Inhibitory ITAM signaling by FcαRI-FcRγ chain controls multiple activating responses and prevents renal inflammation

Journal of Immunology

Volumn 180, Issue 4, 2008, Pages 2669-2678

  Kanamaru, Yutaka ^a,b   Pfirsch, Séverine ^a,b   Aloulou, Meryem ^a,b   Vrtovsnik, François ^a,b,c   Essig, Marie ^a,b,c   Loirat, Chantal ^a,b,d   Deschênes, Georges ^d   Guérin Marchand, Claudine ^a,b   Blank, Ulrich ^a,b   Monteiro, Renato C ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c BICHAT HOSPITAL   (France)

^d HÔPITAL ROBERT DEBRÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE RECEPTOR; FAB 320; FAB A77; FC ALPHA RECEPTOR INHIBITOR; FC RECEPTOR; IMMUNOGLOBULIN A; IMMUNOGLOBULIN F(AB) FRAGMENT; MEMBRANE RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE 1; PROTEIN TYROSINE PHOSPHATASE SHP 1; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; FC(ALPHA) RECEPTOR; IMMUNOGLOBULIN RECEPTOR; LEUKOCYTE ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RECOGNITION; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DISEASE COURSE; ENZYME INHIBITION; EX VIVO STUDY; GLOMERULONEPHRITIS; HOMEOSTASIS; HUMAN; HUMAN CELL; IMMUNE COMPLEX NEPHRITIS; IMMUNE RESPONSE; IMMUNOGLOBULIN A NEPHROPATHY; IMMUNORECEPTOR TYROSINE BASED ACTIVATION MOTIF; IN VIVO STUDY; INFLAMMATION; INHIBITORY POSTSYNAPTIC POTENTIAL; KIDNEY DISEASE; KIDNEY FIBROSIS; LUPUS ERYTHEMATOSUS NEPHRITIS; MEMBRANOUS GLOMERULONEPHRITIS; MONOCYTE; MOUSE; NEPHRITIS; NONHUMAN; OBSTRUCTIVE UROPATHY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN MOTIF; RENOVASCULAR DISEASE; SIGNAL TRANSDUCTION; SRC HOMOLOGY DOMAIN; URETER OBSTRUCTION; VASCULITIS; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW CELL; C57BL MOUSE; CELL CULTURE; CELL MOTION; IMMUNOLOGY; KIDNEY; LEUKOCYTE; LEUKOCYTE MIGRATION INHIBITION TEST; METABOLISM; PATHOLOGY; PHYSIOLOGY; RAT; TRANSGENIC MOUSE; TUMOR CELL LINE;

AMINO ACID MOTIFS; ANIMALS; ANTIGENS, CD; CELL LINE, TUMOR; CELL MIGRATION INHIBITION; CELL MOVEMENT; CELLS, CULTURED; GLOMERULONEPHRITIS, IGA; HUMANS; KIDNEY; LEUKOCYTES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELOID CELLS; RATS; RECEPTORS, FC; RECEPTORS, IGG; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION;

EID: 42149085674     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.180.4.2669     Document Type: Article

References (49)

1. Meguid El Nahas, A., and A. K. Bello. 2005. Chronic kidney disease: the global challenge. Lancet 365: 331-340.
2. Alexopoulos, E., D. Seron, R. B. Hartley, F. Nolasco, and J. S. Cameron. 1989. Immune mechanisms in idiopathic membranous nephropathy: the role of the interstitial infiltrates. Am. J. Kidney Dis. 13: 404-412.
3. Arima, S., M. Nakayama, M. Naito, T. Sato, and K. Takahashi. 1991. Significance of mononuclear phagocytes in IgA nephropathy. Kidney Int. 39: 684-692.
4. Falk, M. C., G. Ng, G. Y. Zhang, G. C. Fanning, L. P. Roy, K. M. Bannister, A. C. Thomas, A. R. Clarkson, A. J. Woodroffe, and J. F. Knight. 1995. Infiltration of the kidney by αβ and γδ T cells: effect on progression in IgA nephropathy. Kidney Int. 47: 177-185.
5. Eddy, A. Role of cellular infiltrates in response to proteinuria. 2001. Am. J. Kidney Dis. 37: S25-S29.
6. Kawasaki, Y., J. Suzuki, N. Sakai, M. Tanji, and H. Suzuki. 2003. Predicting the prognosis of renal dysfunction by renal expression of α-smooth muscle actin in children with MPGN type 1. Am. J. Kidney Dis. 42: 1131-1138.
7. Clynes, R., C. Dumitru, and J. V. Ravetch. 1998. Uncoupling of immune complex formation and kidney damage in autoimmune glomerulonephritis. Science 279: 1052-1054.
8. Saito, K., T. Abe, and T. Takeuchi. 1998. Decreased Fcγ receptor III (CD16) expression on peripheral blood mononuclear cells in patients with Sjogren's syndrome. J. Rheumatol. 25: 689-696.
9. Fujii, T., Y. Hamano, S. Ueda, B. Akikusa, S. Yamasaki, M. Ogawa, H. Saisho, J. S. Verbeek, S. Taki, and T. Saito. 2003. Predominant role of FcRγIII in the induction of accelerated nephrotoxic glomerulonephritis. Kidney Int. 64: 1406-1416.
10. Kanamaru, Y., M. Arcos-Fajardo, I. C. Moura, T. Tsuge, H. Cohen, M. Essig, F. Vrtovsnik, C. Loirat, M. Peuchmaur, L. Beaudoin, et al. 2007. Fcα receptor I activation induces leukocyte recruitment and promotes aggravation of glomerulonephritis through the FcRγ adaptor. Eur. J. Immunol. 37: 1116-1128.
11. Diamond, J. R., S. D. Ricardo, and S. Klahr. 1998. Mechanisms of interstitial fibrosis in obstructive nephropathy. Semin. Nephrol. 18: 594-602.
12. Klahr, S., and J. Morrissey. 2002. Obstructive nephropathy and renal fibrosis. Am. J. Physiol. 283: F861-F875.
13. Segerer, S., P. J. Nelson, and D. Schlöndorff. 2000. Chemokines, chemokine receptors, and renal disease: from basic science to pathophysiologic and therapeutic studies. J. Am. Soc. Nephrol. 11: 152-176.
14. Nishida, M., H. Fujinaka, T. Matsusaka, J. Price, V. Kon, A. B. Fogo, J. M. Davidson, M. F. Linton, S. Fazio, T. Homma, H. Yoshida, and I. Ichikawa. 2002. Absence of angiotensin II type 1 receptor in bone marrow-derived cells is detrimental in the evolution of renal fibrosis. J. Clin. Invest. 110: 1859 -1868.
15. Kitagawa, K., T. Wada, K. Furuichi, H. Hashimoto, Y. Ishiwata, M. Asano, M. Takeya, W. A. Kuziel, K. Matsushima, N. Mukaida, and H. Yokoyama. 2004. Blockade of CCR2 ameliorates progressive fibrosis in kidney. Am. J. Pathol. 165: 237-246.
16. Eis, V., B. Luckow, V. Vielhauer, J. T. Siveke, Y. Linde, S. Segerer, G. Perez De Lema, C. D. Cohen, M. Kretzler, M. Mack, et al. 2004. Chemokine receptor CCR1 but not CCR5 mediates leukocyte recruitment and subsequent renal fibrosis after unilateral ureteral obstruction. J. Am. Soc. Nephrol. 15: 337-347.
17. Taal, M. W., and B. M. Brenner. 2001. Evolving strategies for renoprotection: non-diabetic chronic renal disease. Curr. Opin. Nephrol. Hypertens. 10: 523-531.
18. Scott, D. L., and G. H. Kingsley. 2006. Tumor necrosis factor inhibitors for rheumatoid arthritis. N. Engl. J. Med. 355: 704-712.
19. Hamerman, J. A., and L. L. Lanier. 2006. Inhibition of immune responses by ITAM-bearing receptors. Sci. STKE 2006: re1.
20. Pasquier, B., P. Launay, Y. Kanamaru, I. C. Moura, S. Pfirsch, C. Ruffie, D. Henin, M. Benhamou, M. Pretolani, U. Blank, and R. C. Monteiro. 2005. Identification of FcαRI as an inhibitory receptor that controls inflammation: dual role of FcRγ ITAM. Immunity 22: 31-42.
21. Hamerman, J. A., J. R. Jarjoura, M. B. Humphrey, M. C. Nakamura, W. E. Seaman, and L. L. Lanier. 2006. Cutting edge: inhibition of TLR and FcR responses in macrophages by triggering receptor expressed on myeloid cells (TREM)-2 and DAP12. J. Immunol. 177: 2051-2055.
22. Turnbull, I. R., S. Gilfillan, M. Cella, T. Aoshi, M. Miller, L. Piccio, M. Hernandez, and M. Colonna. 2006. Cutting edge: TREM-2 attenuates macrophage activation. J. Immunol. 177: 3520-3524.
23. Blasius, A. L., and M. Colonna. 2006. Sampling and signaling in plasmacytoid dendritic cells: the potential roles of Siglec-H. Trends Immunol. 27: 255-260.
24. Launay, P., B. Grossetête, M. Arcos-Fajardo, E. Gaudin, S. P. Torres, L. Beaudoin, N. Patey-Mariaud de Serre, A. Lehuen, and R. C. Monteiro. 2000. Fcα receptor (CD89) mediates the development of immunoglobulin A (IgA) nephropathy (Berger's disease): evidence for pathogenic soluble receptor-IgA complexes in patients and CD89 transgenic mice. J. Exp. Med. 191: 1999-2009.
25. Inazaki, K., Y. Kanamaru, Y. Kojima, N. Sueyoshi, K. Okumura, K. Kaneko, Y. Yamashiro, H. Ogawa, and A. Nakao. 2004. Smad3 deficiency attenuates renal fibrosis, inflammation, and apoptosis after unilateral ureteral obstruction. Kidney Int. 66: 597-604.
26. Vitale, S., A. Schmid-Alliana, V. Breuil, M. Pomeranz, M. A. Millet, B. Rossi, and H. Schmid-Antomarchi. 2004. Soluble fractalkine prevents monocyte chemoattractant protein-1-induced monocyte migration via inhibition of stress-activated protein kinase 2/p38 and matrix metalloproteinase activities. J. Immunol. 172: 585-592.
27. Hsu, H. Y., and Y. C. Twu. 2000. Tumor necrosis factor-α-mediated protein kinases in regulation of scavenger receptor and foam cell formation on macrophage. J. Biol. Chem. 275: 41035-41048.
28. Cambien, B., M. Pomeranz, M. A. Millet, B. Rossi, and A. Schmid-Alliana. 2001. Signal transduction involved in MCP-1-mediated monocytic transendothelial migration. Blood 97: 359-366.
29. Zu, Y. L., J. Qi, A. Gilchrist, G. A. Fernandez, D. Vazquez-Abad, D. L. Kreutzer, C. K. Huang, and R. I. Sha'afi. 1998. p38 mitogen-activated protein kinase activation is required for human neutrophil function triggered by TNF-α or FMLP stimulation. J. Immunol. 160: 1982-1989.
30. Unanue, E. R., and F. J. Dixon. 1967. Experimental glomerulonephritis: immunological events and pathogenetic mechanisms. Adv. Immunol. 6: 1-90.
31. Park, S. Y., S. Ueda, H. Ohno, Y. Hamano, M. Tanaka, T. Shiratori, T. Yamazaki, H. Arase, N. Arase, A. Karasawa, et al. 1998. Resistance of Fc receptor-deficient mice to fatal glomerulonephritis. J. Clin. Invest. 102: 1229-1238.
32. Le Hir, M., C. Haas, M. Marino, and B. Ryffel. 1998. Prevention of crescentic glomerulonephritis induced by anti-glomerular membrane antibody in tumor necrosis factor-deficient mice. Lab Invest. 78: 1625-1631.
33. Crisman, J. M., L. L. Richards, D. P. Valach, D. F. Franzoni, and J. R. Diamond. 2001. Chemokine expression in the obstructed kidney. Exp. Nephrol. 9: 241-248.
34. Vielhauer, V., H. J. Anders, M. Mack, J. Cihak, F. Strutz, M. Stangassinger, B. Luckow, H. J. Gröne, and D. Schlöndorff. 2001. Obstructive nephropathy in the mouse: progressive fibrosis correlates with tubulointerstitial chemokine expression and accumulation of CC chemokine receptor 2- and 5-positive leukocytes. J. Am. Soc. Nephrol. 12: 1173-1187.
35. Wada, T., K. Furuichi, N. Sakai, Y. Iwata, K. Kitagawa, Y. Ishida, T. Kondo, H. Hashimoto, Y. Ishiwata, N. Mukaida, et al. 2004. Gene therapy via blockade of monocyte chemoattractant protein-1 for renal fibrosis. J. Am. Soc. Nephrol. 15: 940-948.
36. Suzuki, S., Y. Nakatomi, H. Sato, H. Tsukada, and M. Arakawa. 1994. Haemophilus parainfluenzae antigen and antibody in renal biopsy samples and serum of patients with IgA nephropathy. Lancet 343: 12-16.
37. Monteiro, R. C., I. C. Moura, P. Launay, T. Tsuge, E. Haddad, M. Benhamou, M. D. Cooper, and M. Arcos-Fajardo. 2002. Pathogenic significance of IgA receptor interactions in IgA nephropathy. Trends Mol. Med. 8: 464-468.
38. Monteiro, R. C., M. D. Cooper, and H. Kubagawa. 1992. Molecular heterogeneity of Fcα receptors detected by receptor-specific monoclonal antibodies. J. Immunol. 148: 1764-1770.
39. Grossetête, B., P. Launay, A. Lehuen, P. Jungers, J. F. Bach, and R. C. Monteiro. 1998. Down-regulation of Fcα receptors on blood cells of IgA nephropathy patients: evidence for a negative regulatory role of serum IgA. Kidney Int. 53: 1321-1335.
40. Kanamaru, Y., H. Tamouza, S. Pfirsch, D. El-Mehdi, C. Guérin-Marchand, M. Pretolani, U. Blank, and R. C. Monteiro. 2007. IgA Fc receptor I signals apoptosis through the FcRγ ITAM and affects tumor growth. Blood 109: 203-211.
41. Stefanova, I., B. Hemmer, M. Vergelli, R. Martin, W. E. Biddison, and R. N. Germain. 2003. TCR ligand discrimination is enforced by competing ERK positive and SHP-1 negative feedback pathways. Nat. Immunol. 4: 248-254.
42. Turnbull, I. R., and M. Colonna. 2007. Activating and inhibitory functions of DAP12. Nat. Rev. Immunol. 7: 155-161.
43. Holdsworth, S. R., T. J. Neale, and C. B. Wilson. 1981. Abrogation of macrophage-dependent injury in experimental glomerulonephritis in the rabbit: use of an antimacrophage serum. J. Clin. Invest. 68: 686-698.
44. Schreiner, G. F., K. P. Harris, M. L. Purkerson, and S. Klahr. 1988. Immunological aspects of acute ureteral obstruction: immune cell infiltrate in the kidney. Kidney Int. 34: 487-493.
45. Kuroiwa, T., R. Schlimgen, G. G. Illei, I. B. McInnes, and D. T. Boumpas. 2000. Distinct T cell/renal tubular epithelial cell interactions define differential chemokine production: implications for tubulointerstitial injury in chronic glomerulonephritides. J. Immunol. 164: 3323-3329.
46. Monteiro, R. C., and J. G. J. van de Winkel. 2003. IgA Fc receptors. Annu. Rev. Immunol. 21: 177-204.
47. Campbell, D. J., G. F. Debes, B. Johnston, E. Wilson, and E. C. Butcher. 2003. Targeting T cell responses by selective chemokine receptor expression. Semin. Immunol. 15: 277-286.
48. Sean Eardley, K., and P. Cockwell. 2005. Macrophages and progressive tubulointerstitial disease. Kidney Int. 68: 437-455.
49. Launay, P., A. Lehuen, T. Kawakami, U. Blank, and R. C. Monteiro. 1998. IgA Fc receptor (CD89) activation enables coupling to syk and Btk tyrosine kinase pathways: differential signaling after IFN-γ or phorbol ester stimulation. J. Leukocyte Biol. 63: 636-642.