The response of T cells to interleukin-6 is differentially regulated by the microenvironment of the rheumatoid synovial fluid and tissue

Arthritis and Rheumatism

Volumn 63, Issue 11, 2011, Pages 3284-3293

  Hidalgo, Ester ^a   Essex, Sarah J ^a   Yeo, Lorraine ^a   Curnow, S John ^a   Filer, Andrew ^a   Cooper, Mark S ^a   Thomas, Andrew M ^b   McGettrick, Helen M ^a   Salmon, Michael ^a   Buckley, Christopher D ^a   Raza, Karim ^a   Scheel Toellner, Dagmar ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b ROYAL ORTHOPAEDIC HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN GP 130; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR;

ADULT; AGED; ARTICLE; CD4+ T LYMPHOCYTE; CLINICAL ARTICLE; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE MICROSCOPY; MALE; MICROENVIRONMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; RHEUMATOID ARTHRITIS; SYNOVIAL FLUID; SYNOVIUM;

ADULT; AGED; AGED, 80 AND OVER; ARTHRITIS, RHEUMATOID; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINE RECEPTOR GP130; HUMANS; INTERLEUKIN-6; INTERLEUKIN-6 RECEPTOR ALPHA SUBUNIT; JOINTS; MALE; MIDDLE AGED; SYNOVIAL FLUID; SYNOVIAL MEMBRANE;

EID: 80155130171     PISSN: 00043591     EISSN: 15290131     Source Type: Journal    
DOI: 10.1002/art.30570     Document Type: Article

References (45)

1. Nishimoto N, Yoshizaki K, Miyasaka N, Yamamoto K, Kawai S, Takeuchi T, et al. Treatment of rheumatoid arthritis with humanized anti-interleukin-6 receptor antibody: a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum 2004; 50: 1761-9. (Pubitemid 38725087)
2. Kavanaugh A,. Interleukin-6 inhibition and clinical efficacy in rheumatoid arthritis treatment: data from randomized clinical trials. Bull NYU Hosp Jt Dis 2007; 65 Suppl 1: S16-20.
3. Houssiau FA, Devogelaer JP, Van Damme J, de Deuxchaisnes CN, Van Snick J,. Interleukin-6 in synovial fluid and serum of patients with rheumatoid arthritis and other inflammatory arthritides. Arthritis Rheum 1988; 31: 784-8.
4. Tak PP, Smeets TJ, Daha MR, Kluin PM, Meijers KA, Brand R, et al. Analysis of the synovial cell infiltrate in early rheumatoid synovial tissue in relation to local disease activity. Arthritis Rheum 1997; 40: 217-25. (Pubitemid 27114085)
5. Prowse KR, Baumann H,. Interleukin-1 and interleukin-6 stimulate acute-phase protein production in primary mouse hepatocytes. J Leukoc Biol 1989; 45: 55-61. (Pubitemid 19043371)
6. H17 and regulatory T cells. Nature 2006; 441: 235-8.
7. H-17 cells requires transforming growth factor-β and induction of the nuclear receptor RORγt. Nat Immunol 2008; 9: 641-9. (Pubitemid 351714729)
8. Heinrich PC, Behrmann I, Haan S, Hermanns HM, Muller-Newen G, Schaper F,. Principles of interleukin (IL)-6-type cytokine signalling and its regulation. Biochem J 2003; 374: 1-20. (Pubitemid 37046923)
9. Taga T, Hibi M, Hirata Y, Yamasaki K, Yasukawa K, Matsuda T, et al. Interleukin-6 triggers the association of its receptor with a possible signal transducer, gp130. Cell 1989; 58: 573-81. (Pubitemid 19203542)
10. Wang X, Lupardus P, Laporte SL, Garcia KC,. Structural biology of shared cytokine receptors. Annu Rev Immunol 2009; 27: 29-60.
11. Rose-John S, Scheller J, Elson G, Jones SA,. Interleukin-6 biology is coordinated by membrane-bound and soluble receptors: role in inflammation and cancer. J Leukoc Biol 2006; 80: 227-36. (Pubitemid 44835496)
12. Zohlnhofer D, Graeve L, Rose-John S, Schooltink H, Dittrich E, Heinrich PC,. The hepatic interleukin-6 receptor: down-regulation of the interleukin-6 binding subunit (gp80) by its ligand. FEBS Lett 1992; 306: 219-22.
13. Arnett FC, Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, et al. The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 1988; 31: 315-24. (Pubitemid 18091653)
14. Cooke BM, Usami S, Perry I, Nash GB,. A simplified method for culture of endothelial cells and analysis of adhesion of blood cells under conditions of flow. Microvasc Res 1993; 45: 33-45.
15. Wang Y, Nesbitt JE, Fuentes NL, Fuller GM,. Molecular cloning and characterization of the rat liver IL-6 signal transducing molecule, gp130. Genomics 1992; 14: 666-72.
16. high regulatory T cells. Int Immunol 2006; 18: 555-63.
17. Steiner G, Tohidast-Akrad M, Witzmann G, Vesely M, Studnicka-Benke A, Gal A, et al. Cytokine production by synovial T cells in rheumatoid arthritis. Rheumatology (Oxford) 1999; 38: 202-13. (Pubitemid 29507155)
18. Katsikis PD, Chu CQ, Brennan FM, Maini RN, Feldmann M,. Immunoregulatory role of interleukin 10 in rheumatoid arthritis. J Exp Med 1994; 179: 1517-27. (Pubitemid 24129569)
19. Nishimoto N,. Interleukin-6 in rheumatoid arthritis. Curr Opin Rheumatol 2006; 18: 277-81. (Pubitemid 43740380)
20. Gabay C,. Interleukin-6 and chronic inflammation. Arthritis Res Ther 2006; 8 Suppl 2: S3.
21. H17 cells. J Allergy Clin Immunol 2009; 123: 588-95, 595e1-7.
22. Rochman I, Paul WE, Ben-Sasson SZ,. IL-6 increases primed cell expansion and survival. J Immunol 2005; 174: 4761-7.
23. Keul R, Heinrich PC, Muller-Newen G, Muller K, Woo P,. A possible role for soluble IL-6 receptor in the pathogenesis of systemic onset juvenile chronic arthritis. Cytokine 1998; 10: 729-34. (Pubitemid 28457118)
24. Desgeorges A, Gabay C, Silacci P, Novick D, Roux-Lombard P, Grau G, et al. Concentrations and origins of soluble interleukin 6 receptor-α in serum and synovial fluid. J Rheumatol 1997; 24: 1510-6. (Pubitemid 27320690)
25. Kotake S, Sato K, Kim KJ, Takahashi N, Udagawa N, Nakamura I, et al. Interleukin-6 and soluble interleukin-6 receptors in the synovial fluids from rheumatoid arthritis patients are responsible for osteoclast-like cell formation. J Bone Miner Res 1996; 11: 88-95. (Pubitemid 26026748)
26. Peters M, Blinn G, Solem F, Fischer M, Meyer zum Buschenfelde KH, Rose-John S,. In vivo and in vitro activities of the gp130-stimulating designer cytokine Hyper-IL-6. J Immunol 1998; 161: 3575-81.
27. + T cell IL-6R expression during inflammation underlines a role for IL-6 trans signaling in the local maintenance of Th17 cells. J Immunol 2010; 184: 2130-9.
28. Nowell MA, Williams AS, Carty SA, Scheller J, Hayes AJ, Jones GW, et al. Therapeutic targeting of IL-6 trans signaling counteracts STAT3 control of experimental inflammatory arthritis. J Immunol 2009; 182: 613-22.
29. Narazaki M, Yasukawa K, Saito T, Ohsugi Y, Fukui H, Koishihara Y, et al. Soluble forms of the interleukin-6 signal-transducing receptor component gp130 in human serum possessing a potential to inhibit signals through membrane-anchored gp130. Blood 1993; 82: 1120-6. (Pubitemid 23253984)
30. Richards PJ, Nowell MA, Horiuchi S, McLoughlin RM, Fielding CA, Grau S, et al. Functional characterization of a soluble gp130 isoform and its therapeutic capacity in an experimental model of inflammatory arthritis. Arthritis Rheum 2006; 54: 1662-72.
31. Betz UA, Muller W,. Regulated expression of gp130 and IL-6 receptor α chain in T cell maturation and activation. Int Immunol 1998; 10: 1175-84. (Pubitemid 28362692)
32. Teague TK, Schaefer BC, Hildeman D, Bender J, Mitchell T, Kappler JW, et al. Activation-induced inhibition of interleukin 6-mediated T cell survival and signal transducer and activator of transcription 1 signaling. J Exp Med 2000; 191: 915-26.
33. Tak PP, Hintzen RQ, Teunissen JJ, Smeets TJ, Daha MR, van Lier RA, et al. Expression of the activation antigen CD27 in rheumatoid arthritis. Clin Immunol Immunopathol 1996; 80: 129-38. (Pubitemid 26246979)
34. Isomaki P, Alanara T, Isohanni P, Lagerstedt A, Korpela M, Moilanen T, et al. The expression of SOCS is altered in rheumatoid arthritis. Rheumatology (Oxford) 2007; 46: 1538-46. (Pubitemid 47500566)
35. Salmon M, Scheel-Toellner D, Huissoon AP, Pilling D, Shamsadeen N, Hyde H, et al. Inhibition of T cell apoptosis in the rheumatoid synovium. J Clin Invest 1997; 99: 439-46. (Pubitemid 27414801)
36. Raza K, Scheel-Toellner D, Lee CY, Pilling D, Curnow SJ, Falciani F, et al. Synovial fluid leukocyte apoptosis is inhibited in patients with very early rheumatoid arthritis. Arthritis Res Ther 2006; 8: R120.
37. Pilling D, Akbar AN, Girdlestone J, Orteu CH, Borthwick NJ, Amft N, et al. Interferon-β mediates stromal cell rescue of T cells from apoptosis. Eur J Immunol 1999; 29: 1041-50. (Pubitemid 29119085)
38. McInnes IB, al-Mughales J, Field M, Leung BP, Huang FP, Dixon R, et al. The role of interleukin-15 in T-cell migration and activation in rheumatoid arthritis. Nat Med 1996; 2: 175-82. (Pubitemid 26057554)
39. Mosser DM, Zhang X,. Interleukin-10: new perspectives on an old cytokine. Immunol Rev 2008; 226: 205-18.
40. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM,. B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002; 3: 944-50. (Pubitemid 35154008)
41. Lelievre E, Sarrouilhe D, Morel F, Preud'Homme JL, Wijdenes J, Lecron JC,. Preincubation of human resting T cell clones with interleukin 10 strongly enhances their ability to produce cytokines after stimulation. Cytokine 1998; 10: 831-40. (Pubitemid 29002735)
42. Rousset F, Garcia E, Defrance T, Peronne C, Vezzio N, Hsu DH, et al. Interleukin 10 is a potent growth and differentiation factor for activated human B lymphocytes. Proc Natl Acad Sci U S A 1992; 89: 1890-3.
43. Van Roon J, Wijngaarden S, Lafeber FP, Damen C, van de Winkel J, Bijlsma JW,. Interleukin 10 treatment of patients with rheumatoid arthritis enhances Fcγ receptor expression on monocytes and responsiveness to immune complex stimulation. J Rheumatol 2003; 30: 648-51. (Pubitemid 36402754)
44. Kirkham BW, Lassere MN, Edmonds JP, Juhasz KM, Bird PA, Lee CS, et al. Synovial membrane cytokine expression is predictive of joint damage progression in rheumatoid arthritis: a two-year prospective study (the DAMAGE study cohort). Arthritis Rheum 2006; 54: 1122-31. (Pubitemid 43672925)
45. Lard LR, van Gaalen FA, Schonkeren JJ, Pieterman EJ, Stoeken G, Vos K, et al. Association of the -2849 interleukin-10 promoter polymorphism with autoantibody production and joint destruction in rheumatoid arthritis. Arthritis Rheum 2003; 48: 1841-8. (Pubitemid 36828678)