Skip to main content
Top
Published in: Clinical Rheumatology 9/2013

01-09-2013 | Review Article

Role of interleukin-10 and interleukin-10 receptor in systemic lupus erythematosus

Authors: Hui Peng, Wei Wang, Mo Zhou, Rui Li, Hai-Feng Pan, Dong-Qing Ye

Published in: Clinical Rheumatology | Issue 9/2013

Login to get access

Abstract

Systemic lupus erythematosus (SLE) is a prototypic autoimmune disease characterized by excessive production of a variety of autoantibodies, accumulation of immune complexes, and multiple organ systems involvement. Interleukin-10 (IL-10) has an important role in the growth, survival, differentiation, and function of B cells. Abnormally increased IL-10 synthesis seems contributing to the spontaneous hyperactivity of the B cell compartment, so that it can directly result in autoantibody production by committed plasma cells, circulating immune complexes formation, and eventually in tissue and organ damage, suggesting it might associate with the development of SLE. A better understanding of the regulation of IL-10 and its receptors (IL-10R) can likely provide more valuable clues to the pathogenic mechanisms underlying specific forms of SLE, so as to pave the way toward more effective therapeutics.
Literature
1.
go back to reference Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG (2011) Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 29:71–109PubMedCrossRef Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG (2011) Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol 29:71–109PubMedCrossRef
2.
go back to reference Fiorentino DF, Bond MW, Mosmann TR (1989) Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 170(6):2081–2095PubMedCrossRef Fiorentino DF, Bond MW, Mosmann TR (1989) Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 170(6):2081–2095PubMedCrossRef
3.
go back to reference Wolk K, Kunz S, Asadullah K, Sabat R (2002) Cutting edge: immune cells as sources and targets of the IL-10 family members? J Immunol 168(11):5397–5402PubMed Wolk K, Kunz S, Asadullah K, Sabat R (2002) Cutting edge: immune cells as sources and targets of the IL-10 family members? J Immunol 168(11):5397–5402PubMed
4.
go back to reference Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H et al (2009) Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol 10(11):1178–1184PubMedCrossRef Murai M, Turovskaya O, Kim G, Madan R, Karp CL, Cheroutre H et al (2009) Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol 10(11):1178–1184PubMedCrossRef
5.
go back to reference Roers A, Siewe L, Strittmatter E, Deckert M, Schlüter D, Stenzel W et al (2004) T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J Exp Med 200(10):1289–1297PubMedCrossRef Roers A, Siewe L, Strittmatter E, Deckert M, Schlüter D, Stenzel W et al (2004) T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J Exp Med 200(10):1289–1297PubMedCrossRef
6.
go back to reference Blanco P, Palucka AK, Pascual V, Banchereau J (2008) Dendritic cells and cytokines in human inflammatory and autoimmune diseases. Cytokine Growth Factor Rev 19(1):41–52PubMedCrossRef Blanco P, Palucka AK, Pascual V, Banchereau J (2008) Dendritic cells and cytokines in human inflammatory and autoimmune diseases. Cytokine Growth Factor Rev 19(1):41–52PubMedCrossRef
7.
go back to reference Chomarat P, Rissoan MC, Banchereau J, Miossec P (1993) Interferon gamma inhibits interleukin 10 production by monocytes. J Exp Med 177(2):523–527PubMedCrossRef Chomarat P, Rissoan MC, Banchereau J, Miossec P (1993) Interferon gamma inhibits interleukin 10 production by monocytes. J Exp Med 177(2):523–527PubMedCrossRef
8.
go back to reference Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM (2002) B cells regulate autoimmunity by provision of IL-10. Nat Immunol 3(10):944–950PubMedCrossRef Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM (2002) B cells regulate autoimmunity by provision of IL-10. Nat Immunol 3(10):944–950PubMedCrossRef
9.
go back to reference Grant LR, Yao ZJ, Hedrich CM, Wang F, Moorthy A, Wilson K et al (2008) Stat4-dependent, T-bet-independent regulation of IL-10 in NK cells. Genes Immun 9(4):316–327PubMedCrossRef Grant LR, Yao ZJ, Hedrich CM, Wang F, Moorthy A, Wilson K et al (2008) Stat4-dependent, T-bet-independent regulation of IL-10 in NK cells. Genes Immun 9(4):316–327PubMedCrossRef
10.
go back to reference Mehrotra PT, Donnelly RP, Wong S, Kanegane H, Geremew A, Mostowski HS et al (1998) Production of IL-10 by human natural killer cells stimulated with IL-2 and/or IL-12. J Immunol 160(6):2637–2644PubMed Mehrotra PT, Donnelly RP, Wong S, Kanegane H, Geremew A, Mostowski HS et al (1998) Production of IL-10 by human natural killer cells stimulated with IL-2 and/or IL-12. J Immunol 160(6):2637–2644PubMed
11.
go back to reference Speiran K, Bailey DP, Fernando J, Macey M, Barnstein B, Kolawole M et al (2009) Endogenous suppression of mast cell development and survival by IL-4 and IL-10. J Leukoc Biol 85(5):826–836PubMedCrossRef Speiran K, Bailey DP, Fernando J, Macey M, Barnstein B, Kolawole M et al (2009) Endogenous suppression of mast cell development and survival by IL-4 and IL-10. J Leukoc Biol 85(5):826–836PubMedCrossRef
12.
go back to reference Tan JC, Indelicato S, Narula SK, Zavodny PJ, Chou CC (1993) Characterization of interleukin-10 receptors on human and mouse cells. J Biol Chem 268(28):21053–21059PubMed Tan JC, Indelicato S, Narula SK, Zavodny PJ, Chou CC (1993) Characterization of interleukin-10 receptors on human and mouse cells. J Biol Chem 268(28):21053–21059PubMed
13.
go back to reference Windsor WT, Syto R, Tsarbopoulos A, Zhang R, Durkin J, Baldwin S et al (1993) Disulfide bond assignments and secondary structure analysis of human and murine interleukin 10. Biochemistry 32(34):8807–8815PubMedCrossRef Windsor WT, Syto R, Tsarbopoulos A, Zhang R, Durkin J, Baldwin S et al (1993) Disulfide bond assignments and secondary structure analysis of human and murine interleukin 10. Biochemistry 32(34):8807–8815PubMedCrossRef
14.
go back to reference Walter MR, Nagabhushan TL (1995) Crystal structure of interleukin 10 reveals an interferon gamma-like fold. Biochemistry 34(38):12118–12125PubMedCrossRef Walter MR, Nagabhushan TL (1995) Crystal structure of interleukin 10 reveals an interferon gamma-like fold. Biochemistry 34(38):12118–12125PubMedCrossRef
15.
go back to reference Zdanov A, Schalk-Hihi C, Wlodawer A (1996) Crystal of human interleukin-10 at 1.6 A resolution and a model of a complex with its soluble receptor. Protein Sci 5(10):1955–1962PubMedCrossRef Zdanov A, Schalk-Hihi C, Wlodawer A (1996) Crystal of human interleukin-10 at 1.6 A resolution and a model of a complex with its soluble receptor. Protein Sci 5(10):1955–1962PubMedCrossRef
16.
go back to reference Syto R, Murgolo NJ, Braswell EH, Mui P, Huang E, Windsor WT (1998) Structural and biological stability of the human interleukin 10 homodimer. Biochemistry 37(48):16943–16951PubMedCrossRef Syto R, Murgolo NJ, Braswell EH, Mui P, Huang E, Windsor WT (1998) Structural and biological stability of the human interleukin 10 homodimer. Biochemistry 37(48):16943–16951PubMedCrossRef
17.
go back to reference Walter MR, Windsor WT, Nagabhushan TL, Lundell DJ, Lunn CA, Zavodny PJ et al (1995) Crystal structure of a complex between interferon-gamma and its soluble high affinity receptor. Nature 376(6537):230–235PubMedCrossRef Walter MR, Windsor WT, Nagabhushan TL, Lundell DJ, Lunn CA, Zavodny PJ et al (1995) Crystal structure of a complex between interferon-gamma and its soluble high affinity receptor. Nature 376(6537):230–235PubMedCrossRef
18.
go back to reference Moore KW, de Waal MR, Coffman RL, O’Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683–765PubMedCrossRef Moore KW, de Waal MR, Coffman RL, O’Garra A (2001) Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683–765PubMedCrossRef
19.
go back to reference Moore KW, O’Garra A, de Waal MR, Vieira P, Mosmann TR (1993) Interleukin-10. Annu Rev Immunol 11:165–190PubMedCrossRef Moore KW, O’Garra A, de Waal MR, Vieira P, Mosmann TR (1993) Interleukin-10. Annu Rev Immunol 11:165–190PubMedCrossRef
20.
go back to reference Akdis CA, Blaser K (2001) Mechanisms of interleukin-10-mediated immune suppression. Immunology 103(2):131–136PubMedCrossRef Akdis CA, Blaser K (2001) Mechanisms of interleukin-10-mediated immune suppression. Immunology 103(2):131–136PubMedCrossRef
21.
go back to reference Schall TJ, Bacon K, Toy KJ, Goeddel DV (1990) Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347(6294):669–671PubMedCrossRef Schall TJ, Bacon K, Toy KJ, Goeddel DV (1990) Selective attraction of monocytes and T lymphocytes of the memory phenotype by cytokine RANTES. Nature 347(6294):669–671PubMedCrossRef
22.
go back to reference Cai G, Kastelein RA, Hunter CA (1999) IL-10 enhances NK cell proliferation, cytotoxicity and production of IFN-gamma when combined with IL-18. Eur J Immunol 29(9):2658–2665PubMedCrossRef Cai G, Kastelein RA, Hunter CA (1999) IL-10 enhances NK cell proliferation, cytotoxicity and production of IFN-gamma when combined with IL-18. Eur J Immunol 29(9):2658–2665PubMedCrossRef
23.
go back to reference Donnelly RP, Dickensheets H, Finbloom DS (1999) The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J Interferon Cytokine Res 19(6):563–573PubMedCrossRef Donnelly RP, Dickensheets H, Finbloom DS (1999) The interleukin-10 signal transduction pathway and regulation of gene expression in mononuclear phagocytes. J Interferon Cytokine Res 19(6):563–573PubMedCrossRef
24.
go back to reference Kotenko SV, Pestka S (2000) Jak-Stat signal transduction pathway through the eyes of cytokine class II receptor complexes. Oncogene 19(21):2557–2565PubMedCrossRef Kotenko SV, Pestka S (2000) Jak-Stat signal transduction pathway through the eyes of cytokine class II receptor complexes. Oncogene 19(21):2557–2565PubMedCrossRef
25.
go back to reference Logsdon NJ, Jones BC, Josephson K, Cook J, Walter MR (2002) Comparison of interleukin-22 and interleukin-10 soluble receptor complexes. J Interferon Cytokine Res 22(11):1099–1112PubMedCrossRef Logsdon NJ, Jones BC, Josephson K, Cook J, Walter MR (2002) Comparison of interleukin-22 and interleukin-10 soluble receptor complexes. J Interferon Cytokine Res 22(11):1099–1112PubMedCrossRef
26.
go back to reference Ding Y, Qin L, Zamarin D, Kotenko SV, Pestka S, Moore KW et al (2001) Differential IL-10R1 expression plays a critical role in IL-10-mediated immune regulation. J Immunol 167(12):6884–6892PubMed Ding Y, Qin L, Zamarin D, Kotenko SV, Pestka S, Moore KW et al (2001) Differential IL-10R1 expression plays a critical role in IL-10-mediated immune regulation. J Immunol 167(12):6884–6892PubMed
27.
go back to reference Kunz S, Wolk K, Witte E, Witte K, Doecke WD, Volk HD et al (2006) Interleukin (IL)-19, IL-20 and IL-24 are produced by and act on keratinocytes and are distinct from classical ILs. Exp Dermatol 15(12):991–1004PubMedCrossRef Kunz S, Wolk K, Witte E, Witte K, Doecke WD, Volk HD et al (2006) Interleukin (IL)-19, IL-20 and IL-24 are produced by and act on keratinocytes and are distinct from classical ILs. Exp Dermatol 15(12):991–1004PubMedCrossRef
28.
go back to reference Wolk K, Witte E, Reineke U, Witte K, Friedrich M, Sterry W et al (2005) Is there an interaction between interleukin-10 and interleukin-22? Genes Immun 6(1):8–18PubMed Wolk K, Witte E, Reineke U, Witte K, Friedrich M, Sterry W et al (2005) Is there an interaction between interleukin-10 and interleukin-22? Genes Immun 6(1):8–18PubMed
29.
go back to reference Reineke U, Schneider-Mergener J, Glaser RW, Stigler RD, Seifert M, Volk HD et al (1999) Evidence for conformationally different states of interleukin-10: binding of a neutralizing antibody enhances accessibility of a hidden epitope. J Mol Recognit 12(4):242–248PubMedCrossRef Reineke U, Schneider-Mergener J, Glaser RW, Stigler RD, Seifert M, Volk HD et al (1999) Evidence for conformationally different states of interleukin-10: binding of a neutralizing antibody enhances accessibility of a hidden epitope. J Mol Recognit 12(4):242–248PubMedCrossRef
30.
go back to reference Yoon SI, Logsdon NJ, Sheikh F, Donnelly RP, Walter MR (2006) Conformational changes mediate interleukin-10 receptor 2 (IL-10R2) binding to IL-10 and assembly of the signaling complex. J Biol Chem 281(46):35088–35096PubMedCrossRef Yoon SI, Logsdon NJ, Sheikh F, Donnelly RP, Walter MR (2006) Conformational changes mediate interleukin-10 receptor 2 (IL-10R2) binding to IL-10 and assembly of the signaling complex. J Biol Chem 281(46):35088–35096PubMedCrossRef
31.
go back to reference Weber-Nordt RM, Riley JK, Greenlund AC, Moore KW, Darnell JE, Schreiber RD (1996) Stat3 recruitment by two distinct ligand-induced, tyrosine-phosphorylated docking sites in the interleukin-10 receptor intracellular domain. J Biol Chem 271(44):27954–27961PubMedCrossRef Weber-Nordt RM, Riley JK, Greenlund AC, Moore KW, Darnell JE, Schreiber RD (1996) Stat3 recruitment by two distinct ligand-induced, tyrosine-phosphorylated docking sites in the interleukin-10 receptor intracellular domain. J Biol Chem 271(44):27954–27961PubMedCrossRef
32.
go back to reference Dummer W, Bastian BC, Ernst N, Schänzle C, Schwaaf A, Bröcker EB (1996) Interleukin-10 production in malignant melanoma: preferential detection of IL-10-secreting tumor cells in metastatic lesions. Int J Cancer 66(5):607–610PubMedCrossRef Dummer W, Bastian BC, Ernst N, Schänzle C, Schwaaf A, Bröcker EB (1996) Interleukin-10 production in malignant melanoma: preferential detection of IL-10-secreting tumor cells in metastatic lesions. Int J Cancer 66(5):607–610PubMedCrossRef
33.
go back to reference Park YB, Lee SK, Kim DS, Lee J, Lee CH, Song CH (1998) Elevated interleukin-10 levels correlated with disease activity in systemic lupus erythematosus. Clin Exp Rheumatol 16(3):283–288PubMed Park YB, Lee SK, Kim DS, Lee J, Lee CH, Song CH (1998) Elevated interleukin-10 levels correlated with disease activity in systemic lupus erythematosus. Clin Exp Rheumatol 16(3):283–288PubMed
34.
go back to reference Hasegawa M, Fujimoto M, Kikuchi K, Takehara K (1997) Elevated serum levels of interleukin 4 (IL-4), IL-10 and IL-13 in patients with systemic sclerosis. J Rheumatol 24(2):328–332PubMed Hasegawa M, Fujimoto M, Kikuchi K, Takehara K (1997) Elevated serum levels of interleukin 4 (IL-4), IL-10 and IL-13 in patients with systemic sclerosis. J Rheumatol 24(2):328–332PubMed
35.
go back to reference Fayad L, Keating MJ, Reuben JM, O’Brien S, Lee BN, Lerner S et al (2001) Interleukin-6 and interleukin-10 levels in chronic lymphocytic leukemia: correlation with phenotypic characteristics and outcome. Blood 97(1):256–263PubMedCrossRef Fayad L, Keating MJ, Reuben JM, O’Brien S, Lee BN, Lerner S et al (2001) Interleukin-6 and interleukin-10 levels in chronic lymphocytic leukemia: correlation with phenotypic characteristics and outcome. Blood 97(1):256–263PubMedCrossRef
36.
go back to reference van Montfrans C, Camoglio L, van Deventer SJ (1998) Immunotherapy of Crohn’s disease. Mediators Inflamm 7(3):149–152PubMedCrossRef van Montfrans C, Camoglio L, van Deventer SJ (1998) Immunotherapy of Crohn’s disease. Mediators Inflamm 7(3):149–152PubMedCrossRef
37.
go back to reference Zou K, Liu S, Xie X, Yi C (2001) Clinical significance and assessment of cytokines in various stages of ulcerative colitis. J Tongji Med Univ 21(4):308–309PubMedCrossRef Zou K, Liu S, Xie X, Yi C (2001) Clinical significance and assessment of cytokines in various stages of ulcerative colitis. J Tongji Med Univ 21(4):308–309PubMedCrossRef
38.
go back to reference Asadullah K, Sterry W, Stephanek K, Jasulaitis D, Leupold M, Audring H et al (1998) IL-10 is a key cytokine in psoriasis. Proof of principle by IL-10 therapy: a new therapeutic approach. J Clin Invest 101(4):783–794PubMedCrossRef Asadullah K, Sterry W, Stephanek K, Jasulaitis D, Leupold M, Audring H et al (1998) IL-10 is a key cytokine in psoriasis. Proof of principle by IL-10 therapy: a new therapeutic approach. J Clin Invest 101(4):783–794PubMedCrossRef
39.
go back to reference Katsikis PD, Chu CQ, Brennan FM, Maini RN, Feldmann M (1994) Immunoregulatory role of interleukin 10 in rheumatoid arthritis. J Exp Med 179(5):1517–1527PubMedCrossRef Katsikis PD, Chu CQ, Brennan FM, Maini RN, Feldmann M (1994) Immunoregulatory role of interleukin 10 in rheumatoid arthritis. J Exp Med 179(5):1517–1527PubMedCrossRef
40.
go back to reference Ishida H, Muchamuel T, Sakaguchi S, Andrade S, Menon S, Howard M (1994) Continuous administration of anti-interleukin 10 antibodies delays onset of autoimmunity in NZB/W F1 mice. J Exp Med 179(5):305–310PubMedCrossRef Ishida H, Muchamuel T, Sakaguchi S, Andrade S, Menon S, Howard M (1994) Continuous administration of anti-interleukin 10 antibodies delays onset of autoimmunity in NZB/W F1 mice. J Exp Med 179(5):305–310PubMedCrossRef
41.
go back to reference Jacob CO, McDevitt HO (1988) Tumor necrosis factor-or in murine autoimmune 'lupus' nephritis. Nature 331(6154):356–358PubMedCrossRef Jacob CO, McDevitt HO (1988) Tumor necrosis factor-or in murine autoimmune 'lupus' nephritis. Nature 331(6154):356–358PubMedCrossRef
42.
go back to reference Postal M, Appenzeller S (2011) The role of tumor necrosis factor-alpha (TNF-α) in the pathogenesis of systemic lupus erythematosus. Cytokine 56(3):537–543PubMedCrossRef Postal M, Appenzeller S (2011) The role of tumor necrosis factor-alpha (TNF-α) in the pathogenesis of systemic lupus erythematosus. Cytokine 56(3):537–543PubMedCrossRef
43.
go back to reference Ravirajan CT, Wang Y, Matis LA, Papadaki L, Griffiths MH, Latchman DS et al (2004) Effect of neutralizing antibodies to IL-10 and C5 on the renal damage caused by a pathogenic human anti-dsDNA antibody. Rheumatology (Oxford) 43(4):442–447CrossRef Ravirajan CT, Wang Y, Matis LA, Papadaki L, Griffiths MH, Latchman DS et al (2004) Effect of neutralizing antibodies to IL-10 and C5 on the renal damage caused by a pathogenic human anti-dsDNA antibody. Rheumatology (Oxford) 43(4):442–447CrossRef
44.
go back to reference Yin Z, Bahtiyar G, Zhang N, Liu L, Zhu P, Robert ME et al (2002) IL-10 regulates murine lupus. J Immunol 169(4):2148–2155PubMed Yin Z, Bahtiyar G, Zhang N, Liu L, Zhu P, Robert ME et al (2002) IL-10 regulates murine lupus. J Immunol 169(4):2148–2155PubMed
45.
go back to reference Ma L, Chan KW, Trendell-Smith NJ, Wu A, Tian L, Lam AC et al (2005) Systemic autoimmune disease induced by dendritic cells that have captured necrotic but not apoptotic cells in susceptible mouse strains. Eur J Immunol 35(11):3364–3375PubMedCrossRef Ma L, Chan KW, Trendell-Smith NJ, Wu A, Tian L, Lam AC et al (2005) Systemic autoimmune disease induced by dendritic cells that have captured necrotic but not apoptotic cells in susceptible mouse strains. Eur J Immunol 35(11):3364–3375PubMedCrossRef
46.
go back to reference Blenman KR, Duan B, Xu Z, Wan S, Atkinson MA, Flotte TR et al (2006) IL-10 regulation of lupus in the NZM2410 murine model. Lab Invest 86(11):1136–1148PubMed Blenman KR, Duan B, Xu Z, Wan S, Atkinson MA, Flotte TR et al (2006) IL-10 regulation of lupus in the NZM2410 murine model. Lab Invest 86(11):1136–1148PubMed
47.
go back to reference Ling GS, Cook HT, Botto M, Lau YL, Huang FP (2011) An essential protective role of IL-10 in the immunological mechanism underlying resistance vs. susceptibility to lupus induction by dendritic cells and dying cells. Rheumatology (Oxford) 50(10):1773–1784CrossRef Ling GS, Cook HT, Botto M, Lau YL, Huang FP (2011) An essential protective role of IL-10 in the immunological mechanism underlying resistance vs. susceptibility to lupus induction by dendritic cells and dying cells. Rheumatology (Oxford) 50(10):1773–1784CrossRef
48.
go back to reference Mikita N, Ikeda T, Ishiguro M, Furukawa F (2011) Recent advances in cytokines in cutaneous and systemic lupus erythematosus. J Dermatol 38(9):839–849PubMed Mikita N, Ikeda T, Ishiguro M, Furukawa F (2011) Recent advances in cytokines in cutaneous and systemic lupus erythematosus. J Dermatol 38(9):839–849PubMed
49.
go back to reference Balomenos D, Rumold R, Theofilopoulos AN (1998) Interferon-gamma is required for lupus-like disease and lymphoaccumulation in MRL-lpr mice. J Clin Invest 101(2):364–371PubMedCrossRef Balomenos D, Rumold R, Theofilopoulos AN (1998) Interferon-gamma is required for lupus-like disease and lymphoaccumulation in MRL-lpr mice. J Clin Invest 101(2):364–371PubMedCrossRef
50.
go back to reference Haas C, Ryffel B, Le Hir M (1998) IFN-gamma receptor deletion prevents autoantibody production and glomerulonephritis in lupus-prone (NZB × NZW) F1 mice. J Immunol 160(8):3713–3718PubMed Haas C, Ryffel B, Le Hir M (1998) IFN-gamma receptor deletion prevents autoantibody production and glomerulonephritis in lupus-prone (NZB × NZW) F1 mice. J Immunol 160(8):3713–3718PubMed
51.
go back to reference O’Garra A, Chang R, Go N, Hastings R, Haughton G, Howard M (1992) Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur J Immunol 22(3):711–717PubMedCrossRef O’Garra A, Chang R, Go N, Hastings R, Haughton G, Howard M (1992) Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur J Immunol 22(3):711–717PubMedCrossRef
52.
go back to reference Hayakawa K, Hardy RR, Herzenberg LA (1986) Peritoneal Ly-1 B-cells: genetic control, autoantibody production, increased lambda light chain expression. Eur J Immunol 16(4):450–456PubMedCrossRef Hayakawa K, Hardy RR, Herzenberg LA (1986) Peritoneal Ly-1 B-cells: genetic control, autoantibody production, increased lambda light chain expression. Eur J Immunol 16(4):450–456PubMedCrossRef
53.
go back to reference Mohan C, Morel L, Yang P, Wakeland EK (1998) Accumulation of splenic B1a cells with potent antigen-presenting capability in NZM2410 lupus-prone mice. Arthritis Rheum 41(9):1652–1662PubMedCrossRef Mohan C, Morel L, Yang P, Wakeland EK (1998) Accumulation of splenic B1a cells with potent antigen-presenting capability in NZM2410 lupus-prone mice. Arthritis Rheum 41(9):1652–1662PubMedCrossRef
54.
go back to reference Xu Z, Duan B, Croker BP, Wakeland EK, Morel L (2005) Genetic dissection of the murine lupus susceptibility locus Sle2: contributions to increased peritoneal B-1a cells and lupus nephritis map to different loci. J Immunol 175(2):936–943PubMed Xu Z, Duan B, Croker BP, Wakeland EK, Morel L (2005) Genetic dissection of the murine lupus susceptibility locus Sle2: contributions to increased peritoneal B-1a cells and lupus nephritis map to different loci. J Immunol 175(2):936–943PubMed
55.
go back to reference Brummel R, Lenert P (2005) Activation of marginal zone B cells from lupus mice with type A(D) CpG-oligodeoxynucleotides. J Immunol 174(4):2429–2434PubMed Brummel R, Lenert P (2005) Activation of marginal zone B cells from lupus mice with type A(D) CpG-oligodeoxynucleotides. J Immunol 174(4):2429–2434PubMed
56.
go back to reference Lenert P, Brummel R, Field EH, Ashman RF (2005) TLR-9 activation of marginal zone B cells in lupus mice regulates immunity through increased IL-10 production. J Clin Immunol 25(1):29–40PubMedCrossRef Lenert P, Brummel R, Field EH, Ashman RF (2005) TLR-9 activation of marginal zone B cells in lupus mice regulates immunity through increased IL-10 production. J Clin Immunol 25(1):29–40PubMedCrossRef
57.
go back to reference Gelati M, Lamperti E, Dufour A, Corsini E, Venegoni E, Milanese C et al (1997) IL-10 production in multiple sclerosis patients, SLE patients and healthy controls: preliminary findings. Ital J Neurol Sci 18(4):191–194PubMedCrossRef Gelati M, Lamperti E, Dufour A, Corsini E, Venegoni E, Milanese C et al (1997) IL-10 production in multiple sclerosis patients, SLE patients and healthy controls: preliminary findings. Ital J Neurol Sci 18(4):191–194PubMedCrossRef
58.
go back to reference Lacki JK, Samborski W, Mackiewicz SH (1997) Interleukin-10 and interleukin-6 in lupus erythematosus and rheumatoid arthritis, correlations with acute phase proteins. Clin Rheumatol 16(3):275–278PubMedCrossRef Lacki JK, Samborski W, Mackiewicz SH (1997) Interleukin-10 and interleukin-6 in lupus erythematosus and rheumatoid arthritis, correlations with acute phase proteins. Clin Rheumatol 16(3):275–278PubMedCrossRef
59.
go back to reference Waszczykowska E, Robak E, Wozniacka A, Narbutt J, Torzecka JD, Sysa-Jedrzejowska A (1999) Estimation of SLE activity based on the serum level of chosen cytokines and superoxide radical generation. Mediators Inflamm 8(2):93–100PubMedCrossRef Waszczykowska E, Robak E, Wozniacka A, Narbutt J, Torzecka JD, Sysa-Jedrzejowska A (1999) Estimation of SLE activity based on the serum level of chosen cytokines and superoxide radical generation. Mediators Inflamm 8(2):93–100PubMedCrossRef
60.
go back to reference Liu TF, Jones BM (1998) Impaired production of IL-12 in system lupus erythematosus. II: IL-12 production in vitro is correlated negatively with serum IL-10, positively with serum IFN-gamma and negatively with disease activity in SLE. Cytokine 10(2):148–153PubMedCrossRef Liu TF, Jones BM (1998) Impaired production of IL-12 in system lupus erythematosus. II: IL-12 production in vitro is correlated negatively with serum IL-10, positively with serum IFN-gamma and negatively with disease activity in SLE. Cytokine 10(2):148–153PubMedCrossRef
61.
go back to reference Hase K, Tani K, Shimizu T, Ohmoto Y, Matsushima K, Sone S (2001) Increased CCR4 expression in active systemic lupus erythematosus. J Leukoc Biol 70(5):749–755PubMed Hase K, Tani K, Shimizu T, Ohmoto Y, Matsushima K, Sone S (2001) Increased CCR4 expression in active systemic lupus erythematosus. J Leukoc Biol 70(5):749–755PubMed
62.
go back to reference Yang PT, Kasai H, Zhao LJ, Xiao WG, Tanabe F, Ito M (2004) Increased CCR4 expression on circulating CD4 (+) T cells in ankylosing spondylitis, rheumatoid arthritis and systemic lupus erythematosus. Clin Exp Immunol 138(2):342–347PubMedCrossRef Yang PT, Kasai H, Zhao LJ, Xiao WG, Tanabe F, Ito M (2004) Increased CCR4 expression on circulating CD4 (+) T cells in ankylosing spondylitis, rheumatoid arthritis and systemic lupus erythematosus. Clin Exp Immunol 138(2):342–347PubMedCrossRef
63.
go back to reference Chun HY, Chung JW, Kim HA, Yun JM, Jeon JY, Ye YM et al (2007) Cytokine IL-6 and IL-10 as biomarkers in systemic lupus erythematosus. J Clin Immunol 27(5):461–466PubMedCrossRef Chun HY, Chung JW, Kim HA, Yun JM, Jeon JY, Ye YM et al (2007) Cytokine IL-6 and IL-10 as biomarkers in systemic lupus erythematosus. J Clin Immunol 27(5):461–466PubMedCrossRef
64.
go back to reference Mellor-Pita S, Citores MJ, Castejon R, Yebra-Bango M, Tutor-Ureta P, Rosado S et al (2009) Monocytes and T lymphocytes contribute to a predominance of interleukin 6 and interleukin 10 in systemic lupus erythematosus. Cytometry B Clin Cytom 76(4):261–270PubMed Mellor-Pita S, Citores MJ, Castejon R, Yebra-Bango M, Tutor-Ureta P, Rosado S et al (2009) Monocytes and T lymphocytes contribute to a predominance of interleukin 6 and interleukin 10 in systemic lupus erythematosus. Cytometry B Clin Cytom 76(4):261–270PubMed
65.
go back to reference Liu Y, Zhu T, Cai G, Qin Y, Wang W, Tang G et al (2011) Elevated circulating CD4+ ICOS + Foxp3+ T cells contribute to overproduction of IL-10 and are correlated with disease severity in patients with systemic lupus erythematosus. Lupus 20(6):620–627PubMedCrossRef Liu Y, Zhu T, Cai G, Qin Y, Wang W, Tang G et al (2011) Elevated circulating CD4+ ICOS + Foxp3+ T cells contribute to overproduction of IL-10 and are correlated with disease severity in patients with systemic lupus erythematosus. Lupus 20(6):620–627PubMedCrossRef
66.
go back to reference Arora V, Verma J, Marwah V, Kumar A, Anand D, Das N (2012) Cytokine imbalance in systemic lupus erythematosus: a study on northern Indian subjects. Lupus 21(6):596–603PubMedCrossRef Arora V, Verma J, Marwah V, Kumar A, Anand D, Das N (2012) Cytokine imbalance in systemic lupus erythematosus: a study on northern Indian subjects. Lupus 21(6):596–603PubMedCrossRef
67.
go back to reference Houssiau FA, Lefebvre C, Vanden Berghe M, Lambert M, Devogelaer JP, Renauld JC (1995) Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus 4(5):393–395PubMedCrossRef Houssiau FA, Lefebvre C, Vanden Berghe M, Lambert M, Devogelaer JP, Renauld JC (1995) Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus 4(5):393–395PubMedCrossRef
68.
go back to reference El-Sayed M, Nofal E, al Mokadem S, al Makhzangy I, Gaballah H, Akl H (2008) Correlative study of serum Th1/Th2 cytokines levels in patients with systemic lupus erythematosus with SLEDAI. Egypt Dermatol Online J 4(1):3–19 El-Sayed M, Nofal E, al Mokadem S, al Makhzangy I, Gaballah H, Akl H (2008) Correlative study of serum Th1/Th2 cytokines levels in patients with systemic lupus erythematosus with SLEDAI. Egypt Dermatol Online J 4(1):3–19
69.
go back to reference Zhi-Chun L, Qiao-Ling Z, Zhi-Qin L, Xiao-Zhao L, Xiao-xia Z, Rong T (2012) Tumor necrosis factor-like weak inducer of apoptosis (TWEAK) mediates p38 mitogen-activated protein kinase activation and signal transduction in peripheral blood mononuclear cells from patients with lupus nephritis. Inflammation 35(3):935–943PubMedCrossRef Zhi-Chun L, Qiao-Ling Z, Zhi-Qin L, Xiao-Zhao L, Xiao-xia Z, Rong T (2012) Tumor necrosis factor-like weak inducer of apoptosis (TWEAK) mediates p38 mitogen-activated protein kinase activation and signal transduction in peripheral blood mononuclear cells from patients with lupus nephritis. Inflammation 35(3):935–943PubMedCrossRef
70.
go back to reference Dhir V, Singh AP, Aggarwal A, Naik S, Misra R (2009) Increased T-lymphocyte apoptosis in lupus correlates with disease activity and may be responsible for reduced T-cell frequency: a cross-sectional and longitudinal study. Lupus 18(9):785–791PubMedCrossRef Dhir V, Singh AP, Aggarwal A, Naik S, Misra R (2009) Increased T-lymphocyte apoptosis in lupus correlates with disease activity and may be responsible for reduced T-cell frequency: a cross-sectional and longitudinal study. Lupus 18(9):785–791PubMedCrossRef
71.
go back to reference Chen J, Shen B, Jiang Y, Jun L, Zhu M, Chen B et al (2013) Analysis of immunoglobulin-like transcripts (ILTs) in lymphocytes with sHLA-G and IL10 from SLE patients. Clin Exp Med 13(2):135–42 Chen J, Shen B, Jiang Y, Jun L, Zhu M, Chen B et al (2013) Analysis of immunoglobulin-like transcripts (ILTs) in lymphocytes with sHLA-G and IL10 from SLE patients. Clin Exp Med 13(2):135–42
72.
go back to reference Uhm WS, Na K, Song GW, Jung SS, Lee T, Park MH et al (2003) Cytokine balance in kidney tissue from lupus nephritis patients. Rheumatology (Oxford) 42(8):935–938CrossRef Uhm WS, Na K, Song GW, Jung SS, Lee T, Park MH et al (2003) Cytokine balance in kidney tissue from lupus nephritis patients. Rheumatology (Oxford) 42(8):935–938CrossRef
73.
go back to reference Wang Y, Ito S, Chino Y, Goto D, Matsumoto I, Murata H et al (2010) Laser microdissection-based analysis of cytokine balance in the kidneys of patients with lupus nephritis. Clin Exp Immunol 159(1):1–10PubMedCrossRef Wang Y, Ito S, Chino Y, Goto D, Matsumoto I, Murata H et al (2010) Laser microdissection-based analysis of cytokine balance in the kidneys of patients with lupus nephritis. Clin Exp Immunol 159(1):1–10PubMedCrossRef
74.
go back to reference Gross JA, Johnston J, Mudri S, Enselman R, Dillon SR, Madden K et al (2000) TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404(6781):995–999PubMedCrossRef Gross JA, Johnston J, Mudri S, Enselman R, Dillon SR, Madden K et al (2000) TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease. Nature 404(6781):995–999PubMedCrossRef
75.
go back to reference Hondowicz BD, Alexander ST, Quinn WJ 3rd, Pagán AJ, Metzgar MH, Cancro MP et al (2007) The role of BLyS/BLyS receptors in anti-chromatin B cell regulation. Int Immunol 19(4):465–475PubMedCrossRef Hondowicz BD, Alexander ST, Quinn WJ 3rd, Pagán AJ, Metzgar MH, Cancro MP et al (2007) The role of BLyS/BLyS receptors in anti-chromatin B cell regulation. Int Immunol 19(4):465–475PubMedCrossRef
76.
go back to reference Moulin V, Andris F, Thielemans K, Maliszewski C, Urbain J, Moser M (2000) B lymphocytes regulate dendritic cell (DC) function in vivo: increased interleukin 12 production by DCs from B cell-deficient mice results in T helper cell type 1 deviation. J Exp Med 192(4):475–482PubMedCrossRef Moulin V, Andris F, Thielemans K, Maliszewski C, Urbain J, Moser M (2000) B lymphocytes regulate dendritic cell (DC) function in vivo: increased interleukin 12 production by DCs from B cell-deficient mice results in T helper cell type 1 deviation. J Exp Med 192(4):475–482PubMedCrossRef
77.
go back to reference Jacobi AM, Odendahl M, Reiter K, Bruns A, Burmester GR, Radbruch A et al (2003) Correlation between circulating CD27 high plasma cells and disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 48(5):1332–1342PubMedCrossRef Jacobi AM, Odendahl M, Reiter K, Bruns A, Burmester GR, Radbruch A et al (2003) Correlation between circulating CD27 high plasma cells and disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 48(5):1332–1342PubMedCrossRef
78.
go back to reference Ito T, Hanabuchi S, Wang YH, Park WR, Arima K, Bover L et al (2008) Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 28(6):870–880PubMedCrossRef Ito T, Hanabuchi S, Wang YH, Park WR, Arima K, Bover L et al (2008) Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 28(6):870–880PubMedCrossRef
79.
go back to reference Huber S, Gagliani N, Esplugues E, O’Connor W Jr, Huber FJ, Chaudhry A et al (2011) Th17 cells express interleukin-10 receptor and are controlled by Foxp3- and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34(4):554–565PubMedCrossRef Huber S, Gagliani N, Esplugues E, O’Connor W Jr, Huber FJ, Chaudhry A et al (2011) Th17 cells express interleukin-10 receptor and are controlled by Foxp3- and Foxp3+ regulatory CD4+ T cells in an interleukin-10-dependent manner. Immunity 34(4):554–565PubMedCrossRef
80.
go back to reference Zhao XF, Pan HF, Yuan H, Zhang WH, Li XP, Wang GH et al (2010) Increased serum interleukin 17 in patients with systemic lupus erythematosus. Mol Biol Rep 37(1):81–85PubMedCrossRef Zhao XF, Pan HF, Yuan H, Zhang WH, Li XP, Wang GH et al (2010) Increased serum interleukin 17 in patients with systemic lupus erythematosus. Mol Biol Rep 37(1):81–85PubMedCrossRef
81.
go back to reference Llorente L, Zou W, Levy Y, Richaud-Patin Y, Wijdenes J, Alcocer-Varela J et al (1995) Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J Exp Med 181(3):839–844PubMedCrossRef Llorente L, Zou W, Levy Y, Richaud-Patin Y, Wijdenes J, Alcocer-Varela J et al (1995) Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J Exp Med 181(3):839–844PubMedCrossRef
82.
go back to reference Lauwerys BR, Garot N, Renauld JC, Houssiau FA (2000) Interleukin-10 blockade corrects impaired in vitro cellular immune responses of systemic lupus erythematosus patients. Arthritis Rheum 43(9):1976–1981PubMedCrossRef Lauwerys BR, Garot N, Renauld JC, Houssiau FA (2000) Interleukin-10 blockade corrects impaired in vitro cellular immune responses of systemic lupus erythematosus patients. Arthritis Rheum 43(9):1976–1981PubMedCrossRef
83.
go back to reference Llorente L, Richaud-Patin Y, García-Padilla C, Claret E, Jakez-Ocampo J, Cardiel MH et al (2000) Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum 43(8):1790–1800PubMedCrossRef Llorente L, Richaud-Patin Y, García-Padilla C, Claret E, Jakez-Ocampo J, Cardiel MH et al (2000) Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic lupus erythematosus. Arthritis Rheum 43(8):1790–1800PubMedCrossRef
84.
go back to reference Yuan W, DiMartino SJ, Redecha PB, Ivashkiv LB, Salmon JE (2011) Systemic lupus erythematosus monocytes are less responsive to interleukin-10 in the presence of immune complexes. Arthritis Rheum 63(1):212–218PubMedCrossRef Yuan W, DiMartino SJ, Redecha PB, Ivashkiv LB, Salmon JE (2011) Systemic lupus erythematosus monocytes are less responsive to interleukin-10 in the presence of immune complexes. Arthritis Rheum 63(1):212–218PubMedCrossRef
85.
go back to reference Johanneson B, Lima G, von Salomé J, Alarcón-Segovia D, Alarcón-Riquelme ME, Collaborative Group on the Genetics of SLE, The BIOMED II Collaboration on the Genetics of SLE and Sjögrens syndrome (2002) A major susceptibility locus for systemic lupus erythemathosus maps to chromosome 1q31. Am J Hum Genet 71(5):1060–1071PubMedCrossRef Johanneson B, Lima G, von Salomé J, Alarcón-Segovia D, Alarcón-Riquelme ME, Collaborative Group on the Genetics of SLE, The BIOMED II Collaboration on the Genetics of SLE and Sjögrens syndrome (2002) A major susceptibility locus for systemic lupus erythemathosus maps to chromosome 1q31. Am J Hum Genet 71(5):1060–1071PubMedCrossRef
86.
go back to reference Guzowski D, Chandrasekaran A, Gawel C, Palma J, Koenig J, Wang XP et al (2005) Analysis of single nucleotide polymorphisms in the promoter region of interleukin-10 by denaturing high-performance liquid chromatography. J Biomol Tech 16(2):154–166PubMed Guzowski D, Chandrasekaran A, Gawel C, Palma J, Koenig J, Wang XP et al (2005) Analysis of single nucleotide polymorphisms in the promoter region of interleukin-10 by denaturing high-performance liquid chromatography. J Biomol Tech 16(2):154–166PubMed
87.
go back to reference Lazarus M, Hajeer AH, Turner D, Sinnott P, Worthington J, Ollier WE et al (1997) Genetic variation in the interleukin 10 gene promoter and systemic lupus erythematosus. J Rheumatol 24(12):2314–2317PubMed Lazarus M, Hajeer AH, Turner D, Sinnott P, Worthington J, Ollier WE et al (1997) Genetic variation in the interleukin 10 gene promoter and systemic lupus erythematosus. J Rheumatol 24(12):2314–2317PubMed
88.
go back to reference Mok CC, Lanchbury JS, Chan DW, Lau CS (1998) Interleukin-10 promoter polymorphisms in Southern Chinese patients with systemic lupus erythematosus. Arthritis Rheum 41(6):1090–1095PubMedCrossRef Mok CC, Lanchbury JS, Chan DW, Lau CS (1998) Interleukin-10 promoter polymorphisms in Southern Chinese patients with systemic lupus erythematosus. Arthritis Rheum 41(6):1090–1095PubMedCrossRef
89.
go back to reference Rood MJ, Keijsers V, van der Linden MW, Tong TQ, Borggreve SE, Verweij CL et al (1999) Neuropsychiatric systemic lupus erythematosus is associated with imbalance in interleukin 10 promoter haplotypes. Ann Rheum Dis 58(2):85–89PubMedCrossRef Rood MJ, Keijsers V, van der Linden MW, Tong TQ, Borggreve SE, Verweij CL et al (1999) Neuropsychiatric systemic lupus erythematosus is associated with imbalance in interleukin 10 promoter haplotypes. Ann Rheum Dis 58(2):85–89PubMedCrossRef
90.
go back to reference Crawley E, Woo P, Isenberg DA (1999) Single nucleotide polymorphic haplotypes of the interleukin-10 5′ flanking region are not associated with renal disease or serology in Caucasian patients with systemic lupus erythematosus. Arthritis Rheum 42(9):2017–2018PubMedCrossRef Crawley E, Woo P, Isenberg DA (1999) Single nucleotide polymorphic haplotypes of the interleukin-10 5′ flanking region are not associated with renal disease or serology in Caucasian patients with systemic lupus erythematosus. Arthritis Rheum 42(9):2017–2018PubMedCrossRef
91.
go back to reference van der Linden MW, Westendorp RG, Sturk A, Bergman W, Huizinga TW (2000) High interleukin-10 production in first-degree relatives of patients with generalized but not cutaneous lupus erythematosus. J Investig Med 48(5):327–334PubMed van der Linden MW, Westendorp RG, Sturk A, Bergman W, Huizinga TW (2000) High interleukin-10 production in first-degree relatives of patients with generalized but not cutaneous lupus erythematosus. J Investig Med 48(5):327–334PubMed
92.
go back to reference Dijstelbloem HM, Hepkema BG, Kallenberg CG, van der Linden MW, Keijsers V, Huizinga TW et al (2002) The R-H polymorphism of FCgamma receptor IIa as a risk factor for systemic lupus erythematosus is independent of single-nucleotide polymorphisms in the interleukin-10 gene promoter. Arthritis Rheum 46(4):1125–1126PubMedCrossRef Dijstelbloem HM, Hepkema BG, Kallenberg CG, van der Linden MW, Keijsers V, Huizinga TW et al (2002) The R-H polymorphism of FCgamma receptor IIa as a risk factor for systemic lupus erythematosus is independent of single-nucleotide polymorphisms in the interleukin-10 gene promoter. Arthritis Rheum 46(4):1125–1126PubMedCrossRef
93.
go back to reference D’ Alfonso S, Giordano M, Mellai M, Lanceni M, Barizzone N, Marchini M et al (2002) Association tests with systemic lupus erythematosus (SLE) of IL10 markers indicate a direct involvement of a CA repeat in the 5′ regulatory region. Genes Immun 3(8):454–463CrossRef D’ Alfonso S, Giordano M, Mellai M, Lanceni M, Barizzone N, Marchini M et al (2002) Association tests with systemic lupus erythematosus (SLE) of IL10 markers indicate a direct involvement of a CA repeat in the 5′ regulatory region. Genes Immun 3(8):454–463CrossRef
94.
go back to reference Chong WP, Ip WK, Wong WH, Lau CS, Chan TM, Lau YL (2004) Association of interleukin-10 promoter polymorphisms with systemic lupus erythematosus. Genes Immun 5(6):484–492PubMedCrossRef Chong WP, Ip WK, Wong WH, Lau CS, Chan TM, Lau YL (2004) Association of interleukin-10 promoter polymorphisms with systemic lupus erythematosus. Genes Immun 5(6):484–492PubMedCrossRef
95.
go back to reference Fei GZ, Svenungsson E, Frostegård J, Padyukov L (2004) The A-1087IL-10 allele is associated with cardiovascular disease in SLE. Atherosclerosis 177(2):409–414PubMedCrossRef Fei GZ, Svenungsson E, Frostegård J, Padyukov L (2004) The A-1087IL-10 allele is associated with cardiovascular disease in SLE. Atherosclerosis 177(2):409–414PubMedCrossRef
96.
go back to reference Zhu LJ, Liu ZH, Zeng CH, Chen ZH, Yu C, Li LS (2005) Association of interleukin-10 gene -592A/C polymorphism with the clinical and pathological diversity of lupus nephritis. Clin Exp Rheumatol 23(6):854–860PubMed Zhu LJ, Liu ZH, Zeng CH, Chen ZH, Yu C, Li LS (2005) Association of interleukin-10 gene -592A/C polymorphism with the clinical and pathological diversity of lupus nephritis. Clin Exp Rheumatol 23(6):854–860PubMed
97.
go back to reference Lu LY, Cheng HH, Sung PK, Tai MH, Yeh JJ, Chen A (2005) Tumor necrosis factor-beta +252A polymorphism is associated with systemic lupus erythematosus in Taiwan. J Formos Med Assoc 104(8):563–570PubMed Lu LY, Cheng HH, Sung PK, Tai MH, Yeh JJ, Chen A (2005) Tumor necrosis factor-beta +252A polymorphism is associated with systemic lupus erythematosus in Taiwan. J Formos Med Assoc 104(8):563–570PubMed
98.
go back to reference Suárez A, López P, Mozo L, Gutiérrez C (2005) Differential effect of IL10 and TNF{alpha} genotypes on determining susceptibility to discoid and systemic lupus erythematosus. Ann Rheum Dis 64(11):1605–1610PubMedCrossRef Suárez A, López P, Mozo L, Gutiérrez C (2005) Differential effect of IL10 and TNF{alpha} genotypes on determining susceptibility to discoid and systemic lupus erythematosus. Ann Rheum Dis 64(11):1605–1610PubMedCrossRef
99.
go back to reference Hrycek A, Siekiera U, Cieślik P, Szkróbka W (2005) HLA-DRB1 and -DQB1 alleles and gene polymorphisms of selected cytokines in systemic lupus erythematosus. Rheumatol Int 26(1):1–6PubMedCrossRef Hrycek A, Siekiera U, Cieślik P, Szkróbka W (2005) HLA-DRB1 and -DQB1 alleles and gene polymorphisms of selected cytokines in systemic lupus erythematosus. Rheumatol Int 26(1):1–6PubMedCrossRef
100.
go back to reference Khoa PD, Sugiyama T, Yokochi T (2005) Polymorphism of interleukin-10 promoter and tumor necrosis factor receptor II in Vietnamese patients with systemic lupus erythematosus. Clin Rheumatol 24(1):11–13PubMedCrossRef Khoa PD, Sugiyama T, Yokochi T (2005) Polymorphism of interleukin-10 promoter and tumor necrosis factor receptor II in Vietnamese patients with systemic lupus erythematosus. Clin Rheumatol 24(1):11–13PubMedCrossRef
101.
go back to reference Sung YK, Park BL, Shin HD, Kim LH, Kim SY, Bae SC (2006) Interleukin-10 gene polymorphisms are associated with the SLICC/ACR Damage Index in systemic lupus erythematosus. Rheumatology (Oxford) 45(4):400–404CrossRef Sung YK, Park BL, Shin HD, Kim LH, Kim SY, Bae SC (2006) Interleukin-10 gene polymorphisms are associated with the SLICC/ACR Damage Index in systemic lupus erythematosus. Rheumatology (Oxford) 45(4):400–404CrossRef
102.
go back to reference Hirankarn N, Wongpiyabovorn J, Hanvivatvong O, Netsawang J, Akkasilpa S, Wongchinsri J et al (2006) The synergistic effect of FC gamma receptor IIa and interleukin-10 genes on the risk to develop systemic lupus erythematosus in Thai population. Tissue Antigens 68(5):399–406PubMedCrossRef Hirankarn N, Wongpiyabovorn J, Hanvivatvong O, Netsawang J, Akkasilpa S, Wongchinsri J et al (2006) The synergistic effect of FC gamma receptor IIa and interleukin-10 genes on the risk to develop systemic lupus erythematosus in Thai population. Tissue Antigens 68(5):399–406PubMedCrossRef
103.
go back to reference Guarnizo-Zuccardi P, Lopez Y, Giraldo M, Garcia N, Rodriguez L, Ramirez L et al (2007) Cytokine gene polymorphisms in Colombian patients with systemic lupus erythematosus. Tissue Antigens 70(5):376–382PubMedCrossRef Guarnizo-Zuccardi P, Lopez Y, Giraldo M, Garcia N, Rodriguez L, Ramirez L et al (2007) Cytokine gene polymorphisms in Colombian patients with systemic lupus erythematosus. Tissue Antigens 70(5):376–382PubMedCrossRef
104.
go back to reference Lin PW, Huang CM, Huang CC, Tsai CH, Tsai JJ, Chang CP et al (2007) The association of −627 interleukin-10 promoter polymorphism in Chinese patients with systemic lupus erythematosus. Clin Rheumatol 26(3):298–301PubMedCrossRef Lin PW, Huang CM, Huang CC, Tsai CH, Tsai JJ, Chang CP et al (2007) The association of −627 interleukin-10 promoter polymorphism in Chinese patients with systemic lupus erythematosus. Clin Rheumatol 26(3):298–301PubMedCrossRef
105.
go back to reference Rosado S, Rua-Figueroa I, Vargas JA, Garcia-Laorden MI, Losada-Fernandez I, Martin-Donaire T et al (2008) Interleukin-10 promoter polymorphisms in patients with systemic lupus erythematosus from the Canary Islands. Int J Immunogenet 35(3):235–242PubMedCrossRef Rosado S, Rua-Figueroa I, Vargas JA, Garcia-Laorden MI, Losada-Fernandez I, Martin-Donaire T et al (2008) Interleukin-10 promoter polymorphisms in patients with systemic lupus erythematosus from the Canary Islands. Int J Immunogenet 35(3):235–242PubMedCrossRef
106.
go back to reference Sobkowiak A, Lianeri M, Wudarski M, Łacki JK, Jagodziński PP (2009) Genetic variation in the interleukin-10 gene promoter in Polish patients with systemic lupus erythematosus. Rheumatol Int 29(8):921–925PubMedCrossRef Sobkowiak A, Lianeri M, Wudarski M, Łacki JK, Jagodziński PP (2009) Genetic variation in the interleukin-10 gene promoter in Polish patients with systemic lupus erythematosus. Rheumatol Int 29(8):921–925PubMedCrossRef
107.
go back to reference Lin YJ, Wan L, Huang CM, Sheu JJ, Chen SY, Lin TH et al (2010) IL-10 and TNF-alpha promoter polymorphisms in susceptibility to systemic lupus erythematosus in Taiwan. Clin Exp Rheumatol 28(3):318–324PubMed Lin YJ, Wan L, Huang CM, Sheu JJ, Chen SY, Lin TH et al (2010) IL-10 and TNF-alpha promoter polymorphisms in susceptibility to systemic lupus erythematosus in Taiwan. Clin Exp Rheumatol 28(3):318–324PubMed
108.
go back to reference Zhou M, Ding L, Peng H, Wang B, Huang F, Xu WD et al (2013) Association of the interleukin-10 gene polymorphism (−1082A/G) with systemic lupus erythematosus: a meta-analysis. Lupus 22(2):128–135PubMedCrossRef Zhou M, Ding L, Peng H, Wang B, Huang F, Xu WD et al (2013) Association of the interleukin-10 gene polymorphism (−1082A/G) with systemic lupus erythematosus: a meta-analysis. Lupus 22(2):128–135PubMedCrossRef
109.
go back to reference Song GG, Choi SJ, Ji JD, Lee YH (2013) Associations between interleukin-10 polymorphisms and susceptibility to systemic lupus erythematosus: a meta-analysis. Hum Immunol 74(3):364–370PubMedCrossRef Song GG, Choi SJ, Ji JD, Lee YH (2013) Associations between interleukin-10 polymorphisms and susceptibility to systemic lupus erythematosus: a meta-analysis. Hum Immunol 74(3):364–370PubMedCrossRef
110.
go back to reference Eskdale J, Kube D, Gallagher G (1996) A second polymorphic dinucleotide repeat in the 5′ flanking region of the human IL10 gene. Immunogenetics 45(1):82–83PubMedCrossRef Eskdale J, Kube D, Gallagher G (1996) A second polymorphic dinucleotide repeat in the 5′ flanking region of the human IL10 gene. Immunogenetics 45(1):82–83PubMedCrossRef
111.
go back to reference Eskdale J, Wordsworth P, Bowman S, Field M, Gallagher G (1997) Association between polymorphisms at the human IL-10 locus and systemic lupus erythematosus. Tissue Antigens 49(6):635–639PubMedCrossRef Eskdale J, Wordsworth P, Bowman S, Field M, Gallagher G (1997) Association between polymorphisms at the human IL-10 locus and systemic lupus erythematosus. Tissue Antigens 49(6):635–639PubMedCrossRef
112.
go back to reference Mehrian R, Quismorio FP Jr, Strassmann G, Stimmler MM, Horwitz DA, Kitridou RC et al (1998) Synergistic effect between IL-10 and bcl-2 genotypes in determining susceptibility to systemic lupus erythematosus. Arthritis Rheum 41(4):596–602PubMedCrossRef Mehrian R, Quismorio FP Jr, Strassmann G, Stimmler MM, Horwitz DA, Kitridou RC et al (1998) Synergistic effect between IL-10 and bcl-2 genotypes in determining susceptibility to systemic lupus erythematosus. Arthritis Rheum 41(4):596–602PubMedCrossRef
113.
go back to reference Alarcón-Riquelme ME, Lindqvist AK, Jonasson I, Johanneson B, Sandino S, Alcocer-Varela J et al (1999) Genetic analysis of the contribution of IL10 to systemic lupus erythematosus. J Rheumatol 26(10):2148–2152PubMed Alarcón-Riquelme ME, Lindqvist AK, Jonasson I, Johanneson B, Sandino S, Alcocer-Varela J et al (1999) Genetic analysis of the contribution of IL10 to systemic lupus erythematosus. J Rheumatol 26(10):2148–2152PubMed
114.
go back to reference Schotte H, Gaubitz M, Willeke P, Tidow N, Assmann G, Domschke W et al (2004) Interleukin-10 promoter microsatellite polymorphisms in systemic lupus erythematosus: association with the anti-Sm immune response. Rheumatology (Oxford) 43(11):1357–1363CrossRef Schotte H, Gaubitz M, Willeke P, Tidow N, Assmann G, Domschke W et al (2004) Interleukin-10 promoter microsatellite polymorphisms in systemic lupus erythematosus: association with the anti-Sm immune response. Rheumatology (Oxford) 43(11):1357–1363CrossRef
115.
go back to reference Ou TT, Tsai WC, Chen CJ, Chang JG, Yen JH, Wang WS et al (1998) Genetic analysis of interleukin-10 promoter region in patients with systemic lupus erythematosus in Taiwan. Kaohsiung J Med Sci 14(10):599–606PubMed Ou TT, Tsai WC, Chen CJ, Chang JG, Yen JH, Wang WS et al (1998) Genetic analysis of interleukin-10 promoter region in patients with systemic lupus erythematosus in Taiwan. Kaohsiung J Med Sci 14(10):599–606PubMed
116.
go back to reference Nath SK, Harley JB, Lee YH (2005) Polymorphisms of complement receptor 1 and interleukin-10 genes and systemic lupus erythematosus: a meta-analysis. Hum Genet 118(2):225–234PubMedCrossRef Nath SK, Harley JB, Lee YH (2005) Polymorphisms of complement receptor 1 and interleukin-10 genes and systemic lupus erythematosus: a meta-analysis. Hum Genet 118(2):225–234PubMedCrossRef
117.
go back to reference Lin SY, Hsieh SC, Lin YC, Lee CN, Tsai MH, Lai LC et al (2012) A whole genome methylation analysis of systemic lupus erythematosus: hypomethylation of the IL10 and IL1R2 promoters is associated with disease activity. Genes Immun 13(3):214–220PubMedCrossRef Lin SY, Hsieh SC, Lin YC, Lee CN, Tsai MH, Lai LC et al (2012) A whole genome methylation analysis of systemic lupus erythematosus: hypomethylation of the IL10 and IL1R2 promoters is associated with disease activity. Genes Immun 13(3):214–220PubMedCrossRef
118.
go back to reference Zhao M, Tang J, Gao F, Wu X, Liang Y, Yin H et al (2010) Hypomethylation of IL10 and IL13 promoters in CD4+ T cells of patients with systemic lupus erythematosus. J Biomed Biotechnol 2010:931018PubMed Zhao M, Tang J, Gao F, Wu X, Liang Y, Yin H et al (2010) Hypomethylation of IL10 and IL13 promoters in CD4+ T cells of patients with systemic lupus erythematosus. J Biomed Biotechnol 2010:931018PubMed
119.
go back to reference DiMartino SJ, Yuan W, Redecha P, Ivashkiv LB, Salmon JE (2008) Insoluble immune complexes are most effective at triggering IL-10 production in human monocytes and synergize with TLR ligands and C5a. Clin Immunol 127(1):56–65PubMedCrossRef DiMartino SJ, Yuan W, Redecha P, Ivashkiv LB, Salmon JE (2008) Insoluble immune complexes are most effective at triggering IL-10 production in human monocytes and synergize with TLR ligands and C5a. Clin Immunol 127(1):56–65PubMedCrossRef
120.
go back to reference Cairns AP, Crockard AD, Bell AL (2003) Interleukin-10 receptor expression in systemic lupus erythematosus and rheumatoid arthritis. Clin Exp Rheumatol 21(1):83–86PubMed Cairns AP, Crockard AD, Bell AL (2003) Interleukin-10 receptor expression in systemic lupus erythematosus and rheumatoid arthritis. Clin Exp Rheumatol 21(1):83–86PubMed
121.
go back to reference Valencia-Pacheco G, Layseca-Espinosa E, Niño-Moreno P, Portales-Pérez DP, Baranda L, Rosenstein Y et al (2006) Expression and function of IL-10R in mononuclear cells from patients with systemic lupus erythematosus. Scand J Rheumatol 35(5):368–378PubMedCrossRef Valencia-Pacheco G, Layseca-Espinosa E, Niño-Moreno P, Portales-Pérez DP, Baranda L, Rosenstein Y et al (2006) Expression and function of IL-10R in mononuclear cells from patients with systemic lupus erythematosus. Scand J Rheumatol 35(5):368–378PubMedCrossRef
122.
go back to reference Cui HD, Qi ZM, Yang LL, Qi L, Zhang N, Zhang XL et al (2011) Interleukin-10 receptor expression and signaling were down-regulated in CD4+ T cells of lupus nephritis patients. Clin Exp Immunol 165(2):163–171PubMedCrossRef Cui HD, Qi ZM, Yang LL, Qi L, Zhang N, Zhang XL et al (2011) Interleukin-10 receptor expression and signaling were down-regulated in CD4+ T cells of lupus nephritis patients. Clin Exp Immunol 165(2):163–171PubMedCrossRef
123.
go back to reference Figueroa-Vega N, Galindo-Rodríguez G, Bajaña S, Portales-Pérez D, Abud-Mendoza C, Sánchez-Torres C et al (2006) Phenotypic analysis of IL-10-treated, monocyte-derived dendritic cells in patients with systemic lupus erythematosus. Scand J Immunol 64(6):668–676PubMedCrossRef Figueroa-Vega N, Galindo-Rodríguez G, Bajaña S, Portales-Pérez D, Abud-Mendoza C, Sánchez-Torres C et al (2006) Phenotypic analysis of IL-10-treated, monocyte-derived dendritic cells in patients with systemic lupus erythematosus. Scand J Immunol 64(6):668–676PubMedCrossRef
124.
go back to reference Li YM, Chen ZQ, Yao X, Yang AZ, Li AS, Liu DM et al (2010) mRNA expression of chemokine receptors on peripheral blood mononuclear cells and correlation with clinical features in systemic lupus erythematosus patients. Chin Med Sci J 25(3):162–168PubMedCrossRef Li YM, Chen ZQ, Yao X, Yang AZ, Li AS, Liu DM et al (2010) mRNA expression of chemokine receptors on peripheral blood mononuclear cells and correlation with clinical features in systemic lupus erythematosus patients. Chin Med Sci J 25(3):162–168PubMedCrossRef
125.
go back to reference Qi ZM, Wang J, Sun ZR, Ma FM, Zhang QR, Hirose S et al (2005) Polymorphism of the mouse gene for the interleukin 10 receptor alpha chain (IL-10ra) and its association with the autoimmune phenotype. Immunogenetics 57(9):697–702PubMedCrossRef Qi ZM, Wang J, Sun ZR, Ma FM, Zhang QR, Hirose S et al (2005) Polymorphism of the mouse gene for the interleukin 10 receptor alpha chain (IL-10ra) and its association with the autoimmune phenotype. Immunogenetics 57(9):697–702PubMedCrossRef
126.
go back to reference Nakashima H, Akahoshi M, Tanaka Y, Yamaoka K, Ogami E, Nagano S et al (1999) Polymorphisms within the interleukin-10 receptor cDNA gene (IL10R) in Japanese patients with systemic lupus erythematosus. Rheumatology (Oxford) 38(11):1142–1144CrossRef Nakashima H, Akahoshi M, Tanaka Y, Yamaoka K, Ogami E, Nagano S et al (1999) Polymorphisms within the interleukin-10 receptor cDNA gene (IL10R) in Japanese patients with systemic lupus erythematosus. Rheumatology (Oxford) 38(11):1142–1144CrossRef
127.
go back to reference Xu Y, Chen ZQ, Li YM, Gong JQ, Li AS, Chen M et al (2007) Correlation between some Th1 and Th2 cytokine receptor gene polymorphisms and systemic lupus erythematosus in Chinese patients. Int J Dermatol 46(11):1129–1135PubMedCrossRef Xu Y, Chen ZQ, Li YM, Gong JQ, Li AS, Chen M et al (2007) Correlation between some Th1 and Th2 cytokine receptor gene polymorphisms and systemic lupus erythematosus in Chinese patients. Int J Dermatol 46(11):1129–1135PubMedCrossRef
128.
go back to reference Hermann J, Gruber S, Neufeld JB, Grundtner P, Graninger M, Graninger WB et al (2009) IL10R1 loss-of-function alleles in rheumatoid arthritis and systemic lupus erythematosus. Clin Exp Rheumatol 27(4):603–608PubMed Hermann J, Gruber S, Neufeld JB, Grundtner P, Graninger M, Graninger WB et al (2009) IL10R1 loss-of-function alleles in rheumatoid arthritis and systemic lupus erythematosus. Clin Exp Rheumatol 27(4):603–608PubMed
129.
go back to reference Gasche C, Grundtner P, Zwirn P, Reinisch W, Shaw SH, Zdanov A et al (2003) Novel variants of the IL-10 receptor 1 affect inhibition of monocyte TNF-alpha production. J Immunol 170(11):5578–5582PubMed Gasche C, Grundtner P, Zwirn P, Reinisch W, Shaw SH, Zdanov A et al (2003) Novel variants of the IL-10 receptor 1 affect inhibition of monocyte TNF-alpha production. J Immunol 170(11):5578–5582PubMed
130.
go back to reference Hikami K, Ehara Y, Hasegawa M, Fujimoto M, Matsushita M, Oka T et al (2008) Association of IL-10 receptor 2 (IL10RB) SNP with systemic sclerosis. Biochem Biophys Res Commun 373(3):403–407PubMedCrossRef Hikami K, Ehara Y, Hasegawa M, Fujimoto M, Matsushita M, Oka T et al (2008) Association of IL-10 receptor 2 (IL10RB) SNP with systemic sclerosis. Biochem Biophys Res Commun 373(3):403–407PubMedCrossRef
Metadata
Title
Role of interleukin-10 and interleukin-10 receptor in systemic lupus erythematosus
Authors
Hui Peng
Wei Wang
Mo Zhou
Rui Li
Hai-Feng Pan
Dong-Qing Ye
Publication date
01-09-2013
Publisher
Springer London
Published in
Clinical Rheumatology / Issue 9/2013
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI
https://doi.org/10.1007/s10067-013-2294-3

Other articles of this Issue 9/2013

Clinical Rheumatology 9/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

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.

Developed by: Springer Medicine