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Journal of Biomedicine and Biotechnology
Volume 2011 (2011), Article ID 594809, 7 pages
http://dx.doi.org/10.1155/2011/594809
Review Article

The Role of Cytokine in the Lupus Nephritis

1Department of Disease Control and Homeostasis, School of Medicine, College of Medical, Pharmaceutical and Health Sciences, Kanazawa University, 13-1 Takara-machi, Kanazawa 920-8641, Japan
2Division of Blood Purification, Kanazawa University Hospital, Kanazawa, Japan
3Department of Laboratory Sciences, School of Medicine, College of Medical, Pharmaceutical and Health Sciences, Kanazawa University, Kanazawa, Japan

Received 26 May 2011; Accepted 12 August 2011

Academic Editor: Brian Poole

Copyright © 2011 Yasunori Iwata et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. S. Bomback and G. B. Appel, “Updates on the treatment of lupus nephritis,” Journal of the American Society of Nephrology, vol. 21, no. 12, pp. 2028–2035, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  2. H. Yokoyama, T. Wada, A. Hara et al., “The outcome and a new ISN/RPS 2003 classification of lupus nephritis in Japanese,” Kidney International, vol. 66, no. 6, pp. 2382–2388, 2004.
  3. V. R. Kelley, “Leukocyte-renal epithelial cell interactions regulate lupus nephritis,” Seminars in Nephrology, vol. 27, no. 1, pp. 59–68, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  4. D. Perry, A. Sang, Y. Yin, Y. Y. Zheng, and L. Morel, “Murine models of systemic lupus erythematosus,” Journal of Biomedicine and Biotechnology, vol. 2011, Article ID 271694, 19 pages, 2011. View at Publisher · View at Google Scholar · View at PubMed
  5. C. Gómez-Guerrero, P. Hernández-Vargas, O. López-Franco, G. Ortiz-Muñoz, and J. Egido, “Mesangial cells and glomerular inflammation: from the pathogenesis to novel therapeutic approaches,” Current Drug Targets, vol. 4, no. 3, pp. 341–351, 2005. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Yung, R. C. W. Tsang, J. K. H. Leung, and T. M. Chan, “Increased mesangial cell hyaluronan expression in lupus nephritis is mediated by anti-DNA antibody-induced IL-1β,” Kidney International, vol. 69, no. 2, pp. 272–280, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  7. S. Yung, Q. Zhang, Z. Z. Chen, W. C. Kwok, L. L. Sing, and M. C. Tak, “Anti-DNA antibody induction of protein kinase C phosphorylation and fibronectin synthesis in human and murine lupus and the effect of mycophenolic acid,” Arthritis and Rheumatism, vol. 60, no. 7, pp. 2071–2082, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. C. Gordon, G. E. Ranges, J. S. Greenspan, and D. Wofsy, “Chronic therapy with recombinant tumor necrosis factor-α in autoimmune NZB/NZW F1 mice,” Clinical Immunology and Immunopathology, vol. 52, no. 3, pp. 421–434, 1989. View at Scopus
  9. C. Gordon and D. Wofsy, “Effects of recombinant murine tumor necrosis factor-α on immune function,” Journal of Immunology, vol. 144, no. 5, pp. 1753–1758, 1990. View at Scopus
  10. D. Kontoyiannis and G. Kollias, “Accelerated autoimmunity and lupus nephritis in NZB mice with an engineered heterozygous deficiency in tumor necrosis factor,” European Journal of Immunology, vol. 30, no. 7, pp. 2038–2047, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. N. Jacob, H. Yang, L. Pricop et al., “Accelerated pathological and clinical nephritis in systemic lupus erythematosus-prone New Zealand mixed 2328 mice doubly deficient in TNF receptor 1 and TNF receptor 2 via a Th17-associated pathway,” Journal of Immunology, vol. 182, no. 4, pp. 2532–2541, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. C. K. Edwards III, T. Zhou, J. Zhang et al., “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, vol. 157, no. 4, pp. 1758–1772, 1996. View at Scopus
  13. Y. Deguchi and S. Kishimoto, “Tumour necrosis factor/cachectin plays a key role in autoimmune pulmonary inflammation in lupus-prone mice,” Clinical and Experimental Immunology, vol. 85, no. 3, pp. 392–395, 1991. View at Scopus
  14. T. Wada, T. Naito, R. C. Griffiths, T. M. Coffman, and V. R. Kelley, “Systemic autoimmune nephritogenic components induce CSF-1 and TNF-α in MRL kidneys,” Kidney International, vol. 52, no. 4, pp. 934–941, 1997. View at Scopus
  15. T. Wada, A. Schwarting, M. S. Chesnutt, D. Wofsy, and V. R. Kelly, “Nephritogenic cytokines and disease in MRL-Faslpr kidneys are dependent on multiple T-cell subsets,” Kidney International, vol. 59, no. 2, pp. 565–578, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  16. X. Su, T. Zhou, P. Yang, C. K. Edwards, and J. D. Mountz, “Reduction of arthritis and pneumonitis in motheaten mice by soluble tumor necrosis factor receptor,” Arthritis and Rheumatism, vol. 41, no. 1, pp. 139–149, 1998. View at Scopus
  17. R. Segal, M. Dayan, H. Zinger, and E. Mozes, “Suppression of experimental systemic lupus erythematosus (SLE) in mice via TNF inhibition by an anti-TNFα monoclonal antibody and by pentoxiphylline,” Lupus, vol. 10, no. 1, pp. 23–31, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Rahman and D. A. Isenberg, “Systemic lupus erythematosus,” The New England Journal of Medicine, vol. 358, no. 9, pp. 929–939, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  19. H. Yokoyama, M Takaeda, T. Wada, et al., “Glomerular ICAM-1 expression related to circulating TNF-α in human glomerulonephritis,” Nephron, vol. 76, no. 4, pp. 425–433, 1997.
  20. M. Aringer and J. S. Smolen, “The role of tumor necrosis factor-alpha in systemic lupus erythematosus,” Arthritis Research and Therapy, vol. 10, no. 1, article 202, 2008. View at Publisher · View at Google Scholar · View at PubMed
  21. R. Matsumura, K. Umemiya, T. Sugiyama et al., “Anti-tumor necrosis factor therapy in patients with difficult-to-treat lupus nephritis: a prospective series of nine patients,” Clinical and Experimental Rheumatology, vol. 27, no. 3, pp. 416–421, 2009.
  22. M. De Bandt, J. Sibilia, X. Le Loët et al., “Systemic lupus erythematosus induced by anti-tumour necrosis factor alpha therapy: a French national survey,” Arthritis Research & Therapy., vol. 7, no. 3, pp. R545–551, 2005. View at Scopus
  23. M. B. Stokes, K. Foster, G. S. Markowitz et al., “Development of glomerulonephritis during anti-TNF-alpha; therapy for rheumatoid arthritis,” Nephrology Dialysis Transplantation, vol. 20, no. 7, pp. 1400–1406, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  24. B. Liang, D. B. Gardner, D. E. Griswold, P. J. Bugelski, and X. Y. R. Song, “Anti-interleukin-6 monoclonal antibody inhibits autoimmune responses in a murine model of systemic lupus erythematosus,” Immunology, vol. 119, no. 3, pp. 296–305, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  25. B. A. Kiberd, “Interleukin-6 receptor blockage ameliorates murine lupus nephritis,” Journal of the American Society of Nephrology, vol. 4, no. 1, pp. 58–61, 1993. View at Scopus
  26. B. Ryffel, B. D. Car, H. Gunn, D. Roman, P. Hiestand, and M. J. Mihatsch, “Interleukin-6 exacerbates glomerulonephritis in (NZB × NZW)F1 mice,” American Journal of Pathology, vol. 144, no. 5, pp. 927–937, 1994. View at Scopus
  27. H. B. Richards, M. Satoh, M. Shaw, C. Libert, V. Poli, and W. H. Reeves, “Interleukin 6 dependence of anti-DNA antibody production: evidence for two pathways of autoantibody formation in pristane-induced lupus,” Journal of Experimental Medicine, vol. 188, no. 5, pp. 985–990, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Wan, C. Xia, and L. Morel, “IL-6 produced by dendritic cells from lupus-prone mice inhibits CD4+ CD25+ T cell regulatory functions,” Journal of Immunology, vol. 178, no. 1, pp. 271–279, 2007. View at Scopus
  29. Y. Nishitani, A. Kubo, M. Iwano et al., “Imbalance between interleukin-6 and adrenomedullin mRNA levels in peripheral blood mononuclear cells of patients with lupus nephritis,” Clinical and Experimental Immunology, vol. 124, no. 2, pp. 330–336, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. G. G. Illei, Y. Shirota, C. H. Yarboro et al., “Tocilizumab in systemic lupus erythematosus: data on safety, preliminary efficacy, and impact on circulating plasma cells from an open-label phase I dosage-escalation study,” Arthritis and Rheumatism, vol. 62, no. 2, pp. 542–552, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  31. J. F. McHale, O. A. Harari, D. Marshall, and D. O. Haskard, “TNF-α and IL-1 sequentially induce endothelial ICAM-1 and VCAM-1 expression in MRL/lpr lupus-prone mice,” Journal of Immunology, vol. 163, no. 7, pp. 3993–4000, 1999. View at Scopus
  32. T. V. Lebedeva and A. K. Singh, “Increased responsiveness of B cells in the murine MRL/Lpr model of lupus nephritis to interleukin-1β,” Journal of the American Society of Nephrology, vol. 5, no. 7, pp. 1530–1534, 1995. View at Scopus
  33. T. Takemura, K. Yoshioka, K. Murakami et al., “Cellular localization of inflammatory cytokines in human glomerulonephritis,” Virchows Archiv, vol. 424, no. 5, pp. 459–464, 1994. View at Scopus
  34. B. A. Kiberd and A. W. Stadnyk, “Established murine lupus nephritis does not respond to exogenous interleukin-1 receptor antagonist; a role for the endogenous molecule?” Immunopharmacology, vol. 30, no. 2, pp. 131–137, 1995. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Iwata, T. Wada, K. Furuichi et al., “p38 mitogen-activated protein kinase contributes to autoimmune renal injury in MRL-Faslpr mice,” Journal of the American Society of Nephrology, vol. 14, no. 1, pp. 57–67, 2003. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Iwata, K. Furuichi, N. Sakai et al., “Dendritic cells contribute to autoimmune kidney injury in MRL-Fas lpr mice,” Journal of Rheumatology, vol. 36, no. 2, pp. 306–314, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  37. V. D. D’Agati, “Renal Disease in Systemic Lupus Erythematosus, Mixed Connective Tissue Disease, Sjögren’s Syndrome, and Rheumatoid Arthritis,” in Heptinstall’s Pathology of the Kidney, 2006.
  38. Z. Zhang, V. C. Kyttaris, and G. C. Tsokos, “The role of IL-23/IL-17 axis in lupus nephritis,” Journal of Immunology, vol. 183, no. 5, pp. 3160–3169, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  39. O. M. Steinmetz, J. E. Turner, H. J. Paust et al., “CXCR3 mediates renal Th1 and Th17 immune response in murine lupus nephritis,” Journal of Immunology, vol. 183, no. 7, pp. 4693–4704, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  40. V. C. Kyttaris, Z. Zhang, V. K. Kuchroo, M. Oukka, and G. C. Tsokos, “Cutting edge: IL-23 receptor deficiency prevents the development of lupus nephritis in C57BL/6-lpr/lpr mice,” Journal of Immunology, vol. 184, no. 9, pp. 4605–4609, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  41. Y. Wang, S. Ito, Y. Chino et al., “Laser microdissection-based analysis of cytokine balance in the kidneys of patients with lupus nephritis,” Clinical and Experimental Immunology, vol. 159, no. 1, pp. 1–10, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  42. J. C. Crispín and G. C. Tsokos, “Human TCR-αβ+ CD4 CD8 T cells can derive from CD8+ T cells and display an inflammatory effector phenotype,” Journal of Immunology, vol. 183, no. 7, pp. 4675–4681, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  43. E. Kikawada, D. M. Lenda, and V. R. Kelley, “IL-12 deficiency in MRL-Faslpr mice delays nephritis and intrarenal IFN-γ expression, and diminishes systemic pathology,” Journal of Immunology, vol. 170, no. 7, pp. 3915–3925, 2003. View at Scopus
  44. C. E. Carvalho-Pinto, M. I. García, M. Mellado et al., “Autocrine production of IFN-γ by macrophages controls their recruitment to kidney and the development of glomerulonephritis in MRL/lpr mice,” Journal of Immunology, vol. 169, no. 2, pp. 1058–1067, 2002. View at Scopus
  45. A. Schwarting, T. Wada, K. Kinoshita, G. Tesch, and V. R. Kelley, “IFN-γ receptor signaling is essential for the initiation, acceleration, and destruction of autoimmune kidney disease in MRL-Fas(lpr) mice,” Journal of Immunology, vol. 161, no. 1, pp. 494–503, 1998. View at Scopus
  46. M. Ramanujam, P. Kahn, W. Huang et al., “Interferon-α treatment of Female (NZW × BXSB)F1 mice mimics some but not all features associated with the Yaa mutation,” Arthritis and Rheumatism, vol. 60, no. 4, pp. 1096–1101, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  47. Z. Liu, R. Bethunaickan, W. Huang et al., “Interferon-α accelerates murine systemic lupus erythematosus in a T cell-dependent manner,” Arthritis and Rheumatism, vol. 63, no. 1, pp. 219–229, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  48. H. Agrawal, N. Jacob, E. Carreras et al., “Deficiency of type I IFN receptor in lupus-prone New Zealand mixed 2328 mice decreases dendritic cell numbers and activation and protects from disease,” Journal of Immunology, vol. 183, no. 9, pp. 6021–6029, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  49. J. D. Hron and S. L. Peng, “Type I IFN protects against murine lupus,” Journal of Immunology, vol. 173, no. 3, pp. 2134–2142, 2004. View at Scopus
  50. A. Schwarting, K. Paul, S. Tschirner et al., “Interferon-β: a therapeutic for autoimmune lupus in MRL-Fas lpr mice,” Journal of the American Society of Nephrology, vol. 16, no. 11, pp. 3264–3272, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  51. A. N. Theofilopoulos, R. Baccala, B. Beutler, and D. H. Kono, “Type I interferons (α/β) in immunity and autoimmunity,” Annual Review of Immunology, vol. 23, pp. 307–336, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  52. S. C. Satchell, O. Buchatska, S. B. Khan et al., “Interferon-β reduces proteinuria in experimental glomerulonephritis,” Journal of the American Society of Nephrology, vol. 18, no. 11, pp. 2875–2884, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  53. J. Faust, J. Menke, J. Kriegsmann et al., “Correlation of renal tubular epithelial cell-derived interleukin-18 up-regulation with disease activity in MRL-Faslpr mice with autoimmune lupus nephritis,” Arthritis and Rheumatism, vol. 46, no. 11, pp. 3083–3095, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  54. H. A. Shui, S. M. Ka, W. M. Wu et al., “LPS-evoked IL-18 expression in mesangial cells plays a role in accelerating lupus nephritis,” Rheumatology, vol. 46, no. 8, pp. 1277–1284, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  55. P. Bossù, D. Neumann, E. Del Giudice et al., “IL-18 cDNA vaccination protects mice from spontaneous lupus-like autoimmune disease,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 2, pp. 14181–14186, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  56. G. V. Halade, M. M. Rahman, A. Bhattacharya, J. L. Barnes, B. Chandrasekar, and G. Fernandes, “Docosahexaenoic acid-enriched fish oil attenuates kidney disease and prolongs median and maximal life span of autoimmune lupus-prone mice,” Journal of Immunology, vol. 184, no. 9, pp. 5280–5286, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  57. K. Masutani, M. Akahoshi, K. Tsuruya et al., “Predominance of Th1 immune response in diffuse proliferative lupus nephritis,” Arthritis and Rheumatism, vol. 44, no. 9, pp. 2097–2106, 2001. View at Scopus
  58. H. Yokoyama, T. Takabatake, M. Takaeda et al., “Up-regulated MHC-class II expression and γ-IFN and soluble IL-2R in lupus nephritis,” Kidney International, vol. 42, no. 3, pp. 755–763, 1992. View at Scopus
  59. W. S. Uhm, K. Na, G. W. Song et al., “Cytokine balance in kidney tissue from lupus nephritis patients,” Rheumatology, vol. 42, no. 8, pp. 935–938, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  60. R. W. Y. Chan, F. M. M. Lai, E. K. M. Li et al., “Intrarenal cytokine gene expression in lupus nephritis,” Annals of the Rheumatic Diseases, vol. 66, no. 7, pp. 886–892, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  61. M. Tucci, C. Quatraro, L. Lombardi, C. Pellegrino, F. Dammacco, and F. Silvestris, “Glomerular accumulation of plasmacytoid dendritic cells in active lupus nephritis: role of interleukin-18,” Arthritis and Rheumatism, vol. 58, no. 1, pp. 251–262, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  62. N. Charles, D. Hardwick, E. Daugas, G. G. Illei, and J. Rivera, “Basophils and the T helper 2 environment can promote the development of lupus nephritis,” Nature Medicine, vol. 16, no. 6, pp. 701–707, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  63. S. V. Kaveri, L. Mouthon, and J. Bayry, “Basophils and nephritis in lupus,” The New England Journal of Medicine, vol. 363, no. 11, pp. 1080–1082, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  64. S. Shimizu, N. Sugiyama, K. Masutani et al., “Membranous glomerulonephritis development with Th2-type immune deviations in MRL/lpr mice deficient for IL-27 receptor (WSX-1),” Journal of Immunology, vol. 175, no. 11, pp. 7185–7192, 2005. View at Scopus
  65. M. Akahoshi, H. Nakashima, Y. Tanaka et al., “Th1/Th2 balance of peripheral T helper cells in systemic lupus erythematosus,” Arthritis and Rheumatism, vol. 42, no. 8, pp. 1644–1648, 1999. View at Publisher · View at Google Scholar · View at Scopus
  66. D. J. Huss, R. C. Winger, G. M. Cox, et al., “TGF-β signaling via smad4 drives IL-10 production in effector Th1 cells and reduces T cell trafficking in EAE,” The European Journal of Immunology, vol. 41, no. 10, pp. 2987–2996, 2011. View at Publisher · View at Google Scholar · View at PubMed
  67. A. O'Garra and P. Vieira, “TH1 cells control themselves by producing interleukin-10,” Nature Reviews Immunology, vol. 7, no. 6, pp. 425–428, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  68. D. Jankovic, D. G. Kugler, and A. Sher, “IL-10 production by CD4+ effector T cells: a mechanism for self-regulation,” Mucosal Immunology, vol. 3, no. 3, pp. 239–246, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  69. R. L. Brunsing and E. R. Prossnitz, “Induction of interleukin-10 in the T helper type 17 effector population by the G protein coupled estrogen receptor (GPER) agonist G-1,” Immunology, vol. 134, no. 1, pp. 93–106, 2011. View at Publisher · View at Google Scholar · View at PubMed
  70. H. Ishida, T. Muchamuel, S. Sakaguchi, S. Andrade, S. Menon, and M. Howard, “Continuous administration of anti-interleukin 10 antibodies delays onset of autoimmunity in NZB/W F1 mice,” Journal of Experimental Medicine, vol. 179, no. 1, pp. 305–310, 1994. View at Publisher · View at Google Scholar · View at Scopus
  71. C. T. Ravirajan, Y. Wang, L. A. Matis et al., “Effect of neutralizing antibodies to IL-10 and C5 on the renal damage caused by a pathogenic human anti-dsDNA antibody,” Rheumatology, vol. 43, no. 4, pp. 442–447, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  72. K. R. M. Blenman, B. Duan, Z. Xu et al., “IL-10 regulation of lupus in the NZM2410 murine model,” Laboratory Investigation, vol. 86, no. 11, pp. 1136–1148, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  73. L. Llorente, Y. Richaud-Patin, C. García-Padilla, et al., “Clinical and biologic effects of anti-interleukin-10 monoclonal antibody administration in systemic Lupus erythematosus,” Arthritis and Rheumatism, vol. 43, no. 8, pp. 1790–1800, 2000.