CXCR3 mediates renal Th1 and Th17 immune response in murine lupus nephritis

Journal of Immunology

Volumn 183, Issue 7, 2009, Pages 4693-4704

  Steinmetz, Oliver M ^a   Turner, Jan Eric ^a   Paust, Hans Joachim ^a   Lindner, Matthias ^a   Peters, Anett ^a   Heiss, Kirstin ^a   Velden, Joachim ^a   Hopfer, Helmut ^b   Fehr, Susanne ^a   Krieger, Thorsten ^a   Meyer Schwesinger, Catherine ^a   Meyer, Tobias N ^a   Helmchen, Udo ^a   Mittrücker, Hans Willi ^a   Stahl, Rolf A K ^a   Panzer, Ulf ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON; INTERLEUKIN 17; MONOCYTE CHEMOTACTIC PROTEIN 1; CXCR3 PROTEIN, MOUSE; IMMUNOGLOBULIN G;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; FLOW CYTOMETRY; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; LEUKOCYTE; LUPUS ERYTHEMATOSUS NEPHRITIS; LYMPH NODE; MICROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SMALL INTESTINE; SPLEEN; T LYMPHOCYTE; TH1 CELL; TH17 CELL; TISSUE INJURY; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL MOTION; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KIDNEY; MALE; METABOLISM; MOUSE MUTANT; MURPHY ROTHS LARGE LYMPHOPROLIFERATIVE MOUSE; PATHOLOGY; PHYSIOLOGY; SYSTEMIC LUPUS ERYTHEMATOSUS;

ANIMALS; CELL MOVEMENT; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOGLOBULIN G; INTERLEUKIN-17; KIDNEY; LUPUS ERYTHEMATOSUS, SYSTEMIC; LUPUS NEPHRITIS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED MRL LPR; MICE, KNOCKOUT; RECEPTORS, CXCR3; TH1 CELLS;

EID: 70449729971     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0802626     Document Type: Article

References (43)

1. Ruiz-Irastorza, G., M. A. Khamashta, G. Castellino, and G. R. Hughes. 2001. Systemic lupus erythematosus. Lancet 357: 1027-1032.
2. Ward, M. M., E. Pyun, and S. Studenski. 1996. Mortality risks associated with specific clinical manifestations of systemic lupus erythematosus. Arch. Intern. Med. 156: 1337-1344. (Pubitemid 26196894)
3. Tipping, P. G., and S. R. Holdsworth. 2006. T cells in crescentic glomerulonephritis. J. Am. Soc. Nephrol. 17: 1253-1263.
4. Tipping, P. G., and A. R. Kitching. 2005. Glomerulonephritis, Th1 and Th2: what's new? Clin. Exp. Immunol. 142: 207-215.
5. H2 hypothesis of T cell-mediated tissue damage. Nat. Med. 13: 139-145.
6. Cua, D. J., J. Sherlock, Y. Chen, C. A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748.
7. Murphy, C. A., C. L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R. A. Kastelein, J. D. Sedgwick, and D. J. Cua. 2003. Divergent pro and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198: 1951-1957.
8. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
9. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6: 1123-1132.
10. + T effector cells involved in organ-specific autoimmunity. Nephrol. Dial. Transplant. 23: 816-819.
11. Paust, H. J., J. E. Turner, O. M. Steinmetz, A. Peters, F. Heymann, C. Holscher, G. Wolf, C. Kurts, H. W. Mittrucker, R. A. Stahl, and U. Panzer. 2009. The IL-23/Th17 axis contributes to renal injury in experimental glomerulonephritis. J. Am. Soc. Nephrol. 20: 969-979.
12. Ooi, J. D., R. K. Phoon, S. R. Holdsworth, and A. R. Kitching. 2009. IL-23, not IL-12, directs autoimmunity to the Goodpasture antigen. J. Am. Soc. Nephrol. 20: 980-989.
13. Charo, I. F., and R. M. Ransohoff. 2006. The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 354: 610-621.
14. Moser, B., M. Wolf, A. Walz, and P. Loetscher. 2004. Chemokines: multiple levels of leukocyte migration control. Trends Immunol. 25: 75-84. (Pubitemid 38167488)
15. Panzer, U., O. M. Steinmetz, R. A. Stahl, and G. Wolf. 2006. Kidney diseases and chemokines. Curr. Drug Targets 7: 65-80.
16. Kulkarni, O., and H. J. Anders. 2008. Chemokines in lupus nephritis. Front. Biosci. 13: 3312-3320.
17. Rovin, B. H. 2008. The chemokine network in systemic lupus erythematous nephritis. Front. Biosci. 13: 904-922.
18. Sallusto, F., and A. Lanzavecchia. 2000. Understanding dendritic cell and T-lymphocyte traffic through the analysis of chemokine receptor expression. Immunol. Rev. 177: 134-140.
19. Singh, S. P., H. H. Zhang, J. F. Foley, M. N. Hedrick, and J. M. Farber. 2008. Human T cells that are able to produce IL-17 express the chemokine receptor CCR6. J. Immunol. 180: 214-221.
20. + regulatory T cells. J. Immunol. 180: 122-129.
21. Hirota, K., H. Yoshitomi, M. Hashimoto, S. Maeda, S. Teradaira, N. Sugimoto, T. Yamaguchi, T. Nomura, H. Ito, T. Nakamura, et al. 2007. Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J. Exp. Med. 204: 2803-2812.
22. Panzer, U., O. M. Steinmetz, H. J. Paust, C. Meyer-Schwesinger, A. Peters, J. E. Turner, G. Zahner, F. Heymann, C. Kurts, H. Hopfer, et al. 2007. Chemokine receptor CXCR3 mediates T cell recruitment and tissue injury in nephrotoxic nephritis in mice. J. Am. Soc. Nephrol. 18: 2071-2084.
23. Panzer, U., F. Thaiss, G. Zahner, P. Barth, M. Reszka, R. R. Reinking, G. Wolf, U. Helmchen, and R. A. Stahl. 2001. Monocyte chemoattractant protein-1 and osteopontin differentially regulate monocytes recruitment in experimental glomerulonephritis. Kidney Int. 59: 1762-1769.
24. Panzer, U., O. M. Steinmetz, R. R. Reinking, T. N. Meyer, S. Fehr, A. Schneider, G. Zahner, G. Wolf, U. Helmchen, P. Schaerli, et al. 2006. Compartment-specific expression and function of the chemokine IP-10/CXCL10 in a model of renal endothelial microvascular injury. J. Am. Soc. Nephrol. 17: 454-464.
25. Panzer, U., R. R. Reinking, O. M. Steinmetz, G. Zahner, U. Sudbeck, S. Fehr, B. Pfalzer, A. Schneider, F. Thaiss, M. Mack, et al. 2004. CXCR3 and CCR5 positive T-cell recruitment in acute human renal allograft rejection. Transplantation 78: 1341-1350.
26. Vielhauer, V., H. J. Anders, G. Perez de Lema, B. Luckow, D. Schlondorff, and M. Mack. 2003. Phenotyping renal leukocyte subsets by four-color flow cytometry: characterization of chemokine receptor expression. Nephron Exp. Nephrol. 93: e63.
27. Kursar, M., U. E. Hopken, M. Koch, A. Kohler, M. Lipp, S. H. Kaufmann, and H. W. Mittrucker. 2005. Differential requirements for the chemokine receptor CCR7 in T cell activation during Listeria monocytogenes infection. J. Exp. Med. 201: 1447-1457.
28. + T cell response during Listeria monocytogenes infection. J. Immunol. 168: 6382-6387.
29. Korn, T., J. Reddy, W. Gao, E. Bettelli, A. Awasthi, T. R. Petersen, B. T. Backstrom, R. A. Sobel, K. W. Wucherpfennig, T. B. Strom, et al. 2007. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. 13: 423-431.
30. Niess, J. H., F. Leithauser, G. Adler, and J. Reimann. 2008. Commensal gut flora drives the expansion of proinflammatory CD4 T cells in the colonic lamina propria under normal and inflammatory conditions. J. Immunol. 180: 559-568.
31. Segerer, S., B. Banas, M. Wornle, H. Schmid, C. D. Cohen, M. Kretzler, M. Mack, E. Kiss, P. J. Nelson, D. Schlondorff, and H. J. Grone. 2004. CXCR3 is involved in tubulointerstitial injury in human glomerulonephritis. Am. J. Pathol. 164: 635-649.
32. Romagnani, P., C. Beltrame, F. Annunziato, L. Lasagni, M. Luconi, G. Galli, L. Cosmi, E. Maggi, M. Salvadori, C. Pupilli, and M. Serio. 1999. Role for interactions between IP-10/Mig and CXCR3 in proliferative glomerulonephritis. J. Am. Soc. Nephrol. 10: 2518-2526.
33. + activated T cells in chronic allograft nephropathy with transplant glomerulopathy. Am. J. Transplant. 3: 1116-1120.
34. Qin, S., J. B. Rottman, P. Myers, N. Kassam, M. Weinblatt, M. Loetscher, A. E. Koch, B. Moser, and C. R. Mackay. 1998. The chemokine receptors CXCR3 and CCR5 mark subsets of T cells associated with certain inflammatory reactions. J. Clin. Invest. 101: 746-754. (Pubitemid 28096070)
35. + T cells are increased in multiple sclerosis and their ligands MIP-1α and IP-10 are expressed in demyelinating brain lesions. Proc. Natl. Acad. Sci. USA 96: 6873-6878.
36. Hancock, W. W., B. Lu, W. Gao, V. Csizmadia, K. Faia, J. A. King, S. T. Smiley, M. Ling, N. P. Gerard, and C. Gerard. 2000. Requirement of the chemokine receptor CXCR3 for acute allograft rejection. J. Exp. Med. 192: 1515-1520.
37. Frigerio, S., T. Junt, B. Lu, C. Gerard, U. Zumsteg, G. A. Hollander, and L. Piali. 2002. β cells are responsible for CXCR3-mediated T-cell infiltration in insulitis. Nat. Med. 8: 1414-1420. (Pubitemid 36024137)
38. Fiorina, P., M. J. Ansari, M. Jurewicz, M. Barry, V. Ricchiuti, R. N. Smith, S. Shea, T. K. Means, H. Auchincloss, Jr., A. D. Luster, et al. 2006. Role of CXC chemokine receptor 3 pathway in renal ischemic injury. J. Am. Soc. Nephrol. 17: 716-723.
39. Steinmetz, O. M., S. Sadaghiani, U. Panzer, C. Krebs, C. Meyer-Schwesinger, T. Streichert, S. Fehr, I. Hamming, H. van Goor, R. A. Stahl, and U. Wenzel. 2007. Antihypertensive therapy induces compartment-specific chemokine expression and a Th1 immune response in the clipped kidney of Goldblatt hypertensive rats. Am. J. Physiol. 292: F876-F887.
40. Menke, J., G. C. Zeller, E. Kikawada, T. K. Means, X. R. Huang, H. Y. Lan, B. Lu, J. Farber, A. D. Luster, and V. R. Kelley. 2008. CXCL9, but not CXCL10, promotes CXCR3-dependent immune-mediated kidney disease. J. Am. Soc. Nephrol. 19: 1177-1189.
41. Teramoto, K., N. Negoro, K. Kitamoto, T. Iwai, H. Iwao, M. Okamura, and K. Miura. 2008. Microarray analysis of glomerular gene expression in murine lupus nephritis. J. Pharmacol. Sci. 106: 56-67. (Pubitemid 351159069)
42. Rot, A., and U. H. von Andrian. 2004. Chemokines in innate and adaptive host defense: basic chemokinese grammar for immune cells. Annu. Rev. Immunol. 22: 891-928. (Pubitemid 38680444)
43. + T cells are enriched in inflamed kidneys and urine and provide a new biomarker for acute nephritis flares in systemic lupus erythematosus patients. Arthritis Rheum. 60: 199-206.