Synovial fluid-derived T helper 17 cells correlate with inflammatory activity in arthritis, irrespectively of diagnosis

Clinical Immunology

Volumn 138, Issue 1, 2011, Pages 107-116

  Zizzo, Gaetano ^a   De Santis, Maria ^a   Bosello, Silvia Laura ^a   Fedele, Anna Laura ^a   Peluso, Giusy ^a   Gremese, Elisa ^a   Tolusso, Barbara ^a   Ferraccioli, GianFranco ^a  

^a CATHOLIC UNIVERSITY   (Italy)

Author keywords

Arthritis; Disease activity; Inflammation; Microcrystal; TCR zeta; Th1; Th17; ZAP 70

Indexed keywords

C REACTIVE PROTEIN; FIBRINOGEN; INTERLEUKIN 17; PROTEIN KINASE ZAP 70; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR ZETA CHAIN; UNCLASSIFIED DRUG;

ADULT; AGED; ARTHRITIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; ERYTHROCYTE SEDIMENTATION RATE; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; LEUKOCYTE COUNT; LYMPHOCYTE; MALE; MICROCRYSTAL ARTHRITIS; NEUTROPHIL; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RHEUMATOID ARTHRITIS; SPONDYLOARTHRITIS; SYNOVIAL FLUID; TH1 CELL; TH17 CELL;

ADULT; AGED; AGED, 80 AND OVER; ARTHRITIS; BLOOD CELLS; BLOOD SEDIMENTATION; C-REACTIVE PROTEIN; CELL COUNT; FEMALE; FIBRINOGEN; HUMANS; INFLAMMATION; INTERFERON-GAMMA; LEUKOCYTES; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; MALE; MIDDLE AGED; MONOCYTES; NEUTROPHILS; RECEPTORS, ANTIGEN, T-CELL; SYNOVIAL FLUID; TH1 CELLS; TH17 CELLS; ZAP-70 PROTEIN-TYROSINE KINASE;

EID: 78651371338     PISSN: 15216616     EISSN: 15217035     Source Type: Journal    
DOI: 10.1016/j.clim.2010.10.002     Document Type: Article

References (52)

1. Park H., Li Z., Yang X.O., Chang S.H., Nurieva R., Wang Y.H., Wang Y., Hood L., Zhu Z., Tian Q., Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 2005, 6:1133-1141.
2. Harrington L.E., Hatton R.D., Mangan P.R., Turner H., Murphy T.L., Murphy K.M., Weaver C.T. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 2005, 6:1123-1132.
3. Wilson N.J., Boniface K., Chan J.R., McKenzie B.S., Blumenschein W.M., Mattson J.D., Basham B., Smith K., Chen T., Morel F., Lecron J.C., Kastelein R.A., Cua D.J., McClanahan T.K., Bowman E.P., de Waal Malefyt R. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 2007, 8:950-957.
4. Chung D.R., Kasper D.L., Panzo R.J., Chitnis T., Grusby M.J., Sayegh M.H., Tzianabos A.O. CD4+ T cells mediate abscess formation in intra-abdominal sepsis by an IL-17-dependent mechanism. J. Immunol. 2003, 170:1958-1963.
5. Infante-Duarte C., Horton H.F., Byrne M.C., Kamradt T. Microbial lipopeptides induce the production of IL-17 in Th cells. J. Immunol. 2000, 165:6107-6115.
6. Khader S.A., Gaffen S.L., Kolls J.K. Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol. 2009, 2:403-411.
7. Huang S.H., Frydas S., Kempuraj D., Barbacane R.C., Grilli A., Boucher W., Letourneau R., Madhappan B., Papadopoulou N., Verna N., De Lutiis M.A., Iezzi T., Riccioni G., Theoharides T.C., Conti P. Interleukin-17 and the interleukin-17 family member network. Allergy Asthma Proc. 2004, 25:17-21.
8. Chabaud M., Fossiez F., Taupin J.L., Miossec P. Enhancing effect of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor production by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines. J. Immunol. 1998, 161:409-414.
9. Kirkham B.W., Lassere M.N., Edmonds J.P., Juhasz K.M., Bird P.A., Lee C.S., Shnier R., Portek I.J. 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, 54:1122-1131.
10. Matusevicius D., Kivisäkk P., He B., Kostulas N., Ozenci V., Fredrikson S., Link H. Interleukin-17 mRNA expression in blood and CSF mononuclear cells is augmented in multiple sclerosis. Mult. Scler. 1999, 5:101-104.
11. Krueger G.G., Langley R.G., Leonardi C., Yeilding N., Guzzo C., Wang Y., Dooley L.T., Lebwohl M. CNTO 1275 Psoriasis Study Group, A human interleukin-12/23 monoclonal antibody for the treatment of psoriasis. N Engl J. Med. 2007, 356:580-592.
12. Annunziato F., Cosmi L., Santarlasci V., Maggi L., Liotta F., Mazzinghi B., Parente E., FilÌ 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.
13. Molet S., Hamid Q., Davoine F., Nutku E., Taha R., Pagé N., Olivenstein R., Elias J., Chakir J. IL-17 is increased in asthmatic airways and induces human bronchial fibroblasts to produce cytokines. J. Allergy Clin. Immunol. 2001, 108:430-438.
14. Mosmann T.R., Coffman R.L. TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Ann. Rev. Immunol. 1989, 7:145-173.
15. Murphy C.A., Langrish C.L., Chen Y., Blumenschein W., McClanahan T., Kastelein R.A., Sedgwick J.D., Cua D.J. Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 2003, 198:1951-1957.
16. Kelchtermans H., Schurgers E., Geboes L., Mitera T., Van Damme J., Van Snick J., Uyttenhove C., Matthys P. Effector mechanisms of interleukin-17 in collagen induced arthritis in the absence of interferon-gamma and counteraction by interferon-gamma. Arthritis Res. Ther. 2009, 11:R122.
17. Toh M.L., Kawashima M., Zrioual S., Hot A., Miossec P. IL-17 inhibits human Th1 differentiation through IL-12R beta 2 downregulation. Cytokine 2009, 48:226-230.
18. Chu C.Q., Swart D., Alcorn D., Tocker J., Elkon K.B. Interferon-gamma regulates susceptibility to collagen-induced arthritis through suppression of interleukin-17. Arthritis Rheum. 2007, 56:1145-1151.
19. Aarvak T., Chabaud M., Miossec P., Natvig J.B. IL-17 is produced by some proinflammatory Th1/Th0 cells but not by Th2 cells. J. Immunol. 1999, 162:1246-1251.
20. 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.
21. Hirota K., Hashimoto M., Yoshitomi H., Tanaka S., Nomura T., Yamaguchi T., Iwakura Y., Sakaguchi N., Sakaguchi S. T cell self-reactivity forms a cytokine milieu for spontaneous development of IL-17+ Th cells that cause autoimmune arthritis. J. Exp. Med. 2007, 204:41-47.
22. Koenders M.I., Kolls J.K., Oppers-Walgreen B., van den Bersselaar L., Joosten L.A., Schurr J.R., Schwarzenberger P., van den Berg W.B., Lubberts E. IL-17 receptor deficiency results in impaired synovial expression of IL-1 and matrix metalloproteinases 3, 9, and 13 and prevents cartilage destruction during chronic reactivated streptococcal cell wall induced arthritis. Arthritis Rheum. 2005, 52:3239-3247.
23. Kotake S., Udagawa N., Takahashi N., Matsuzaki K., Itoh K., Ishiyama S., Saito S., Inoue K., Kamatani N., Gillespie M.T., Martin T.J., Suda T. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J. Clin. Invest. 1999, 103:1345-1352.
24. Chabaud M., Durand J.M., Buchs N., Fossiez F., Page G., Frappart L., Miossec P. IL-17: a T cell-derived proinflammatory cytokine produced by the rheumatoid synovium. Arthritis Rheum. 1999, 42:963-970.
25. Cua D.J., Sherlock J., Chen Y., Murphy C.A., Joyce B., Seymour B., Lucian L., To W., Kwan S., Churakova T., Zurawski S., Wiekowski M., Lira S.A., Gorman D., Kastelein R.A., Sedgwick J.D. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 2003, 421:744-748.
26. Yen D., Cheung J., Scheerens H., Poulet F., McClanahan T., McKenzie B., Kleinschek M.A., Owyang A., Mattson J., Blumenschein W., Murphy E., Sathe M., Cua D.J., Kastelein R.A., Rennick D. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 2006, 116:1310-1316.
27. Zheng Y., Danilenko D.M., Valdez P., Kasman I., Eastham-Anderson J., Wu J., Ouyang W. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 2007, 445:648-651.
28. Sharara S., Huang Q., Mandelin A.M., Pope R.M. TH-17 cells in rheumatoid arthritis. Arthritis Res. Ther. 2008, 10:R93.
29. Agarwal S., Misra R., Aggarwal A. Interleukin 17 levels are increased in juvenile idiopathic arthritis synovial fluid and induce synovial fibroblasts to produce proinflammatory cytokines and matrix metalloproteinases. J. Rheumatol. 2008, 35:515-519.
30. Peck A., Mellins E.D. Breaking old paradigms: Th17 cells in autoimmune arthritis. Clin. Immunol. 2009, 132:295-304.
31. Yamada H., Nakashima Y., Okazaki K., Mawatari T., Fukushi J.I., Kaibara N., Hori A., Iwamoto Y., Yoshikai Y. Th1 but not Th17 cells predominate in the joints of patients with rheumatoid arthritis. Ann. Rheum. Dis. 2008, 67:1299-1304.
32. Kohno M., Tsutsumi A., Matsui H., Sugihara M., Suzuki T., Mamura M., Goto D., Matsumoto I., Ito S., Suguro T., Sumida T. IL-17 gene expression in patients with rheumatoid arthritis. Rheumatology 2008, 18:15-22.
33. Shen H., Goodall J.C., Hill Gaston J.S. Frequency and phenotype of peripheral blood Th17 cells in ankylosing spondylitis and rheumatoid arthritis. Arthritis Rheum. 2009, 60:1647-1656.
34. Jandus C., Bioley G., Rivals J.P., 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.
35. Singh R., Aggarwal A., Misra R. Th1/Th17 cytokine profiles in patients with reactive arthritis/undifferentiated spondyloarthropathy. J. Rheumatol. 2007, 34:2285-2290.
36. Kageyama Y., Ichikawa T., Nagafusa T., Torikai E., Shimazu M., Nagano A. Etanercept reduces the serum levels of interleukin-23 and macrophage inflammatory protein-3 alpha in patients with rheumatoid arthritis. Rheumatol. Int. 2007, 28:137-143.
37. Zhang Z., Gorman C.L., Vermi A.C., Monaco C., Foey A., Owen S., Amjadi P., Vallance A., McClinton C., Marelli-Berg F., Isomäki P., Russell A., Dazzi F., Vyse T.J., Brennan F.M., Cope A.P. TCRzetadim lymphocytes define populations of circulating effector cells that migrate to inflamed tissues. Blood 2007, 109:4328-4335.
38. Berg L., Rönnelid J., Klareskog L., Bucht A. Down-regulation of the T cell receptor CD3 zeta chain in rheumatoid arthritis (RA) and its influence on T cell responsiveness. Clin. Exp. Immunol. 2000, 120:174-182.
39. Maurice M.M., Lankester A.C., Bezemer A.C., Geertsma M.F., Tak P.P., Breedveld F.C., van Lier R.A., Verweij C.L. Defective TCR-mediated signaling in synovial T cells in rheumatoid arthritis. J. Immunol. 1997, 159:2973-2978.
40. Sakaguchi N., Takahashi T., Hata H., Nomura T., Tagami T., Yamazaki S., Sakihama T., Matsutani T., Negishi I., Nakatsuru S., Sakaguchi S. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 2003, 426:454-460.
41. Siggs O.M., Miosge L.A., Yates A.L., Kucharska E.M., Sheahan D., Brdicka T., Weiss A., Liston A., Goodnow C.C. Opposing functions of the T cell receptor kinase ZAP-70 in immunity and tolerance differentially titrate in response to nucleotide substitutions. Immunity 2007, 27:912-926.
42. Liu-Bryan R., Scott P., Sydlaske A., Rose D.M., Terkeltaub R. Innate immunity conferred by Toll-like receptors 2 and 4 and myeloid differentiation factor 88 expression is pivotal to monosodium urate monohydrate crystal-induced inflammation. Arthritis Rheum. 2005, 52:2936-2946.
43. Martinon F., Pétrilli V., Mayor A., Tardivel A., Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006, 440:237-241.
44. Webb R., Jeffries M., Sawalha A.H. Uric acid directly promotes human T-cell activation. Am. J. Med. Sci. 2009, 337:23-27.
45. Acosta-Rodriguez E.V., Napolitani G., Lanzavecchia A., Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 2007, 8:942-949.
46. Lubberts E., Joosten L.A., Oppers B., van den Bersselaar L., Coenen-de Roo C.J., Kolls J.K., Schwarzenberger P., van de Loo F.A., van den Berg W.B. IL-1-independent role of IL-17 in synovial inflammation and joint destruction during collagen-induced arthritis. J. Immunol. 2001, 167:1004-1013.
47. Lemos H.P., Grespen R., Vieira S.M., Cunha T.M., Verri W.A., Fernandes K.S., Souto F.O., McInnes I.B., Ferreira S.H., Liew F.Y., Cunha F.Q. Prostaglandin mediates IL-23/IL-17-induced neutrophil migration in inflammation by inhibiting IL-12 and IFNgamma production. Proc. Natl Acad. Sci. USA 2009, 106:5954-5959.
48. Eklund C.M. Proinflammatory cytokines in CRP baseline regulation. Adv. Clin. Chem. 2009, 48:111-136.
49. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 cells. Ann. Rev. Immunol. 2009, 27:485-517.
50. Ziolkowska M., Koc A., Luszczykiewicz G., Ksiezopolska-Pietrzak K., Klimczak E., Chwalinska-Sadowska H., Maslinski W. High levels of IL-17 in rheumatoid arthritis patients: IL-15 triggers in vitro IL-17 production via cyclosporin A-sensitive mechanism. J. Immunol. 2000, 164:2832-2838.
51. Rostaining L., Tkaczuk J., Durand M., Peres C., Durand D., de Préval C., Ohayon E., Abbal M. Kinetics of intracytoplasmic Th1 and Th2 cytokine production assessed by flow cytometry following in vitro activation of peripheral blood mononuclear cells. Cytometry 1999, 35:318-328.
52. Picard C., Dogniaux S., Chemin K., Maciorowski Z., Lim A., Mazerolles F., Rieux-Laucat F., Stolzenberg M.C., Debre M., Magny J.P., Le Deist F., Fischer A., Hivroz C. Hypomorphic mutation of ZAP70 in human results in a late onset immunodeficiency and no autoimmunity. Eur. J. Immunol. 2009, 39:1966-1976.