Clinical aspects and molecular basis of primary deficiencies of complement component C3 and its regulatory proteins factor I and factor H

Scandinavian Journal of Immunology

Volumn 63, Issue 3, 2006, Pages 155-168

  S Reis, E ^a   Falcao D A ^a   Isaac, L ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

APOFERRITIN; COMPLEMENT COMPONENT C3; COMPLEMENT FACTOR H; FIBRINOGEN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M;

AUTOIMMUNITY; BLOOD CLOTTING FACTOR DEFICIENCY; CELL INFILTRATION; CLINICAL FEATURE; COMPLEMENT DEFICIENCY; FIBRINOGEN DEFECT; GENE FREQUENCY; GENETIC POLYMORPHISM; GLOMERULONEPHRITIS; HUMAN; IMMUNIZATION; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOLOGY; MOLECULAR BIOLOGY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; REVIEW;

AFIBRINOGENEMIA; ANIMALS; AUTOIMMUNE DISEASES; COMPLEMENT ACTIVATION; COMPLEMENT C3; COMPLEMENT FACTOR H; FIBRINOGEN; HUMANS; IMMUNOLOGIC DEFICIENCY SYNDROMES; INFECTION; MODELS, ANIMAL;

EID: 33644830187     PISSN: 03009475     EISSN: 13653083     Source Type: Journal    
DOI: 10.1111/j.1365-3083.2006.01729.x     Document Type: Review

References (141)

1. Müller-Eberhard HJ Molecular organization and function of the complement system Annu Rev Biochem 1988 57 321 47
2. Lambris JD The multifunctional role of C3. The third component of complement Immunol Today 1988 9 387 93
3. Ember JA Jagels MA Hugli TE Characterization of complement anaphylatoxins and their biological responses. In: Volanakis JE Frank MM, eds The Human Complement System in Health and Disease New York Marcel Dekker 1998: 241 84
4. Davies ME Horner A Loveland BE Mckenzie IF Complement deficiency and immune complex disease Springer Semin Immunopathol 1994 15 397 16
5. Dempsey PW Allison MED Akkaraju S Goodnow CC Fearon D C3d of complement as a molecular adjuvant: bridging innate and acquired immunity Science 1996 271 348 50
6. Carroll MC The role of complement and complement receptors in induction and regulation of immunity Annu Rev Immunol 1998 16 545 68
7. Mevorach D Mascarenhas JO Gershov D Elkon KB Complement-dependent clearance of apoptotic cells by human macrophages J Exp Med 1998 188 2313 20
8. Pickering MC Botto M Taylor PR Lachmann PJ Walport MJ Systemic lupus erythematosus, complement deficiency, and apoptosis Adv Immunol 2001 76 227 02
9. De Bruijn MHL Fey CH Human complement component C3: cDNA coding sequence and derived primary structure Proc Natl Acad Sci USA 1985 82 708 12
10. Fong KY Botto M Walport MJ So AK Genomic organization of human complement component C3 Genomics 1990 7 579 86
11. Law SK Lichtenberg NA Levine RP Evidence for an ester linkage between the labile binding site of C3b and receptive surfaces J Immunol 1979 123 1388 94
12. Isaac L Isenman DE Structural requirements for thioester bond formation in human complement component C3. Reassessment of the role of thioester bond integrity on the conformation of C3 J Biol Chem 1992 267 10062 9
13. Law SK Levine RP Interaction between the third complement protein and cell surface macromolecules Proc Natl Acad Sci USA 1977 74 2701 5
14. Ritchie RF Palomaki GE Neveux LM Navolotskaia O Ledue TB Craig WY Reference distributions for complement proteins C3 and C4: a practical, simple and clinically relevant approach in a large cohort J Clin Lab Anal 2003 16 1 5
15. Alper CA Johnson AAM Birtch AG Moore FD Human C′3: evidence for the liver as the primary site of synthesis Science 1969 163 286 8
16. Einstein LP Hansen PJ Ballow M et al. Biosynthesis of the third component of complement (C3) in vitro by monocytes from both normal and homozygous C3-deficient human J Clin Invest 1977 60 963 9
17. Reis ES Barbuto JAM Isaac L Human monocyte-derived dendritic cells produce complement proteins (abstract) Inflammation Research 2006 (in press)
18. Botto M Lissandrini D Sorio C Walport MJ Biosynthesis and secretion of complement component (C3) by activated polymorphonuclear leukocytes J Immunol 1992 149 1348 55
19. Katz Y Revel M Strunk RC Interleukin 6 stimulates synthesis of complement proteins factor B and C3 in human skin fibroblasts Eur J Immunol 1989 19 983 8
20. Warren HP Pantazis P Davies PF The third component of complement is transcribed and secrete by cultured human endothelial cells Am J Pathol 1987 129 9 13
21. Mitchell TJ Naughton M Norsworthy P Davues KA Walport MJ Morley BJ IFN-gamma up-regulates expression of the complement components C3 and C4 by stabilization of mRNA J Immunol 1996 156 4429 34
22. Lambris JD Lao Z Oglesby TJ Atkinson JP Hack CE Becherer JD Dissection of CR1, factor H, membrane cofactor protein, and factor B binding and functional sites in the third complement component J Immunol 1996 156 4821 32
23. Ross GD Lambris JD Cain JA Newman SL Generation of three different fragments of bound C3 with purified factor I or serum J Immunol 1982 129 2051 60
24. Medicus RG Melamed J Arnaout MA Role of human factor I and C3b receptor in the cleavage of surface-bound C3bi molecules Eur J Immunol 1983 13 465 70
25. Davis AE Harrison RA Structural characterization of factor I mediated cleavage of the third component of complement Biochemistry 1982 21 5745 9
26. Taniguchi-Sidle A Isenman DE Interactions of human complement 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 302
27. Oran AE Isenman DE Identification of residues within the 727-767 segment of human complement component C3 important for its interaction with factor H and with complement receptor 1 (CR1, CD35) J Biol Chem 1999 274 5120 30
28. Jokiranta TS Hellwage J Koistinen V Zipfel PF Meri S Each of the three binding sites on complement factor H interacts with a distinct site on C3b J Biol Chem 2000 275 27657 62
29. Jokiranta TS Westin J Nilsson UR et al. Complement C3b interactions studied with surface plasmon resonance technique Int Immunopharmacol 2001 1 495 506
30. Pangburn MK Muller-Eberhard HJ The alternative pathway of complement Springer Semin Immunopathol 1984 7 163 92
31. Alper CA Propp RP Genetic polymorphism of the third component of human complement (C′3) J Clin Invest 1968 47 2181 91
32. Botto M Fong KY So AK Koch C Walport MJ Molecular basis of polymorphisms of human complement component C3 J Exp Med 1990 172 1011 7
33. Rittner C Stradmann-Bellinghausen B C3 reference typing report and nomenclature revision Complement Inflamm 1990 7 230 3
34. Finn JE Mathieson PW Molecular analysis of C3 allotypes in patients with nephritic factor Clin Exp Immunol 1993 91 410 4
35. Hohler T Botto M Rittner C Schneider PM Buschenfelde K-HM Complement component C3: molecular basis of the C3*S025 variant and evidence for molecular heterogeneity of other variants Hum Genet 1995 96 539 41
36. Reis ES Baracho GV Lima AS Farah CS Isaac L Homozygous hereditary C3 deficiency due to a premature stop codon J Clin Immunol 2002 22 321 30
37. Reis ES Nudelman V Isaac L Nonsense codon-mediated decay in human hereditary complement C3 deficiency Immunogenetics 2004 55 667 73
38. Alper CA Colten HR Rosen FS Rabson AR Macnab GM Homozygous deficiency of C3 in a patient with repeated infections Lancet 1972 ii 1179 81
39. Alper CA Colten HR Gear JS Rabson AR Rosen FS Homozygous human C3 deficiency. The role of C3 in antibody production, C-1s-induced vasopermeability, and cobra venom-induced passive hemolysis J Clin Invest 1976 57 222 9
40. Botto M Fong KY So AK et al. Homozygous hereditary C3 deficiency due to a partial gene deletion Proc Natl Acad Sci USA 1992 89 4957 61
41. Weiss RM Schulz EJ Complement deficiency in Sweet's syndrome Br J Dermatol 1989 121 413 5
42. Ballow M Shira JE Harden L Yang SY Day NK Complete absence of the third component of complement in man J Clin Invest 1975 56 703 10
43. Berger M Balow JE Wilson CB Frank MM Circulating immune complexes and glomerulonephritis in a patient with congenital absence of the third component of complement N Engl J Med 1983 308 1009 12
44. Grace HJ Brereton-Stiles GG Vos GH Scholand M A family with partial and total deficiency of complement C3 S Afr Med J 1976 50 139 40
45. Osofsky SG Thompson BH Lint TF Gewurz H Hereditary deficiency of the third component of complement in a child with fever, skin rash and arthralgias: response to transfusion of whole blood J Pediatr 1977 90 180 6
46. Davies AE Davies JS Rabson AR et al. Homozygous C3 deficiency: detection of C3 by radioimmunoassay Clin Immunol Immunopathol 1977 8 543 50
47. Pussel BA Nayef M Bourke E Morris S Peters DK Complement deficiency and nephritis: a report of a family Lancet 1980 I 675 7
48. Sano Y Nishimukai H Kitamura H et al. Hereditary deficiency of the third component of complement in two sisters with systemic lupus erythematosus-like symptoms Arthritis Rheum 1981 24 1255 60
49. Hsieh KH Lin CY Lee TC Complete absence of the third component of complement in a patient with repeated infections Clin Immunol Immunopathol 1981 20 305 12
50. Huang JL Lin CY A hereditary C3 deficiency due to aberrant splicing of exon 10 Clin Immunol Immunopathol 1994 73 267 73
51. Roord JJ Daha M Kuis W et al. Inherited deficiency of the third component of complement associated with recurrent pyogenic infections, circulating immune complexes and vasculitis in a Dutch family Pediatrics 1983 71 81 7
52. Borzy MS Houghton D Mixed-pattern immune deposit glomerulonephritis in a child with inherited deficiency of the third component of complement Am J Kidney Dis 1985 5 54 9
53. Borzy MS Gerwurz A Wolff L Houghton D Lovrien E Inherited C3 deficiency with recurrent infections and glomerulonephritis Am J Dis Child 1988 142 79 83
54. Singer L Van Hee M Lokki ML Kramer J Borzy MS Wetsel RA Inherited complement C3 deficiency: reduced mRNA and protein levels in a laotian kindred Clin Immunol Immunopathol 1996 81 244 52
55. Cozma G Aburumeih S Malik-Cozma MC Johny KV CAPD in a patient with complete absence of C3 Clin Nephrol 1987 27 269
56. Grumach AS Vilela MMS Gonzalez CH et al. Inherited C3 deficiency of the complement system Braz J Med Biol Res 1988 21 247 57
57. Botto M Fong KY So AK Rudge A Walport MJ Molecular basis of hereditary C3 deficiency J Clin Invest 1990 86 1158 63
58. Imai K Nakajima K Eguchi K et al. Homozygous C3 deficiency associated with IgA nephropathy Nephron 1991 9 148 12
59. Katz Y Singer L Wetsel RA Schlesinger M Fishelson Z Inherited complement C3 deficiency: a defect in C3 secretion Eur J Immunol 1994 24 1517 22
60. Peleg D Harit-Bustan H Katz Y Peller S Schlesinger M Schonfeld S Inherited C3 deficiency and meningococcal disease in a teenager Pediatr Infect Dis J 1992 11 401 4
61. Singer L Whitehead WT Akama H Katz Y Fishelson Z Wetsel RA Inherited human complement C3 deficiency J Biol Chem 1994 269 28494 9
62. Sanal O Loos M Ersoy F Kanra G Secmeer G Tezcan I Complement component deficiencies and infection: C5, C8 and C3 deficiencies in three families Eur J Pediatr 1992 151 676 9
63. Ulbrich AG Florido MPC Nudelman V Reis ES Baracho G Isaac L Hereditary human complement C3 deficiency owing to reduced levels of C3 mRNA Scand J Immunol 2001 53 622 6
64. Matsuyama W Nakagawa M Hakashima H Muranaga F Sano Y Osame M Identification of a novel mutation (Tyr1081Ter) in sisters with hereditary component C3 deficiency and SLE-like symptoms Hum Mutat 2000 17 79
65. Tsukamoto H Horiuchi T Kokuba H et al. Molecular analysis of a novel hereditary C3 deficiency with systemic lupus erythematosus Biochem Biophys Res Commun 2005 330 298 04
66. Kovarik J Siegrist CA Immunity in early life Immunol Today 1998 19 150 2
67. Turnberg D Cook HT Complement and glomerulonephritis: new insights Curr Opin Nephrol Hypertens 2005 14 223 8
68. Miller GW Nussenzweig V A new complement function: solubilization of antigen-antibody aggregates Proc Natl Acad Sci USA 1975 72 418 22
69. Schifferli JA Steiger G Hauptmann G Spaeth PJ Sjoholm AG Formation of soluble immune complexes by complement in sera of patients with various hypocomplementemic states. Difference between inhibition of immune precipitation and solubilization J Clin Invest 1985 76 2127 33
70. Blum JR Cork LC Morris JM Olson JL Winkelstein JA The clinical manifestations of a genetically determined deficiency of the third component of complement in the dog Clin Immunol Immunopathol 1985 34 304 15
71. Quigg RJ Lim A Haas M Alexander JJ He C Carroll MC Immune complex glomerulonephritis in C4- and C3-deficient mice Kidney Int 1998 53 320 30
72. Sheerin NS Springall T Carroll MC Hartley B Sacks SH Protection against anti-glomerular basement membrane (GBM) -mediated nephritis in C3- and C4-deficient mice Clin Exp Immunol 1997 110 403 9
73. Sekine H Reilly CM Molano ID et al. Complement component C3 is not required for full expression of immune complex glomerulonephritis in MRL/lpr mice J Immunol 2001 166 6444 51
74. Zhou W Marsh JE Sacks SH Intrarenal synthesis of complement Kidney Int 2001 59 1227 35
75. Daha MR Fearon DT Austen F C3 nephritic factor (C3Nef) stabilization of fluid phase and cell-bound alternative pathway convertase J Immunol 1976 116 1 7
76. Ferreira de Paula P Barbosa JE Roxo P Jr. Ontogeny of complement regulatory proteins: concentrations of factor H, factor I, C4b binding protein, properdin and vitronectin in healthy children of different ages and in adults Scand J Immunol 2003 58 572 7
77. Alper CA Abramson N Johnston JB Jandl JH Rosen FS Increased susceptibility to infection associated with abnormalities of complement-mediated functions and of the third component (C3) N Engl J Med 1970 282 350 4
78. Abramson N Alper CA Lachmann PJ Rosen FS Jandl JH Deficiency of C3 inactivator in man J Immunol 1971 107 19 27
79. Alper CA Rosen FS Lachmann PJ Inactivator of the third component of complement as in inhibitor in the properdin pathway Proc Natl Acad Sci USA 1972 69 2910 3
80. Ziegler JB Alper CA Rosen FS Lachman PJ Sherington L Restoration by purified C3b inactivator of complement-mediated function in vivo in a patient with C3b inactivator deficiency J Clin Invest 1975 55 668 72
81. Thompson RA Lachmann PJ A second case of human C3b inhibitor (KAF) deficiency Clin Exp Immunol 1977 27 23 9
82. Vyse TJ Morley BJ Bartók I Theodoridis EL Davies KA Webster ADB The molecular basis of hereditary complement factor I deficiency J Clin Invest 1996 97 925 33
83. Eng RK Seligman SJ Arnout M Alper CA Variable expression of homozygous C3b inactivator deficiency Clin Res 1978 26 394
84. Wahn V Rother U Rauterberg EW Day NK Laurel AB C3b inactivator deficiency: association with na alpha-migrating factor H J Clin Immunol 1981 1 228 33
85. Solal-Celigny P Laviolette M Herbert J et al. C3b inativator deficiency with immune complex manifestations Clin Exp Immunol 1982 47 197 5
86. Teisner B Brandsland I Folkersen J Rasmussen JM Poulsen LO Svehag SE Factor I deficiency and C3 nephritic factor: immunochemical findings and association with Neisseria meningitidis Scand J Immunol 1984 20 291 7
87. Rasmussen JM Teisner B Brandsland I Svehag SE A family with complement factor I deficiency Scand J Immunol 1986 23 711 5
88. Barret DJ Boyle MDP Restoration of complement function in vivo by plasma infusion in factor I (C3b inactivator) deficiency J Pediatr 1984 104 76 81
89. Porteu F Fischer A Descamps-Lastcha B Halbwachs-Mecarelli L Defective complement receptors (CR1 and CR3) on erythrocytes and leukocytes of factor I (C3b-inactivator) deficient patient Clin Exp Immunol 1986 66 463 71
90. Rasmussen JM Teisner B Jepsen HH et al. Three cases of factor I deficiency: the effect of treatment with plasma Clin Exp Immunol 1988 74 131 6
91. Maillet F Weiss L Chibani J Kazatchine MD Déficit en facteur I, une proteine regulatrice du complément Presse Med 1990 19 762 8
92. Floret D Stamm D Ponard D Increased susceptibility to infection in children with congenital deficiency of factor I Pediatr Infect Dis J 1991 10 615 8
93. Tottori DH Hilman B Daul CB Concomitant factor I and IgA deficiencies Ann Allergy Asthma Immunol 1992 68 115.
94. Bonnin AJ Zeitz HJ Gewurz A Complement factor I deficiency with recurrent infections aseptic meningitis Arch Intern Med 1993 153 1380 3
95. Vyse TJ Spath PJ Davies KA et al. Hereditary complement factor I deficiency QJM 1994 87 385 01
96. Leitão MF Vilela MMS Rutz R Grumach AS Condino-Neto A Kirschfink M Complement, factor I deficiency in a family with recurrent infection Immunopharmacology 1997 38 207 13
97. Naked GM Pereira MCF Vinet AMR Inostroza JS Isaac L Deficiency of human complement factor I associated with lowered factor H Clin Immunol 2000 96 162 7
98. Amadei N Baracho GV Nudelman V Bastos W Florido MPC Isaac L Inherited complete factor I deficiency associated with systemic lupus erythematosus, higher susceptibility to infection and low levels of factor H Scand J Immunol 2001 53 614 21
99. Baracho GV Nudelman V Isaac L Molecular characterization of homozygous factor I deficiency Clin Exp Immunol 2003 131 280 6
100. González-Rubio C Ferreira-Cerdán A Ponce M Arpa J Fontán G López-Trascasa M Complement factor I deficiency associated with recurrent meningitis coinciding with menstruation Arch Neurol 2001 58 1923 8
101. Genel F Sjoholm AG Skattum L Truedsson L Complement factor I deficiency associated with recurrent infections, vasculitis and immune complex glomerulonephritis Scand J Infect Dis 2005 37 615 8
102. Morley BJ Bartók I Spath PJ Vyse TJ Schneider PM Walport MJ Molecular basis of hereditary factor I deficiency (abstract) Mol Immunol 1998 35 344
103. Zipfel PF Skerka C Caprioli J et al. Complement factor H and hemolytic uremic syndrome Int Immunopharmacol 2001 1 461 8
104. Thompson RA Winterborn MH Hypocomplementemia due to a genetic deficiency of beta 1H globulin Clin Exp Immunol 1981 46 110 9
105. Levy M Halbwachs-Mecarelli L Gubler MC et al. Factor H deficiency in two brothers with atypical dense intramembranous deposit disease Kidney Int 1986 30 949 56
106. Dragon-Durey MA Frémeaux-Bacchi V Loirat C et al. 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 95
107. Lopez-Larrea C Diegez MA Enguix A Dominguez O Marin B Gomez E A family deficiency of complement factor H Biochem Soc Trans 1987 15 648 9
108. Brai M Misiano G Maringhini S Cutaja I Hauptmann G Combined homozygous factor H and heterozygous C2 deficiency in a Italian family J Clin Immunol 1988 8 50 6
109. Sánchez-Corral P Bellavia D Amico L Brai M de Córdoba SR Molecular basis for factor H and FHL-1 deficiency in an Italian family Immunogenetics 2000 51 366 9
110. Nielsen HE Christensen KC Koch C Thomsen BS Heegard NH Tranum-Jensen J Hereditary complete deficiency of complement factor H associated with recurrent meningococcal disease Scand J Immunol 1989 30 711 8
111. Pichette V Quérin S Schürch W Brun G Lehner-Netsch G Delâge J Familial hemolytic-uremic syndrome and homozygous factor H deficiency Am J Kidney Dis 1994 24 936 41
112. Vogt BA Wyatt RJ Burke BA Simonton SC Kashtan CE Inherited factor H deficiency and collagen type III glomerulopathy Pediatr Nephrol 1995 9 11 5
113. Ault BH Schmidt BZ Fowler NL et al. Human factor H deficiency. Mutations in framework cysteine residues and block in H protein secretion and intracellular catabolism J Biol Chem 1997 271 25168 75
114. Fijen CA Kuijper EJ Te Bulte M et al. Heterozygous and homozygous factor H deficiency states in a Dutch family Clin Exp Immunol 1996 105 511 6
115. Ohali M Shalev H Schlesinger M et al. Hypocomplementemic autosomal recessive hemolytic uremic syndrome with decreased factor H Pediatr Nephrol 1998 12 619 24
116. Rougier N Kazatchkine MD Rougier JP et al. Human complement factor H deficiency associated with hemolytic uremic syndrome J Am Soc Nephrol 1998 9 2318 26
117. Schmidt BZ Fowler NL Hidvegi T Perlmutter DH Colten HR Disruption of disulfide bonds is responsible for impaired secretion in human factor H deficiency J Biol Chem 1999 274 11782 8
118. Remuzzi G Ruggenenti P The hemolytic uremic syndrome Kidney Int 1995 48 2 19
119. Warwicker P Donne RL Goodship JA et al. Familial relapsing haemolytic uraemic syndrome and complement factor H deficiency Nephrol Dial Transplant 1999 14 1229 33
120. Richards A Kemp EJ Liszewski MK et al. Mutations in human complement regulato, membrane cofactor protein (CD46), predispose to development of familiarhemolytic uremic syndrome Proc Natl Acad Sci USA 2003 100 12966 71
121. Noris M Brioschi S Caprioli J et al. Familial haemolytic uraemic syndrome and MCP mutation Lancet 2003 362 1542 7
122. Fremeaux-Bacchi V Dragon-Durey MA Blouin J et al. Complement factor I: a susceptibility gene for atypical haemolytic uraemic syndrome J Med Genet 2004 41 e84
123. Richards A Goodship JA Goodship THJ The genetics and pathogenesis of haemolytic uraemic syndrome and thrombotic thrombocytopenic purpura Curr Opin Nephrol Hypertens 2002 11 431 5
124. Józsi M Manuelian T Heinen S Oppermann M Zipfel PF Attachment of the soluble complement regulator factor H to cell and tissue surfaces: relevance for pathology Histol Histopathol 2004 19 251 8
125. Klein RJ Zeiss C Chew EY et al. Complement factor H polymorphism in age-related macular degeneration Science 2005 308 385 9
126. Haines JL Hauser MA Schmidt S et al. Complement factor H variant increases the risk of age-related macular degeneration Science 2005 308 419 21
127. Edwards AO Ritter R Abel KJ Manning A Panhuysen C Farrer LA Complement factor H polymorphism and age-related macular degeneration Science 2005 308 421 4
128. Blackmore TK Sadlon TA Ward HM Lublin DM Gordon DL Identification of a heparin binding domain in the seventh short consensus repeat of complement factor H J Immunol 1996 157 5422 7
129. Jarva H Jokiranta TS Hellwage J Zipfel PF Meri S Regulation of complement activation by C-reactive protein: targeting the complement inhibitory activity of factor H bu an interaction with short consensus repeat domains 7 and 8-11 J Immunol 1999 163 3957 62
130. Vogel CW Smith CA Muller-Eberhard HJ Cobra venom factor: structural homology with the third component of human complement J Immunol 1984 133 3235 41
131. Auerbach HS Burger R Dodds AW Colten HR Molecular basis of complement C3 deficiency in guinea-pigs J Clin Invest 1990 86 96 06
132. Winkelstein JA Cork LC Griffin DE Griffin JW Adams RJ Price DL Genetically determined deficiency of the third component of complement in the dog Science 1981 212 1169 70
133. Komatsu M Yamamoto K Nakano Y et al. Hereditary C3 hypocomplementemia in the rabbit Immunology 1988 64 363 8
134. Ameratunga R Winkelstein JA Brody L et al. Molecular analysis of the third component of canine complement (C3) and identification of the mutation responsible for hereditary canine C3 deficiency J Immunol 1998 160 2824 30
135. Pepys MB Role of complement in induction of antibody production in vivo J Exp Med 1974 140 126 5
136. Wessels MR Butko P Ma M Warren HB Lage AL Carroll MC Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity Proc Natl Acad Sci USA 1995 92 11490 4
137. Fischer MB Ma M Goerg S et al. Regulation of the B cell response to T-dependent antigens by classical pathway complement J Immunol 1996 157 549 56
138. Circolo A Garnier G Fukuda W et al. Genetic disruption of the murine complement C3 promoter region generates deficient mice with extrahepatic expression of C3 mRNA Immunopharmacology 1999 42 135 49
139. Høgåsen K Jansen JH Mollnes TE Hovdenes J Harboe M Hereditary porcine membranoproliferative glomerulonephritis type II is caused by factor H deficiency J Clin Invest 1995 95 1054 61
140. Hegasy GA Manuelian T Hogasen K Jansen JH Zipfel PF Molecular basis for hereditary porcine membranoproliferative glomerulonephritis type II. Point mutations in the factor H coding sequence block protein secretion Am J Pathol 2002 161 2027 34
141. Pickering MC Cook HT Warren J et al. Uncontrolled C3 activation causes membranoproliferative glomerulonephritis in mice deficient in complement factor H Nat Genet 2002 31 424 8