Complement factor b mutations in atypical hemolytic uremic syndrome-disease-relevant or benign?

Journal of the American Society of Nephrology

Volumn 25, Issue 9, 2014, Pages 2053-2065

  Marinozzi, Maria Chiara ^a,b,c   Vergoz, Laura ^a,b,d   Rybkine, Tania ^a,b,d   Ngo, Stephanie ^c   Bettoni, Serena ^e   Pashov, Anastas ^f   Cayla, Mathieu ^a,b,d   Tabarin, Fanny ^a,b,d   Jablonski, Mathieu ^a,b,d   Hue, Christophe ^a,b,d   Smith, Richard J ^g   Noris, Marina ^e   Halbwachs Mecarelli, Lise ^a,b,d   Donadelli, Roberta ^e   Fremeaux Bacchi, Veronique ^a,b   Roumenina, Lubka T ^a,b,d  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c HÔPITAL EUROPÉEN GEORGES POMPIDOU   (France)

^d SORBONNE UNIVERSITÉ   (France)

^e MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^f INSTITUTE OF MICROBIOLOGY   (Bulgaria)

^g UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; CLASSICAL COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C3B; SERINE PROTEINASE; VON WILLEBRAND FACTOR; LIGAND; MULTIPROTEIN COMPLEX; RECOMBINANT PROTEIN;

ADULT; ALGORITHM; ANIMAL CELL; ARTICLE; CELL SURFACE; COHORT ANALYSIS; COMPLEMENT ACTIVATION; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; FUNCTIONAL ASSESSMENT; GAIN OF FUNCTION MUTATION; GENE FREQUENCY; GENE MUTATION; HEMOLYTIC UREMIC SYNDROME; HUMAN; HUMAN CELL; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SURFACE PLASMON RESONANCE; AMINO ACID SUBSTITUTION; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; COMPLEMENT ALTERNATIVE PATHWAY; COMPUTER SIMULATION; GENETIC POLYMORPHISM; GENETICS; IMMUNOLOGY; METABOLISM; MUTATION; UMBILICAL VEIN ENDOTHELIAL CELL;

AMINO ACID SUBSTITUTION; ATYPICAL HEMOLYTIC UREMIC SYNDROME; BINDING SITES; COMPLEMENT C3 CONVERTASE, ALTERNATIVE PATHWAY; COMPLEMENT C3B; COMPLEMENT C5 CONVERTASE, ALTERNATIVE PATHWAY; COMPLEMENT FACTOR B; COMPLEMENT PATHWAY, ALTERNATIVE; COMPUTER SIMULATION; GENE FREQUENCY; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LIGANDS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTATION; POLYMORPHISM, GENETIC; RECOMBINANT PROTEINS;

EID: 84902283995     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013070796     Document Type: Article

References (46)

1. Noris M, Remuzzi G: Atypical hemolytic-uremic syndrome. N Engl J Med 361: 1676-1687, 2009
2. Roumenina LT, Loirat C, Dragon-Durey MA, Halbwachs-Mecarelli L, Sautes-Fridman C, Fremeaux-Bacchi V: Alternative complement pathway assessment in patients with atypical HUS. J Immunol Methods 365: 8-26, 2011
3. Dragon-Durey MA, Sethi SK, Bagga A, Blanc C, Blouin J, Ranchin B, André JL, Takagi N, Cheong HI, Hari P, Le Quintrec M, Niaudet P, Loirat C, Fridman WH, Frémeaux-Bacchi V: Clinical features of anti-factor H autoantibody-associated hemolytic uremic syndrome. J Am Soc Nephrol 21: 2180-2187, 2010
4. 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 hemolytic-uremic syndrome. NEnglJ Med 368: 2169-2181, 2013
5. 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
6. Le Quintrec M, Zuber J, Moulin B, Kamar N, Jablonski M, Lionet A, Chatelet V, Mousson C, Mourad G, Bridoux F, Cassuto E, Loirat C, Rondeau E, Delahousse M, Frémeaux-Bacchi V: Complement genes strongly predict recurrence and graft outcome in adult renal transplant recipients with atypical hemolytic and uremic syndrome. Am J Transplant 13: 663-675, 2013
7. Zuber J, Le Quintrec M, Sberro-Soussan R, Loirat C, Fremeaux-Bacchi V, Legendre C: New insights into postrenal transplant hemolytic uremic syndrome. Nat Rev Nephrol 7: 23-35, 2011
8. Békássy ZD, Kristoffersson AC, Cronqvist M, Roumenina LT, Rybkine T, Vergoz L, Hue C, Fremeaux-Bacchi V, Karpman D: Eculizumab in an anephric patient with atypical haemolytic uraemic syndrome and advanced vascular lesions. Nephrol Dial Transplant 28:2899-2907,2013
9. Nilsson SC, Karpman D, Vaziri-Sani F, Kristoffersson AC, Salomon R, Provot F, Fremeaux-Bacchi V, Trouw LA, Blom AM: A mutation in factor I that is associated with atypical hemolytic uremic syndrome does not affect the function of factor I in complement regulation. Mol Immunol 44: 1835-1844, 2007
10. Tortajada A, Pinto S, Martínez-Ara J, López-Trascasa M, Sánchez-Corral P, de Córdoba SR: Complement factor H variants I890 and L1007 while commonly associated with atypical hemolytic uremic syndrome are polymorphisms with no functional significance. Kidney Int 81: 56-63, 2012
11. Kavanagh D, Burgess R, Spitzer D, Richards A, Diaz-Torres ML, Goodship JA, Hourcade DE, Atkinson JP, Goodship TH: The decay accelerating factor mutation I197V found in hemolytic uraemic syndrome does not impair complement regulation. Mol Immunol 44: 3162-3167, 2007
12. Kavanagh D, Anderson HE: Interpretation of genetic variants of uncertain significance in atypical hemolytic uremic syndrome. Kidney Int 81: 11-13, 2012
13. Fremeaux-Bacchi V, Fakhouri F, Garnier A, Bienaimé F, Dragon-Durey MA, Ngo S, Moulin B, Servais A, Provot F, Rostaing L, Burtey S, Niaudet P, Deschênes G, Lebranchu Y, Zuber J, Loirat C: Genetics and outcome of atypical hemolytic uremic syndrome: A nationwide French series comparing children and adults. Clin J Am Soc Nephrol 8: 554-562, 2013
14. Kavanagh D, Kemp EJ, Richards A, Burgess RM, Mayland E, Goodship JA, Goodship TH: Does complement factor B have a role in the pathogenesis of atypical HUS? Mol Immunol 43: 856-859, 2006
15. Maga TK, Nishimura CJ, Weaver AE, Frees KL, Smith RJ: Mutations in alternative pathway complement proteins in American patients with atypical hemolytic uremic syndrome. Hum Mutat 31: E1445-E1460, 2010
16. Westra D, Volokhina E, van der Heijden E, Vos A, Huigen M, Jansen J, van Kaauwen E, van der Velden T, van de Kar N, van den Heuvel L: Genetic disorders in complement (regulating) genes in patients with atypical haemolytic uraemic syndrome (aHUS). Nephrol Dial Transplant 25: 2195-2202, 2010
17. 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: Gain-of-function mutations in complement factor B are associated with atypical hemolytic uremic syndrome. Proc Natl Acad Sci U S A 104: 240-245, 2007
18. 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 Am Soc Nephrol 5: 1844-1859, 2010
19. Roumenina LT, Jablonski M, Hue C, Blouin J, Dimitrov JD, Dragon-Durey MA, Cayla M, 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
20. Tawadrous H, Maga T, Sharma J, Kupferman J, Smith RJ, Schoeneman M: A novel mutation in the complement factor B gene (CFB) and atypical hemolytic uremic syndrome. Pediatr Nephrol 25: 947-951, 2010
21. Feng S, Eyler SJ, Zhang Y, Maga T, Nester CM, Kroll MH, Smith RJ, Afshar-KharghanV: PartialADAMTS13deficiency in atypical hemolytic uremic syndrome. Blood 122: 1487-1493, 2013
22. Forneris F, Ricklin D, Wu J, Tzekou A, Wallace RS, Lambris JD, Gros P: Structures of C3b in complex with factors B and D give insight into complement convertase formation. Science 330: 1816-1820, 2010
23. Milder FJ, Gomes L, Schouten A, Janssen BJ, Huizinga EG, Romijn RA, Hemrika W, Roos A, Daha MR, Gros P: Factor B structure provides insights into activation of the central protease of the complement system. Nat Struct Mol Biol 14: 224-228, 2007
24. Rooijakkers SH, Wu J, Ruyken M, van Domselaar R, Planken KL, Tzekou A, Ricklin D, Lambris JD, Janssen BJ, van Strijp JA, Gros P: Structural and functional implications of the alternative complement pathway C3 convertase stabilized by a staphylococcal inhibitor. Nat Immunol 10: 721-727, 2009
25. Montes T, Tortajada A, Morgan BP, Rodríguez de Córdoba S, Harris CL: Functional basis of protection against age-related macular degeneration conferred by a common polymorphism in complement factor B. Proc Natl Acad Sci U S A 106: 4366-4371, 2009
26. Clarke L, Zheng-Bradley X, Smith R, Kulesha E, Xiao C, Toneva I, Vaughan B, Preuss D, Leinonen R, Shumway M, Sherry S, Flicek P; 1000 Genomes Project Consortium: The 1000 Genomes Project: Data management and community access. Nat Methods 9: 459-462, 2012
27. Bettoni S, Donadelli R, Roumenina L, Fremeaux-Bacchi V, Noris M: A user-friendly method to study the effect of FH and impact of FB variants on C3bBb convertase and C3bB proconvertase formation. Immunobiology 217: 1034-1046, 2012
28. Hourcade DE, Mitchell LM, Oglesby TJ: Mutations of the type A domain of complement factor B that promote high-affinity C3b-binding. J Immunol 162: 2906-2911, 1999
29. Roumenina LT, Frimat M, Miller EC, Provot F, Dragon-Durey MA, 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 causesadirectC3convertasegainoffunction.Blood 119: 4182-4191, 2012
30. Cronbach LJ, Warrington WG: Time-limit tests: Estimating their reliability and degree of speeding. Psychometrika 16: 167-188, 1951
31. Ferreira VP, Herbert AP, Cortés C, McKee KA, Blaum BS, Esswein ST, Uhrín D, Barlow PN, Pangburn MK, Kavanagh D: The binding of factor H to a complex of physiological polyanions and C3b on cells is impaired in atypical hemolytic uremic syndrome. J Immunol 182:7009-7018,2009
32. Lehtinen MJ, Rops AL, Isenman DE, van der Vlag J, Jokiranta TS: Mutations of factor H impair regulation of surface-bound C3b by three mechanisms in atypical hemolytic uremic syndrome. J Biol Chem 284: 15650-15658, 2009
33. Manuelian T, Hellwage J, Meri S, Caprioli J, Noris M, Heinen S, Jozsi M, Neumann HP, Remuzzi G, Zipfel PF: Mutations in factor H reduce binding affinity to C3b and heparin and surface attachment to endothelial cells in hemolytic uremic syndrome. J Clin Invest 111: 1181-1190, 2003
34. Roumenina LT, Roquigny R, Blanc C, Poulain N, Ngo S, Dragon-Durey MA, Frémeaux-Bacchi V: Functional evaluation of factor H genetic and acquired abnormalities: Application for atypical hemolytic uremic syndrome (aHUS). Methods Mol Biol 1100: 237-247, 2014
35. Sánchez-Corral P, González-Rubio C, Rodríguez de Córdoba S, López-Trascasa M: Functional analysis in serum from atypical Hemolytic Uremic Syndrome patients reveals impaired protection of host cells associated with mutations in factor H. Mol Immunol 41: 81-84, 2004
36. Wu J, Wu YQ, Ricklin D, Janssen BJ, Lambris JD, Gros P: Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Nat Immunol 10: 728-733, 2009
37. Ermini L, Goodship TH, Strain L, Weale ME, Sacks SH, Cordell HJ, Fremeaux-Bacchi V, Sheerin NS: Common genetic variants in complement genes other than CFH, CD46 and the CFHRs are not associated with aHUS. Mol Immunol 49: 640-648, 2012
38. 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. JAm Soc Nephrol 24: 475-486, 2013
39. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE: UCSF Chimera-a visualization system for exploratory research and analysis.JComputChem25: 1605-1612,2004
40. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR: A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249, 2010
41. TavtigianSV,DeffenbaughAM,YinL,JudkinsT,SchollT,SamollowPB, de Silva D, Zharkikh A, Thomas A: Comprehensive statistical study of 452 BRCA1 missense substitutions with classification of eight recurrent substitutions as neutral. J Med Genet 43: 295-305, 2006
42. Schwarz JM, Rödelsperger C, Schuelke M, Seelow D: MutationTaster evaluates disease-causing potential of sequence alterations. Nat Methods 7: 575-576, 2010
43. Kumar P, Henikoff S, Ng PC: Predicting the effects of coding nonsynonymous variants on protein function using the SIFT algorithm. Nat Protoc 4: 1073-1081, 2009
44. Frimat M, Tabarin F, Dimitrov JD, Poitou C, Halbwachs-Mecarelli L, Fremeaux-Bacchi V, Roumenina LT: Complement activation by heme as a secondary hit for atypical hemolytic uremic syndrome. Blood 122: 282-292, 2013
45. Gilbert RD, Fowler DJ, Angus E, Hardy SA, Stanley L, Goodship TH: Eculizumab therapy for atypical haemolytic uraemic syndrome due to a gain-of-function mutation of complement factor B. Pediatr Nephrol 28: 1315-1318, 2013
46. Bienaime F, Dragon-Durey MA, Regnier CH, Nilsson SC, Kwan WH, Blouin J, Jablonski M, Renault N, Rameix-Welti MA, Loirat C, Sautés-Fridman C, Villoutreix BO, Blom AM, Fremeaux-Bacchi V: Mutations in components of complement influence the outcome of Factor I-associated atypical hemolyticuremicsyndrome.Kidney Int 77: 339-349, 2010