Complement-mediated dysfunction of glomerular filtration barrier accelerates progressive renal injury

Journal of the American Society of Nephrology

Volumn 19, Issue 6, 2008, Pages 1158-1167

  Abbate, Mauro ^a,b   Zoja, Carla ^a   Corna, Daniela ^a   Rottoli, Daniela ^a   Zanchi, Cristina ^a   Azzollini, Nadia ^a   Tomasoni, Susanna ^a   Bedingeri, Silvia ^a   Noris, Marina ^a   Morigi, Marina ^a   Remuzzi, Giuseppe ^a  

^a OSPEDALI RIUNITI   (Italy)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3 RECEPTOR; LISINOPRIL; PLASMA PROTEIN; COMPLEMENT COMPONENT C3;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; DISEASE COURSE; DISEASE PREDISPOSITION; GLOMERULUS FILTRATION; INTERVENTION STUDY; KIDNEY CELL; KIDNEY DISEASE; KIDNEY INJURY; KIDNEY INTERSTITIUM; KIDNEY PROXIMAL TUBULE; KIDNEY TRANSPLANTATION; MALE; MODEL; MOUSE; NEPHRITIS; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEINURIA; RAT; SYNTHESIS; TISSUE INJURY; WILD TYPE; ANIMAL; GLOMERULUS FILTRATION RATE; KIDNEY FAILURE; PHYSIOLOGY;

ANIMALS; COMPLEMENT C3; DISEASE PROGRESSION; GLOMERULAR FILTRATION RATE; KIDNEY FAILURE; MALE; MICE;

EID: 48049093069     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2007060686     Document Type: Article

References (58)

1. Perico N, Codreanu I, Schieppati A, Remuzzi G: Pathophysiology of disease progression in proteinuric nephropathies. Kidney Int Suppl S79-S82, 2005
2. Sarnak MJ, Levey AS, Schoolwerth AC, Coresh J, Culleton B, Hamm LL, McCullough PA, Kasiske BL, Kelepouris E, Klag MJ, Parfrey P, Pfeffer M, Raij L, Spinosa DJ, Wilson PW: Kidney disease as a risk factor for development of cardiovascular disease: A statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation 108: 2154-2169, 2003
3. Hostetter TH: Chronic kidney disease predicts cardiovascular disease. N Engl J Med 351: 1344-1346, 2004
4. Irie F, Iso H, Sairenchi T, Fukasawa N, Yamagishi K, Ikehara S, Kanashiki M, Saito Y, Ota H, Nose T: The relationships of proteinuria, serum creatinine, glomerular filtration rate with cardiovascular disease mortality in Japanese general population. Kidney Int 69: 1264-1271, 2006
5. Brenner BM, Meyer TW, Hostetter TH: Dietary protein intake and the progressive nature of kidney disease: The role of hemodynamically mediated glomerular injury in the pathogenesis of progressive glomerular sclerosis in aging, renal ablation, and intrinsic renal disease. N Engl J Med 307: 652-659, 1982
6. Anderson S, Meyer TW, Rennke HG, Brenner BM: Control of glomerular hypertension limits glomerular injury in rats with reduced renal mass. J Clin Invest 76: 612-619, 1985
7. Remuzzi G: Nephropathic nature of proteinuria. Curr Opin Nephrol Hypertens 8: 655-663, 1999
8. Abbate M, Zoja C, Remuzzi G: How does proteinuria cause progressive renal damage? J Am Soc Nephrol 17: 2974-2984, 2006
9. Quigg RJ: Complement and the kidney. J Immunol 171: 3319-3324, 2003
10. Camussi G, Stratta P, Mazzucco G, Gaido M, Tetta C, Castello R, Rotunno M, Vercellone A: In vivo localization of C3 on the brush border of proximal tubules of kidneys from nephrotic patients. Clin Nephrol 23: 134-141, 1985
11. Hsu SI-H, Couser WG: Chronic progression of tubulointerstitial damage in proteinuric renal disease is mediated by complement activation: A therapeutic role for complement inhibitors? J Am Soc Nephrol 14: S186-S191, 2003
12. Nath KA, Hostetter MK, Hostetter TH: Pathophysiology of chronic tubulo-interstitial disease in rats: Interactions of dietary acid load, ammonia, and complement component C3. J Clin Invest 76: 667-675, 1985
13. Abbate M, Zoja C, Corna D, Capitanio M, Bertani T, Remuzzi G: In progressive nephropathies, overload of tubular cells with filtered proteins translates glomerular permeability dysfunction into cellular signals of interstitial inflammation. J Am Soc Nephrol 9: 1213-1224, 1998
14. Abbate M, Zoja C, Rottoli D, Corna D, Perico N, Bertani T, Remuzzi G: Antiproteinuric therapy while preventing the abnormal protein traffic in proximal tubule abrogates protein and complement-dependent interstitial inflammation in experimental renal disease. J Am Soc Nephrol 10: 804-813, 1999
15. Nomura A, Morita Y, Maruyama S, Hotta N, Nadai M, Wang L, Hasegawa T, Matsuo S: Role of complement in acute tubulointerstitial injury of rats with aminonucleoside nephrosis. Am J Pathol 151: 539-547, 1997
16. Nangaku M, Pippin J, Couser WG: Complement membrane attack complex (C5b-9) mediates interstitial disease in experimental nephrotic syndrome. J Am Soc Nephrol 10: 2323-2331, 1999
17. Nangaku M, Pippin J, Couser WG: C6 mediates chronic progression of tubulointerstitial damage in rats with remnant kidneys. J Am Soc Nephrol 13: 928-936, 2002
18. Bao L, Haas M, Boackle SA, Kraus DM, Cunningham PN, Park P, Alexander JJ, Anderson RK, Culhane K, Holers VM, Quigg RJ: Transgenic expression of a soluble complement inhibitor protects against renal disease and promotes survival in MRL/lpr mice. J Immunol 168: 3601-3607, 2002
19. He C, Imai M, Song H, Quigg RJ, Tomlinson S: Complement inhibitors targeted to the proximal tubule prevent injury in experimental nephrotic syndrome and demonstrate a key role for C5b-9. J Immunol 174: 5750-5757, 2005
20. Wang Y, Hu Q, Madri JA, Rollins SA, Chodera A, Malis LA: Amelioration of lupus-like autoimmune disease in NZB/WF1 mice after treatment with a blocking monoclonal antibody specific for complement component C5. Proc Natl Acad Sci U S A 93: 8563-8568, 1996
21. Abbate M, Zoja C, Rottoli D, Corna D, Tomasoni S, Remuzzi G: Proximal tubular cells promote fibrogenesis by TGF-β1-mediated induction of peritubular myofibroblasts. Kidney Int 61: 2066-2077, 2002
22. Rangan GK, Pippin JW, Coombes JD, Couser WG: C5b-9 does not mediate chronic tubulointerstitial disease in the absence of protein-uria. Kidney Int 67: 492-503, 2005
23. Pratt JR, Basheer SA, Sacks SH: Local synthesis of complement component C3 regulates acute renal transplant rejection. Nat Med 8: 582-587, 2002
24. Eddy AA: Interstitial nephritis induced by protein-overload protein-uria. Am J Pathol 135: 719-733, 1989
25. Zhou W, Marsh JE, Sacks SH: Intrarenal synthesis of complement. Kidney Int 59: 1227-1235, 2001
26. Biancone L, David S, Della Pietra V, Montrucchio G, Cambi V, Camussi G: Alternative pathway activation of complement by cultured human proximal tubular epithelial cells. Kidney Int 45: 451-460, 1994
27. Peake PW, O'Grady S, Pussell BA, Charlesworth JA: C3a is made by proximal tubular HK-2 cells and activates them via the C3a receptor. Kidney Int 56: 1729-1736, 1999
28. Braun MC, Reins RY, Li TB, Hollmann TJ, Dutta R, Rick WA, Teng BB, Ke B: Renal expression of the C3a receptor and functional responses of primary human proximal tubular epithelial cells. J Immunol 173: 4190-4196, 2004
29. Boor P, Konieczny A, Villa L, Schult AL, Bucher E, Rong S, Kunter U, van Roeyen CR, Polakowski T, Hawlisch H, Hillebrandt S, Lammert F, Eitner F, Floege J, Ostendorf T: Complement C5 mediates experimental tubulointerstitial fibrosis. J Am Soc Nephrol 18: 1508-1515, 2007
30. Weening JJ, Van Guldener C, Daha MR, Klar N, Van Der Wal A, Prins FA: The pathophysiology of protein-overload proteinuria. Am J Pathol 129: 64-73, 1987
31. Macconi D, Ghilardi M, Bonassi ME, Mohamed El, Abbate M, Colombi F, Remuzzi G, Remuzzi A: Effect of angiotensin-converting enzyme inhibition on glomerular basement membrane permeability and distribution of zonula occludens-1 in MWF rats. J Am Soc Nephrol 11: 477-489, 2000
32. Macconi D, Abbate M, Morigi M, Angioletti S, Mister M, Buelli S, Bonomelli M, Mundel P, Endlich K, Remuzzi A, Remuzzi G: Permselective dysfunction of podocyte-podocyte contact upon angiotensin II unravels the molecular target for renoprotective intervention. Am J Pathol 168: 1073-1085, 2006
33. Welch TR, Blystone LW: C3 is central to the interstitial component of experimental immune complex glomerulonephritis. Clin Immunol 115: 80-84, 2005
34. Farrar CA, Zhou W, Lin T, Sacks SH: Local extravascular pool of C3 is a determinant of postischemic acute renal failure. FASEB J 20: 217-226, 2006
35. Tang S, Lai KN, Sacks SH: Role of complement in tubulointerstitial injury from proteinuria. Kidney Blood Press Res 25: 120-126, 2002
36. Tang S, Neng Lai K, Mao Chan T, Lan HY, Ho SK, Sacks SH: Transferrin but not albumin mediates stimulation of complement C3 biosynthesis in human proximal tubular epithelial cells. Am J Kidney Dis 37: 94-103, 2001
37. Tang S, Sheerin NS, Zhou W, Brown Z, Sacks SH: Apical proteins stimulate complement synthesis by cultured human proximal tubular epithelial cells. J Am Soc Nephrol 10: 69-76, 1999
38. Rudnicki M, Eder S, Perco P, Enrich J, Scheiber K, Koppelstatter C, Schratzberger G, Mayer B, Oberbauer R, Meyer TW, Mayer G: Gene expression profiles of human proximal tubular epithelial cells in proteinuric nephropathies. Kidney Int 71: 325-335, 2007
39. Zou Z, Chung B, Nguyen T, Mentone S, Thomson B, Biemesderfer D: Linking receptor-mediated endocytosis and cell signaling: Evidence for regulated intramembrane proteolysis of megalin in proximal tubule. J Biol Chem 279: 34302-34310, 2004
40. Caruso-Neves C, Pinheiro AA, Cai H, Souza-Menezes J, Guggino WB: PKB and megalin determine the survival or death of renal proximal tubule cells. Proc Natl Acad Sci U S A 103: 18810-18815, 2006
41. Abbate M, Morigi M, Buelli S, Moioli D, Zanchi C, Noris M, Zoja C, Remuzzi G: Loss of factor H-dependent complement regulation mediates proximal tubular cells dysfunction on protein overload [Abstract]. J Am Soc Nephrol 17: 596A, 2006
42. Abbate M, Zoja C, Morigi M, Rottoli D, Angioletti S, Tomasoni S, Zanchi C, Longaretti L, Donadelli R, Remuzzi G: Transforming growth factor-β1 is up-regulated by podocytes in response to excess intraglomerular passage of proteins. Am J Pathol 161: 2179-2193, 2002
43. Turnberg D, Lewis M, Moss J, Xu Y, Botto M, Cook HT: Complement activation contributes to both glomerular and tubulointerstitial damage in Adriamycin nephropathy in mice. J Immunol 177: 4094-4102, 2006
44. Alexander JJ, Wang Y, Chang A, Jacob A, Minto AW, Karmegam M, Haas M, Quigg RJ: Mouse podocyte complement factor H: The functional analog to human complement receptor 1. J Am Soc Nephrol 18: 1157-1166, 2007
45. Hillmen P, Hall C, Marsh JC, Elebute M, Bombara MP, Petro BE, Cullen MJ, Richards SJ, Rollins SA, Mojcik CF, Rother RP: Effect of eculizumab on hemolysis and transfusion requirements in patients with paroxysmal nocturnal hemoglobinuria. N Engl J Med 350: 552-559, 2004
46. Granger CB, Mahaffey KW, Weaver WD, Theroux P, Hochman JS, Filloon TG, Rollins S, Todaro TG, Nicolau JC, Ruzyllo W, Armstrong PW: Pexelizumab, an anti-C5 complement antibody, as adjunctive therapy to primary percutaneous coronary intervention in acute myocardial infarction: The COMplement inhibition in Myocardial infarction treated with Angioplasty (COMMA) trial. Circulation 108: 1184-1190, 2003
47. Li JS, Sanders SP, Perry AE, Stinnett SS, Jaggers J, Bokesch P, Reynolds L, Nassar R, Anderson PA: Pharmacokinetics and safety of TP10, soluble complement receptor 1, in infants undergoing cardiopulmonary bypass. Am Heart J 147: 173-180, 2004
48. Benigni A, Corna D, Zoja C, Longaretti L, Gagliardini E, Perico N, Coffman TM, Remuzzi G: Targeted deletion of angiotensin II type 1A receptor does not protect mice from progressive nephropathy of overload proteinuria. J Am Soc Nephrol 15: 2666-2674, 2004
49. Eddy AA, Kim H, Lopez-Guisa J, Oda T, Soloway PD, McCulloch L, Liu E, Wing D: Interstitial fibrosis in mice with overload proteinuria: Deficiency of TIMP-1 is not protective. Kidney Int 58: 618-628, 2000
50. Noble B, Olson KA, Milgrom M, Albini B: Tissue deposition of immune complexes in mice receiving daily injections of bovine serum albumin. Clin Exp Immunol 42: 255-262, 1980
51. Wada T, Tomosugi N, Naito T, Yokoyama H, Kobayashi K, Harada A, Mukaida N, Matsushima K: Prevention of proteinuria by the administration of anti-interleukin 8 antibody in experimental acute immune complex-induced glomerulonephritis. J Exp Med 180: 1135-1140, 1994
52. Ouchterlony O: Diffusion-in-gel methods for immunological analysis. II. Prog Allergy 6: 30-154, 1962
53. Zhang Z, Schlachta C, Duff J, Stiller C, Grant D, Zhong R: Improved techniques for kidney transplantation in mice. Microsurgery 16: 103-109, 1995
54. Han WR, Murray-Segal LJ, Mottram PL: Modified technique for kidney transplantation in mice. Microsurgery 19: 272-274, 1999
55. Ishola DA Jr, van der Giezen DM, Hahnel B, Goldschmeding R, Kriz W, Koomans HA, Joles JA: In mice, proteinuria and renal inflammatory responses to albumin overload are strain-dependent. Nephrol Dial Transplant 21: 591-597, 2006
56. van Timmeren MM, Bakker SJ, Stegeman CA, Gans RO, van Goor H: Addition of oleic acid to delipidated bovine serum albumin aggravates renal damage in experimental protein-overload nephrosis. Nephrol Dial Transplant 20: 2349-2357, 2005
57. Benigni A, Zoja C, Tomasoni S, Carnpana M, Corna D, Zanchi C, Gagliardini E, Garofano E, Rottoli D, Ito T, Remuzzi G: Transcriptional regulation of nephrin gene by peroxisome proliferator-activated receptor-gamma agonist: Molecular mechanism of the antiproteinuric effect of pioglitazone. J Am Soc Nephrol 17: 1624-1632, 2006
58. Benigni A, Tomasoni S, Gagliardini E, Zoja C, Grunkemeyer JA, Kalluri R, Remuzzi G: Blocking angiotensin II synthesis/activity preserves glomerular nephrin in rats with severe nephrosis. J Am Soc Nephrol 12: 941-948, 2001