a regulatory/suppressive phenotype. Haematologica. 2005, 90: 516-525.
69.
Annunziato F, Cosmi L, Santarlasci V, Maggi L, Liotta F, Mazzinghi B, Parente E, Fili L, Ferri S, Frosali F, Giudici F, Romagnani P, Parronchi P, Tonelli F, Maggi E, Romagnani S: Phenotypic and functional features of human Th17 cells. J Exp Med. 2007, 204: 1849-1861. 10.1084/jem.20070663.
70.
Parekkadan B, van Poll D, Megeed Z, Kobayashi N, Tilles AW, Berthiaume F, Yarmush ML: Immunomodulation of activated hepatic stellate cells by mesenchymal stem cells. Biochem Biophys Res Commun. 2007, 363: 247-252. 10.1016/j.bbrc.2007.05.150.
71.
Gonzalez MA, Gonzalez-Rey E, Rico L, Buscher D, Delgado M: Treatment of experimental arthritis by inducing immune tolerance with human adipose-derived mesenchymal stem cells. Arthritis Rheum. 2009, 60: 1006-1019. 10.1002/art.24405.
72.
Kong QF, Sun B, Wang GY, Zhai DX, Mu LL, Wang DD, Wang JH, Li R, Li HL: BM stromal cells ameliorate experimental autoimmune myasthenia gravis by altering the balance of Th cells through the secretion of IDO. Eur J Immunol. 2009, 39: 800-809. 10.1002/eji.200838729.
73.
Uccelli A, Moretta L, Pistoia V: Mesenchymal stem cells in health and disease. Nat Rev Immunol. 2008, 8: 726-736. 10.1038/nri2395.
74.
Schambach F, Schupp M, Lazar MA, Reiner SL: Activation of retinoic acid receptor-alpha favours regulatory T cell induction at the expense of IL-17-secreting T helper cell differentiation. Eur J Immunol. 2007, 37: 2396-2399. 10.1002/eji.200737621.
Metadata
Title
RETRACTED ARTICLE: Reduced immunomodulation potential of bone marrow-derived mesenchymal stem cells induced CCR4+CCR6+Th/Treg cell subset imbalance in ankylosing spondylitis
Authors
Yanfeng Wu
Mingliang Ren
Rui Yang
Xinjun Liang
Yuanchen Ma
Yong Tang
Lin Huang
Jichao Ye
Keng Chen
Peng Wang
Huiyong Shen
Publication date
01-02-2011
Publisher
BioMed Central
Published in
Arthritis Research & Therapy / Issue 1/2011
Electronic ISSN: 1478-6362
DOI
https://doi.org/10.1186/ar3257

Other articles of this Issue 1/2011

Arthritis Research & Therapy 1/2011 Go to the issue

Review

What have we learned from clinical trials in primary Sjögren's syndrome about pathogenesis?

Research article

Association of the D repeat polymorphism in the ASPNgene with developmental dysplasia of the hip: a case-control study in Han Chinese

Research article

(Sub)clinical cardiovascular disease is associated with increased bone loss and fracture risk; a systematic review of the association between cardiovascular disease and osteoporosis

Research article

Antibodies of IgG, IgA and IgM isotypes against cyclic citrullinated peptide precede the development of rheumatoid arthritis

Research article

Single-nucleotide polymorphisms and haplotype of CYP2E1gene associated with systemic lupus erythematosus in Chinese population

Research article

Modulation of transforming growth factor beta signalling pathway genes by transforming growth factor beta in human osteoarthritic chondrocytes: involvement of Sp1 in both early and late response cells to transforming growth factor beta
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits