The associations of circulating CD4⁺CD25^high regulatory T cells and TGF-β with disease activity and clinical course in patients with adult-onset Still's disease

REFERENCES

• Sakaguchi, S. (2004). Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22:531–562.
   PubMed Web of Science ®Google Scholar
• Shevach, E.M., McHugh, R.S., Piccirillo, C.A., and Thornton, A.M. (2001). Control of T-cell activation by CD4+CD25+ suppressor T cells. Immunol. Rev. 182:58–67.
   PubMed Web of Science ®Google Scholar
• Jonuleit, H., Schmitt, E., Stassen, M., Tuettenberg, A., Knop, J., and Enk, A.H. (2001). Identification and functional characterization of human CD4+CD25+ T cells with regulatory properties isolated from peripheral blood. J. Exp. Med. 193:1285–1294.
   PubMed Web of Science ®Google Scholar
• Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M., and Toda, M. (1995). Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155:1151–1164.
   PubMed Web of Science ®Google Scholar
• Nakamura, K., Kitani, A., and Strober, W. (2001). Cell contact-dependent immunosuppression of CD4+CD25+ regulatory T cells is mediated by cell surface-bound transforming growth factor-β. J. Exp. Med. 194:629–644.
   PubMed Web of Science ®Google Scholar
• Zheng, S.G., Wang, J.H., Gray, J.D., Soucier, H., and Horwitz, D.A. (2004). Natural and induced CD4+CD25+ cells educate CD4+CD25− cells to develop suppressive activity: The role of IL-2, TGF-β, and IL-10. J. Immunol. 172:5213–5221.
   PubMed Web of Science ®Google Scholar
• Marie, J.C., Letterio, J.J., Gavin, M., and Rudensky, A.Y. (2005). TGF-β1 maintains suppressor function and FoxP3 expression in CD4+CD25+ regulatory T cells. J. Exp. Med. 201:1061–1067.
   PubMed Web of Science ®Google Scholar
• Baecher-Alllan, C., Brown, J.A., Freeman, G.J., and Hafler, D.A. (2001). CD4+CD25high regulatory cells in human peripheral blood. J. Immunol. 167:1245–1253.
   PubMed Web of Science ®Google Scholar
• Cao, D., Malmstrom, V., Baecher-Allan, C., Hafler, D., Klareskog, L., and Trollmo, C. (2003). Isolation and functional characterization of regulatory CD25 bright CD4+ T cells from the target organ of patients with rheumatoid arthritis. Eur. J. Immunol. 33:215–223.
   PubMed Web of Science ®Google Scholar
• Möttönen, M., Heikkinen, J., Mustonen, L., Isomäki, P., Luukkainen, R., and Lassila, O. (2005). CD4+CD25+ T cells with the phenotypic and functional characteristics of regulatory T cells are enriched in the synovial fluid of patients with rheumatoid arthritis. Clin. Exp. Immunol. 140:360–367.
   PubMed Web of Science ®Google Scholar
• Wildin, R.S., Ramsdell, F., Peake, J., Faravelli, F., Casanova, J.L., Buist, N., Levy-Lahad, E., Mazzella, M., Goulet, O., Perroni, L., Bricarelli, F.D., Byrne, G., McEuen, M., Proll, S., Appleby, M., and Brunkow, M.E. (2001). X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat. Genet. 27:18–20.
   PubMed Web of Science ®Google Scholar
• Loughry, A., Fairchild, S., Athanasou, N., Edwards, J., and Hall, F.C. (2005). Inflammatory arthritis and dermatitis in thymectomized, CD25+ cell-depleted adult mice. Rheumatology (Oxford) 44:299–308.
   PubMed Web of Science ®Google Scholar
• Morgan, M.E., Sutmuller, R.P., Witteveen, H.J., van Duivenvoorde, L.M., Zanelli, E., Melief, C.J., Snijders, A., Offringa, R., de Vries, R.R., and Toes, R.E. (2003). CD25+ cell depletion hastens the onset of severe disease in collagen-induced arthritis. Arthritis Rheum. 48:1452–1460.
   PubMed Web of Science ®Google Scholar
• Frey, O., Petrow, P.K., Gajda, M., Siegmund, K., Huehn, J., Scheffold, A., Hamann, A., Radbruch, A., and Bräuer, R. (2005). The role of regulatory T cells in antigen-induced arthritis: Aggravation of arthritis after depletion and amelioration after transfer of CD4+CD25+ T cells. Arthritis Res. Ther. 7:294–301.
   Google Scholar
• Randolph, D.A., and Fathman, C.G. (2006). CD4+CD25+ regulatory T cells and their therapeutic potential [review]. Annu. Rev. Med. 57:381–402.
   PubMed Web of Science ®Google Scholar
• Bywaters, E.G.L. (1971). Still's disease of the adults. Ann. Rheum. Dis. 30:121–133.
   PubMed Web of Science ®Google Scholar
• Ohta, A., Yamaguchi, M., Kaneoka, H., Nagayoshi, T., and Hiida, M. (1987). Adult Still's disease: Review of 228 cases from the literature. J. Rheumatol. 14:1139–1146.
   PubMed Web of Science ®Google Scholar
• Chen, D.Y., Lan, J.L., Lin, F.J., Hsieh, T.Y., and Wen, M.C. (2004). A predominance of Th1 cytokine in peripheral blood and pathological tissues of patients with active untreated adult-onset Still's disease. Ann. Rheum. Dis. 63:1300–1306.
   PubMed Web of Science ®Google Scholar
• Kawashima, M., Yamamura, M., Taniai, M., Yamauchi, H., Tanimoto, T., Kurimoto, M., Miyawaki, S., Amano, T., Takeuchi, T., and Makino, H. (2001). Levels of interleukin-18 and its binding inhibitors in the blood circulation of patients with adult-onset Still's disease. Arthritis Rheum. 44:550–560.
   PubMed Web of Science ®Google Scholar
• Choi, J.H., Suh, C.H., Lee, Y.M., Suh, Y.J., Lee, S.K., Kim, S.S., Nahm, D.H., and Park, H.S. (2003). Serum cytokine profiles in patients with adult onset Still's disease. J. Rheumatol. 30:2422–2427.
   PubMed Web of Science ®Google Scholar
• Pouchot, J., Sampalis, J.S., Beaudet, F., Carette, S., Decary, F., Salusinsky-Sternbach, M., Hill, R.O., Gutkowski, A., Harth, M., and Myhal, D. (1991). Adult Still's disease: Manifestations, disease course, and outcome in 62 patients. Medicine 70:118–136.
   PubMed Web of Science ®Google Scholar
• Cush, J.J., Medsger, T.A., Christy, W.C., Herbert, D.C., and Cooperstein, L.A. (1987). Adult-onset Still's disease: Clinical course and outcome. Arthritis Rheum. 30:186–194.
   PubMed Web of Science ®Google Scholar
• Liu, M.F., Wang, C.R., Fung, L.L., and Wu, C.R. (2004). Decreased CD+CD25 T cells in peripheral blood of patients with systemic lupus erythematosus. Scand. J. Immunol. 59:198–202.
   PubMed Web of Science ®Google Scholar
• Crispin, J.C., Martinez, A., and Alcocer-Varela, J. (2003). Quantification of regulatory T cells in patients with systemic lupus erythematosus. J. Autoimmun. 21:273–276.
   PubMed Web of Science ®Google Scholar
• Mellor-Pita, S., Citores, M.J., Castejon, R., Tutor-Ureta, P., Yebra-Bango, M., Andreu, J.L., and Vargas, J.A. (2006). Decrease of regulatory T cells in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 65:553–554.
   PubMed Web of Science ®Google Scholar
• Lee, J.H., Wang, L.C., Lin, Y.T., Yang, Y.H., Lin, D.T., and Chiang, B.L. (2006). Inverse correlation between CD4+ regulatory T-cell population and autoantibody levels in paediatric patients with systemic lupus erythematosus. Immunology 117:280–286.
   PubMed Web of Science ®Google Scholar
• Valencia, X., Yarboro, C., Illei, G., and Lipsky, P.E. (2007). Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus. J. Immunol. 178:2579–2588.
   PubMed Web of Science ®Google Scholar
• Yamaguchi, M., Ohta, A., Tsunematsu, T., Kasukawa, R., Mizushima, Y., Kashiwagi, S., Kashiwazaki, S., Tanimoto, K., Matsumoto, Y., and Ota, T. (1992). Preliminary criteria for classification of adult Still's disease. J. Rheumatol. 19:424–430.
   PubMed Web of Science ®Google Scholar
• Hochberg, M.C. (1997). Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40:1725.
   PubMed Web of Science ®Google Scholar
• Bombaridier, C., Gladman, D.D., Urowitz, M.B., Caron, D., and Chang, C.H. (1992). The committee on prognosis studies in SLE. Derivation of the SLEDAI: A disease activity index for lupus patients. Arthritis Rheum. 35:630–640.
   PubMedGoogle Scholar
• Isenberg, D.A., Rahman, A., Allen, E., Farewell, V., Akil, M., Bruce, I.N., D'Cruz, D., Griffiths, B., Khamashta, M.A., Maddison, P., McHugh, N., Snaith, M., The, L.S., Yee, C.S., Zoma, A., and Gordon, C. (2005) BILAG 2004: Development and initial validation of an updated version of the British Isles Lupus Assessment Group's disease activity index for patients with systemic lupus erythematosus. Rheumatology (Oxford) 44:902–906.
   PubMed Web of Science ®Google Scholar
• Yee, C.S., Farewell, V., Isenberg, D.A., Rahman, A., Teh, L.S., Griffiths, B., Bruce, I.N., Ahmad, Y., Prabu, A., Akil, M., McHugh, N., D'Cruz, D., Khamashta, M.A., Maddison, P., and Gordon, C. (2007). British Isles Lupus Assessment Group 2004 index is valid for assessment of disease activity in systemic lupus erythematosus. Arthritis Rheum. 56:4113–4119.
   PubMed Web of Science ®Google Scholar
• Cao, D., van Vollenhoven, R., Klareskog, L., Trollmo, C., and Malmstrom, V. (2004). CD25brightCD4+ regulatory T cells are enriched in inflamed joints of patients with chronic rheumatic disease. Arthritis Res. Ther. 6:335–346.
   PubMed Web of Science ®Google Scholar
• Miyara, M., Amoura, Z., Parizot, C., Badoual, C., Dorgham, K., Trad, S., Nochy, D., Debré, P., Piette, J.C., and Gorochov, G. (2005). Global natural regulatory T cell depletion in active systemic lupus erythematosus. J. Immunol. 175:8392–8400.
   PubMed Web of Science ®Google Scholar
• Bonelli, M., von Dalwigk, K., Savitskaya, A., Smolen, J.S., and Scheinecker, C. (2008). Foxp3 expression in CD4+ T cells of patients with systemic lupus erythematosus: A comparative phenotypic analysis. Ann. Rheum. Dis. 67:664–671.
   PubMed Web of Science ®Google Scholar
• Ehrenstein, M.R., Evans, J.G., Singh, A., Moore, S., Warnes, G., Isenberg, D.A., and Mauri, C. (2004). Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNF alpha therapy. J. Exp. Med. 200:277–285.
   PubMed Web of Science ®Google Scholar
• Chen, X., Oppenheim, J.J., Winkler-Pickett, R.T., Ortaldo, J.R., and Howard, O.M.Z. (2006). Glucocorticoid amplifies IL-2-dependent expansion of functional FoxP3+CD4+CD25+ T regulatory cells in vivo and enhances their capacity to suppress EAE. Eur. J. Immunol. 36:2139–2149.
   PubMed Web of Science ®Google Scholar
• Navarro, J., Aristimuño, C., Sánchez-Ramón, S., Vigil, D., Martínez-Ginés, M.L., Fernández-Cruz, E., and de Andrés, C. (2006). Circulating dendritic cells subsets and regulatory T‐cells at multiple sclerosis relapse: Differential short-term changes on corticosteroids therapy. J. Neuroimmunol. 176:153–161.
   PubMed Web of Science ®Google Scholar
• Gorelik, L., and Flavell, R.A. (2002). Transforming growth factor-beta in T-cell biology. Nat. Rev. Immunol. 2:46–53.
   PubMed Web of Science ®Google Scholar
• Gorelik, L., and Flavell, R.A. (2000). Abrogation of TGF beta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12:171–181.
   PubMed Web of Science ®Google Scholar
• Liu, H., Hu, B., Xu, D., and Liew, F.Y. (2003). CD4+CD25+ regulatory T cells cure murine colitis: The role of IL-10, TGF-beta, and CTLA4. J. Immunol. 171:5012–5017.
   PubMed Web of Science ®Google Scholar
• Chen, Y., Kuchroo, V.K., Inobe, J., Hafler, D.A., and Weiner, H.L. (1994). Regulatory T cell clones induced by oral tolerance: Suppression of autoimmune encephalomyelitis. Science 265:1237–1240.
   PubMed Web of Science ®Google Scholar
• Rao, P.E., Petrone, A.L., and Ponath, P.D. (2005). Differentiation and expansion of T cells with regulatory function from human peripheral lymphocytes by stimulation in the presence of TGF-β. J. Immunol. 174:1446–1455.
   PubMed Web of Science ®Google Scholar
• Yamagiwa, S., Gray, J.D., Hashimoto, S., and Horwitz, D.A. (2001). A role for TGF-β in generation and expansion of CD4+CD25+ regulatory T cells form human peripheral blood. J. Immunol. 166:7282–7289.
   PubMed Web of Science ®Google Scholar
• Levings, M.K., Sangregorio, R., Sartirana, C., Moschin, A.L., Battaglia, M., Orban, P.C., and Roncarolo, M.G. (2002). Human CD25+CD4+ T suppressor cell clones produce transforming growth factor β, but not interleukin-10, and are distinct from type 1 T regulatory cells. J. Exp. Med. 196:1335–1346.
   PubMed Web of Science ®Google Scholar
• De Kleer, I.M., Wedderburn, L.R., Taams, L.S., Patel, A., Varsani, H., Klein, M., de Jager, W., Pugayung, G., Giannoni, F., Rijkers, G., Albani, S., Kuis, W., and Prakken, B. (2004). CD4+CD25bright regulatory T cells actively regulate inflammation in the joints of patients with the remitting form of juvenile idiopathic arthritis. J. Immunol. 172:6435–6443.
   PubMed Web of Science ®Google Scholar
• Lawson, C.A., Brown, A.K., Bejarano, V., Douglas, S.H., Burgoyne, C.H., Greenstein, A.S., Boylston, A.W., Emery, P., Ponchel, F., and Isaacs, J.D. (2006) Early rheumatoid arthritis is associated with a deficit in the CD4+CD25high regulatory T cell population in peripheral blood. Rheumatology 45:1210–1217.
   PubMed Web of Science ®Google Scholar
• Appel, H., Neure, L., Kuhne, M., Braun, J., Rudwaleit, M., and Sieper, J. (2004). An elevated level of IL-10- and TGF-β-secreting T cells, B cells and macrophages in the synovial membrane of patients with reactive arthritis compared to rheumatoid arthritis. Clin. Rheumatol. 23:435–440.
   PubMed Web of Science ®Google Scholar
• Sharabi, A., Zinger, H., Zborowsky, M., Sthoeger, Z.M., and Mozes, E. (2006). A peptide based on the complementarity-determining region 1 of an autoantibody ameliorates lupus by up-regulating CD4+CD25+ regulatory cells and TGF-β. Proc. Natl. Acad. Sci. U.S.A. 103:8810–8815.
   PubMed Web of Science ®Google Scholar
• Hahn, B.H., Anderson, M., Le, E., and Cava, A.L. (2008). Anti-DNA Ig peptides promote Treg cell activitity in systemic lupus erythematosus. Arthritis Rheum. 58:2488–2497.
   PubMed Web of Science ®Google Scholar
• Nadkarni, S., Mauri, C., and Ehrenstein, M.R. (2007). Anti-TNF-α therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-β. J. Exp. Med. 204:33–39.
   PubMed Web of Science ®Google Scholar
• Sakaguchi, S. (2005). Naturally arising Foxp3-expressing CD4+CD25+ regulatory T cells in immunological tolerance to self and non-self [review]. Nat. Immunol. 6:345–352.
   PubMed Web of Science ®Google Scholar
• Hori, S., Nomura, T., and Sakaguchi, S. (2003). Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057.
   PubMed Web of Science ®Google Scholar