Cytokines and their roles in the pathogenesis of systemic lupus erythematosus: From basics to recent advances

Journal of Biomedicine and Biotechnology

Volumn 2010, Issue , 2010, Pages

  Lai, Kar Neng ^a   Yap, Desmond Yat Hin ^a  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERFERON TYPE 1; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 6; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CYTOKINE;

AUTOIMMUNITY; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL MATURATION; CYTOKINE PRODUCTION; CYTOKINE RELEASE; HUMAN; IMMUNOPATHOGENESIS; INFLAMMATION; LYMPHOCYTE PROLIFERATION; NONHUMAN; REVIEW; SYSTEMIC LUPUS ERYTHEMATOSUS; TH17 CELL; ANIMAL; BIOLOGICAL MODEL; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CYTOKINES; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MODELS, BIOLOGICAL;

EID: 77952540303     PISSN: 11107243     EISSN: 11107251     Source Type: Journal    
DOI: 10.1155/2010/365083     Document Type: Review

References (104)

1. Hiran T., IL-6 and its receptor International Reviews of Immunology 1998 16 249 284
2. Schimpl A., Wecker E., Replacement of T-cell function by a T-cell product Nature: New Biology 1972 237 70 15 17
3. Tackey E., Lipsky P. E., Illei G. G., Rationale for interleukin-6 blockade in systemic lupus erythematosus Lupus 2004 13 5 339 343 (Pubitemid 38788493)
4. Suzuki H., Yasukawa K., Saito T., Serum soluble interleukin-6 receptor in MRL/lpr mice is elevated with age and mediates the interleukin-6 signal European Journal of Immunology 1993 23 5 1078 1082
5. Tang B., Matsuda T., Akira S., Age-associated increase in interleukin 6 in MRL/lpr mice International Immunology 1991 3 3 273 278
6. Ryffel B., Car B. D., Gunn H., Roman D., Hiestand P., Mihatsch M. J., Interleukin-6 exacerbates glomerulonephritis in (NZBxNZW)F1 mice American Journal of Pathology 1994 144 5 927 937
7. Cash H., Relle M., Menke J., Interleukin 6 (IL-6) deficiency delays lupus nephritis in MRL-F a s l p r mice: the IL-6 pathway as a new therapeutic target in treatment of autoimmune kidney disease in systemic lupus erythematosus Journal of Rheumatology 2010 37 1 60 70
8. Finck B. K., Chan B., Wofsy D., Interleukin 6 promotes murine lupus in NZB/NZW F1 mice Journal of Clinical Investigation 1994 94 2 585 591
9. Mihara M., Takagi N., Takeda Y., Ohsugi Y., IL-6 receptor blockage inhibits the onset of autoimmune kidney disease in NZB/WF1 mice Clinical and Experimental Immunology 1998 112 3 397 402
10. Maeda K., Malykhin A., Teague-Weber B. N., Sun X.-H., Farris A. D., Coggeshall K. M., Interleukin-6 aborts lymphopoiesis and elevates production of myeloid cells in systemic lupus erythematosus-prone B6.Sle1.Yaa animals Blood 2009 113 19 4534 4540
11. Tagoh H., Kishi H., Muraguchi A., Molecular cloning and characterization of a novel stromal cell-derived cDNA encoding a protein that facilitates gene activation of recombination activating gene (RAG)-1 in human lymphoid progenitors Biochemical and Biophysical Research Communications 1996 221 3 744 749
12. Pflegerl P., Vesely P., Hantusch B., Epidermal loss of JunB leads to a SLE phenotype due to hyper IL-6 signaling Proceedings of the National Academy of Sciences of the United States of America 2010 106 48 20423 20428
13. Grondal G., Gunnarsson I., Ronnelid J., Cytokine production, serum levels and disease activity in systemic lupus erythematosus Clinical and Experimental Rheumatology 2000 18 565 570
14. Linker-Israeli M., Deans R. J., Wallace D. J., Prehn J., Ozeri-Chen T., Klinenberg J. R., Elevated levels of endogenous IL-6 in systemic lupus erythematosus: a putative role in pathogenesis Journal of Immunology 1991 147 1 117 123
15. Klashman D. J., Martin R. A., Martinez-Maza O., Stevens R. H., In vitro regulation of B cell differentiation by interleukin-6 and soluble CD23 in systemic lupus erythematosus B cell subpopulations and antigen-induced normal B cells Arthritis Rheumatism 1991 34 3 276 286
16. Kitani A., Hara M., Hirose T., Autostimulatory effects of IL-6 on excessive B cell differentiation in patients with systemic lupus erythematosus: analysis of IL-6 production and IL-6R expression Clinical and Experimental Immunology 1992 88 1 75 83
17. Kitani A., Hara M., Hirose T., Heterogeneity of B cell responsiveness to interleukin 4, interleukin 6 and low molecular weight B cell growth factor in discrete stages of B cell activation in patients with systemic lupus erythematosus Clinical and Experimental Immunology 1989 77 1 31 36
18. Garaud S., Le Dantec C., Jousse-Joulin S., IL-6 modulates CD5 expression in B cells from patients with lupus by regulating DNA methylation Journal of Immunology 2009 182 9 5623 5632
19. Iwano M., Dohi K., Hirata E., Urinary levels of IL-6 in patients with active lupus nephritis Clinical Nephrology 1993 40 1 16 21
20. Tsai C.-Y., Wu T.-H., Yu C.-L., Lu J.-Y., Tsai Y.-Y., Increased excretions of 2-microglobulin, IL-6, and IL-8 and decreased excretion of Tamm-Horsfall glycoprotein in urine of patients with active lupus nephritis Nephron 2000 85 3 207 214
21. Herrera-Esparza R., Barbosa-Cisneros O., Villalobos-Hurtado R., Avalos-Diaz E., Renal expression of IL-6 and TNF-α genes in lupus nephritis Lupus 1998 7 3 154 158 (Pubitemid 28190678)
22. Hirohata S., Kanai Y., Mitsuo A., Tokano Y., Hashimoto H., Accuracy of cerebrospinal fluid IL-6 testing for diagnosis of lupus psychosis. A multicenter retrospective study Clinical Rheumatology 2009 28 11 1319 1323
23. Esposito P., Balletta M. M., Procino A., Postiglione L., Memoli B., Interleukin-6 release from peripheral mononuclear cells is associated to disease activity and treatment response in patients with lupus nephritis Lupus 2009 18 14 1329 1330
24. De La Torre M., Urra J. M., Blanco J., Raised expression of cytokine receptor gp130 subunit on peripheral lymphocytes of patients with active lupus. A useful tool for monitoring the disease activity? Lupus 2009 18 3 216 222
25. Illei G., Yarboro C., Shirota Y., Tocilizumab (humanized anti-IL6 Receptor Monoclonal Antibody) in patients with systemic lupus erythematosus (SLE): safety, tolerability and preliminary efficacy Arthritis Rheumatism 2006 54 12, supplement 4043
26. Llorente L., Zou W., Levy Y., Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus Journal of Experimental Medicine 1995 181 3 839 844
27. Ronnelid J., Tejde A., Mathsson L., Nilsson-Ekdahl K., Nilsson B., Immune complexes from SLE sera induce IL10 production from normal peripheral blood mononuclear cells by an FcγRII dependent mechanismml: implications for a possible vicious cycle maintaining B cell hyperactivity in SLE Annals of the Rheumatic Diseases 2003 62 1 37 42
28. Sun K. H., Yu C. L., Tang S. J., Sun G. H., Monoclonal anti-double-stranded DNA autoantibody stimulates the expression and release of IL1-, IL-6, IL-8, IL-10 and TNF-α from normal human mononuclear cells involving in the lupus pathogenesis Immunology 2000 99 352 360
29. Uhm W.-S., Na K., Song G.-W., Cytokine balance in kidney tissue from lupus nephritis patients Rheumatology 2003 42 8 935 938
30. Ishida H., Muchamuel T., Sakaguchi S., Andrade S., Menon S., Howard M., Continuous administration of anti-interleukin 10 antibodies delays onset of autoimmunity in NZB/W F1 mice Journal of Experimental Medicine 1994 179 1 305 310
31. + suppressor T cells: more questions than answers Nature Reviews Immunology 2002 2 6 389 400
32. Lauwerys B. R., Garot N., Renauld J.-C., Houssiau F. A., Interleukin-10 blockade corrects impaired in vitro cellular immune responses of systemic lupus erythematosus patients Arthritis Rheumatism 2000 43 9 1976 1981
33. Ravirajan C. T., Wang Y., Matis L. A., Effect of neutralizing antibodies to IL-10 and C5 on the renal damage caused by a pathogenic human anti-ds DNA antibody Rheumatology 2004 43 4 442 447
34. Llorente L., Richaud-Patin Y., Garca-Padilla C, Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic Lupus erythematosus Arthritis Rheumatism 2000 43 8 1790 1800
35. Rouvier E., Luciani M.-F., Mattei M.-G., Denizot F., Golstein P., CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus Saimiri gene Journal of Immunology 1993 150 12 5445 5456
36. Weaver C. T., Hatton R. D., Mangan P. R., Harrington L. E., IL-17 family cytokines and the expanding diversity of effector T cell lineages Annual Review of Immunology 2007 25 821 852
37. 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 Journal of Rheumatology 2008 35 3 515 519
38. Albanesi C., Cavani A., Girolomoni G., IL-17 is produced by nickel-specific T lymphocytes and regulates ICAM-1 expression and chemokine production in human keratinocytes: synergistic or antagonist effects with IFN-and TNF-α Journal of Immunology 1999 162 1 494 502
39. Bettelli E., Carrier Y., Gao W., Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells Nature 2006 441 7090 235 238
40. Mangan P. R., Harrington L. E., O'Quinn D. B., Transforming growth factor-β induces development of the T H 17 lineage Nature 2006 441 7090 231 234
41. Langrish C. L., Chen Y., Blumenschein W. M., IL-23 drives a pathogenic T cell population that induces autoimmune inflammation Journal of Experimental Medicine 2005 201 2 233 240
42. Aggarwal S., Ghilardi N., Xie M.-H., De Sauvage F. J., Gurney A. L., Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17 Journal of Biological Chemistry 2003 278 3 1910 1914
43. Nalbandian A., Crispin J. C., Tsokos G. C., Interleukin-17 and systemic lupus erythematosus: current concepts Clinical and Experimental Immunology 2009 157 2 209 215
44. + T cells mediate accelerated ischemia/reperfusion-induced injury in autoimmunity-prone mice Clinical Immunology 2009 130 3 313 321
45. Hsu H.-C., Yang P. A., Wang J., Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice Nature Immunology 2008 9 2 166 175
46. Kang H.-K., Liu M., Datta S. K., Low-dose peptide tolerance therapy of lupus generates plasmacytoid dendritic cells that cause expansion of autoantigen-specific regulatory T cells and contraction of inflammatory Th17 cells Journal of Immunology 2007 178 12 7849 7858
47. Zhang Z., Kyttaris V. C., Tsokos G. C., The role of IL-23/IL-17 axis in lupus nephritis Journal of immunology 2009 183 5 3160 3169
48. Wong C. K., Lit L. C. W., Tam L. S., Li E. K. M., Wong P. T. Y., Lam C. W. K., Hyperproduction of IL-23 and IL-17 in patients with systemic lupus erythematosus: implications for Th17-mediated inflammation in auto-immunity Clinical Immunology 2008 127 3 385 393
49. Crispin J. C., Oukka M., Bayliss G., Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys Journal of Immunology 2008 181 12 8761 8766
50. Nardelli B., Belvedere O., Roschke V., Synthesis and release of B-lymphocyte stimulator from myeloid cells Blood 2001 97 1 198 204
51. Moore P. A., Belvedere O., Orr A., BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator Science 1999 285 5425 260 263
52. Schiemann B., Gommerman J. L., Vora K., An essential role for BAFF in the normal development of B cells through a BCMA-independent pathway Science 2001 293 5537 2111 2114
53. Bossen C., Cachero T. G., Tardivel A., TACI, unlike BAFF-R, is solely activated by oligomeric BAFF and APRIL to support survival of activated B cells and plasmablasts Blood 2008 111 3 1004 1012
54. Xu S., Lam K.-P., B-cell maturation protein, which binds the tumor necrosis factor family members BAFF and APRIL, is dispensable for humoral immune responses Molecular and Cellular Biology 2001 21 12 4067 4074
55. Yan M., Brady J. R., Chan B., Identification of a novel receptor for B lymphocyte stimulator that is mutated in a mouse strain with severe B cell deficiency Current Biology 2001 11 19 1547 1552
56. Hikida M., Johmura S., Hashimoto A., Takezaki M., Kurosaki T., Coupling between B cell receptor and phospholipase C-2 is essential for mature B cell development Journal of Experimental Medicine 2003 198 4 581 589
57. Hatada E. N., Do R. K. G., Orlofsky A., NF-κB1 p50 is required for BLyS attenuation of apoptosis but dispensable for processing of NF-κB2 p100 to p52 in quiescent mature B cells Journal of Immunology 2003 171 2 761 768
58. Mackay F., Woodcock S. A., Lawton P., Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations Journal of Experimental Medicine 1999 190 11 1697 1710
59. Gross J. A., Johnston J., Mudri S., TACI and BCMA are receptors for a TNF homologue implicated in B-cell autoimmune disease Nature 2000 404 6781 995 999
60. Hondowicz B. D., Alexander S. T., Quinn W. J., The role of BLyS/BLyS receptors in anti-chromatin B cell regulation International Immunology 2007 19 4 465 475
61. Thompson J. S., Schneider P., Kalled S. L., BAFF binds to the tumor necrosis factor receptor-like molecule B cell maturation antigen and is important for maintaining the peripheral B cell population Journal of Experimental Medicine 2000 192 1 129 135
62. Groom J., Mackay F., B cells flying solo Immunology and Cell Biology 2008 86 1 40 46
63. Cheema G. S., Roschke V., Hilbert D. M., Stohl W., Elevated serum B lymphocyte stimulator levels in patients with systemic immune-based rheumatic diseases Arthritis Rheumatism 2001 44 6 1313 1319
64. Stohl W., Metyas S., Tan S.-M., B lymphocyte stimulator overexpression in patients with systemic lupus erythematosus: longitudinal observations Arthritis Rheumatism 2003 48 12 3475 3486
65. Furie R., Stohl W., Ginzler E. M., Biologic activity and safety of belimumab, a neutralizing anti-B-lymphocyte stimulator (BLyS) monoclonal antibody: a phase I trial in patients with systemic lupus erythematosus Arthritis Research and Therapy 2008 10 5, article R109
66. Dall'Era M., Chakravarty E., Wallace D., Reduced B lymphocyte and immunoglobulin levels after atacicept treatment in patients with systemic lupus erythematosus: results of a multicenter, phase Ib, double-blind, placebo-controlled, dose-escalating trial Arthritis Rheumatism 2007 56 12 4142 4150
67. Takeuchi O., Akira S., Innate immunity to virus infection Immunological Reviews 2009 227 1 75 86
68. Beutler B., The Toll-like receptors: analysis by forward genetic methods Immunogenetics 2005 57 6 385 392
69. Fitzgerald-Bocarsly P., Dai J., Singh S., Plasmacytoid dendritic cells and type I IFN: 50 years of convergent history Cytokine and Growth Factor Reviews 2008 19 1 3 19
70. Lovgren T., Eloranta M.-L., Bave U., Induction of interferon-production in plasmacytoid dendritic cells by immune complexes containing nucleic acid released by necrotic or late apoptotic cells and lupus IgG Arthritis Rheumatism 2004 50 6 1861 1872
71. Baechler E. C., Batliwalla F. M., Karypis G., Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus Proceedings of the National Academy of Sciences of the United States of America 2003 100 5 2610 2615
72. Strandberg L., Ambrosi A., Espinosa A., Interferon-induces up-regulation and nuclear translocation of the Ro52 autoantigen as detected by a panel of novel Ro52-specific monoclonal antibodies Journal of Clinical Immunology 2008 28 3 220 231
73. Baccala R., Hoebe K., Kono D. H., Beutler B., Theofilopoulos A. N., TLR-dependent and TLR-independent pathways of type I interferon induction in systemic autoimmunity Nature Medicine 2007 13 5 543 551
74. Le Bon A., Thompson C., Kamphuis E., Cutting edge: enhancement of antibody responses through direct stimulation of B and T cells by type I IFN Journal of Immunology 2006 176 4 2074 2078
75. Uccellini M. B., Busconi L., Green N. M., Autoreactive B cells discriminate CpG-rich and CpG-poor DNA and this response is modulated by IFN-Journal of Immunology 2008 181 9 5875 5884
76. Bengtsson A. A., Sturfelt G., Truedsson L., Activation of type I interferon system in systemic lupus erythematosus correlates with disease activity but not with antiretroviral antibodies Lupus 2000 9 9 664 671
77. Blomberg S., Eloranta M. L., Cederblad B., Presence of cutaneous interferon-producing cells in patients with systemic lupus erythematosus Lupus 2001 10 7 484 490
78. Tucci M., Quatraro C., Lombardi L., Pellegrino C., Dammacco F., Silvestris F., Glomerular accumulation of plasmacytoid dendritic cells in active lupus nephritis: role of interleukin-18 Arthritis Rheumatism 2008 58 1 251 262
79. Fairhurst A.-M., Mathian A., Connolly J. E., Systemic IFN-drives kidney nephritis in B6.Sle123 mice European Journal of Immunology 2008 38 7 1948 1960
80. Santer D. M., Yoshio T., Minota S., Potent induction of IFN-and chemokines by autoantibodies in the cerebrospinal fluid of patients with neuropsychiatric lupus Journal of Immunology 2009 182 2 1192 1201
81. Santiago-Raber M.-L., Baccala R., Haraldsson K. M., Type-I interferon receptor deficiency reduces lupus-like disease in NZB mice Journal of Experimental Medicine 2003 197 6 777 788
82. Ioannou Y., Isenberg D. A., Current evidence for the induction of autoimmune rheumatic manifestations by cytokine therapy Arthritis Rheumatism 2000 43 7 1431 1442
83. Sigurdsson S., Nordmark G., Goring H. H. H., Polymorphisms in the tyrosine kinase 2 and interferon regulatory factor 5 genes are associated with systemic lupus erythematosus American Journal of Human Genetics 2005 76 3 528 537
84. Niewold T. B., Kelly J. A., Flesch M. H., Espinoza L. R., Harley J. B., Crow M. K., Association of the IRF5 risk haplotype with high serum interferon-activity in systemic lupus erythematosus patients Arthritis Rheumatism 2008 58 8 2481 2487
85. Remmers E. F., Plenge R. M., Lee A. T., STAT4 and the risk of rheumatoid arthritis and systemic lupus erythematosus The New England Journal of Medicine 2007 357 10 977 986
86. Graham D. S. C., Akil M., Vyse T. J., Association of polymorphisms across the tyrosine kinase gene, TYK2 in UK SLE families Rheumatology 2007 46 6 927 930
87. Niewold T. B., Hua J., Lehman T. J. A., Harley J. B., Crow M. K., High serum IFN-activity is a heritable risk factor for systemic lupus erythematosus Genes and Immunity 2007 8 6 492 502
88. Niewold T. B., Adler J. E., Glenn S. B., Lehman T. J. A., Harley J. B., Crow M. K., Age-and sex-related patterns of serum interferon-activity in lupus families Arthritis Rheumatism 2008 58 7 2113 2119
89. Sigurdsson S., Nordmark G., Garnier S., A risk haplotype of STAT4 for systemic lupus erythematosus is over-expressed, correlates with anti-dsDNA and shows additive effects with two risk alleles of IRF5 Human Molecular Genetics 2008 17 18 2868 2876
90. Bauer J. W., Baechler E. C., Petri M., Elevated serum levels of interferon-regulated chemokines are biomarkers for active human systemic lupus erythematosus PLoS Medicine 2006 3 12, article e491 2274 2284
91. Fu Q., Chen X., Cui H., Association of elevated transcript levels of interferon-inducible chemokines with disease activity and organ damage in systemic lupus erythematosus patients Arthritis Research and Therapy 2008 10 5, article R112
92. Wallace D. J., Petri M., Olsen N., MEDI-545, an anti-interferon monoclonal antibody, shows evidence of clinical activity in systemic lupus erythematosus Arthritis Rheumatism 2007 56 S562 S563
93. Jacob C. O., McDevitt H. O., Tumor necrosis factor-in murine autoimmune lupus nephritis Nature 1988 331 356 358
94. Kontoyiannis D., Kollias G., Accelerated autoimmunity and lupus nephritis in NZB mice with an engineered heterozygous deficiency in tumor necrosis factor European Journal of Immunology 2000 30 7 2038 2047
95. Yokoyama H., Kreft B., Kelley V. R., Biphasic increase in circulating and renal TNF-α in MRL-lpr mice with differing regulatory mechanisms Kidney International 1995 47 1 122 130
96. Brennan D. C., Yui M. A., Wuthrich R. P., Kelley V. E., Tumor necrosis factor and IL-1 in New Zealand black/white mice. Enhanced gene expression and acceleration of renal injury Journal of Immunology 1989 143 11 3470 3475
97. Edwards C. K., Zhou T., Zhang J., Inhibition of superantigen-induced proinflammatory cytokine production and inflammatory arthritis in MRL-Ipr/Ipr mice by a transcriptional inhibitor of TNF-α Journal of Immunology 1996 157 4 1758 1772
98. Deguchi Y., Kishimoto S., Tumour necrosis factor/cachectin plays a key role in autoimmune pulmonary inflammation in lupus-prone mice Clinical and Experimental Immunology 1991 85 3 392 395
99. Gabay C., Cakir N., Moral F., Circulating levels of tumor necrosis factor soluble receptors in systemic lupus erythematosus are significantly higher than in other rheumatic diseases and correlate with disease activity Journal of Rheumatology 1997 24 2 303 308
100. Mohan A. K., Edwards E. T., Cote T. R., Siegel J. N., Braun M. M., Drug-induced systemic lupus erythematosus and TNF-α blockers The Lancet 2002 360 9333 646
101. Shakoor N., Michalska M., Harris C. A., Block J. A., Drug-induced systemic lupus erythematosus associated with etanercept therapy The Lancet 2002 359 9306 579 580 (Pubitemid 34178442)
102. Neale T. J., Ruger B. M., Macaulay H., Tumor necrosis factor-is expressed by glomerular visceral epithelial cells in human membranous nephropathy American Journal of Pathology 1995 146 6 1444 1454
103. Aringer M., Graninger W. B., Steiner G., Smolen J. S., Safety and efficacy of tumor necrosis factor blockade in systemic lupus erythematosus: an open-label study Arthritis Rheumatism 2004 50 10 3161 3169
104. Hayat S. J., Uppal S. S., Narayanan Nampoory M. R., Johny K. V., Gupta R., Al-Oun M., Safety and efficacy of infliximab in a patient with active WHO class IV lupus nephritis Clinical Rheumatology 2007 26 6 973 975