Lessons from functional and structural analyses of disease-associated genetic variants in the complement alternative pathway

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1812, Issue 1, 2011, Pages 12-22

  de Córdoba, Santiago Rodríguez ^a,b   Harris, Claire L ^c   Morgan, B Paul ^c   Llorca, Oscar ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE ENFERMEDADES RARAS CIBERER   (Spain)

^c CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Age related macular degeneration (AMD); Atypical hemolytic uremic syndrome (aHUS); Complement; Dense deposit disease (DDD); Membranoproliferative glomerulonephritis type II (MPGN2)

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT FACTOR B; FIBRINOGEN; MEMBRANE COFACTOR PROTEIN; UNCLASSIFIED DRUG;

CELL DAMAGE; CHRONIC INFLAMMATION; COMPLEMENT FACTOR; DENSE DEPOSIT DISEASE; ENZYME ACTIVATION; GENE MUTATION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GLOMERULONEPHRITIS; HEMOLYTIC UREMIC SYNDROME; HOMEOSTASIS; HOST CELL; HUMAN; INFECTION SENSITIVITY; NONHUMAN; PRIORITY JOURNAL; RETINA MACULA AGE RELATED DEGENERATION; REVIEW; RISK FACTOR; STRUCTURE ANALYSIS; TISSUE INJURY;

COMPLEMENT C3; COMPLEMENT C3 CONVERTASE, ALTERNATIVE PATHWAY; COMPLEMENT FACTOR B; COMPLEMENT PATHWAY, ALTERNATIVE; HEMOLYTIC-UREMIC SYNDROME; HUMANS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 78649450284     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2010.09.002     Document Type: Review

References (89)

1. Walport M.J. Complement - second of two parts. N Engl J. Med. 2001, 344:1140-1144.
2. Walport M.J. Complement - first of two parts. N Engl J. Med. 2001, 344:1058-1066.
3. Lachmann P.J., Frederick W.A. The amplification loop of the complement pathways. Adv. Immunol. 2009, 104:115-149.
4. Amara U., Rittirsch D., Flierl M., Bruckner U., Klos A., Gebhard F., Lambris J.D., Huber-Lang M. Interaction between the coagulation and complement system. Adv. Exp. Med. Biol. 2008, 632:71-79.
5. Pangburn M.K., Schreiber R.D., M.-E.H.J. Formation of the initial C3 convertase of the alternative complement pathway. Acquisition of C3b-like activities by spontaneous hydrolysis of the putative thioester in native C3. J. Exp. Med. 1981, 154:856-867.
6. Kemper C., Atkinson J.P., Hourcade D.E. Properdin: emerging roles of a pattern-recognition molecule. Annu. Rev. Immunol. 2010, 28:131-155.
7. Morgan B.P. Regulation of the complement membrane attack pathway. Crit. Rev. Immunol. 1999, 19:173-198.
8. Holers V.M. The spectrum of complement alternative pathway-mediated diseases. Immunol. Rev. 2008, 223:300-316.
9. Dragon-Durey M.-A., Fremeaux-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. 2004, 15:787-795.
10. Levy M., Halbwachs-Mecarelli L., Gubler M., Kohout G., Bensenouci A., Niaudet P., Hauptmann G., Lesavre P. H deficiency in two brothers with atypical dense intramembranous deposit disease. Kidney Int. 1986, 30:949-956.
11. Licht C., Heinen S., Jozsi M., Loschmann I., Saunders R.E., Perkins S.J., Waldherr R., Skerka C., Kirschfink M., Hoppe B., Zipfel P.F. Deletion of Lys224 in regulatory domain 4 of Factor H reveals a novel pathomechanism for dense deposit disease. Kidney Int. 2006, 70:42-50.
12. López-Larrea C., Dieguez M., Enguix A., Dominguez O., Marin B., Gomez E. A familial deficiency of complement factor H. Biochem. Soc. Trans. 1987, 15:648-649.
13. Caprioli J., Bettinaglio P., Zipfel P.F., Amadei B., Daina E., Gamba S., Skerka C., Marziliano N., Remuzzi G., Noris M. The molecular basis of familial hemolytic uremic syndrome: mutation analysis of factor H gene reveals a hot spot in short consensus repeat 20. J. Am. Soc. Nephrol. 2001, 12:297-307.
14. Fremeaux-Bacchi V., Dragon-Durey M.A., Blouin J., Vigneau C., Kuypers D., Boudailliez B., Loirat C., Rondeau E., Fridman W.H. Complement factor I: a susceptibility gene for atypical haemolytic uraemic syndrome. J. Med. Genet. 2004, 41:e84.
15. Fremeaux-Bacchi V., Miller E.C., Liszewski M.K., Strain L., Blouin J., Brown A.L., Moghal N., Kaplan B.S., Weiss R.A., Lhotta K., Kapur G., Mattoo T., Nivet H., Wong W., Gie S., de Ligny B.H., Fischbach M., Gupta R., Hauhart R., Meunier V., Loirat C., Dragon-Durey M.-A., Fridman W.H., Janssen B.J.C., Goodship T.H.J., Atkinson J.P. Mutations in complement C3 predispose to development of atypical hemolytic uremic syndrome. Blood 2008, 112:4948-4952.
16. Goicoechea de Jorge E., Harris C.L., Esparza-Gordillo J., Carreras L., Arranz E.A., Garrido C.A., Lopez-Trascasa M., Sanchez-Corral P., Morgan B.P., Rodriguez de Cordoba S. Gain-of-function mutations in complement factor B are associated with atypical hemolytic uremic syndrome. Proc. Natl Acad. Sci. USA 2007, 104:240-245.
17. Kavanagh D., Kemp E.J., Mayland E., Winney R.J., Duffield J.S., Warwick G., Richards A., Ward R., Goodship J.A., Goodship T.H.J. Mutations in complement factor I predispose to development of atypical hemolytic uremic syndrome. J. Am. Soc. Nephrol. 2005, 16:2150-2155.
18. Noris M., Brioschi S., Caprioli J., Todeschini M., Bresin E., Porrati F., Gamba S., Remuzzi G. Familial haemolytic uraemic syndrome and an MCP mutation. Lancet 2003, 362:1542-1547.
19. Pérez-Caballero D., González-Rubio C., Gallardo M.E., 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. 2001, 68:478-484.
20. Richards A., Buddles M.R., Donne R.L., Kaplan B.S., Kirk E., Venning M.C., Tielemans C.L., Goodship J.A., Goodship T.H.J. Factor H mutations in hemolytic uremic syndrome cluster in exons 18-20, a domain important for host cell recognition. Am. J. Hum. Genet. 2001, 68:485-490.
21. Richards A., Kemp E.J., Liszewski M.K., Goodship J.A., Lampe A.K., Decorte R., Muslumanoglu M.H., Kavukcu S., Filler G., Pirson Y., Wen L.S., Atkinson J.P., Goodship T.H.J. Mutations in human complement regulator, membrane cofactor protein (CD46), predispose to development of familial hemolytic uremic syndrome. Proc. Natl Acad. Sci. USA 2003, 100:12966-12971.
22. Warwicker P., Goodship T.H.J., Donne R.L., Pirson Y., Nicholls A., Ward R.M., Turnpenny P., Goodship J.A. Genetic studies into inherited and sporadic hemolytic uremic syndrome. Kidney Int. 1998, 53:836-844.
23. Edwards A.O., Ritter R., Abel K.J., Manning A., Panhuysen C., Farrer L.A. Complement factor H polymorphism and age-related macular degeneration. Science 2005, 308:421-424.
24. Ennis S., Jomary C., Mullins R., Cree A., Chen X., MacLeod A., Jones S., Collins A., Stone E., Lotery A. Association between the SERPING1 gene and age-related macular degeneration: a two-stage case-control study. Lancet 2008, 372:1828-1834.
25. Gold B., Merriam J.E., Zernant J., Hancox L.S., Taiber A.J., Gehrs K., Cramer K., Neel J., Bergeron J., Barile G.R., Smith R.T., Hageman G.S., Dean M., Allikmets R. Variation in factor B (BF) and complement component 2 (C2) genes is associated with age-related macular degeneration. Nat. Genet. 2006, 38:458-462.
26. Hageman G.S., Anderson D.H., Johnson L.V., Hancox L.S., Taiber A.J., Hardisty L.I., Hageman J.L., Stockman H.A., Borchardt J.D., Gehrs K.M., Smith R.J.H., Silvestri G., Russell S.R., Klaver C.C.W., Barbazetto I., Chang S., Yannuzzi L.A., Barile G.R., Merriam J.C., Smith R.T., Olsh A.K., Bergeron J., Zernant J., Merriam J.E., Gold B., Dean M., Allikmets R. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc. Natl Acad. Sci. USA 2005, 102:7227-7232.
27. Haines J.L., Hauser M.A., Schmidt S., Scott W.K., Olson L.M., Gallins P., Spencer K.L., Kwan S.Y., Noureddine M., Gilbert J.R., Schnetz-Boutaud N., Agarwal A., Postel E.A., Pericak-Vance M.A. Complement factor H variant increases the risk of age-related macular degeneration. Science 2005, 308:419-421.
28. Hughes A.E., Orr N., Esfandiary H., Diaz-Torres M., Goodship T., Chakravarthy U. A common CFH haplotype, with deletion of CFHR1 and CFHR3, is associated with lower risk of age-related macular degeneration. Nat. Genet. 2006, 38:1173-1177.
29. Klein R.J., Zeiss C., Chew E.Y., Tsai J.-Y., Sackler R.S., Haynes C., Henning A.K., SanGiovanni J.P., Mane S.M., Mayne S.T., Bracken M.B., Ferris F.L., Ott J., Barnstable C., Hoh J. Complement factor H polymorphism in age-related macular degeneration. Science 2005, 308:385-389.
30. Li M., Atmaca-Sonmez P., Othman M., Branham K.E.H., Khanna R., Wade M.S., Li Y., Liang L., Zareparsi S., Swaroop A., Abecasis G.R. CFH haplotypes without the Y402H coding variant show strong association with susceptibility to age-related macular degeneration. Nat. Genet. 2006, 38:1049-1054.
31. Maller J., George S., Purcell S., Fagerness J., Altshuler D., Daly M.J., Seddon J.M. Common variation in three genes, including a noncoding variant in CFH, strongly influences risk of age-related macular degeneration. Nat. Genet. 2006, 38:1055-1059.
32. Yates J.R.W., Sepp T., Matharu B.K., Khan J.C., Thurlby D.A., Shahid H., Clayton D.G., Hayward C., Morgan J., Wright A.F., Armbrecht A.M., Dhillon B., Deary I.J., Redmond E., Bird A.C., Moore A.T. Complement C3 variant and the risk of age-related macular degeneration. N Engl J. Med. 2007, 357:553-561. A.M.D.S.G. the Genetic Factors in.
33. Noris M., Remuzzi G. Hemolytic uremic syndrome. J. Am. Soc. Nephrol. 2005, 16:1035-1050.
34. Noris M., Remuzzi G. Atypical hemolytic-uremic syndrome. N Engl J. Med. 2009, 361:1676-1687.
35. Caprioli J., Castelletti F., Bucchioni S., Bettinaglio P., Bresin E., Pianetti G., Gamba S., Brioschi S., Daina E., Remuzzi G., Noris M. Complement factor H mutations and gene polymorphisms in haemolytic uraemic syndrome: the C-257T, the A2089G and the G2881T polymorphisms are strongly associated with the disease. Hum. Mol. Genet. 2003, 12:3385-3395.
36. Esparza-Gordillo J., Goicoechea de Jorge E., Buil A., Berges L.C., Lopez-Trascasa M., Sanchez-Corral P., Rodriguez de Cordoba S. Predisposition to atypical hemolytic uremic syndrome involves the concurrence of different susceptibility alleles in the regulators of complement activation gene cluster in 1q32. Hum. Mol. Genet. 2005, 14:703-712.
37. Smith R.J.H., Alexander J., Barlow P.N., Botto M., Cassavant T.L., Cook H.T., de Cordoba S.R., Hageman G.S., Jokiranta T.S., Kimberling W.J., Lambris J.D., Lanning L.D., Levidiotis V., Licht C., Lutz H.U., Meri S., Pickering M.C., Quigg R.J., Rops A.L., Salant D.J., Sethi S., Thurman J.M., Tully H.F., Tully S.P., van der Vlag J., Walker P.D., Wurzner R., Zipfel P.F., Dense Deposit G. Disease focus, new approaches to the treatment of dense deposit disease. J. Am. Soc. Nephrol. 2007, 18:2447-2456.
38. Martínez-Barricarte R., Heurich M., Valdes-Cañero F., Vázquez-Martul E., Torreira E., Montes T., Tortajada A., Pinto S., López-Trascasa M., Morgan B.P., Llorca O., Harris C.L., Rodríguez de Córdoba S. First human C3 mutation associated with dense deposit disease unravels distinct structural requirements for factor H, MCP and DAF regulation. J. Clin. Invest. 2010, 120:3702-3712.
39. Høgåsen K., Jansen J.H., Mollnes T.E., Hovdenes J., Harboe M. Hereditary porcine membranoproliferative glomerulonephritis type II is caused by factor H deficiency. J. Clin. Invest. 1995, 95:1054-1061.
40. Pickering M.C., Cook H.T., Warren J., Bygrave A.E., Moss J., Walport M.J., Botto M. Uncontrolled C3 activation causes membranoproliferative glomerulonephritis in mice deficient in complement factor H. Nat. Genet. 2002, 31:424-428.
41. Rose K.L., Paixao-Cavalcante D., Fish J., Manderson A.P., Malik T.H., Bygrave A.E., Lin T., Sacks S.H., Walport M.J., Cook H.T., Botto M., Pickering M.C. Factor I is required for the development of membranoproliferative glomerulonephritis in factor H-deficient mice. J. Clin. Invest. 2008, 118:608-618.
42. Anderson D.H., Mullins R.F., Hageman G.S., Johnson L.V. A role for local inflammation in the formation of drusen in the aging eye. Am. J. Ophthalmol. 2002, 134:411-431.
43. Rivera A., Fisher S.A., Fritsche L.G., Keilhauer C.N., Lichtner P., Meitinger T., Weber B.H.F. Hypothetical LOC387715 is a second major susceptibility gene for age-related macular degeneration, contributing independently of complement factor H to disease risk. Hum. Mol. Genet. 2005, 14:3227-3236.
44. Janssen B.J.C., Huizinga E.G., Raaijmakers H.C.A., Roos A., Daha M.R., Nilsson-Ekdahl K., Nilsson B., Gros P. Structures of complement component C3 provide insights into the function and evolution of immunity. Nature 2005, 437:505-511.
45. Janssen B.J.C., Christodoulidou A., McCarthy A., Lambris J.D., Gros P. Structure of C3b reveals conformational changes that underlie complement activity. Nature 2006, 444:213-216.
46. Nishida N., Walz T., Springer T.A. Structural transitions of complement component C3 and its activation products. Proc. Natl Acad. Sci. USA 2006, 103:19737-19742.
47. Wiesmann C., Katschke K.J., Yin J., Helmy K.Y., Steffek M., Fairbrother W.J., McCallum S.A., Embuscado L., DeForge L., Hass P.E., van Lookeren Campagne M. Structure of C3b in complex with CRIg gives insights into regulation of complement activation. Nature 2006, 444:217-220.
48. Kölln J., Bredehorst R., Spillner E. Engineering of human complement component C3 for catalytic inhibition of complement. Immunol. Lett. 2005, 98:49-56.
49. Kolln J., Spillner E., Andra J., Klensang K., Bredehorst R. Complement inactivation by recombinant human C3 derivatives. J. Immunol. 2004, 173:5540-5545.
50. Taniguchi-Sidle A., Isenman D.E. Interactions of human complement component C3 with factor B and with complement receptors type 1 (CR1, CD35) and type 3 (CR3, CD11b/CD18) involve an acidic sequence at the N-terminus of C3 alpha'-chain. J. Immunol. 1994, 153:5285-5302.
51. Gros P., Milder F.J., Janssen B.J.C. Complement driven by conformational changes. Nat. Rev. Immunol. 2008, 8:48-58.
52. Hinshelwood J., Spencer D.I.R., Edwards Y.J.K., Perkins S.J. Identification of the c3b binding site in a recombinant vWF-A domain of complement factor B by surface-enhanced laser desorption-ionisation affinity mass spectrometry and homology modelling: implications for the activity of factor B. J. Mol. Biol. 1999, 294:587-599.
53. Hourcade D.E., Mitchell L.M., Oglesby T.J. Mutations of the type A domain of complement factor B that promote high-affinity C3b-binding. J. Immunol. 1999, 162:2906-2911.
54. Tuckwell D.S., Xu Y., Newham P., Humphries M.J., Volanakis J.E. Surface loops adjacent to the cation-binding site of the complement factor B von Willebrand factor type A module determine C3b binding specificity. Biochemistry 1997, 36:6605-6613.
55. Hourcade D.E., Wagner L.M., Oglesby T.J. Analysis of the short consensus repeats of human complement factor B by site-directed mutagenesis. J. Biol. Chem. 1995, 270:19716-19722.
56. Pryzdial E.L., Isenman D.E. Alternative complement pathway activation fragment Ba binds to C3b. Evidence that formation of the factor B-C3b complex involves two discrete points of contact. J. Biol. Chem. 1987, 262:1519-1525.
57. Thurman J.M., Kraus D.M., Girardi G., Hourcade D., Kang H.J., Royer P.A., Mitchell L.M., Giclas P.C., Salmon J., Gilkeson G., Holers V.M. A novel inhibitor of the alternative complement pathway prevents antiphospholipid antibody-induced pregnancy loss in mice. Mol. Immunol. 2005, 42:87-97.
58. Xu Y., Volanakis J.E. Contribution of the complement control protein modules of C2 in C4b binding assessed by analysis of C2/factor B chimeras. J. Immunol. 1997, 158:5958-5965.
59. Milder F.J., Gomes L., Schouten A., Janssen B.J.C., Huizinga E.G., Romijn R.A., Hemrika W., Roos A., Daha M.R., Gros P. Factor B structure provides insights into activation of the central protease of the complement system. Nat. Struct. Mol. Biol. 2007, 14:224-228.
60. Ponnuraj K., Xu Y., Macon K., Moore D., Volanakis J.E., Narayana S.V.L. Structural analysis of engineered Bb fragment of complement factor B: insights into the activation mechanism of the alternative pathway C3-convertase. Mol. Cell 2004, 14:17-28.
61. Rooijakkers S.H.M., Wu J., Ruyken M., van Domselaar R., Planken K.L., Tzekou A., Ricklin D., Lambris J.D., Janssen B.J.C., van Strijp J.A.G., Gros P. Structural and functional implications of the alternative complement pathway C3 convertase stabilized by a staphylococcal inhibitor. Nat. Immunol. 2009, 10:721-727.
62. Torreira E., Tortajada A., Montes T., Rodriguez de Cordoba S., Llorca O. 3D structure of the C3bB complex provides insights into the activation and regulation of the complement alternative pathway convertase. Proc. Natl Acad. Sci. USA 2009, 106:882-887.
63. Torreira E., Tortajada A., Montes T., Rodriguez de Cordoba S., Llorca O. Coexistence of closed and open conformations of complement factor B in the alternative pathway C3bB(Mg2+) proconvertase. J. Immunol. 2009, 183:7347-7351.
64. Janssen B.J.C., Gomes L., Koning R.I., Svergun D.I., Koster A.J., Fritzinger D.C., Vogel C.-W., Gros P. Insights into complement convertase formation based on the structure of the factor B-cobra venom factor complex. EMBO J. 2009, 28:2469-2478.
65. Roumenina L.T., Jablonski M., Hue C., Blouin J., Dimitrov J.D., Dragon-Durey M.-A., Cayla M., Fridman W.H., Macher M.-A., Ribes D., Moulonguet L., Rostaing L., Satchell S.C., Mathieson P.W., Sautes-Fridman C., Loirat C., Regnier C.H., Halbwachs-Mecarelli L., Fremeaux-Bacchi V. Hyperfunctional C3 convertase leads to complement deposition on endothelial cells and contributes to atypical hemolytic uremic syndrome. Blood 2009, 114:2837-2845.
66. Maga T.K., Nishimura C.J., Weaver A., E., Frees K.L., Smith R., J. Mutations in alternative pathway complement proteins in American patients with atypical hemolytic uremic syndrome. Hum. Mutat. 2010, 31:1445-1460.
67. Hourcade D.E., Mitchell L., Kuttner-Kondo L.A., Atkinson J.P., Medof M.E. Decay-accelerating factor (DAF), complement receptor 1 (CR1), and factor H dissociate the complement AP C3 convertase (C3bBb) via sites on the type A domain of Bb. J. Biol. Chem. 2002, 277:1107-1112.
68. Montes T., Tortajada A., Morgan B.P., Rodriguez de Cordoba S., Harris C.L. Functional basis of protection against age-related macular degeneration conferred by a common polymorphism in complement factor B. Proc. Natl Acad. Sci. USA 2009, 106:4366-4371.
69. Martínez-Barricarte R., Montes T., Pinto S., Sánchez-Corral P., López-Trascasa M., Morgan B.P., Harris C.L., Rodríguez de Cordoba S. Novel C3 mutations associated with atypical haemolytic uraemic syndrome (aHUS). Mol. Immunol. 2008, 45:4130.
70. Wu J., Wu Y.-Q., Ricklin D., Janssen B.J.C., Lambris J.D., Gros P. Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Nat. Immunol. 2009, 10:728-733.
71. Janssen B.J.C., Halff E.F., Lambris J.D., Gros P. Structure of compstatin in complex with complement component C3c reveals a new mechanism of complement inhibition. J. Biol. Chem. 2007, 282:29241-29247.
72. Katschke K.J., Stawicki S., Yin J., Steffek M., Xi H., Sturgeon L., Hass P.E., Loyet K.M., DeForge L., Wu Y., van Lookeren Campagne M., Wiesmann C. Structural and functional analysis of a C3b-specific antibody that selectively inhibits the alternative pathway of complement. J. Biol. Chem. 2009, 284:10473-10479.
73. Rodríguez de Córdoba S., Esparza-Gordillo J., Goicoechea de Jorge E., Lopez-Trascasa M., Sánchez-Corral P. The human complement factor H: functional roles, genetic variations and disease associations. Mol. Immunol. 2004, 41:355-367.
74. [74] M.K. Liszewski, J.P. Atkinson, Regulatory proteins of complement, in: F.M. In: Volanakis J.A., editors. (Ed.), The Human Complement System in Health and Disease, Marcel Dekker, New York, 1998, pp. 149-166.
75. Harris C.L., Abbott R.J.M., Smith R.A., Morgan B.P., Lea S.M. Molecular dissection of interactions between components of the alternative pathway of complement and decay accelerating factor (CD55). J. Biol. Chem. 2005, 280:2569-2578.
76. Sánchez-Corral P., Pérez-Caballero D., Huarte O., Simckes A.M., Goicoechea E., López-Trascasa M., Rodríguez de Córdoba S. Structural and functional characterization of factor H mutations associated with atypical hemolytic uremic syndrome. Am. J. Hum. Genet. 2002, 71:1285-1295.
77. Manuelian T., Hellwage J., Meri S., Caprioli J., Noris M., Heinen S., Jozsi M., Neumann H.P.H., Remuzzi G., Zipfel P.F. Mutations in factor H reduce binding affinity to C3b and heparin and surface attachment to endothelial cells in hemolytic uremic syndrome. J. Clin. Invest. 2003, 111:1181-1190.
78. 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. 2004, 41:81-84.
79. Atkinson J.P., Liszewski M.K., Richards A., Kavanagh D., Moulton E.A. Hemolytic uremic syndrome: an example of insufficient complement regulation on self-tissue. Ann. NY Acad. Sci. 2005, 1056:144-152.
80. Hageman G.S., Hancox L.S., Taiber A.J., Gehrs K., Anderson D.H., Johnson L.V., Radeke M.J., Kavanagh D., Richards A., Atkinson J.P., Meri S., Bergeron J., Zernant J., Merriam J.E., Gold B., Allikmets R., Dean M. Extended haplotypes in the complement factor H (CFH) and CFH-related (CFHR) family of genes protect against age-related macular degeneration: characterization, ethnic distribution and evolutionary implications. Ann. Med. 2006, 38:592-604. t.A.C.S. Group*.
81. Herbert A.P., Deakin J.A., Schmidt C.Q., Blaum B.S., Egan C., Ferreira V.P., Pangburn M.K., Lyon M., Uhrin D., Barlow P.N. Structure shows that a glycosaminoglycan and protein recognition site in factor H is perturbed by age-related macular degeneration-linked single nucleotide polymorphism. J. Biol. Chem. 2007, 282:18960-18968.
82. Clark S.J., Higman V.A., Mulloy B., Perkins S.J., Lea S.M., Sim R.B., Day A.J. His-384 allotypic variant of factor H associated with age-related macular degeneration has different heparin binding properties from the non-disease-associated form. J. Biol. Chem. 2006, 281:24713-24720.
83. Prosser B., Johnson S., Roversi P., Herbert A., Blaum B., Tyrrell J., Jowitt T., Clark S., Tarelli E., Uhrín D., Barlow P., Sim R., Day A., Lea S. Structural basis for complement factor H linked age-related macular degeneration. J. Exp. Med. 2007, 204:2277-2283.
84. Skerka C., Lauer N., Weinberger A.A.W.A., Keilhauer C.N., Sühnel J., Smith R., Schlötzer-Schrehardt U., Fritsche L., Heinen S., Hartmann A., Weber B.H.F., Zipfel P.F. Defective complement control of factor H (Y402H) and FHL-1 in age-related macular degeneration. Mol. Immunol. 2007, 44:3398-3406.
85. Laine M., Jarva H., Seitsonen S., Haapasalo K., Lehtinen M.J., Lindeman N., Anderson D.H., Johnson P.T., Jarvela I., Jokiranta T.S., Hageman G.S., Immonen I., Meri S. Y402H polymorphism of complement factor H affects binding affinity to C-reactive protein. J. Immunol. 2007, 178:3831-3836.
86. Sjoberg A.P., Trouw L.A., Clark S.J., Sjolander J., Heinegard D., Sim R.B., Day A.J., Blom A.M. The factor H variant associated with age-related macular degeneration (His-384) and the non-disease-associated form bind differentially to C-reactive protein, fibromodulin, DNA, and necrotic cells. J. Biol. Chem. 2007, 282:10894-10900.
87. Hakobyan S., Harris C.L., van den Berg C.W., Fernandez-Alonso M.C., Goicoechea de Jorge E., Rodriguez de Cordoba S., Rivas G., Mangione P., Pepys M.B., Morgan B.P. Complement factor H binds to denatured rather than to native pentameric C-reactive protein. J. Biol. Chem. 2008, 283:30451-30460.
88. Pickering M.C., Goicoechea de Jorge E., Martinez-Barricarte R., Recalde S., Garcia-Layana A., Rose K.L., Moss J., Walport M.J., Cook H.T., Rodriguez de Cordoba S., Botto M. Spontaneous hemolytic uremic syndrome triggered by complement factor H lacking surface recognition domains. J. Exp. Med. 2007, 204:1249-1256.
89. Tortajada A., Montes T., Martinez-Barricarte R., Morgan B.P., Harris C.L., Rodriguez de Cordoba S. The disease-protective complement factor H allotypic variant Ile62 shows increased binding affinity for C3b and enhanced cofactor activity. Hum. Mol. Genet. 2009, 18:3452-3461.