Efficacy of targeted complement inhibition in experimental C3 glomerulopathy

Journal of the American Society of Nephrology

Volumn 27, Issue 2, 2016, Pages 405-416

  Ruseva, Marieta M ^a   Peng, Tao ^b   Lasaro, Melissa A ^b   Bouchard, Keith ^b   Liu Chen, Susan ^b   Sun, Fang ^b   Yu, Zhao Xue ^b   Marozsan, Andre ^b   Wang, Yi ^b   Pickering, Matthew C ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b ALEXION PHARMACEUTICALS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C3D; COMPLEMENT COMPONENT C9; COMPLEMENT INHIBITOR; COMPLEMENT MEMBRANE ATTACK COMPLEX; COMPLEMENT RECEPTOR 2 COMPLEMENT FACTOR H FUSION PROTEIN; HYBRID PROTEIN; UNCLASSIFIED DRUG; CR2-FH PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPLEMENT BLOOD LEVEL; COMPLEMENT COMPONENT C3 GLOMERULOPATHY; COMPLEMENT DEPOSITION; COMPLEMENT INHIBITION; CONTROLLED STUDY; DRUG EFFICACY; GLOMERULOPATHY; GLOMERULUS BASEMENT MEMBRANE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TREATMENT OUTCOME; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; KIDNEY DISEASES; METABOLISM;

ANIMALS; COMPLEMENT C3; DISEASE MODELS, ANIMAL; GLOMERULAR BASEMENT MEMBRANE; KIDNEY DISEASES; MICE; RECOMBINANT FUSION PROTEINS;

EID: 84970928343     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2014121195     Document Type: Article

References (41)

1. Pickering MC, D'Agati VD, Nester CM, Smith RJ, Haas M, Appel GB, Alpers CE, Bajema IM, Bedrosian C, Braun M, Doyle M, Fakhouri F, Fervenza FC, Fogo AB, Frémeaux-Bacchi V, Gale DP, Goicoechea de Jorge E, Griffin G, Harris CL, Holers VM, Johnson S, Lavin PJ,Medjeral-Thomas N, Paul Morgan B, Nast CC, Noel LH, Peters DK, Rodríguez de Córdoba S, Servais A, Sethi S, Song WC, Tamburini P, Thurman JM, Zavros M, Cook HT: C3 glomerulopathy: consensus report. Kidney Int 84: 1079-1089, 2013
2. Hou J, Markowitz GS, Bomback AS, Appel GB, Herlitz LC, Barry Stokes M, D'Agati VD: Toward a working definition of C3 glomerulopathy by immunofluorescence. Kidney Int 85: 450-456, 2014
3. Servais A, Frémeaux-Bacchi V, Lequintrec M, Salomon R, Blouin J, Knebelmann B, Grünfeld JP, Lesavre P, Noël LH, Fakhouri F: Primary glomerulonephritiswith isolated C3 deposits: a new entity which shares common genetic risk factors with haemolytic uraemic syndrome. JMed Genet 44: 193-199, 2007
4. Smith RJ, Harris CL, Pickering MC: Dense deposit disease. Mol Immunol 48: 1604-1610, 2011
5. Martínez-Barricarte R, Heurich M, Valdes-Cañedo F, Vazquez-Martul E, Torreira E, Montes T, Tortajada A, Pinto S, Lopez-Trascasa M, Morgan BP, Llorca O, Harris CL, Rodríguez de Córdoba S: Human C3 mutation reveals a mechanism of dense deposit disease pathogenesis and provides insights into complement activation and regulation. J Clin Invest 120: 3702-3712, 2010
6. Heurich M, Martínez-Barricarte R, Francis NJ, Roberts DL, Rodríguez de Córdoba S, Morgan BP, Harris CL: Common polymorphisms in C3, factor B, and factor H collaborate to determine systemic complement activity and disease risk. Proc Natl Acad Sci U S A 108: 8761-8766, 2011
7. Spitzer RE, Vallota EH, Forristal J, Sudora E, Stitzel A, Davis NC, West CD: Serum C'3 lytic systemin patients with glomerulonephritis. Science 164: 436-437, 1969
8. Athanasiou Y, Voskarides K, Gale DP, Damianou L, Patsias C, ZavrosM, Maxwell PH, Cook HT, Demosthenous P, Hadjisavvas A, Kyriacou K, Zouvani I, Pierides A, Deltas C: Familial C3 glomerulopathy associated with CFHR5 mutations: clinical characteristics of 91 patients in 16 pedigrees. Clin J Am Soc Nephrol 6: 1436-1446, 2011
9. Medjeral-Thomas NR, O'Shaughnessy MM, O'Regan JA, Traynor C, Flanagan M, Wong L, TeohCW, Awan A,Waldron M, Cairns T,O'Kelly P, Dorman AM, Pickering MC, Conlon PJ, Cook HT: C3 glomerulopathy: clinicopathologic features and predictors of outcome. Clin J Am Soc Nephrol 9: 46-53, 2014
10. Bomback AS, Smith RJ, Barile GR, Zhang Y, Heher EC, Herlitz L, Stokes MB, Markowitz GS, D'Agati VD, Canetta PA, Radhakrishnan J, Appel GB: Eculizumab for dense deposit disease and C3 glomerulonephritis. Clin J Am Soc Nephrol 7: 748-756, 2012
11. Herlitz LC, Bomback AS, Markowitz GS, Stokes MB, Smith RN, Colvin RB, Appel GB, D'Agati VD: Pathology after eculizumab in dense deposit disease and C3 GN. J Am Soc Nephrol 23: 1229-1237, 2012
12. McCaughan JA, O'Rourke DM, Courtney AE: Recurrent dense deposit disease after renal transplantation: an emerging role for complementary therapies. Am J Transplant 12: 1046-1051, 2012
13. Besbas N, Gulhan B, Gucer S, Korkmaz E, Ozaltin F: A novel CFHR5 mutation associated with C3 glomerulonephritis in a Turkish girl. J Nephrol 27: 457-460, 2014
14. Daina E, Noris M, Remuzzi G: Eculizumab in a patient with densedeposit disease. N Engl JMed 366: 1161-1163, 2012
15. Berthe-Aucejo A, Sacquépée M, Fila M, Peuchmaur M, Perrier-Cornet E, Frémeaux-Bacchi V, Deschênes G: Blockade of alternative complement pathway in dense deposit disease [published online ahead of print February 6, 2014]. Case Rep Nephrol doi:10. 1155/2014/201568
16. Sánchez-Moreno A, De la Cerda F, Cabrera R, Fijo J, López-TrascasaM, Bedoya R, Rodríguez de Córdoba S, Ybot-González P: Eculizumab in dense-deposit disease after renal transplantation. Pediatr Nephrol 29: 2055-2059, 2014
17. OzkayaO,Nalcacioglu H, TekcanD, Genc G,Meydan BC,Ozdemir BH, Baysal MK, Keceligil HT: Eculizumab therapy in a patient with densedeposit disease associated with partial lipodystropy. Pediatr Nephrol 29: 1283-1287, 2014
18. Gurkan S, Fyfe B, Weiss L, Xiao X, Zhang Y, Smith RJ: Eculizumab and recurrent C3 glomerulonephritis. Pediatr Nephrol 28: 1975-1981, 2013
19. Vivarelli M, Pasini A, Emma F: Eculizumab for the treatment of densedeposit disease. N Engl JMed 366: 1163-1165, 2012
20. Pickering MC, Warren J, Rose KL, Carlucci F, Wang Y, Walport MJ, Cook HT, Botto M: Prevention of C5 activation ameliorates spontaneous and experimental glomerulonephritis in factor H-deficient mice. Proc Natl Acad Sci U S A 103: 9649-9654, 2006
21. Huang Y, Qiao F, Atkinson C, Holers VM, Tomlinson S: A novel targeted inhibitor of the alternative pathway of complement and its therapeutic application in ischemia/reperfusion injury. J Immunol 181: 8068-8076, 2008
22. Risitano AM,Notaro R, Pascariello C, SicaM, del Vecchio L, Horvath CJ, Fridkis-Hareli M, Selleri C, Lindorfer MA, Taylor RP, Luzzatto L, Holers VM: The complement receptor 2/factor H fusion protein TT30 protects paroxysmal nocturnal hemoglobinuria erythrocytes from complementmediated hemolysis and C3 fragment. Blood 119: 6307-6316, 2012
23. Renner B, Ferreira VP, Cortes C, Goldberg R, Ljubanovic D, Pangburn MK, Pickering MC, Tomlinson S, Holland-Neidermyer A, Strassheim D, Holers VM, Thurman JM: BinDing of factor H to tubular epithelial cells limits interstitial complement activation in ischemic injury. Kidney Int 80: 165-173, 2011
24. Takeda K, Thurman JM, Tomlinson S,OkamotoM, Shiraishi Y, Ferreira VP, Cortes C, Pangburn MK, Holers VM, Gelfand EW: The critical role of complement alternative pathway regulator factor H in allergen-induced airway hyperresponsiveness and inflammation. J Immunol 188: 661-667, 2012
25. Rohrer B, Long Q, Coughlin B, Wilson RB, Huang Y, Qiao F, Tang PH, Kunchithapautham K, Gilkeson GS, Tomlinson S: A targeted inhibitor of the alternative complement pathway reduces angiogenesis in a mouse model of age-relatedmacular degeneration. Invest Ophthalmol Vis Sci 50: 3056-3064, 2009
26. Rohrer B, Coughlin B, Bandyopadhyay M, Holers VM: Systemic human CR2-targeted complement alternative pathway inhibitor ameliorates mouse laser-induced choroidal neovascularization. J Ocul Pharmacol Ther 28: 402-409, 2012
27. Banda NK, Levitt B, Glogowska MJ, Thurman JM, Takahashi K, Stahl GL, Tomlinson S, Arend WP, Holers VM: Targeted inhibition of the complement alternative pathway with complement receptor 2 and factor H attenuates collagen antibody-induced arthritis in mice. J Immunol 183: 5928-5937, 2009
28. de Jorge EG,Macor P, Paixão-Cavalcante D, Rose KL, Tedesco F, Cook HT, Botto M, Pickering MC: The development of atypical hemolytic uremic syndrome depends on complement C5. J Am SocNephrol 22: 137-145, 2011
29. Pickering MC, Cook HT, Warren J, Bygrave AE, Moss J, Walport MJ, Botto M: Uncontrolled C3 activation causes membranoproliferative glomerulonephritis in mice deficient in complement factor H. Nat Genet 31: 424-428, 2002
30. Paixão-Cavalcante D, Hanson S, Botto M, Cook HT, Pickering MC: Factor H facilitates the clearance of GBMbound iC3b by controlling C3 activation in fluid phase. Mol Immunol 46: 1942-1950, 2009
31. Fakhouri F, de Jorge EG, Brune F, Azam P, Cook HT, Pickering MC: Treatment with human complement factor H rapidly reverses renal complement deposition in factor H-deficient mice. Kidney Int 78: 279-286, 2010
32. Rose KL, Paixao-Cavalcante D, Fish J, Manderson AP, Malik TH, Bygrave AE, Lin T, Sacks SH,Walport MJ, Cook HT, Botto M, Pickering MC: Factor I is required for the development ofmembranoproliferative glomerulonephritis in factor H-deficient mice. J Clin Invest 118: 608-618, 2008
33. Licht C, Weyersberg A, Heinen S, Stapenhorst L, Devenge J, Beck B, Waldherr R, Kirschfink M, Zipfel PF, Hoppe B: Successful plasma therapy for atypical hemolytic uremic syndrome caused by factor H deficiency owing to a novel mutation in the complement cofactor protein domain 15. Am J Kidney Dis 45: 415-421, 2005
34. Rawal N, Pangburn MK: C5 convertase of the alternative pathway of complement. Kinetic analysis of the free and surface-bound forms of the enzyme. J Biol Chem273: 16828-16835, 1998
35. Dragon-Durey MA, Frémeaux-Bacchi V, Loirat C, Blouin J, Niaudet P, Deschenes G, Coppo P, Herman Fridman W, Weiss L: Heterozygous and homozygous factor h deficiencies associated with hemolytic uremic syndrome or membranoproliferative glomerulonephritis: report and genetic analysis of 16 cases. J AmSocNephrol 15: 787-795, 2004
36. Barbour TD, Pickering MC, Terence Cook H: Dense deposit disease and C3 glomerulopathy. Semin Nephrol 33: 493-507, 2013
37. Ruseva MM, Vernon KA, Lesher AM, Schwaeble WJ, Ali YM, Botto M, Cook T, Song W, Stover CM, Pickering MC: Loss of properdin exacerbates C3 glomerulopathy resulting from factor H deficiency. J Am Soc Nephrol 24: 43-52, 2013
38. Lesher AM, Zhou L, Kimura Y, Sato S, Gullipalli D, Herbert AP, Barlow PN, EberhardtHU, Skerka C, ZipfelPF,Hamano T,MiwaT, TungKS, SongWC: Combination of factorHmutation and properdin deficiency causes severe C3 glomerulonephritis. J Am Soc Nephrol 24: 53-65, 2013
39. Pickering MC, de Jorge EG, Martinez-Barricarte R, Recalde S, Garcia-Layana A, Rose KL, Moss J, Walport MJ, Cook HT, de Córdoba SR, Botto M: Spontaneous hemolytic uremic syndrome triggered by complement factor H lacking surface recognition domains. J ExpMed 204: 1249-1256, 2007
40. Fridkis-Hareli M, Storek M, Mazsaroff I, Risitano AM, Lundberg AS, Horvath CJ, Holers VM: Design and development of TT30, a novel C3dtargeted C3/C5 convertase inhibitor for treatment of human complement alternative pathway-mediated diseases. Blood 118: 4705-4713, 2011
41. Morgan BP: Measurement of complement hemolytic activity, generation of complement-depleted sera, and production of hemolytic intermediates. Methods Mol Biol 150: 61-71, 2000