Systemic lupus erythematosus exhibits a dynamic and continuum spectrum of effector/regulatory T cells

References

• Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. 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 1995;155:1151–64.
   PubMed Web of Science ®Google Scholar
• Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA. CD4+CD25high regulatory cells in human peripheral blood. J Immunol 2001;167:1245–53.
   PubMed Web of Science ®Google Scholar
• Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057–61.
   PubMed Web of Science ®Google Scholar
• Cao D, van Vollenhoven R, Klareskog L, Trollmo C, Malmstrom V. CD25brightCD4+ regulatory T cells are enriched in inflamed joints of patients with chronic rheumatic disease. Arthritis Res Ther 2004;6:335–46.
   PubMed Web of Science ®Google Scholar
• Liu W, Putnam AL, Xu-Yu Z, Szot GL, Lee MR, Zhu S, CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J Exp Med 2006;203:1701–11.
   PubMed Web of Science ®Google Scholar
• Seddiki N, Santner-Nanan B, Martinson J, Zaunders J, Sasson S, Landay A, Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells. J Exp Med 2006;203:1693–700.
   PubMed Web of Science ®Google Scholar
• Hartigan-O'Connor DJ, Poon C, Sinclair E, McCune JM. Human CD4+ regulatory T cells express lower levels of the IL-7 receptor alpha chain (CD127), allowing consistent identification and sorting of live cells. J Immunol Methods 2007;319:41–52.
   PubMed Web of Science ®Google Scholar
• Crispin JC, Martinez A, Alcocer-Varela J. Quantification of regulatory T cells in patients with systemic lupus erythematosus. J Autoimmun 2003;21:273–6.
   PubMed Web of Science ®Google Scholar
• Liu MF, Wang CR, Fung LL, Wu CR. Decreased CD4+CD25+ T cells in peripheral blood of patients with systemic lupus erythematosus. Scand J Immunol 2004;59:198–202.
   PubMed Web of Science ®Google Scholar
• Miyara M, Amoura Z, Parizot C, Badoual C, Dorgham K, Trad S, Global natural regulatory T cell depletion in active systemic lupus erythematosus. J Immunol 2005;175:8392–400.
   PubMed Web of Science ®Google Scholar
• Mellor-Pita S, Citores MJ, Castejon R, Tutor-Ureta P, Yebra-Bango M, Andreu JL, Decrease of regulatory T cells in patients with systemic lupus erythematosus. Ann Rheum Dis 2006;65:553–4.
   PubMed Web of Science ®Google Scholar
• HY, Hong YK, Yun HJ, Kim YM, Kim JR, Yoo WH. Altered frequency and migration capacity of CD4+CD25+ regulatory T cells in systemic lupus erythematosus. Rheumatology (Oxford) 2008;47:789–94.
   PubMedGoogle Scholar
• Suarez A, Lopez P, Gomez J, Gutierrez C. Enrichment of CD4+ CD25high T cell population in patients with systemic lupus erythematosus treated with glucocorticoids. Ann Rheum Dis 2006;65:1512–17.
   PubMed Web of Science ®Google Scholar
• Sanchez B, Castro B, Perez, Baranda L, Espinosa E, Mendoza C, Regulatory T cells in patients with systemic lupus erythematosus. J Autoimmun 2006;27:110–18.
   PubMedGoogle Scholar
• Tsutsumi Y, Jie X, Ihara K, Nomura A, Kanemitsu S, Takada H, Phenotypic and genetic analyses of T-cell-mediated immunoregulation in patients with Type 1 diabetes. Diabet Med 2006;23:1145–50.
   PubMed Web of Science ®Google Scholar
• Valencia X, Yarboro C, Illei G, Lipsky PE. Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus. J Immunol 2007;178:2579–88.
   PubMed Web of Science ®Google Scholar
• Barath S, Aleksza M, Tarr T, Sipka S, Szegedi G, Kiss E. Measurement of natural (CD4+CD25high) and inducible (CD4+IL-10+) regulatory T cells in patients with systemic lupus erythematosus. Lupus 2007;16:489–96.
   PubMed Web of Science ®Google Scholar
• Lin SC, Chen KH, Lin CH, Kuo CC, Ling QD, Chan CH. The quantitative analysis of peripheral blood FOXP3-expressing T cells in systemic lupus erythematosus and rheumatoid arthritis patients. Eur J Clin Invest 2007;37:987–96.
   PubMed Web of Science ®Google Scholar
• Franz B, Fritzsching B, Riehl A, Oberle N, Klemke CD, Sykora J, Low number of regulatory T cells in skin lesions of patients with cutaneous lupus erythematosus. Arthritis Rheum 2007;56:1910–20.
   PubMed Web of Science ®Google Scholar
• Bonelli M, Savitskaya A, von Dalwigk K, Steiner CW, Aletaha D, Smolen JS, Foxp3 expression in CD4+ T cells of patients with systemic lupus erythematosus: a comparative phenotypic analysis. Ann Rheum Dis 2008;67:664–71.
   PubMed Web of Science ®Google Scholar
• Zhang B, Zhang X, Tang FL, Zhu LP, Liu Y, Lipsky PE. Clinical significance of increased CD4+CD25–Foxp3+ T cells in patients with new-onset systemic lupus erythematosus. Ann Rheum Dis 2008;67:1037–40.
   PubMed Web of Science ®Google Scholar
• Lee HY, Hong YK, Yun HJ, Kim YM, Kim JR, Yoo WH. Altered frequency and migration capacity of CD4+CD25+ regulatory T cells in systemic lupus erythematosus. Rheumatology (Oxford) 2008;47:789–94.
   PubMedGoogle Scholar
• Yan B, Ye S, Chen G, Kuang M, Shen N, Chen S. Dysfunctional CD4+,CD25+ regulatory T cells in untreated active systemic lupus erythematosus secondary to interferon-alpha-producing antigen-presenting cells. Arthritis Rheum 2008;58:801–12.
   PubMed Web of Science ®Google Scholar
• Zhang B, Zhang X, Tang F, Zhu L, Liu Y. Reduction of forkhead box P3 levels in CD4+CD25high T cells in patients with new-onset systemic lupus erythematosus. Clin Exp Immunol 2008;153:182–7.
   PubMedGoogle Scholar
• Azab NA, Bassyouni IH, Emad Y, Abd El-Wahab GA, Hamdy G, Mashahit MA. CD4+CD25+ regulatory T cells (Treg) in systemic lupus erythematosus (SLE) patients: the possible influence of treatment with corticosteroids. Clin Immunol 2008;127:151–7.
   PubMedGoogle Scholar
• Yates J, Whittington A, Mitchell P, Lechler RI, Lightstone L, Lombardi G. Natural regulatory T cells: number and function are normal in the majority of patients with lupus nephritis. Clin Exp Immunol 2008;153:44–55.
   PubMed Web of Science ®Google Scholar
• Suen JL, Li HT, Jong YJ, Chiang BL, Yen JH. Altered homeostasis of CD4 FoxP3 regulatory T-cell subpopulations in systemic lupus erythematosus. Immunology 2008;127:196–205.
   PubMedGoogle Scholar
• Venigalla RK, Tretter T, Krienke S, Max R, Eckstein V, Blank N, Reduced CD4+,CD25– T cell sensitivity to the suppressive function of CD4+,CD25high,CD127–/low regulatory T cells in patients with active systemic lupus erythematosus. Arthritis Rheum 2008;58:2120–30.
   PubMed Web of Science ®Google Scholar
• Bonelli M, Savitskaya A, von Dalwigk K, Steiner CW, Aletaha D, Smolen JS, Quantitative and qualitative deficiencies of regulatory T cells in patients with systemic lupus erythematosus (SLE). Int Immunol 2008;20:861–8.
   PubMed Web of Science ®Google Scholar
• Bonelli M, Savitskaya A, Steiner CW, Rath E, Smolen JS, Scheinecker C. Phenotypic and functional analysis of CD4+CD25–FoxP3+ T cells in patients with systemic lupus erythematosus. J Immunol 2009;182:1689–95.
   PubMed Web of Science ®Google Scholar
• Barreto M, Ferreira RC, Lourenço L, Moraes-Fontes MF, Santos E, Alves M, Low frequency of CD4+CD25+ Treg in SLE patients: a heritable trait associated with CTLA4 and TGFbeta gene variants. BMC Immunol 2009;10:5.
   PubMedGoogle Scholar
• Yang J, Chu Y, Yang X, Gao D, Zhu L, Yang X. Th17 and natural Treg cell population dynamics in systemic lupus erythematosus. Arthritis Rheum 2009;60:1472–83.
   PubMed Web of Science ®Google Scholar
• Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271–7.
   PubMed Web of Science ®Google Scholar
• Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH. Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis studies in SLE. Arthritis Rheum 1992;35:630–40.
   PubMed Web of Science ®Google Scholar
• Hoffmann P, Boeld TJ, Eder R, Huehn J, Floess S, Wieczorek G, Loss of FOXP3 expression in natural human CD4+CD25+ regulatory T cells upon repetitive in vitro stimulation. Eur J Immunol 2009;39:1088–97.
   PubMed Web of Science ®Google Scholar
• Mandapathil M, Lang S, Gorelik E, Whiteside TL. Isolation of functional human regulatory T cells (Treg) from the peripheral blood based on the CD39 expression. J Immunol Methods 2009;346:55–63.
   PubMed Web of Science ®Google Scholar
• Morgan ME, van Bilsen JH, Bakker AM, Heemskerk B, Schilham MW, Hartgers FC, Expression of FOXP3 mRNA is not confined to CD4+CD25+ T regulatory cells in humans. Hum Immunol 2005;2005;66:13–20.
   Google Scholar
• Wang J, Ioan-Facsinay A, van der Voort EI, Huizinga TW, Toes RE. Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells. Eur J Immunol 2007;37:129–38.
   PubMed Web of Science ®Google Scholar
• Ziegler SF. FOXP3: not just for regulatory T cells anymore. Eur J Immunol 2007;37:21–3.
   PubMed Web of Science ®Google Scholar
• Walker MR, Kasprowicz DJ, Gersuk VH, Benard A, Van Landeghen M, Buckner JH, Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25– T cells. J Clin Invest 2003;112:1437–43.
   PubMed Web of Science ®Google Scholar
• Aandahl EM, Michaelsson J, Moretto WJ, Hecht FM, Nixon DF. Human CD4+ CD25+ regulatory T cells control T-cell responses to human immunodeficiency virus and cytomegalovirus antigens. J Virol 2004;78:2454–9.
   PubMed Web of Science ®Google Scholar
• Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z, FoxP3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006;212:8–27.
   PubMed Web of Science ®Google Scholar
• Zhou X, Bailey-Bucktrout SL, Jeker LT, Penaranda C, Martínez-Llordella M, Ashby M, Instability of the transcription factor FoxP3 leads to the generation of pathogenic memory T cells in vivo. Nat Immunol 2009;10:1000–9.
   PubMed Web of Science ®Google Scholar
• Habib HM, Taher TE, Isenberg DA, Mageed RA. Enhanced propensity of T lymphocytes in patients with systemic lupus erythematosus to apoptosis in the presence of tumour necrosis factor alpha. Scand J Rheumatol 2009;38:112–20.
   PubMed Web of Science ®Google Scholar
• Voo KS, Wang YH, Santori FR, Boggiano C, Wang YH, Arima K, Identification of IL-17-producing FOXP3+ regulatory T cells in humans. Proc Natl Acad Sci USA 2009;106:4793–8.
   PubMed Web of Science ®Google Scholar