Kidney disease caused by dysregulation of the complement alternative pathway: An etiologic approach

Journal of the American Society of Nephrology

Volumn 26, Issue 12, 2015, Pages 2917-2929

  De Vriese, An S ^a   Sethi, Sanjeev ^b   Van Praet, Jens ^a   Nath, Karl A ^b   Fervenza, Fernando C ^b  

^a Department of Internal Medicine   (Belgium)

^b MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; AUTOANTIBODY; CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C3B; COMPLEMENT FACTOR H; ECULIZUMAB; IMMUNOSUPPRESSIVE AGENT; MEMBRANE COFACTOR PROTEIN; MUTANT PROTEIN; NEPHRITIC FACTOR; COMPLEMENT FACTOR I;

COMPLEMENT ACTIVATION; COMPLEMENT ALTERNATIVE PATHWAY; ENZYME INHIBITION; ENZYME STABILITY; GAIN OF FUNCTION MUTATION; GENE PRODUCT; HUMAN; IMMUNE DYSREGULATION; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY DISEASE; LIVER TRANSPLANTATION; MOLECULAR PATHOLOGY; MONOCLONAL IMMUNOGLOBULINEMIA; NONHUMAN; PHASE 2 CLINICAL TRIAL (TOPIC); PLASMA CELL DYSCRASIA; PLASMA TRANSFUSION; PLASMAPHERESIS; PRIORITY JOURNAL; REVIEW; ANIMAL; CLASSIFICATION; DEFICIENCY; GENETICS; IMMUNOLOGY; KIDNEY DISEASES; METABOLISM; PHYSIOLOGY;

ANIMALS; AUTOANTIBODIES; COMPLEMENT C3-C5 CONVERTASES; COMPLEMENT C3B INACTIVATOR PROTEINS; COMPLEMENT FACTOR H; COMPLEMENT PATHWAY, ALTERNATIVE; HUMANS; KIDNEY DISEASES;

EID: 84954040776     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2015020184     Document Type: Review

References (117)

1. Noris M, Remuzzi G: Overview of complement activation and regulation. Semin Nephrol 33: 479-492, 2013
2. Thurman JM, Holers VM: The central role of the alternative complement pathway in human disease. J Immunol 176: 1305-1310, 2006
3. 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
4. Sethi S, Fervenza FC: Pathology of renal diseases associated with dysfunction of the alternative pathway of complement: C3 glomerulopathy and atypical hemolytic uremic syndrome (aHUS). Semin ThrombHemost 40: 416-421, 2014
5. Bomback AS, Appel GB: Pathogenesis of theC3 glomerulopathies and reclassification of MPGN. Nat Rev Nephrol 8: 634-642, 2012
6. Sethi S, Fervenza FC, Zhang Y, Zand L, Meyer NC, Borsa N, Nasr SH, Smith RJ: Atypical postinfectious glomerulonephritis is associated with abnormalities in the alternative pathway of complement. Kidney Int 83: 293-299, 2013
7. Ramadass M, Ghebrehiwet B, Smith RJ, Kew RR: Generation ofmultiple fluid-phase C3b: plasma protein complexes during complement activation: Possible implications in C3 glomerulopathies. J Immunol 192: 1220-1230, 2014
8. Couser WG, Johnson RJ: The etiology of glomerulonephritis: Roles of infection and autoimmunity. Kidney Int 86: 905-914, 2014
9. Pérez-Caballero D, González-Rubio C, Gallardo ME, Vera M, López-Trascasa M, Rodríguez de Córdoba S, Sánchez-Corral P: Clustering of missense mutations in the C-terminal region of factor H in atypical hemolytic uremic syndrome. Am J Hum Genet 68: 478-484, 2001
10. BoelsMG, Lee DH, van den Berg BM, Dane MJ, van der Vlag J, Rabelink TJ: The endothelial glycocalyx as a potential modifier of the hemolytic uremic syndrome. Eur J Intern Med 24: 503-509, 2013
11. Gnappi E, Allinovi M, Vaglio A, Bresin E, Sorosina A, Pilato FP, Allegri L, Manenti L: Membrano-proliferative glomerulonephritis, atypical hemolytic uremic syndrome, and a new complement factor H mutation: Report of a case. Pediatr Nephrol 27: 1995-1999, 2012
12. Vaziri-Sani F, Holmberg L, Sjöholm AG, Kristoffersson AC, Manea M, Frémeaux-Bacchi V, Fehrman-Ekholm I, Raafat R, KarpmanD: Phenotypic expression of factor H mutations in patients with atypical hemolytic uremic syndrome. Kidney Int 69: 981-988, 2006
13. Jha V, Murthy MS, Kohli HS, Sud K, Gupta KL, Joshi K, Sakhuja V: Secondary membranoproliferative glomerulonephritis due to hemolytic uremic syndrome: An unusual presentation. Ren Fail 20: 845-850, 1998
14. Manenti L, Gnappi E, Vaglio A, Allegri L, Noris M, Bresin E, Pilato FP, Valoti E, Pasquali S, Buzio C: Atypical haemolytic uraemic syndrome with underlying glomerulopathies. A case series and a review of the literature. Nephrol Dial Transplant 28: 2246-2259, 2013
15. Boyer O, Noel LH, Balzamo E, Guest G, Biebuyck N, Charbit M, Salomon R, Fremeaux-Bacchi V, Niaudet P: Complement factor H deficiency and posttransplantation glomerulonephritis with isolated C3 deposits. Am J Kidney Dis 51: 671-677, 2008
16. Lorcy N, Rioux-Leclercq N, LombardML, Le Pogamp P, Vigneau C: Three kidneys, two diseases, one antibody? Nephrol Dial Transplant 26: 3811-3813, 2011
17. Brackman D, Sartz L, Leh S, Kristoffersson AC, Bjerre A, Tati R, Fremeaux-Bacchi V, Karpman D: Thrombotic microangiopathy mimicking membranoproliferative glomerulonephritis. Nephrol Dial Transplant 26: 3399-3403, 2011
18. Meleg-Smith S: The many faces of C3 glomerulopathy. Kidney Int 82: 611, 2012
19. Sandhu G, Bansal A, Ranade A, Jones J, Cortell S, Markowitz GS: C3 glomerulopathy masquerading as acute postinfectious glomerulonephritis. Am J Kidney Dis 60: 1039-1043, 2012
20. Bresin E, Rurali E, Caprioli J, Sanchez-Corral P, Fremeaux-Bacchi V, Rodriguez de Cordoba S, Pinto S, Goodship TH, Alberti M, Ribes D, Valoti E, Remuzzi G, Noris M; European Working Party on Complement Genetics in Renal Diseases: Combined complement gene mutations in atypical hemolytic uremic syndrome influence clinical phenotype. J AmSocNephrol 24: 475-486, 2013
21. Roumenina LT, Frimat M, Miller EC, Provot F, Dragon-DureyMA, Bordereau P, Bigot S, Hue C, Satchell SC, Mathieson PW, Mousson C, Noel C, Sautes-Fridman C, Halbwachs-Mecarelli L, Atkinson JP, Lionet A, Fremeaux-Bacchi V: A prevalent C3 mutation in aHUS patients causes a direct C3 convertase gain of function. Blood 119: 4182-4191, 2012
22. Noris M, Caprioli J, Bresin E, Mossali C, Pianetti G, Gamba S, Daina E, Fenili C, Castelletti F, Sorosina A, Piras R, Donadelli R, Maranta R, van der Meer I, Conway EM, Zipfel PF, Goodship TH, Remuzzi G: Relative role of genetic complement abnormalities in sporadic and familial aHUS and their impact on clinical phenotype. Clin J AmSoc Nephrol 5: 1844-1859, 2010
23. Servais A, Noel LH, Roumenina LT, Le Quintrec M, Ngo S, Dragon-Durey MA, Macher MA, Zuber J, Karras A, Provot F, Moulin B, Grünfeld JP, Niaudet P, Lesavre P, Frémeaux-Bacchi V: Acquired and genetic complement abnormalities play a critical role in dense deposit disease and other C3 glomerulopathies. Kidney Int 82: 454-464, 2012
24. Montes T, Goicoechea de Jorge E, Ramos R, Gom M, Pujol O, Sánchez-Corral P, Rodríguez de Córdoba S: Genetic deficiency of complement factor H in a patient with age-related macular degeneration and membranoproliferative glomerulonephritis. Mol Immunol 45: 2897-2904, 2008
25. Schejbel L, Schmidt IM, Kirchhoff M, AndersenCB,MarquartHV, Zipfel P,Garred P: Complement factor H deficiency and endocapillary glomerulonephritis due to paternal isodisomy and a novel factor H mutation. Genes Immun 12: 90-99, 2011
26. Servais A, Noel LH, Dragon-Durey MA, GüblerMC, Rémy P, Buob D, Cordonnier C, Makdassi R, Jaber W, Boulanger E, Lesavre P, Frémeaux-Bacchi V: Heterogeneous pattern of renal disease associated with homozygous factor H deficiency. Hum Pathol 42: 1305-1311, 2011
27. Zipfel PF, Heinen S, Józsi M, Skerka C: Complement and diseases: Defective alternative pathway control results in kidney and eye diseases. Mol Immunol 43: 97-106, 2006
28. Habbig S, Mihatsch MJ, Heinen S, Beck B, Emmel M, Skerka C, Kirschfink M, Hoppe B, Zipfel PF, Licht C: C3 deposition glomerulopathy due to a functional factor H defect. Kidney Int 75: 1230-1234, 2009
29. Licht C, Heinen S, Józsi M, Löschmann I, Saunders RE, Perkins SJ, Waldherr R, Skerka C, Kirschfink M, Hoppe B, Zipfel PF: Deletion of Lys224 in regulatory domain 4 of Factor H reveals a novel pathomechanism for dense deposit disease (MPGNII). Kidney Int 70: 42-50, 2006
30. Wong EK, Anderson HE, Herbert AP, Challis RC, Brown P, Reis GS, Tellez JO, Strain L, Fluck N, Humphrey A, Macleod A, Richards A, Ahlert D, Santibanez-Koref M, Barlow PN,Marchbank KJ, Harris CL, Goodship TH, Kavanagh D: Characterization of a factor H mutation that perturbs the alternative pathway of complement in a family with membranoproliferative GN. J Am Soc Nephrol 25: 2425-2433, 2014
31. Leroy V, Fremeaux-Bacchi V, PeuchmaurM, Baudouin V, Deschnes G, Macher MA, Loirat C: Membranoproliferative glomerulonephritis with C3NeF and genetic complement dysregulation. Pediatr Nephrol 26: 419-424, 2011
32. Sethi S, Fervenza FC, Zhang Y, Nasr SH, Leung N, Vrana J, Cramer C, Nester CM, Smith RJ: Proliferative glomerulonephritis secondary to dysfunction of the alternative pathway of complement. Clin J Am Soc Nephrol 6: 1009-1017, 2011
33. Couser WG: Basic and translational concepts of immune-mediated glomerular diseases. JAmSocNephrol 23: 381-399, 2012
34. Fervenza FC, Smith RJ, Sethi S: Association of a novel complement factor H mutation with severe crescentic and necrotizing glomerulonephritis. Am J Kidney Dis 60: 126-132, 2012
35. Dragon-Durey MA, Sethi SK, Bagga A, Blanc C, Blouin J, Ranchin B, André JL, Takagi N, Cheong HI, Hari P, Le QuintrecM, Niaudet P, Loirat C, Fridman WH, Frémeaux-Bacchi V: Clinical features of anti-factorHautoantibodyassociated hemolytic uremic syndrome. J Am Soc Nephrol 21: 2180-2187, 2010
36. Hofer J, Janecke AR, Zimmerhackl LB, Riedl M, Rosales A, Giner T, Cortina G, Haindl CJ, Petzelberger B, PawlikM, Jeller V, Vester U, Gadner B, van Husen M, Moritz ML,Würzner R, Jungraithmayr T; German-Austrian HUS Study Group: Complement factor H-related protein 1 deficiency and factor H antibodies in pediatric patients with atypical hemolytic uremic syndrome. Clin J Am Soc Nephrol 8: 407-415, 2013
37. Józsi M, Licht C, Strobel S, Zipfel SL, Richter H, Heinen S, Zipfel PF, Skerka C: Factor H autoantibodies in atypical hemolytic uremic syndrome correlate with CFHR1/CFHR3 deficiency. Blood 111: 1512-1514, 2008
38. Moore I, Strain L, Pappworth I, Kavanagh D, Barlow PN, Herbert AP, Schmidt CQ, Staniforth SJ, Holmes LV, Ward R, Morgan L, Goodship TH,Marchbank KJ: Association of factor H autoantibodies with deletions of CFHR1, CFHR3, CFHR4, and with mutations in CFH, CFI, CD46, and C3 in patients with atypical hemolytic uremic syndrome. Blood 115: 379-387, 2010
39. Sinha A, Gulati A, Saini S, Blanc C, Gupta A, Gurjar BS, Saini H, Kotresh ST, Ali U, Bhatia D, Ohri A, Kumar M, Agarwal I, Gulati S, Anand K, Vijayakumar M, Sinha R, Sethi S, Salmona M, George A, Bal V, Singh G, Dinda AK, Hari P, Rath S, Dragon-Durey MA, Bagga A; Indian HUS Registry: Prompt plasma exchanges and immunosuppressive treatment improves the outcomes of antifactorHautoantibody-associated hemolytic uremic syndrome in children. Kidney Int 85: 1151-1160, 2014
40. Blanc C, Roumenina LT, Ashraf Y, Hyvärinen S, Sethi SK, Ranchin B, Niaudet P, Loirat C, Gulati A, Bagga A, Fridman WH, Sauts-Fridman C, Jokiranta TS, Frémeaux-Bacchi V, Dragon-DureyMA:Overall neutralization of complement factor H by autoantibodies in the acute phase of the autoimmune form of atypical hemolytic uremic syndrome. J Immunol 189: 3528-3537, 2012
41. Meri S, Koistinen V,Miettinen A, Törnroth T, Seppälä IJ: Activation of the alternative pathway of complement by monoclonal lambda light chains in membranoproliferative glomerulonephritis. J Exp Med 175: 939-950, 1992
42. Jokiranta TS, Solomon A, Pangburn MK, Zipfel PF, Meri S: Nephritogenic lambda light chain dimer: A unique human miniautoantibody against complement factor H. J Immunol 163: 4590-4596, 1999
43. Goodship TH, Pappworth IY, Toth T, Denton M, Houlberg K, McCormick F, Warland D, Moore I, Hunze EM, Staniforth SJ, Hayes C, Cavalcante DP, Kavanagh D, Strain L, Herbert AP, Schmidt CQ, Barlow PN, Harris CL, Marchbank KJ: Factor H autoantibodies in membranoproliferative glomerulonephritis. Mol Immunol 52: 200-206, 2012
44. Zhang Y, Meyer NC, Wang K, Nishimura C, Frees K, Jones M, Katz LM, Sethi S, Smith RJ: Causes of alternative pathway dysregulation in dense deposit disease. Clin J Am Soc Nephrol 7: 265-274, 2012
45. Skerka C, Chen Q, Fremeaux-Bacchi V, Roumenina LT: Complement factor H related proteins (CFHRs). Mol Immunol 56: 170-180, 2013
46. Goicoechea de Jorge E, Caesar JJ, Malik TH, Patel M, Colledge M, Johnson S, Hakobyan S, Morgan BP, Harris CL, Pickering MC, Lea SM: Dimerization of complement factor H-related proteins modulates complement activation in vivo. Proc Natl Acad Sci U S A 110: 4685-4690, 2013
47. Athanasiou Y, Voskarides K, Gale DP, Damianou L, Patsias C, Zavros M, 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
48. Chen Q, Wiesener M, Eberhardt HU, Hartmann A, Uzonyi B, Kirschfink M, Amann K, Buettner M, Goodship T, Hugo C, Skerka C, Zipfel PF: Complement factor H-related hybrid protein deregulates complement in dense deposit disease. J Clin Invest 124: 145-155, 2014
49. Gale DP, de Jorge EG, Cook HT, Martinez-Barricarte R, Hadjisavvas A, McLean AG, Pusey CD, Pierides A, Kyriacou K, Athanasiou Y, Voskarides K, Deltas C, Palmer A, Frémeaux-Bacchi V, de Cordoba SR, Maxwell PH, Pickering MC: Identification of amutation in complement factor H-related protein 5 in patients of Cypriot origin with glomerulonephritis. Lancet 376: 794-801, 2010
50. Malik TH, Lavin PJ, Goicoechea de Jorge E, Vernon KA, Rose KL, PatelMP, de LeeuwM, Neary JJ, Conlon PJ, Winn MP, Pickering MC: A hybrid CFHR3-1 gene causes familial C3 glomerulopathy. J Am Soc Nephrol 23: 1155-1160, 2012
51. Medjeral-Thomas N, Malik TH, Patel MP, Toth T, Cook HT, Tomson C, Pickering MC: A novel CFHR5 fusion protein causes C3 glomerulopathy in a family without Cypriot ancestry. Kidney Int 85: 933-937, 2014
52. Tortajada A, Yébenes H, Abarrategui-Garrido C, Anter J, García-Fernández JM, Martínez-Barricarte R, Alba-Domínguez M, Malik TH, Bedoya R, Cabrera Pérez R, López Trascasa M,PickeringMC,HarrisCL, Sánchez-Corral P, Llorca O, Rodríguez de Córdoba S: C3 glomerulopathy-associated CFHR1 mutation alters FHR oligomerization and complement regulation. J Clin Invest 123: 2434-2446, 2013
53. Venables JP, Strain L, Routledge D, Bourn D, PowellHM,Warwicker P, Diaz-TorresML, Sampson A, Mead P, Webb M, Pirson Y, Jackson MS, Hughes A, Wood KM, Goodship JA, Goodship TH: Atypical haemolytic uraemic syndrome associatedwith a hybrid complement gene. PLoS Med 3: e431, 2006
54. Maga TK, Meyer NC, Belsha C, Nishimura CJ, Zhang Y, Smith RJ: A novel deletion in the RCA gene cluster causes atypical hemolytic uremic syndrome. Nephrol Dial Transplant 26: 739-741, 2011
55. Eyler SJ,Meyer NC, Zhang Y, Xiao X, Nester CM, Smith RJ: A novel hybrid CFHR1/CFH gene causes atypical hemolytic uremic syndrome. Pediatr Nephrol 28: 2221-2225, 2013
56. Valoti E, Alberti M, Tortajada A, Garcia-Fernandez J, Gastoldi S, Besso L, Bresin E, Remuzzi G, Rodriguez de Cordoba S, Noris M: A novel atypical hemolytic uremic syndrome-associated hybrid CFHR1/CFHgene encoding a fusion protein that antagonizes factor H-dependent complement regulation. J Am Soc Nephrol 26: 209-219, 2015
57. FrancisNJ,McNicholas B, Awan A,Waldron M, Reddan D, Sadlier D, Kavanagh D, Strain L, Marchbank KJ, Harris CL,Goodship TH: A novel hybrid CFH/CFHR3 gene generated by a microhomology-mediated deletion in familial atypical hemolytic uremic syndrome. Blood 119: 591-601, 2012
58. Vernon KA, Goicoechea de Jorge E, Hall AE, Fremeaux-Bacchi V, Aitman TJ, Cook HT, Hangartner R, Koziell A, Pickering MC: Acute presentation and persistent glomerulonephritis following streptococcal infection in a patient with heterozygous complement factor H-related protein 5 deficiency. Am J Kidney Dis 60: 121-125, 2012
59. Funato M, Uemura O, Ushijima K, Ohnishi H, Orii K, Kato Z, Yamakawa S, Nagai T, Ohara O, Kaneko H, Kondo N: A complement factor B mutation in a large kindred with atypical hemolytic uremic syndrome. J Clin Immunol 34: 691-695, 2014
60. Goicoechea de Jorge E, Harris CL, Esparza-Gordillo J, Carreras L, Arranz EA, Garrido CA, López-Trascasa M, Sánchez-Corral P, Morgan BP, Rodríguez de Córdoba S: Gainof-function mutations in complement factor B are associated with atypical hemolytic uremic syndrome. Proc Natl Acad Sci U S A 104: 240-245, 2007
61. Marinozzi MC, Vergoz L, Rybkine T, Ngo S, Bettoni S, Pashov A, Cayla M, Tabarin F, Jablonski M, Hue C, Smith RJ, Noris M, Halbwachs-Mecarelli L, Donadelli R, Fremeaux-Bacchi V, Roumenina LT: Complement factor B mutations in atypical hemolytic uremic syndrome-disease-relevant or benign? J Am Soc Nephrol 25: 2053-2065, 2014
62. Roumenina LT, Jablonski M, Hue C, Blouin J, Dimitrov JD, Dragon-DureyMA, CaylaM, Fridman WH, Macher MA, Ribes D, Moulonguet L, Rostaing L, Satchell SC, Mathieson PW, Sautes-Fridman C, Loirat C, Regnier CH, Halbwachs-Mecarelli L, Fremeaux-Bacchi V: Hyperfunctional C3 convertase leads to complement deposition on endothelial cells and contributes to atypical hemolytic uremic syndrome. Blood 114: 2837-2845, 2009
63. Frémeaux-Bacchi V, Miller EC, Liszewski MK, Strain L, Blouin J, Brown AL, Moghal N, Kaplan BS, Weiss RA, Lhotta K, Kapur G, Mattoo T, Nivet H, Wong W, Gie S, Hurault de Ligny B, Fischbach M, Gupta R, Hauhart R, Meunier V, Loirat C, Dragon-Durey MA, Fridman WH, Janssen BJ, Goodship TH, Atkinson JP: Mutations in complement C3 predispose to development of atypical hemolytic uremic syndrome. Blood 112: 4948-4952, 2008
64. Lhotta K, Janecke AR, Scheiring J, Petzlberger B, Giner T, Fally V, Würzner R, Zimmerhackl LB, Mayer G, Fremeaux-Bacchi V: A large family with a gain-of-function mutation of complement C3 predisposing to atypical hemolytic uremic syndrome, microhematuria, hypertension and chronic renal failure. Clin J AmSoc Nephrol 4: 1356-1362, 2009
65. Linshaw MA, Stapleton FB, Cuppage FE, Forristal J, West CD, Schreiber RD, Wilson CB: Hypocomplementemic glomerulonephritis in an infant and mother. Evidence for an abnormal form of C3. Am J Nephrol 7: 470-477, 1987
66. Marder HK, Coleman TH, Forristal J, Beischel L, West CD: An inherited defect in the C3 convertase, C3b,Bb, associated with glomerulonephritis. Kidney Int 23: 749-758, 1983
67. Martínez-Barricarte R, Heurich M, Valdes-Cañedo F, Vazquez-Martul E, Torreira E, Montes T, Tortajada A, Pinto S, Lopez-TrascasaM, Morgan BP, LlorcaO, 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
68. 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
69. Sethi S, Fervenza FC, Zhang Y, Zand L, Vrana JA, Nasr SH, Theis JD, Dogan A, Smith RJ: C3 glomerulonephritis: Clinicopathological findings, complement abnormalities, glomerular proteomic profile, treatment, and follow-up. Kidney Int 82: 465-473, 2012
70. Fremeaux-Bacchi V, Weiss L, Demouchy C, May A, Palomera S, Kazatchkine MD: Hypocomplementaemia of poststreptococcal acute glomerulonephritis is associated with C3 nephritic factor (C3NeF) IgG autoantibody activity. Nephrol Dial Transplant 9: 1747-1750, 1994
71. WilliamsDG, Kourilsky O,Morel-Maroger L, Peters DK: C3 breakdown by serum from patients with acute post-streptococcal nephritis. Lancet 2: 360-361, 1972
72. Spitzer RE, Stitzel AE, Tsokos GC: Production of IgG and IgMautoantibody to the alternative pathway C3 convertase in normal individuals and patients with membranoproliferative glomerulonephritis. Clin Immunol Immunopathol 57: 10-18, 1990
73. Radhakrishnan S, Lunn A, Kirschfink M, Thorner P, Hebert D, Langlois V, Pluthero F, Licht C: Eculizumab and refractory membranoproliferative glomerulonephritis. N Engl J Med 366: 1165-1166, 2012
74. Rousset-Rouvire C, Cailliez M, Garaix F, Bruno D, Laurent D, Tsimaratos M: Rituximab fails where eculizumab restores renal function in C3nef-related DDD. Pediatr Nephrol 29: 1107-1111, 2014
75. Daina E, Noris M, Remuzzi G: Eculizumab in a patient with dense-deposit disease. N Engl J Med 366: 1161-1163, 2012
76. Giaime P, Daniel L, Burtey S: Remission of C3 glomerulopathy with rituximab as only immunosuppressive therapy. Clin Nephrol 83: 57-60, 2015
77. Strobel S, Zimmering M, Papp K, Prechl J, Józsi M: Anti-factor B autoantibody in dense deposit disease. Mol Immunol 47: 1476-1483, 2010
78. Chen Q, Müller D, Rudolph B, Hartmann A, Kuwertz-Bröking E, Wu K, Kirschfink M, Skerka C, Zipfel PF: Combined C3b and factor B autoantibodies and MPGN type II. N Engl J Med 365: 2340-2342, 2011
79. Fremeaux-Bacchi V, Dragon-Durey MA, Blouin J, Vigneau C, Kuypers D, Boudailliez B, Loirat C, Rondeau E, Fridman WH: Complement factor I: A susceptibility gene for atypical haemolytic uraemic syndrome. J Med Genet 41: e84, 2004
80. Kavanagh D, Kemp EJ, Mayland E, Winney RJ, Duffield JS, Warwick G, Richards A, Ward R, Goodship JA, Goodship TH: Mutations in complement factor I predispose to development of atypical hemolytic uremic syndrome.JAmSocNephrol 16: 2150-2155, 2005
81. Caprioli J, Noris M, Brioschi S, Pianetti G, Castelletti F, Bettinaglio P,Mele C, Bresin E, Cassis L, Gamba S, Porrati F, Bucchioni S, Monteferrante G, Fang CJ, Liszewski MK, Kavanagh D, Atkinson JP, Remuzzi G; International Registry of Recurrent and Familial HUS/TTP: Genetics of HUS: The impact of MCP, CFH, and IF mutations on clinical presentation, response to treatment, and outcome. Blood 108: 1267-1279, 2006
82. Rose KL, Paixao-Cavalcante D, Fish J, MandersonAP,Malik TH,BygraveAE, LinT, Sacks SH, Walport MJ, Cook HT, Botto M, Pickering MC: Factor I is required for the development of membranoproliferative glomerulonephritis in factor H-deficient mice. J Clin Invest 118: 608-618, 2008
83. Vyse TJ, Späth PJ, Davies KA, Morley BJ, Philippe P, Athanassiou P, Giles CM, Walport MJ: Hereditary complement factor I deficiency. QJM 87: 385-401, 1994
84. Fang CJ, Fremeaux-Bacchi V, LiszewskiMK, Pianetti G, Noris M, Goodship TH, Atkinson JP: Membrane cofactor protein mutations in atypical hemolytic uremic syndrome (aHUS), fatal Stx-HUS, C3 glomerulonephritis, and the HELLP syndrome. Blood 111: 624-632, 2008
85. Couzi L, Contin-Bordes C, Marliot F, Sarrat A, Grimal P, Moreau JF, Merville P, Fremeaux-Bacchi V: Inherited deficiency of membrane cofactor protein expression and varying manifestations of recurrent atypical hemolytic uremic syndrome in a sibling pair. AmJ Kidney Dis 52: e5-e9, 2008
86. Bridoux F, Desport E, Frémeaux-Bacchi V, Chong CF, Gombert JM, Lacombe C, Quellard N, Touchard G: Glomerulonephritis with isolated C3 deposits and monoclonal gammopathy: A fortuitous association? Clin J Am Soc Nephrol 6: 2165-2174, 2011
87. Hill PA, Firkin F, Dwyer KM, Lee P, Murphy BF: Membranoproliferative glomerulonephritis in association with chronic lymphocytic leukaemia: A report of three cases. Pathology 34: 138-143, 2002
88. Sethi S, Zand L, Leung N, Smith RJ, Jevremonic D, Herrmann SS, Fervenza FC: Membranoproliferative glomerulonephritis secondary to monoclonal gammopathy. Clin J Am Soc Nephrol 5: 770-782, 2010
89. Zand L, Kattah A, Fervenza FC, Smith RJ, Nasr SH, Zhang Y, Vrana JA, Leung N, Cornell LD, Sethi S: C3 glomerulonephritis associated with monoclonal gammopathy: A case series.AmJ Kidney Dis 62: 506-514, 2013
90. Nasr SH, ValeriAM, Appel GB, Sherwinter J, StokesMB, Said SM, Markowitz GS, D'Agati VD: Dense deposit disease: Clinicopathologic study of 32 pediatric and adult patients. Clin J Am Soc Nephrol 4: 22-32, 2009
91. Sepandj F, Trillo A: Dense deposit disease in association with monoclonal gammopathy of unknown significance. Nephrol Dial Transplant 11: 2309-2312, 1996
92. Sethi S, Sukov WR, Zhang Y, Fervenza FC, Lager DJ, Miller DV, Cornell LD, Krishnan SG, Smith RJ: Dense deposit disease associated with monoclonal gammopathy of undetermined significance. Am J Kidney Dis 56: 977-982, 2010
93. Loirat C,Garnier A, Sellier-Leclerc AL, Kwon T: Plasmatherapy in atypical hemolytic uremic syndrome. Semin Thromb Hemost 36: 673-681, 2010
94. Davin JC, Buter N, Groothoff J, van Wijk J, Bouts A, Strain L, Goodship T: Prophylactic plasma exchange in CD46-associated atypical haemolytic uremic syndrome. Pediatr Nephrol 24: 1757-1760, 2009
95. Sellier-Leclerc AL, Fremeaux-Bacchi V, Dragon-Durey MA, Macher MA, Niaudet P, GuestG,Boudailliez B, Bouissou F, Deschenes G, Gie S, Tsimaratos M, Fischbach M, Morin D, Nivet H, Alberti C, Loirat C; French Society of Pediatric Nephrology: Differential impact of complement mutations on clinical characteristics in atypical hemolytic uremic syndrome. J Am Soc Nephrol 18: 2392-2400, 2007
96. Saland J: Liver-kidney transplantation to cure atypical HUS: Still an option post-eculizumab? Pediatr Nephrol 29: 329-332, 2014
97. Tran H, Chaudhuri A, Concepcion W, Grimm PC: Use of eculizumab and plasma exchange in successful combined liver-kidney transplantation in a case of atypical HUS associated with complement factor H mutation. Pediatr Nephrol 29: 477-480, 2014
98. 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 Am Soc Nephrol 15: 787-795, 2004
99. Banks RA, May S, Wallington T: Acute renal failure in dense deposit disease: Recovery after plasmapheresis. BrMed J (Clin Res Ed) 284: 1874-1875, 1982
100. Krmar RT, Holtbäck U, Linné T, Berg UB, Celsi G, Söderberg MP, Wernerson A, Szakos A, Larsson S, Skattum L, Bárány P: Acute renal failure in dense deposit disease: Complete recovery after combination therapy with immunosuppressant and plasma exchange. Clin Nephrol 75[Suppl 1]: 4-10, 2011
101. Kurtz KA, Schlueter AJ: Management of membranoproliferative glomerulonephritis type II with plasmapheresis. J Clin Apher 17: 135-137, 2002
102. Boyer O, Balzamo E, Charbit M, Biebuyck-Gouge N, Salomon R, Dragon-Durey MA, Fremeaux-Bacchi V, Niaudet P: Pulse cyclophosphamide therapy and clinical remission in atypical hemolytic uremic syndrome with anti-complement factor H autoantibodies. Am J Kidney Dis 55: 923-927, 2010
103. Zand L, Lorenz EC, Cosio FG, Fervenza FC, Nasr SH, Gandhi MJ, Smith RJ, Sethi S: Clinical findings, pathology, and outcomes of C3GN after kidney transplantation. J Am Soc Nephrol 25: 1110-1117, 2014
104. Ricklin D, Lambris JD: Progress and trends in complement therapeutics. Adv Exp Med Biol 735: 1-22, 2013
105. Zuber J, Fakhouri F, Roumenina LT, Loirat C, Frémeaux-Bacchi V; French Study Group for aHUS/C3G: Use of eculizumab for atypical haemolytic uraemic syndrome and C3 glomerulopathies. Nat Rev Nephrol 8: 643-657, 2012
106. Fakhouri F, Delmas Y, Provot F, Barbet C, Karras A, Makdassi R, Courivaud C, Rifard K, Servais A, Allard C, Besson V, Cousin M, Chatelet V, Goujon JM,Coindre JP, Laurent G, Loirat C, Fremeaux-Bacchi V: Insights from the use in clinical practice of eculizumab in adult patients with atypical hemolytic uremic syndrome affecting the native kidneys: An analysis of 19 cases. Am J Kidney Dis 63: 40-48, 2014
107. Legendre CM, Licht C,Muus P, Greenbaum LA, Babu S, Bedrosian C, Bingham C, Cohen DJ, Delmas Y, Douglas K, Eitner F, Feldkamp T, Fouque D, Furman RR, Gaber O, Herthelius M, Hourmant M, Karpman D, Lebranchu Y, Mariat C, Menne J, Moulin B, Nürnberger J, Ogawa M, Remuzzi G, Richard T, Sberro-Soussan R, Severino B, Sheerin NS, Trivelli A, Zimmerhackl LB, Goodship T, Loirat C: Terminal complement inhibitor eculizumab in atypical hemolyticuremic syndrome. N Engl J Med 368: 2169-2181, 2013
108. Nishimura J, Yamamoto M, Hayashi S, Ohyashiki K, Ando K, Brodsky AL, Noji H, Kitamura K, Eto T, Takahashi T, Masuko M, Matsumoto T, Wano Y, Shichishima T, Shibayama H, Hase M, Li L, Johnson K, Lazarowski A, Tamburini P, Inazawa J, Kinoshita T, Kanakura Y: Genetic variants in C5 and poor response to eculizumab. N Engl J Med 370: 632-639, 2014
109. 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
110. Ozkaya O, Nalcacioglu H, Tekcan D, Genc G, Meydan BC, Ozdemir BH, Baysal MK, Keceligil HT: Eculizumab therapy in a patientwith dense-deposit disease associated with partial lipodystropy. Pediatr Nephrol 29: 1283-1287, 2014
111. Sánchez-Moreno A, De la Cerda F, Cabrera R, Fijo J, López-Trascasa M, Bedoya R, Rodríguez de Córdoba S, Ybot-González P: Eculizumab in dense-deposit disease after renal transplantation. Pediatr Nephrol 29: 2055-2059, 2014
112. Vivarelli M, Pasini A, Emma F: Eculizumab for the treatment of dense-deposit disease. N Engl J Med 366: 1163-1165, 2012
113. Gurkan S, Fyfe B, Weiss L, Xiao X, Zhang Y, Smith RJ: Eculizumab and recurrent C3 glomerulonephritis. Pediatr Nephrol 28: 1975-1981, 2013
114. Herlitz LC, Bomback AS, Markowitz GS, StokesMB, 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
115. Zhang Y, Nester CM, Martin B, SkjoedtMO, Meyer NC, Shao D, Borsa N, Palarasah Y, Smith RJH: Defining the complement biomarker profile of C3 glomerulopathy. Clin J Am Soc Nephrol 9: 1876-1882, 2014
116. Paixão-Cavalcante D, Torreira E, Lindorfer MA, Rodriguez de Cordoba S, Morgan BP, Taylor RP, Llorca O, Harris CL: A humanized antibody that regulates the alternative pathway convertase: Potential for therapy of renal disease associated with nephritic factors. J Immunol 192: 4844-4851, 2014
117. Zhang Y, Nester CM, Holanda DG, Marsh HC, Hammond RA, Thomas LJ, Meyer NC, Hunsicker LG, Sethi S, Smith RJ: Soluble CR1 therapy improves complement regulation in C3 glomerulopathy. J Am Soc Nephrol 24: 1820-1829, 2013