C5a promotes development of experimental lupus nephritis which can be blocked with a specific receptor antagonist

European Journal of Immunology

Volumn 35, Issue 8, 2005, Pages 2496-2506

  Bao, Lihua ^a   Osawe, Iyabo ^a   Puri, Tipu ^a   Lambris, John D ^b   Haas, Mark ^c   Quigg, Richard J ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anaphylatoxin; Complement; Lupus; Nephritis

Indexed keywords

COMPLEMENT COMPONENT C5 INHIBITOR; COMPLEMENT COMPONENT C5A; COMPLEMENT COMPONENT C5A INHIBITOR; INTERLEUKIN 1BETA; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; KIDNEY DYSFUNCTION; LUPUS ERYTHEMATOSUS NEPHRITIS; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

AGE FACTORS; ANIMALS; APOPTOSIS; AUTOIMMUNITY; BLOOD UREA NITROGEN; COMPLEMENT C5A; INFLAMMATION; KIDNEY; LUPUS NEPHRITIS; MICE; MICE, INBRED MRL LPR; RECEPTOR, ANAPHYLATOXIN C5A;

EID: 23844457665     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200526327     Document Type: Article

References (56)

1. Holers, V. M., Complement. In Rich, R. (Ed.) Principles and practices of clinical immunology. Mosby, St. Louis 1995, pp 363-391.
2. Liszewski, M. K. and Atkinson, J. P., The complement system. In Paul, W. E. (Ed.) Fundamental immunology. Raven Press, New York 1993, pp 917-939.
3. Walport, M. J., Advances in immunology: complement. N. Engl. J. Med. 2001. 344: 1058-1066.
4. Nicholson-Weller, A. and Halperin, J. A., Membrane signaling by complement C5b-9, the membrane attack complex. Immunol. Res. 1993. 12: 244-257.
5. Dalmasso, A. P., Complement in the pathophysiology and diagnosis of human diseases. Crit. Rev. Clin. Lab. Sci. 1986. 24: 123-183.
6. Adachi, M., Watanabe-Fukunaga, R. and Nagata, S., Aberrant transcription caused by the insertion of an early transposable element in an intron of the Fas antigen gene of lpr mice. Prot. Natl. Acad. Sci. USA 1993. 90: 1756-1760.
7. Watanbe-Fukunaga, R., Brannan, C. I., Copeland, N. G., Jenkins, N. A. and Nagata, S., Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apotosis. Nature 1992. 356: 314-317.
8. Bao, L., Haas, M., Kraus, D. M., Hack, B. K., Rakstang, J. K., Holers, V. M. and Quigg, R. J., Administration of a soluble recombinant complement C3 inhibitor protects against renal disease in MRL/lpr mice. J. Am. Soc. Nephrol. 2003. 14: 670-679.
9. Bao, L., Haas, M., Boackle, S. A., Kraus, D. M., Cunningham, P. N., Park, P., Alexander, J. J. et al., Transgenic expression of a soluble complement inhibitor protects against renal disease and promotes survival in MRL/lpr mice. J. Immunol. 2002. 168: 3601-3607.
10. Tack, B. F., Morris, S. C. and Prahl, J. W., Fifth component of human complement: purification from plasma and polypeptide chain structure. Biochemistry 1979. 18: 1490-1497.
11. Wetsel, R. A., Structure, function and cellular expression of complement anaphylatoxin receptors. Curr. Opin. Immunol. 1995. 7: 48-53.
12. Chenoweth, D. E. and Hugh, T. E., Demonstration of specific C5a receptor on intact human polymorphonuclear leukocytes. Proc. Natl. Acad. Sci. USA 1978. 75: 3943-3947.
13. Werfel, T., Oppermann, M., Schulze, M., Krieger, G., Weber, M. and Gotze, O., Binding of fluorescein-labeled anaphylatoxin C5a to human peripheral blood, spleen, and bone marrow leukocytes. Blood 1992. 79: 152-160.
14. Hopken, U. E., Lu, B., Gerard, N. P. and Gerard, C., Impaired inflammatory responses in the reverse arthus reaction through genetic deletion of the C5a receptor. J. Exp. Med. 1997. 186: 749-756.
15. Huber-Lang, M. S., Riedeman, N. C., Sarma, J. V., Younkin, E. M., McGuire, S. R., Laudes, I. J., Lu, K. T. et al., Protection of innate immunity by C5aR antagonist in septic mice. FASEB J. 2002. 16: 1567-1574.
16. Braun, M. and Davis, A. E., III Cultured human glomerular mesangial cells express the C5a receptor. Kidney Int. 1998. 54: 1542-1549.
17. Fayyazi, A., Scheel, O., Werfel, T., Schweyer, S., Oppermann, M., Gotze, O., Radzun, H. J. and Zwirner, J., The C5a receptor is expressed in normal renal proximal tubular but not in normal pulmonary or hepatic epithelial cells. Immunology 2000. 99: 38-45.
18. Zahedi, R., Braun, M., Wetsel, R. A., Ault, B. H., Khan, A., Welch, T. R., Frenzke, M. and Davis, A. E., The C5a receptor is expressed by human renal proximal tubular epithelial cells. Clin. Exp. Immunol. 2000. 121: 226-233.
19. Welch, T. R., Frenzke, M., Witte, D. and Davis, A. E., C5a is important in the tubulointerstitial component of experimental immune complex glomerulonephritis. Clin. Exp. Immunol. 2002. 13: 43-48.
20. Abe, K., Miyazaki, M., Koji, T., Furusu, A., Nakamura-Kurashige, T., Nishino, T., Ozono, Y. et al., Enhanced expression of complement C5a receptor mRNA in human diseased kidney assessed by in situ hybridization. Kidney Int. 2001. 60: 137-146.
21. Paczkowski, N. J., Finch, A. M., Whitmore, J. B., Short, A. J., Wong, A. K., Monk, P. N., Cain, S. A. et al., Pharmacological characterization of antagonists of the C5a receptor. Br. J. Pharmacol. 1999. 128: 1461-1466.
22. Hawlisch, H., Wills-Karp, M., Karp, C. L. and Kohl, J., The anaphylatoxins bridge innate and adaptive immune responses in allergic asthma. Mol. Immunol. 2004. 41: 123-131.
23. Ravirajan, C. T., Wang, Y., Matis, L. A., Papadaki, L., Griffiths, M. H., Latchman, D. S. and Isenberg, D. A., Effect of neutralizing antibodies to IL-10 and C5 on the renal damage caused by a pathogenic human anti-dsDNA antibody. Rheumatology 2004. 43: 442-447.
24. Yamamoto, K. and Loskutoff, D. J., Expression of transforming growth factor-beta and tumor necrosis factor-alpha in the plasma and tissues of mice with lupus nephritis. Lab. Invest. 2000. 80: 1561-1570.
25. Lawson, B. R., Prud'homme, G. J., Chang, Y., Gardner, H. A., Kuan, J., Kono, D. H. and Theofilopoulos, A. N., Treatment of murine lupus with cDNA encoding IFN-gammaR/Fc. J. Clin. Invest. 2000. 106: 207-215.
26. Esfandiari, E., McInnes, I. B., Lindop, G., Huang, F. P., Field, M., Komai-Koma, M., Wei, X. and Liew, F. Y., A proinflammatory role of IL-18 in the development of spontaneous autoimmune disease. J. Immunol. 2001. 167: 5338-5347.
27. Huggins, M. L., Huang, F. P., Xu, D., Lindop, G. and Stott, D. I., Modulation of autoimmune disease in the MRL-lpr/lpr mouse by IL-2 and TGF-beta1 gene therapy using attenuated Salmonella typhimurium as gene carrier. Lupus 1999. 8: 29-38.
28. Wuthrich, R. P., Jevnikar, A. M., Takei, F., Glimcher, L. H. and Kelley, V. E., Intercellular adhesion molecule-1 (ICAM-1) expression is upregulated in autoimmune murine lupus nephritis. Am. J. Pathol. 1990. 136: 441-450.
29. Monsinjon, T., Gasque, P., Chan, P., Ischenko, A., Brady, J. J. and Fontaine, M. C., Regulation by complement C3a and C5a anaphylatoxins of cytokine production in human umbilical vein endothelial cells. FASEB J. 2003. 17: 1003-1014.
30. Godau, J., Heller, T., Hawlisch, H., Trappe, M., Howells, E., Best, J., Zwirner, J. et al., C5a initiates the inflammatory cascade in immune complex peritonitis. J. Immunol. 2004. 173: 3437-3445.
31. Grant, E. P., Picarella, D., Burwell, T., Delaney, T., Croci, A., Avitahl, N., Humbles, A. A. et al., Essential role for the C5a receptor in regulating the effector phase of synovial infiltration and joint destruction in experimental arthritis. J. Exp. Med. 2002. 196: 1461-1471.
32. Riedemann, N. C., Guo, R. F., Gao, H., Sun, L., Hoesel, M., Hollmann, T. J., Wetsel, R. A. et al., Regulatory role of C5a on macrophage migration inhibitory factor release from neutrophils. J. Immunol. 2004. 173: 1355-1359.
33. Girardi, G., Berman, J., Redecha, P., Spruce, L., Thurman, J. M., Kraus, D., Hollmann, T. J. et al., Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J. Clin. Invest. 2003. 112: 1644-1654.
34. Strachan, A. J., Woodruff, T. M., Haaima, G., Fairlie, D. P. and Taylor, S. M., A new small molecule C5a receptor antagonist inhibits the reverse-passive Arthus reaction and endotoxic shock in rats. J. Immunol. 2000. 164: 6560-6565.
35. Woodruff, T. M., Strachan, A. J., Dryburgh, N., Shiels, I. A., Reid, R. C., Fairlie, D. P. and Taylor, S. M., Antiarthritic activity of an orally active C5a receptor antagonist against antigen-induced monarticular arthritis in the rat. Arthritis Rheum. 2002. 46: 2476-2485.
36. Andrews, B. S., Eisenberg, R. A., Theofilopoulos, A. N., Izui, S., Wilson, C. B., McConahey, P. J., Murphy, E. D. et al., Spontaneous murine lupus-like syndromes. Clinical and immunopathological manifestations in several strains. J. Exp. Med. 1978. 148: 1198-1215.
37. Theofilopoulos, A. N., Murine models of lupus. In Lahita, R. G. (Ed.) Systemic lupus erythematosus. Churchill Livingston, New York 1992, pp 121-194.
38. Bao, L., Zhou, J., Holers, V. M. and Quigg, R. J., Excessive matrix accumulation in the kidneys of MRL/lpr lupus mice Is dependent on complement activation. J. Am. Soc. Nephrol. 2003. 14: 2516-2525.
39. Boswell, J. M., Yui, M. A., Burt, D. W. and Kelley, V. E., Increased tumor necrosis factor and IL-1 beta gene expression in the kidneys of mice with lupus nephritis. J. Immunol. 1988. 141: 3050-3054.
40. Boswell, J. M., Yui, M. A., Endres, S., Burt, D. W. and Kelley, V. E., Novel and enhanced IL-1 gene expression in autoimmune mice with lupus. J. Immunol. 1988. 141: 118-124.
41. Brennan, D. C., Yui, M. A., Wuthrich, R. P. and Kelley, V. E., Tumor necrosis factor and IL-1 in New Zealand Black/White mice. Enhanced gene expression and acceleration of renal injury. J. Immunol. 1989. 143: 3470-3475.
42. McHale, J. F., Harari, O. A., Marshall, D. and Haskard, D. O., TNF-alpha and IL-1 sequentially induce endothelial ICAM-1 and VCAM-1 expression in MRL/lpr lupus-prone mice. J. Immunol. 1999. 163: 3993-4000.
43. De Vries, B., Kohl, J., Leclercq, W. K., Wolfs, T. G., Van Bijnen, A. A., Heeringa, P. and Buurman, W. A., Complement factor C5a mediates renal ischemia-reperfusion injury independent from neutrophils. J. Immunol. 2003. 170: 3883-3889.
44. Perniok, A., Wedekind, F., Herrmann, M., Specker, C. and Schneider, M., High levels of circulating early apoptic peripheral blood mononuclear cells in systemic lupus erythematosus. Lupus 1998. 7: 113-118.
45. Herrmann, M., Voll, R. E., Zoller, O. M., Hagenhofer, M., Ponner, B. B. and Kalden, J. R., Impaired phagocytosis of apoptotic cell material by monocyte-derived macrophages from patients with systemic lupus erythematosus. Arthritis Rheum. 1998. 41: 1241-1250.
46. Rajagopalan, S., Somers, E. C., Brook, R. D., Kehrer, C., Pfenninger, D., Lewis, E., Chakrabarti, A. et al., Endothelial cell apoptosis in systemic lupus erythematosus: a common pathway for abnormal vascular function and thrombosis propensity. Blood 2004. 103: 3677-3683.
47. Ren, Y., Tang, J., Mok, M. Y., Chan, A. W., Wu, A. and Lau, C. S., Increased apoptotic neutrophils and macrophages and impaired macrophage phagocytic clearance of apoptotic neutrophils in systemic lupus erythematosus. Arthritis Rheum. 2003. 48: 2888-2897.
48. Cunningham, P. N., Dyanov, H. M., Park, P., Wang, J., Newell, K. A. and Quigg, R. J., Acute renal failure in endotoxemia is caused by TNF acting directly on TNF receptor-1 in kidney. J. Immunol. 2002. 168: 5817-5823.
49. Botto, M., Dell'Agnola, C., Bygrave, A. E., Thompson, E. M., Cook, H. T., Petry, F., Loos, M. et al., Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 1998. 19: 56-59.
50. Guo, R. F., Huber-Lang, M., Wang, X., Sarma, V., Padgaonkar, V. A., Craig, R. A., Riedemann, N. C. et al., Protective effects of anti-C5a in sepsis-induced thymocyte apoptosis. J. Clin. Invest 2000. 106: 1271-1280.
51. Lenda, D. M., Stanley, E. R. and Kelley, V. R., Negative role of colony-stimulating factor-1 in macrophage, T cell, and B cell mediated autoimmune disease in MRL-Fas(lpr) mice. J. Immunol. 2004. 173: 4744-4754.
52. Lenda, D. M., Kikawada, E., Stanley, E. R. and Kelley, V. R., Reduced macrophage recruitment, proliferation, and activation in colony-stimulating factor-1-deficient mice results in decreased tubular apoptosis during renal inflammation. J. Immunol. 2003. 170: 3254-3262.
53. Quigg, R. J., Lim, A., Haas, M., Alexander, J. J., He, C. and Carroll, M. C., Immune complex glomerulonephritis in C4- and C3-deficient mice. Kidney Int. 1998. 53: 320-330.
54. Quigg, R. J., He, C., Lim, A., Berthiaume, D., Alexander, J. J., Kraus, D. and Holers, V. M., Transgenic mice overexpressing the complement inhibitor Crry as a soluble protein are protected from antibody-induced glomerular injury. J. Exp. Med. 1998. 188: 1321-1331.
55. Passwell, J., Schreiner, G. F., Nonaka, M., Beuscher, H. U. and Colten, H. R., Local extrahepatic expression of complement genes C3, factor B, C2, and C4 is increased in murine lupus nephritis. J. Clin. Invest. 1988. 82: 1676-1684.
56. Riedemann, N. C., Guo, R. F., Neff, T. A., Landes, I. J., Keller, K. A., Sarma, V. J., Markiewski, M. M. et al., Increased C5a receptor expression in sepsis. J. Clin. Invest. 2002: 101-108.