Local extravascular pool of C3 is a determinant of postischemic acute renal failure

FASEB Journal

Volumn 20, Issue 2, 2006, Pages 217-226

  Farrar, Conrad A ^a   Zhou, Wuding ^a   Lin, Tao ^a   Sacks, Steven H ^a  

^a GUY S HOSPITAL   (United Kingdom)

Author keywords

Complement; Immune regulation; Renal transplant

Indexed keywords

COMPLEMENT COMPONENT C3; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLD ISCHEMIA; CONTROLLED STUDY; FEMALE; ISOGRAFT; KIDNEY FAILURE; KIDNEY ISCHEMIA; KIDNEY TRANSPLANTATION; KIDNEY TUBULE DAMAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; REPERFUSION INJURY; SPACE FLIGHT; TISSUE INJURY; UPREGULATION; ANIMAL; COLD; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; KIDNEY; METABOLISM; METHODOLOGY; TIME;

ANIMALS; COLD; COMPLEMENT C3; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; INTERCELLULAR ADHESION MOLECULE-1; KIDNEY; KIDNEY FAILURE; KIDNEY TRANSPLANTATION; MICE; REPERFUSION INJURY; RNA, MESSENGER; TIME FACTORS; TRANSPLANTATION, ISOGENEIC;

EID: 33644928993     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-4747com     Document Type: Article

References (47)

1. Walport, M. J. (2001) Complement. First of two parts. N. Engl. J. Med. 344, 1058-1066
2. Walport, M. J. (2001) Complement. Second of two parts. N. Engl. J. Med. 344, 1140-1144
3. Weisman, H. F., Bartow, T., Leppo, M. K., Marsh, H. C., Jr., Carson, G. R., Concino, M. F., Boyle, M. P., Roux, K. H., Weisfeldt, M. L., and Fearon, D. T. (1990) Soluble human complement receptor type 1: in vivo inhibitor of complement suppressing post-ischemic myocardial inflammation and necrosis. Science 249, 146-151
4. Eppinger, M. J., Deeb, G. M., Bolling, S. F., and Ward, P. A. (1997) Mediators of ischemia-reperfusion injury of rat lung. Am. J. Pathol. 150, 1773-1784
5. Ikai, M., Itoh, M., Joh, T., Yokoyama, Y., Okada, N., and Okada, H. (1996) Complement plays an essential role in shock after intestinal ischaemia in rats. Clin. Exp. Immunol. 106, 156-159
6. Jaeschke, H., Farhood, A., Bautista, A. P., Spolarics, Z., and Spitzer, J. J. (1993) Complement activates kupffer cells and neutrophils during reperfusion and hepatic ischemia. Am. J. Physiol. 264, G801-G809
7. Zhou, W., Farrar, C. A., Abe, K., Pratt, J. R., Marsh, J. E., Wang, Y., Stahl, G. L., and Sacks, S. H. (2000) Predominant role for C5b-9 in renal ischemia/reperfusion injury. J. Clin. Invest. 105, 1363-1371
8. Morgan, B. P., and Gasque, P. (1997) Extrahepatic complement biosynthesis: where, when and why? Clin. Exp. Immunol. 107, 1-7
9. Brooimans, R. A., Stegmann, A. P. A., van Dorp, W. T., van der Ark, A. A. J., van der Woude, F. J., van Es, L. A., and Daha, M. R. (1991) Interleukin 2 mediates stimulation of complement C3 biosynthesis in human proximal tubular epithelial cells. J. Clin. Invest. 88, 379-384
10. Sheerin, N. S., Zhou, W., Adler, S., and Sacks, S. H. (1997) TNF-alpha regulation of C3 gene expression and protein biosynthesis in rat glomerular endothelial cells. Kidney Int. 51, 703-710
11. McPhaden, A. R., and Whaley, K. (1993) Complement biosynthesis by mononuclear phagocytes. Immunol. Res. 12, 213-232
12. Botto, M., Lissandrini, D., Sorio, C., and Walport, M. J. (1992) Biosynthesis and secretion of complement component (C3) by activated human polymorphonuclear leukocytes. J. Immunol. 149, 1348-1355
13. Springall, T., Sheerin, N. S., Abe, K., Holers, V. M., Wan, H., and Sacks, S. H. (2001) Epithelial secretion of C3 promotes colonization of the upper urinary tract by Escherichia coli. Nat. Med. 7, 801-806
14. Fisher, M. B., Ma, M., Hsu, N. C., and Carrol, M. C. (1998) Local synthesis of C3 within the splenic lymphoid compartment can reconstitute the impaired immune response in C3-deficient mice. J. Immunol. 160, 2619-2625
15. Pratt, J. R., Basheer, S. A., and Sacks, S. H. (2002) Local synthesis of complement component C3 regulates acute renal transplant rejection. Nat. Med. 8, 582-587
16. Farrar, C. A., Wang, Y., Sacks, S. H., and Zhou, W. (2004) Independent pathways of P-selectin and complement-mediated renal ischemia/reperfusion injury. Am. J. Pathol. 164, 133-141
17. Singbartl, K., Green, S. A., and Ley, K. (2000) Blocking Pselectin protects from ischemia/reperfusion-induced acute renal failure. FASEB J. 14, 48-54
18. Takada, M., Nadeau, K. C., Shaw, G. D., Marquette, K. A., and Tilney, N. L. (1997) The cytokine-adhesion molecule cascade in ischemia/reperfusion injury of the rat kidney. Inhibition by a soluble P-selectin ligand. J. Clin. Invest. 99, 2682-2690
19. Yasojima, K., Kilgore, K. S., Washington, R. A., Lucchesi, B. R., and McGreer, P. L. (1998) Complement gene expression by rabbit heart. Circ. Res. 82, 1224-1230
20. Colten, H. R. (1992) Tissue-specific regulation of inflammation. J. Appl. Physiol. 72, 1-7
21. Hoffmann, S., Park, J., Jacobson, L. M., Muehrer, R. J., Lorentzen, D., Kleiner, D., Becker, Y. T., Hullett, D. A., Mannon, R., Kirk, A. D., et al. (2004) Donor genomics influence graft events: the effect of donor polymorphisms on acute rejection and chronic allograft nephropathy. Kidney Int. 66, 1686-1693
22. Bartok, I., and Walport, M. J. (1995) Comparison of the binding of C3S and C3F to complement receptors types 1, 2, and 3. J. Immunol. 154, 5367-5375
23. Pratt, J. R., Jones, M. E., Dong, J., Zhou, W., Chowdhury, P., Smith, R. A., and Sacks, S. H. (2003) Nontransgenic hyperexpression of a complement regulator in donor kidney modulates transplant ischemia/reperfusion damage, acute rejection, and chronic nephropathy. Am. J. Pathol. 163, 1457-1465
24. Fischer, M. B., Ma, M., Goerg, S., Zhou, X., Xia, J., Finco, O., Han, S., Kelsoe, G., Howard, R. G., Rothstein, T. L., et al. (1996) Regulation of the B cell response to T-dependent antigens by classical pathway complement. J. Immunol. 157, 549-556
25. Wessels, M. R., Butko, P., Ma, M., Warren, H. B., Lage, A. L., and Carroll, M. C. (1995) Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc. Natl. Acad. Sci. USA 92, 11490-11494
26. Kalina, S. L., and Mottram, P. L. (1993) A microsurgical technique for renal transplantation in mice. Aust. N. Z. J. Surg. 63, 213-216
27. Kelly, K. J., Williams, W. W., Colvin, R. B., Meehan, S. M., Springer, T. A., Gutierrez-Ramos, J.-C., and Bonventre, J. V. (1996) Intercellular adhesion molecule-1-deficient mice are protected against ischemic renal injury. J. Clin. Invest. 97, 1056-1063
28. Bao, L., Haas, M., Kraus, D. M., Hack, B. K., Rakstang, J. K., Holers, V. M., and Quigg, R. J. (2003) Administration of a soluble recombinant complement C3 inhibitor protects against renal disease in MRL/lpr mice. J. Am. Soc. Nephrol. 14, 670-679
29. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning. A Laboratory Manual, 2nd Ed, Cold Spring Harbour Laboratory Press, p7.8, Cold Spring Harbor, NY
30. Pfaffl, M. W., Horgan, G. W., and Dempfle, L. (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res. 30, e36
31. Bonventre, J. V., and Weinberg, J. M. (2003) Recent advances in the pathophysiology of ischemic acute renal failure. J. Am. Soc. Nephrol. 14, 2199-2210
32. Thurman, J. M., Ljubanovic, D., Edelstein, C. L., Gilkeson, G. S., and Holers, V. M. (2003) Lack of a functional alternative complement pathway ameliorates ischemic acute renal failure in mice. J. Immunol. 170, 1517-1523
33. Brooimans, R. A., Stegmann, A. P. A., van Dorp, W. T., van der Ark, A. A. J., van der Woude, F. J., van Es, L. A., and Daha, M. R. (1991) Interleukin 2 mediates stimulation of complement C3 biosynthesis in human proximal tubular epithelial cells. J. Clin. Invest. 88, 379-384
34. Springer, T. A. (1990) Adhesion receptors of the immune system. Nature (London) 346, 425-434
35. Heinzelmann, M., Mercer-Jones, M. A., and Passmore, J. C. (1999) Neutrophils and renal failure. Am. J. Kidney Dis. 34, 384-399
36. Zhou, W., Marsh, J. E., and Sacks, S. H. (2001) Intrarenal synthesis of complement. Kidney Int. 59, 1227-1235
37. Tang, S., Sheerin, N. S., Zhou, W., Brown, Z., and Sacks, S. H. (1998) Apical proteins stimulate complement synthesis by cultured human proximal tubular epithelial cells. J. Am. Soc. Nephrol. 10, 69-76
38. Tang, S., Zhou, W., Sheerin, N. S., Vaughan, R. W., and Sacks, S. H. (1999) Contribution of renal secreted complement C3 to the circulating pool in humans. J. Immunol. 162, 4336-4341
39. Biancone, L., David, S., Della Pietra, V., Montrucchio, G., Cambi, V., and Camussi, G. (1994) Alternative pathway activation of complement by cultured human proximal tubular epithelial cells. Kidney Int. 45, 451-460
40. David, S., Biancone, L., Caserta, C., Bussolati, B., Cambi, V., and Camussi, G. (1997) Alternative pathway complement activation induces proinflammatory activity in human proximal tubular epithelial cells. Nephrol. Dial. Transplant. 12, 51-56
41. De Vries, B., Köhl, J., Leclercq, W. K. G., Wolfs, T. G. A. M., Van Bijnen, A. A. J., Heeringa, P., and Buurman, W. A. (2003) Complement factor C5a mediates renal ischemia-reperfusion injury independent from neutrophils. J. Immunol. 170, 3883-3889
42. Moller-Kristensen, M., Wang, W., Ruseva, M., Thiel, S., Nielsen, S., Takahashi, K., Shi, L., Ezekowitz, A., Jensenius, J. C., and Gadjeva, M. (2005) Mannan-binding lectin recognizes structures on ischaemic reperfused mouse kidneys and is implicated in tissue injury. Scand. J. Immunol. 61, 426-434
43. Gerritsma, J. S., Gerritsen, A. F., Van Kooten, C., Van Es, L. A., and Daha, M. R. (1996) Interleukin-1 alpha enhances the biosynthesis of complement C3 and factor B by human kidney proximal tubular epithelial cells in vitro. Mol. Immunol. 33, 847-854
44. Shoskes, D. A., and Cecka, J. M. (1998) Deleterious effects of delayed graft function in cadaveric renal transplant recipients independent of acute rejection. Transplantation 66, 1697-1701
45. Molmenti, E. P., Ziambaras, T., and Perlmutter, D. H. (1993) Evidence for an acute phase response in human intestinal epithelial cells. J. Biol. Chem. 268, 14116-14124
46. Passwell, J., Schreiner, G. F., Nonaka, M., Beuscher, H. U., and Colten, H. R. (1988) Local extrahepatic expression of complement genes C3, factor B, C2, and C4 is increased in murine lupus nephritis. J. Clin. Invest. 82, 1676-1684
47. x moieties. J. Immunol. 162, 4952-4959