Complement activation, regulation, and molecular basis for complement-related diseases

EMBO Journal

Volumn 34, Issue 22, 2015, Pages 2735-2757

  Bajic, Goran ^a   Degn, Søren E ^a,b   Thiel, Steffen ^a   Andersen, Gregers R ^a  

^a AARHUS UNIVERSITY   (Denmark)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

complement; inflammation; innate immunity; proteolytic regulation; structural biology

Indexed keywords

COMPLEMENT; COMPLEMENT RECEPTOR;

COMPLEMENT ACTIVATION; COMPLEMENT DISORDER; COMPLEMENT REGULATION; COMPLEMENT SYSTEM; HUMAN; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; ANIMAL; AUTOCRINE EFFECT; GENETICS; IMMUNOLOGY; INFLAMMATION; PATHOLOGY; PROTEIN DEGRADATION;

ANIMALS; AUTOCRINE COMMUNICATION; COMPLEMENT ACTIVATION; HUMANS; INFLAMMATION; PROTEOLYSIS;

EID: 84949497174     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201591881     Document Type: Review

References (228)

1. Agarwal S, Ferreira VP, Cortes C, Pangburn MK, Rice PA, Ram S, (2010) An evaluation of the role of properdin in alternative pathway activation on Neisseria meningitidis and Neisseria gonorrhoeae. J Immunol 185: 507-516
2. Alcorlo M, Tortajada A, Rodriguez de Cordoba S, Llorca O, (2013) Structural basis for the stabilization of the complement alternative pathway C3 convertase by properdin. Proc Natl Acad Sci USA 110: 13504-13509
3. Aleshin AE, DiScipio RG, Stec B, Liddington RC, (2012) Crystal structure of C5b-6 suggests structural basis for priming assembly of the membrane attack complex. J Biol Chem 287: 19642-19652
4. Alper CA, Boenisch T, Watson L, (1972) Genetic polymorphism in human glycine-rich beta-glycoprotein. J Exp Med 135: 68-80
5. Amara U, Rittirsch D, Flierl M, Bruckner U, Klos A, Gebhard F, Lambris JD, Huber-Lang M, (2008) Interaction between the coagulation and complement system. Adv Exp Med Biol 632: 71-79
6. Amara U, Flierl MA, Rittirsch D, Klos A, Chen H, Acker B, Bruckner UB, Nilsson B, Gebhard F, Lambris JD, Huber-Lang M, (2010) Molecular intercommunication between the complement and coagulation systems. J Immunol 185: 5628-5636
7. Andrews PW, Knowles BB, Parkar M, Pym B, Stanley K, Goodfellow PN, (1985) A human cell-surface antigen defined by a monoclonal antibody and controlled by a gene on human chromosome 1. Ann Hum Genet 49: 31-39
8. Arlaud GJ, Gaboriaud C, Thielens NM, Rossi V, Bersch B, Hernandez JF, Fontecilla-Camps JC, (2001) Structural biology of C1: dissection of a complex molecular machinery. Immunol Rev 180: 136-145
9. Asgari E, Le Friec G, Yamamoto H, Perucha E, Sacks SS, Kohl J, Cook HT, Kemper C, (2013) C3a modulates IL-1beta secretion in human monocytes by regulating ATP efflux and subsequent NLRP3 inflammasome activation. Blood 122: 3473-3481
10. Axelgaard E, Jensen L, Dyrlund TF, Nielsen HJ, Enghild JJ, Thiel S, Jensenius JC, (2013) Investigations on collectin liver 1. J Biol Chem 288: 23407-23420
11. Bajic G, Yatime L, Klos A, Andersen GR, (2013a) Human C3a and C3a desArg anaphylatoxins have conserved structures, in contrast to C5a and C5a desArg. Protein Sci 22: 204-212
12. Bajic G, Yatime L, Sim RB, Vorup-Jensen T, Andersen GR, (2013b) Structural insight on the recognition of surface-bound opsonins by the integrin I domain of complement receptor 3. Proc Natl Acad Sci USA 110: 16426-16431
13. Bally I, Rossi V, Lunardi T, Thielens NM, Gaboriaud C, Arlaud GJ, (2009) Identification of the C1q-binding sites of human C1r and C1s: a refined three-dimensional model of the C1 complex of complement. J Biol Chem 284: 19340-19348
14. Bally I, Ancelet S, Moriscot C, Gonnet F, Mantovani A, Daniel R, Schoehn G, Arlaud GJ, Thielens NM, (2013) Expression of recombinant human complement C1q allows identification of the C1r/C1s-binding sites. Proc Natl Acad Sci USA 110: 8650-8655
15. Bamberg CE, Mackay CR, Lee H, Zahra D, Jackson J, Lim YS, Whitfeld PL, Craig S, Corsini E, Lu B, Gerard C, Gerard NP, (2010) The C5a receptor (C5aR) C5L2 is a modulator of C5aR-mediated signal transduction. J Biol Chem 285: 7633-7644
16. Barlow PN, Hageman GS, Lea SM, (2008) Complement factor H: using atomic resolution structure to illuminate disease mechanisms. Adv Exp Med Biol 632: 117-142
17. Barnum SR, (1995) Complement biosynthesis in the central nervous system. Crit Rev Oral Biol Med 6: 132-146
18. Berends ET, Kuipers A, Ravesloot MM, Urbanus RT, Rooijakkers SH, (2014) Bacteria under stress by complement and coagulation. FEMS Microbiol Rev 38: 1146-1171
19. Blackmore TK, Sadlon TA, Ward HM, Lublin DM, Gordon DL, (1996) Identification of a heparin binding domain in the seventh short consensus repeat of complement factor H. J Immunol 157: 5422-5427
20. Blaum BS, Hannan JP, Herbert AP, Kavanagh D, Uhrin D, Stehle T, (2015) Structural basis for sialic acid-mediated self-recognition by complement factor H. Nat Chem Biol 11: 77-82
21. Blom AM, Villoutreix BO, Dahlback B, (2004) Complement inhibitor C4b-binding protein-friend or foe in the innate immune system? Mol Immunol 40: 1333-1346
22. Bokisch VA, Muller-Eberhard HJ, (1970) Anaphylatoxin inactivator of human plasma: its isolation and characterization as a carboxypeptidase. J Clin Invest 49: 2427-2436
23. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH, (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35: 630-640
24. Brier S, Pflieger D, Le Mignon M, Bally I, Gaboriaud C, Arlaud GJ, Daniel R, (2010) Mapping surface accessibility of the C1r/C1s tetramer by chemical modification and mass spectrometry provides new insights into assembly of the human C1 complex. J Biol Chem 285: 32251-32263
25. Brinkmann CR, Jensen L, Dagnaes-Hansen F, Holm IE, Endo Y, Fujita T, Thiel S, Jensenius JC, Degn SE, (2013) Mitochondria and the lectin pathway of complement. J Biol Chem 288: 8016-8027
26. Brodsky RA, (2014) Paroxysmal nocturnal hemoglobinuria. Blood 124: 2804-2811
27. Burton DR, (1985) Immunoglobulin G: functional sites. Mol Immunol 22: 161-206
28. Carroll MC, (2000) The role of complement in B cell activation and tolerance. Adv Immunol 74: 61-88
29. Carroll MC, Isenman DE, (2012) Regulation of humoral immunity by complement. Immunity 37: 199-207
30. Chen CB, Wallis R, (2004) Two mechanisms for mannose-binding protein modulation of the activity of its associated serine proteases. J Biol Chem 279: 26058-26065
31. Chen X, Yu Y, Mi LZ, Walz T, Springer TA, (2012) Molecular basis for complement recognition by integrin alphaXbeta2. Proc Natl Acad Sci USA 109: 4586-4591
32. Chenoweth DE, Goodman MG, Weigle WO, (1982) Demonstration of a specific receptor for human C5a anaphylatoxin on murine macrophages. J Exp Med 156: 68-78
33. Cianflone K, Xia Z, Chen LY, (2003) Critical review of acylation-stimulating protein physiology in humans and rodents. Biochim Biophys Acta 1609: 127-143
34. Clark SJ, Higman VA, Mulloy B, Perkins SJ, Lea SM, Sim RB, Day AJ, (2006) 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 281: 24713-24720
35. Cook WJ, Galakatos N, Boyar WC, Walter RL, Ealick SE, (2010) Structure of human desArg-C5a. Acta Crystallogr D Biol Crystallogr 66: 190-197
36. de Cordoba SR, Tortajada A, Harris CL, Morgan BP, (2012) Complement dysregulation and disease: from genes and proteins to diagnostics and drugs. Immunobiology 217: 1034-1046
37. de Cordoba SR, (2015) Complement genetics and susceptibility to inflammatory disease. Lessons from genotype-phenotype correlations. Immunobiology doi: 10.1016/j.imbio.2015.05.015
38. Cortes C, Ohtola JA, Saggu G, Ferreira VP, (2012) Local release of properdin in the cellular microenvironment: role in pattern recognition and amplification of the alternative pathway of complement. Front Immunol 3: 412
39. Cortesio CL, Jiang W, (2006) Mannan-binding lectin-associated serine protease 3 cleaves synthetic peptides and insulin-like growth factor-binding protein 5. Arch Biochem Biophys 449: 164-170
40. Coulthard LG, Woodruff TM, (2015) Is the complement activation product C3a a proinflammatory molecule? Re-evaluating the evidence and the Myth. J Immunol 194: 3542-3548
41. Cui W, Lapointe M, Gauvreau D, Kalant D, Cianflone K, (2009) Recombinant C3adesArg/acylation stimulating protein (ASP) is highly bioactive: a critical evaluation of C5L2 binding and 3T3-L1 adipocyte activation. Mol Immunol 46: 3207-3217
42. Dahl MR, Thiel S, Matsushita M, Fujita T, Willis AC, Christensen T, Vorup-Jensen T, Jensenius JC, (2001) MASP-3 and its association with distinct complexes of the mannan-binding lectin complement activation pathway. Immunity 15: 127-135
43. Davis AE III, (1988) C1 inhibitor and hereditary angioneurotic edema. Annu Rev Immunol 6: 595-628
44. Degn SE, Hansen AG, Steffensen R, Jacobsen C, Jensenius JC, Thiel S, (2009) MAp44, a human protein associated with pattern recognition molecules of the complement system and regulating the lectin pathway of complement activation. J Immunol 183: 7371-7378
45. Degn SE, Thiel S, Nielsen O, Hansen AG, Steffensen R, Jensenius JC, (2011) MAp19, the alternative splice product of the MASP2 gene. J Immunol Methods 373: 89-101
46. Degn SE, Thiel S, (2013) Humoral pattern recognition and the complement system. Scand J Immunol 78: 181-193
47. Degn SE, Jensen L, Olszowski T, Jensenius JC, Thiel S, (2013a) Co-complexes of MASP-1 and MASP-2 associated with the soluble pattern-recognition molecules drive lectin pathway activation in a manner inhibitable by MAp44. J Immunol 191: 1334-1345
48. Degn SE, Thiel S, Jensenius JC, (2013b) Recombinant expression of the autocatalytic complement protease MASP-1 is crucially dependent on co-expression with its inhibitor, C1 inhibitor. Protein Expr Purif 88: 173-182
49. Degn SE, Jensenius JC, Thiel S, (2014a) The pro-factor D cleaving activity of MASP-1/-3 is not required for alternative pathway function. J Immunol 192: 5447-5448
50. Degn SE, Kjaer TR, Kidmose RT, Jensen L, Hansen AG, Tekin M, Jensenius JC, Andersen GR, Thiel S, (2014b) Complement activation by ligand-driven juxtaposition of discrete pattern recognition complexes. Proc Natl Acad Sci USA 111: 13445-13450
51. Diebolder CA, Beurskens FJ, de Jong RN, Koning RI, Strumane K, Lindorfer MA, Voorhorst M, Ugurlar D, Rosati S, Heck AJ, van de Winkel JG, Wilson IA, Koster AJ, Taylor RP, Saphire EO, Burton DR, Schuurman J, Gros P, Parren PW, (2014) Complement is activated by IgG hexamers assembled at the cell surface. Science 343: 1260-1263
52. Dragon-Durey MA, Fremeaux-Bacchi V, Loirat C, Blouin J, Niaudet P, Deschenes G, Coppo P, Fridman WH, Weiss L, (2004) 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
53. Duncan RC, Bergstrom F, Coetzer TH, Blom AM, Wijeyewickrema LC, Pike RN, (2012) Multiple domains of MASP-2, an initiating complement protease, are required for interaction with its substrate C4. Mol Immunol 49: 593-600
54. Eberhardt HU, Buhlmann D, Hortschansky P, Chen Q, Bohm S, Kemper MJ, Wallich R, Hartmann A, Hallstrom T, Zipfel PF, Skerka C, (2013) Human factor H-related protein 2 (CFHR2) regulates complement activation. PLoS ONE 8: e78617
55. van den Elsen JM, Isenman DE, (2011) A crystal structure of the complex between human complement receptor 2 and its ligand C3d. Science 332: 608-611
56. Esparza-Gordillo J, Soria JM, Buil A, Almasy L, Blangero J, Fontcuberta J, de Cordoba SR, (2004) Genetic and environmental factors influencing the human factor H plasma levels. Immunogenetics 56: 77-82
57. Fang Y, Xu C, Fu YX, Holers VM, Molina H, (1998) Expression of complement receptors 1 and 2 on follicular dendritic cells is necessary for the generation of a strong antigen-specific IgG response. J Immunol 160: 5273-5279
58. Farzan M, Schnitzler CE, Vasilieva N, Leung D, Kuhn J, Gerard C, Gerard NP, Choe H, (2001) Sulfated tyrosines contribute to the formation of the C5a docking site of the human C5a anaphylatoxin receptor. J Exp Med 193: 1059-1066
59. Fearon DT, Austen KF, Ruddy S, (1973) Formation of a hemolytically active cellular intermediate by the interaction between properdin factors B and D and the activated third component of complement. J Exp Med 138: 1305-1313
60. Fearon DT, Austen KF, (1975) Properdin: binding to C3b and stabilization of the C3b-dependent C3 convertase. J Exp Med 142: 856-863
61. Fearon DT, (1980) Identification of the membrane glycoprotein that is the C3b receptor of the human erythrocyte, polymorphonuclear leukocyte, B lymphocyte, and monocyte. J Exp Med 152: 20-30
62. Ferreira VP, Herbert AP, Hocking HG, Barlow PN, Pangburn MK, (2006) Critical role of the C-terminal domains of factor H in regulating complement activation at cell surfaces. J Immunol 177: 6308-6316
63. Ferreira VP, Pangburn MK, Cortes C, (2010) Complement control protein factor H: the good, the bad, and the inadequate. Mol Immunol 47: 2187-2197
64. Forneris F, Ricklin D, Wu J, Tzekou A, Wallace RS, Lambris JD, Gros P, (2010) Structures of C3b in complex with factors B and D give insight into complement convertase formation. Science 330: 1816-1820
65. Fredslund F, Laursen NS, Roversi P, Jenner L, Oliveira CL, Pedersen JS, Nunn MA, Lea SM, Discipio R, Sottrup-Jensen L, Andersen GR, (2008) Structure of and influence of a tick complement inhibitor on human complement component 5. Nat Immunol 9: 753-760
66. Frimat M, Tabarin F, Dimitrov JD, Poitou C, Halbwachs-Mecarelli L, Fremeaux-Bacchi V, Roumenina LT, (2013) Complement activation by heme as a secondary hit for atypical hemolytic uremic syndrome. Blood 122: 282-292
67. Fritsche LG, Lauer N, Hartmann A, Stippa S, Keilhauer CN, Oppermann M, Pandey MK, Kohl J, Zipfel PF, Weber BH, Skerka C, (2010) An imbalance of human complement regulatory proteins CFHR1, CFHR3 and factor H influences risk for age-related macular degeneration (AMD). Hum Mol Genet 19: 4694-4704
68. Gadjeva M, Verschoor A, Brockman MA, Jezak H, Shen LM, Knipe DM, Carroll MC, (2002) Macrophage-derived complement component C4 can restore humoral immunity in C4-deficient mice. J Immunol 169: 5489-5495
69. Ghannam A, Fauquert JL, Thomas C, Kemper C, Drouet C, (2014) Human complement C3 deficiency: Th1 induction requires T cell-derived complement C3a and CD46 activation. Mol Immunol 58: 98-107
70. Gingras AR, Girija UV, Keeble AH, Panchal R, Mitchell DA, Moody PC, Wallis R, (2011) Structural basis of mannan-binding lectin recognition by its associated serine protease MASP-1: implications for complement activation. Structure 19: 1635-1643
71. Gladman DD, Ibanez D, Urowitz MB, (2002) Systemic lupus erythematosus disease activity index 2000. J Rheumatol 29: 288-291
72. Goicoechea de Jorge E, Caesar JJ, Malik TH, Patel M, Colledge M, Johnson S, Hakobyan S, Morgan BP, Harris CL, Pickering MC, Lea SM, (2013) Dimerization of complement factor H-related proteins modulates complement activation in vivo. Proc Natl Acad Sci USA 110: 4685-4690
73. Gordon DL, Kaufman RM, Blackmore TK, Kwong J, Lublin DM, (1995) Identification of complement regulatory domains in human factor H. J Immunol 155: 348-356
74. Guo RF, Ward PA, (2005) Role of C5A in inflammatory responses. Annu Rev Immunol 23: 821-852
75. Hadders MA, Beringer DX, Gros P, (2007) Structure of C8alpha-MACPF reveals mechanism of membrane attack in complement immune defense. Science 317: 1552-1554
76. Hadders MA, Bubeck D, Roversi P, Hakobyan S, Forneris F, Morgan BP, Pangburn MK, Llorca O, Lea SM, Gros P, (2012) Assembly and regulation of the membrane attack complex based on structures of C5b6 and sC5b9. Cell Rep 1: 200-207
77. Harboe M, Ulvund G, Vien L, Fung M, Mollnes TE, (2004) The quantitative role of alternative pathway amplification in classical pathway induced terminal complement activation. Clin Exp Immunol 138: 439-446
78. Harboe M, Garred P, Karlstrom E, Lindstad JK, Stahl GL, Mollnes TE, (2009) The down-stream effects of mannan-induced lectin complement pathway activation depend quantitatively on alternative pathway amplification. Mol Immunol 47: 373-380
79. Harris CL, Heurich M, Rodriguez de Cordoba S, Morgan BP, (2012) The complotype: dictating risk for inflammation and infection. Trends Immunol 33: 513-521
80. Haupt K, Kraiczy P, Wallich R, Brade V, Skerka C, Zipfel PF, (2007) Binding of human factor H-related protein 1 to serum-resistant Borrelia burgdorferi is mediated by borrelial complement regulator-acquiring surface proteins. J Infect Dis 196: 124-133
81. Hawlisch H, Wills-Karp M, Karp CL, Kohl J, (2004) The anaphylatoxins bridge innate and adaptive immune responses in allergic asthma. Mol Immunol 41: 123-131
82. Hawlisch H, Kohl J, (2006) Complement and Toll-like receptors: key regulators of adaptive immune responses. Mol Immunol 43: 13-21
83. Haynes T, Luz-Madrigal A, Reis ES, Echeverri Ruiz NP, Grajales-Esquivel E, Tzekou A, Tsonis PA, Lambris JD, Del Rio-Tsonis K, (2013) Complement anaphylatoxin C3a is a potent inducer of embryonic chick retina regeneration. Nat Commun 4: 2312
84. He S, Atkinson C, Qiao F, Cianflone K, Chen X, Tomlinson S, (2009) A complement-dependent balance between hepatic ischemia/reperfusion injury and liver regeneration in mice. J Clin Invest 119: 2304-2316
85. Hebecker M, Jozsi M, (2012) Factor H-related protein 4 activates complement by serving as a platform for the assembly of alternative pathway C3 convertase via its interaction with C3b protein. J Biol Chem 287: 19528-19536
86. Heesters BA, Chatterjee P, Kim YA, Gonzalez SF, Kuligowski MP, Kirchhausen T, Carroll MC, (2013) Endocytosis and recycling of immune complexes by follicular dendritic cells enhances B cell antigen binding and activation. Immunity 38: 1164-1175
87. Heesters BA, Myers RC, Carroll MC, (2014) Follicular dendritic cells: dynamic antigen libraries. Nat Rev Immunol 14: 495-504
88. Heinen S, Hartmann A, Lauer N, Wiehl U, Dahse HM, Schirmer S, Gropp K, Enghardt T, Wallich R, Halbich S, Mihlan M, Schlotzer-Schrehardt U, Zipfel PF, Skerka C, (2009) Factor H-related protein 1 (CFHR-1) inhibits complement C5 convertase activity and terminal complex formation. Blood 114: 2439-2447
89. Hellwage J, Jokiranta TS, Koistinen V, Vaarala O, Meri S, Zipfel PF, (1999) Functional properties of complement factor H-related proteins FHR-3 and FHR-4: binding to the C3d region of C3b and differential regulation by heparin. FEBS Lett 462: 345-352
90. Helmy KY, Katschke KJ Jr, Gorgani NN, Kljavin NM, Elliott JM, Diehl L, Scales SJ, Ghilardi N, van Lookeren Campagne M, (2006) CRIg: a macrophage complement receptor required for phagocytosis of circulating pathogens. Cell 124: 915-927
91. Henriksen ML, Brandt J, Andrieu JP, Nielsen C, Jensen PH, Holmskov U, Jorgensen TJ, Palarasah Y, Thielens NM, Hansen S, (2013a) Heteromeric complexes of native collectin kidney 1 and collectin liver 1 are found in the circulation with MASPs and activate the complement system. J Immunol 191: 6117-6127
92. Henriksen ML, Brandt J, Iyer SS, Thielens NM, Hansen S, (2013b) Characterization of the interaction between collectin 11 (CL-11, CL-K1) and nucleic acids. Mol Immunol 56: 757-767
93. Herbert AP, Deakin JA, Schmidt CQ, Blaum BS, Egan C, Ferreira VP, Pangburn MK, Lyon M, Uhrin D, Barlow PN, (2007) 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 282: 18960-18968
94. Hillebrandt S, Wasmuth HE, Weiskirchen R, Hellerbrand C, Keppeler H, Werth A, Schirin-Sokhan R, Wilkens G, Geier A, Lorenzen J, Kohl J, Gressner AM, Matern S, Lammert F, (2005) Complement factor 5 is a quantitative trait gene that modifies liver fibrogenesis in mice and humans. Nat Genet 37: 835-843
95. Hofmeyer T, Schmelz S, Degiacomi MT, Dal Peraro M, Daneschdar M, Scrima A, van den Heuvel J, Heinz DW, Kolmar H, (2013) Arranged sevenfold: structural insights into the C-terminal oligomerization domain of human C4b-binding protein. J Mol Biol 425: 1302-1317
96. Honore C, Rorvig S, Hummelshoj T, Skjoedt MO, Borregaard N, Garred P, (2010) Tethering of Ficolin-1 to cell surfaces through recognition of sialic acid by the fibrinogen-like domain. J Leukoc Biol 88: 145-158
97. Huber-Lang MS, Sarma JV, McGuire SR, Lu KT, Padgaonkar VA, Younkin EM, Guo RF, Weber CH, Zuiderweg ER, Zetoune FS, Ward PA, (2003) Structure-function relationships of human C5a and C5aR. J Immunol 170: 6115-6124
98. Huber-Lang M, Sarma JV, Zetoune FS, Rittirsch D, Neff TA, McGuire SR, Lambris JD, Warner RL, Flierl MA, Hoesel LM, Gebhard F, Younger JG, Drouin SM, Wetsel RA, Ward PA, (2006) Generation of C5a in the absence of C3: a new complement activation pathway. Nat Med 12: 682-687
99. Hughes-Jones NC, Gardner B, (1979) Reaction between the isolated globular sub-units of the complement component C1q and IgG-complexes. Mol Immunol 16: 697-701
100. Iwaki D, Kanno K, Takahashi M, Endo Y, Lynch NJ, Schwaeble WJ, Matsushita M, Okabe M, Fujita T, (2006) Small mannose-binding lectin-associated protein plays a regulatory role in the lectin complement pathway. J Immunol 177: 8626-8632
101. Iwaki D, Kanno K, Takahashi M, Endo Y, Matsushita M, Fujita T, (2011) The role of mannose-binding lectin-associated serine protease-3 in activation of the alternative complement pathway. J Immunol 187: 3751-3758
102. Janssen BJ, Huizinga EG, Raaijmakers HC, Roos A, Daha MR, Nilsson-Ekdahl K, Nilsson B, Gros P, (2005) Structures of complement component C3 provide insights into the function and evolution of immunity. Nature 437: 505-511
103. Janssen BJ, Christodoulidou A, McCarthy A, Lambris JD, Gros P, (2006) Structure of C3b reveals conformational changes that underlie complement activity. Nature 444: 213-216
104. Jozsi M, Zipfel PF, (2008) Factor H family proteins and human diseases. Trends Immunol 29: 380-387
105. Kang YH, Tan LA, Carroll MV, Gentle ME, Sim RB, (2009) Target pattern recognition by complement proteins of the classical and alternative pathways. Adv Exp Med Biol 653: 117-128
106. Kawasaki N, Kawasaki T, Yamashina I, (1983) Isolation and characterization of a mannan-binding protein from human serum. J Biochem 94: 937-947
107. Kemper C, Mitchell LM, Zhang L, Hourcade DE, (2008) The complement protein properdin binds apoptotic T cells and promotes complement activation and phagocytosis. Proc Natl Acad Sci USA 105: 9023-9028
108. Khan S, Nan R, Gor J, Mulloy B, Perkins SJ, (2012) Bivalent and co-operative binding of complement factor H to heparan sulfate and heparin. Biochem J 444: 417-428
109. Kidmose RT, Laursen NS, Dobo J, Kjaer TR, Sirotkina S, Yatime L, Sottrup-Jensen L, Thiel S, Gal P, Andersen GR, (2012) Structural basis for activation of the complement system by component C4 cleavage. Proc Natl Acad Sci USA 109: 15425-15430
110. Kim YU, Carroll MC, Isenman DE, Nonaka M, Pramoonjago P, Takeda J, Inoue K, Kinoshita T, (1992) Covalent binding of C3b to C4b within the classical complement pathway C5 convertase. Determination of amino acid residues involved in ester linkage formation. J Biol Chem 267: 4171-4176
111. Kjaer TR, Hansen AG, Sorensen UB, Nielsen O, Thiel S, Jensenius JC, (2011) Investigations on the pattern recognition molecule M-ficolin: quantitative aspects of bacterial binding and leukocyte association. J Leukoc Biol 90: 425-437
112. Kjaer TR, Thiel S, Andersen GR, (2013) Toward a structure-based comprehension of the lectin pathway of complement. Mol Immunol 56: 413-422
113. Kjaer TR, Le LTM, Pedersen JS, Sander B, Golas M, Jensenius JC, Andersen GR, Thiel S, (2015) Structural insights into the initiating complex of the lectin pathway of complement activation. Structure 23: 342-351
114. Klos A, Tenner AJ, Johswich KO, Ager RR, Reis ES, Kohl J, (2009) The role of the anaphylatoxins in health and disease. Mol Immunol 46: 2753-2766
115. Klos A, Wende E, Wareham KJ, Monk PN, (2013) International Union of Basic and Clinical Pharmacology. [corrected]. LXXXVII. Complement peptide C5a, C4a, and C3a receptors. Pharmacol Rev 65: 500-543
116. Krarup A, Sorensen UB, Matsushita M, Jensenius JC, Thiel S, (2005) Effect of capsulation of opportunistic pathogenic bacteria on binding of the pattern recognition molecules mannan-binding lectin, L-ficolin, and H-ficolin. Infect Immun 73: 1052-1060
117. Krisinger MJ, Goebeler V, Lu Z, Meixner SC, Myles T, Pryzdial EL, Conway EM, (2012) Thrombin generates previously unidentified C5 products that support the terminal complement activation pathway. Blood 120: 1717-1725
118. Kuhn S, Zipfel PF, (1996) Mapping of the domains required for decay acceleration activity of the human factor H-like protein 1 and factor H. Eur J Immunol 26: 2383-2387
119. Kunert A, Losse J, Gruszin C, Huhn M, Kaendler K, Mikkat S, Volke D, Hoffmann R, Jokiranta TS, Seeberger H, Moellmann U, Hellwage J, Zipfel PF, (2007) Immune evasion of the human pathogen Pseudomonas aeruginosa: elongation factor Tuf is a factor H and plasminogen binding protein. J Immunol 179: 2979-2988
120. La Bonte LR, Pavlov VI, Tan YS, Takahashi K, Takahashi M, Banda NK, Zou C, Fujita T, Stahl GL, (2012) Mannose-binding lectin-associated serine protease-1 is a significant contributor to coagulation in a murine model of occlusive thrombosis. J Immunol 188: 885-891
121. Lacroix M, Dumestre-Perard C, Schoehn G, Houen G, Cesbron JY, Arlaud GJ, Thielens NM, (2009) Residue Lys57 in the collagen-like region of human L-ficolin and its counterpart Lys47 in H-ficolin play a key role in the interaction with the mannan-binding lectin-associated serine proteases and the collectin receptor calreticulin. J Immunol 182: 456-465
122. Laudisi F, Spreafico R, Evrard M, Hughes TR, Mandriani B, Kandasamy M, Morgan BP, Sivasankar B, Mortellaro A, (2013) Cutting edge: the NLRP3 inflammasome links complement-mediated inflammation and IL-1beta release. J Immunol 191: 1006-1010
123. Laursen NS, Andersen KR, Braren I, Spillner E, Sottrup-Jensen L, Andersen GR, (2011) Substrate recognition by complement convertases revealed in the C5-cobra venom factor complex. EMBO J 30: 606-616
124. Laursen NS, Magnani F, Gottfredsen RH, Petersen SV, Andersen GR, (2012) Structure, function and control of complement C5 and its proteolytic fragments. Curr Mol Med 12: 1083-1097
125. Law SK, Dodds AW, (1997) The internal thioester and the covalent binding properties of the complement proteins C3 and C4. Protein Sci 6: 263-274
126. Li M, Atmaca-Sonmez P, Othman M, Branham KE, Khanna R, Wade MS, Li Y, Liang L, Zareparsi S, Swaroop A, Abecasis GR, (2006) CFH haplotypes without the Y402H coding variant show strong association with susceptibility to age-related macular degeneration. Nat Genet 38: 1049-1054
127. Li R, Coulthard LG, Wu MC, Taylor SM, Woodruff TM, (2013) C5L2: a controversial receptor of complement anaphylatoxin, C5a. FASEB J 27: 855-864
128. Linton SM, Morgan BP, (1999) Complement activation and inhibition in experimental models of arthritis. Mol Immunol 36: 905-914
129. Liszewski MK, Kolev M, Le Friec G, Leung M, Bertram PG, Fara AF, Subias M, Pickering MC, Drouet C, Meri S, Arstila TP, Pekkarinen PT, Ma M, Cope A, Reinheckel T, Rodriguez de Cordoba S, Afzali B, Atkinson JP, Kemper C, (2013) Intracellular complement activation sustains T cell homeostasis and mediates effector differentiation. Immunity 39: 1143-1157
130. Liszewski MK, Atkinson JP, (2015) Complement regulators in human disease: lessons from modern genetics. J Intern Med 277: 294-305
131. Lo JC, Ljubicic S, Leibiger B, Kern M, Leibiger IB, Moede T, Kelly ME, Chatterjee Bhowmick D, Murano I, Cohen P, Banks AS, Khandekar MJ, Dietrich A, Flier JS, Cinti S, Bluher M, Danial NN, Berggren PO, Spiegelman BM, (2014) Adipsin is an adipokine that improves beta cell function in diabetes. Cell 158: 41-53
132. Makou E, Herbert AP, Barlow PN, (2013) Functional anatomy of complement factor H. Biochemistry 52: 3949-3962
133. Manuelian T, Hellwage J, Meri S, Caprioli J, Noris M, Heinen S, Jozsi M, Neumann HPH, Remuzzi G, Zipfel PF, (2003) 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
134. 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, (2014) Complement factor B mutations in atypical hemolytic uremic syndrome-disease-relevant or benign? J Am Soc Nephrol 25: 2053-2065
135. Martin M, Leffler J, Blom AM, (2012) Annexin A2 and A5 serve as new ligands for C1q on apoptotic cells. J Biol Chem 287: 33733-33744
136. Mastellos D, Papadimitriou JC, Franchini S, Tsonis PA, Lambris JD, (2001) A novel role of complement: mice deficient in the fifth component of complement (C5) exhibit impaired liver regeneration. J Immunol 166: 2479-2486
137. Matsushita M, Thiel S, Jensenius JC, Terai I, Fujita T, (2000) Proteolytic activities of two types of mannose-binding lectin-associated serine protease. J Immunol 165: 2637-2642
138. Matsushita M, (2013) Ficolins in complement activation. Mol Immunol 55: 22-26
139. Matthews KW, Mueller-Ortiz SL, Wetsel RA, (2004) Carboxypeptidase N: a pleiotropic regulator of inflammation. Mol Immunol 40: 785-793
140. McRae JL, Duthy TG, Griggs KM, Ormsby RJ, Cowan PJ, Cromer BA, McKinstry WJ, Parker MW, Murphy BF, Gordon DL, (2005) Human factor H-related protein 5 has cofactor activity, inhibits C3 convertase activity, binds heparin and C-reactive protein, and associates with lipoprotein. J Immunol 174: 6250-6256
141. Medicus RG, Gotze O, Muller-Eberhard HJ, (1976) Alternative pathway of complement: recruitment of precursor properdin by the labile C3/C5 convertase and the potentiation of the pathway. J Exp Med 144: 1076-1093
142. Medof ME, Kinoshita T, Nussenzweig V, (1984) Inhibition of complement activation on the surface of cells after incorporation of decay-accelerating factor (DAF) into their membranes. J Exp Med 160: 1558-1578
143. Megyeri M, Mako V, Beinrohr L, Doleschall Z, Prohaszka Z, Cervenak L, Zavodszky P, Gal P, (2009) Complement protease MASP-1 activates human endothelial cells: PAR4 activation is a link between complement and endothelial function. J Immunol 183: 3409-3416
144. Meri S, Pangburn MK, (1990) A mechanism of activation of the alternative complement pathway by the classical pathway: protection of C3b from inactivation by covalent attachment to C4b. Eur J Immunol 20: 2555-2561
145. Meri S, Waldmann H, Lachmann PJ, (1991) Distribution of protectin (CD59), a complement membrane attack inhibitor, in normal human tissues. Lab Invest 65: 532-537
146. Metlay JP, Witmer-Pack MD, Agger R, Crowley MT, Lawless D, Steinman RM, (1990) The distinct leukocyte integrins of mouse spleen dendritic cells as identified with new hamster monoclonal antibodies. J Exp Med 171: 1753-1771
147. Morgan BP, Gasque P, (1997) Extrahepatic complement biosynthesis: where, when and why? Clin Exp Immunol 107: 1-7
148. Morgan BP, Berg CW, Harris CL, (2005) "Homologous restriction" in complement lysis: roles of membrane complement regulators. Xenotransplantation 12: 258-265
149. Morgan HP, Schmidt CQ, Guariento M, Blaum BS, Gillespie D, Herbert AP, Kavanagh D, Mertens HD, Svergun DI, Johansson CM, Uhrin D, Barlow PN, Hannan JP, (2011) Structural basis for engagement by complement factor H of C3b on a self surface. Nat Struct Mol Biol 18: 463-470
150. Mortensen S, Kidmose RT, Petersen SV, Szilagyi A, Prohaszka Z, Andersen GR, (2015) Structural basis for the function of complement component C4 within the classical and lectin pathways of complement. J Immunol 194: 5488-5496
151. Moskovich O, Fishelson Z, (2007) Live cell imaging of outward and inward vesiculation induced by the complement c5b-9 complex. J Biol Chem 282: 29977-29986
152. Mukherjee P, Thomas S, Pasinetti GM, (2008) Complement anaphylatoxin C5a neuroprotects through regulation of glutamate receptor subunit 2 in vitro and in vivo. J Neuroinflammation 5: 5
153. Muller-Eberhard HJ, Polley MJ, Calcott MA, (1967) Formation and functional significance of a molecular complex derived from the second and the fourth component of human complement. J Exp Med 125: 359-380
154. Murphy B, Georgiou T, Machet D, Hill P, McRae J, (2002) Factor H-related protein-5: a novel component of human glomerular immune deposits. Am J Kidney Dis 39: 24-27
155. Nayak A, Pednekar L, Reid KB, Kishore U, (2012) Complement and non-complement activating functions of C1q: a prototypical innate immune molecule. Innate Immun 18: 350-363
156. 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, et al, (2014) Genetic variants in C5 and poor response to eculizumab. N Engl J Med 370: 632-639
157. Noris M, Remuzzi G, (2009) Atypical hemolytic-uremic syndrome. N Engl J Med 361: 1676-1687
158. Oppermann M, Manuelian T, Jozsi M, Brandt E, Jokiranta TS, Heinen S, Meri S, Skerka C, Gotze O, Zipfel PF, (2006) The C-terminus of complement regulator Factor H mediates target recognition: evidence for a compact conformation of the native protein. Clin Exp Immunol 144: 342-352
159. Paidassi H, Tacnet-Delorme P, Garlatti V, Darnault C, Ghebrehiwet B, Gaboriaud C, Arlaud GJ, Frachet P, (2008) C1q binds phosphatidylserine and likely acts as a multiligand-bridging molecule in apoptotic cell recognition. J Immunol 180: 2329-2338
160. Pangburn MK, Schreiber RD, Müller-Eberhard HJ, (1981) 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 154: 856-867
161. Perkins SJ, Fung KW, Khan S, (2014) Molecular interactions between complement factor H and Its heparin and heparan sulfate ligands. Front Immunol 5: 126
162. Phan TG, Grigorova I, Okada T, Cyster JG, (2007) Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat Immunol 8: 992-1000
163. Phan TG, Green JA, Gray EE, Xu Y, Cyster JG, (2009) Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat Immunol 10: 786-793
164. Phillips AE, Toth J, Dodds AW, Girija UV, Furze CM, Pala E, Sim RB, Reid KB, Schwaeble WJ, Schmid R, Keeble AH, Wallis R, (2009) Analogous interactions in initiating complexes of the classical and lectin pathways of complement. J Immunol 182: 7708-7717
165. Pickering MC, Botto M, Taylor PR, Lachmann PJ, Walport MJ, (2000) Systemic lupus erythematosus, complement deficiency, and apoptosis. Adv Immunol 76: 227-324
166. Podack ER, Kolb WP, Muller-Eberhard HJ, (1978) The C5b-6 complex: formation, isolation, and inhibition of its activity by lipoprotein and the S-protein of human serum. J Immunol 120: 1841-1848
167. Poursharifi P, Lapointe M, Fisette A, Lu H, Roy C, Munkonda MN, Fairlie DP, Cianflone K, (2014) C5aR and C5L2 act in concert to balance immunometabolism in adipose tissue. Mol Cell Endocrinol 382: 325-333
168. Prosser BE, Johnson S, Roversi P, Herbert AP, Blaum BS, Tyrrell J, Jowitt TA, Clark SJ, Tarelli E, Uhrín D, Barlow PN, Sim RB, Day AJ, Lea SM, (2007) Structural basis for complement factor H linked age-related macular degeneration. J Exp Med 204: 2277-2283
169. Ramirez-Ortiz ZG, Pendergraft WF 3rd, Prasad A, Byrne MH, Iram T, Blanchette CJ, Luster AD, Hacohen N, El Khoury J, Means TK, (2013) The scavenger receptor SCARF1 mediates the clearance of apoptotic cells and prevents autoimmunity. Nat Immunol 14: 917-926
170. Reynes M, Aubert JP, Cohen JH, Audouin J, Tricottet V, Diebold J, Kazatchkine MD, (1985) Human follicular dendritic cells express CR1, CR2, and CR3 complement receptor antigens. J Immunol 135: 2687-2694
171. Rittirsch D, Flierl MA, Nadeau BA, Day DE, Huber-Lang M, Mackay CR, Zetoune FS, Gerard NP, Cianflone K, Kohl J, Gerard C, Sarma JV, Ward PA, (2008) Functional roles for C5a receptors in sepsis. Nat Med 14: 551-557
172. Rock KL, Latz E, Ontiveros F, Kono H, (2010) The sterile inflammatory response. Annu Rev Immunol 28: 321-342
173. Rodriguez de Cordoba S, Rubinstein P, (1984) Genetic polymorphism of human factor H (beta 1H). J Immunol 132: 1906-1908
174. Rodriguez E, Rallapalli PM, Osborne AJ, Perkins SJ, (2014) New functional and structural insights from updated mutational databases for complement factor H, Factor I, membrane cofactor protein and C3. Biosci Rep 34: e00146
175. Rooijakkers SH, Wu J, Ruyken M, van Domselaar R, Planken KL, Tzekou A, Ricklin D, Lambris JD, Janssen BJ, van Strijp JA, Gros P, (2009) Structural and functional implications of the alternative complement pathway C3 convertase stabilized by a staphylococcal inhibitor. Nat Immunol 10: 721-727
176. Rooryck C, Diaz-Font A, Osborn DP, Chabchoub E, Hernandez-Hernandez V, Shamseldin H, Kenny J, Waters A, Jenkins D, Kaissi AA, Leal GF, Dallapiccola B, Carnevale F, Bitner-Glindzicz M, Lees M, Hennekam R, Stanier P, Burns AJ, Peeters H, Alkuraya FS, et al, (2011) Mutations in lectin complement pathway genes COLEC11 and MASP1 cause 3MC syndrome. Nat Genet 43: 197-203
177. Ross GD, (2000) Regulation of the adhesion versus cytotoxic functions of the Mac-1/CR3/alphaMbeta2-integrin glycoprotein. Crit Rev Immunol 20: 197-222
178. Rossi V, Cseh S, Bally I, Thielens NM, Jensenius JC, Arlaud GJ, (2001) Substrate specificities of recombinant mannan-binding lectin-associated serine proteases-1 and -2. J Biol Chem 276: 40880-40887
179. Rossi V, Teillet F, Thielens NM, Bally I, Arlaud GJ, (2005) Functional characterization of complement proteases C1s/mannan-binding lectin-associated serine protease-2 (MASP-2) chimeras reveals the higher C4 recognition efficacy of the MASP-2 complement control protein modules. J Biol Chem 280: 41811-41818
180. Roversi P, Johnson S, Caesar JJ, McLean F, Leath KJ, Tsiftsoglou SA, Morgan BP, Harris CL, Sim RB, Lea SM, (2011) Structural basis for complement factor I control and its disease-associated sequence polymorphisms. Proc Natl Acad Sci USA 108: 12839-12844
181. Ruseva MM, Takahashi M, Fujita T, Pickering MC, (2014) C3 dysregulation due to factor H deficiency is mannan-binding lectin-associated serine proteases (MASP)-1 and MASP-3 independent in vivo. Clin Exp Immunol 176: 84-92
182. Saggu G, Cortes C, Emch HN, Ramirez G, Worth RG, Ferreira VP, (2013) Identification of a novel mode of complement activation on stimulated platelets mediated by properdin and C3(H2O). J Immunol 190: 6457-6467
183. Sayah S, Jauneau AC, Patte C, Tonon MC, Vaudry H, Fontaine M, (2003) Two different transduction pathways are activated by C3a and C5a anaphylatoxins on astrocytes. Brain Res Mol Brain Res 112: 53-60
184. Schafer DP, Lehrman EK, Kautzman AG, Koyama R, Mardinly AR, Yamasaki R, Ransohoff RM, Greenberg ME, Barres BA, Stevens B, (2012) Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74: 691-705
185. Schatz-Jakobsen JA, Yatime L, Larsen C, Petersen SV, Klos A, Andersen GR, (2014) Structural and functional characterization of human and murine C5a anaphylatoxins. Acta Crystallogr D Biol Crystallogr 70: 1704-1717
186. Schmidt CQ, Herbert AP, Kavanagh D, Gandy C, Fenton CJ, Blaum BS, Lyon M, Uhrin D, Barlow PN, (2008) A new map of glycosaminoglycan and C3b binding sites on factor H. J Immunol 181: 2610-2619
187. Schramm EC, Roumenina LT, Rybkine T, Chauvet S, Vieira-Martins P, Hue C, Maga T, Valoti E, Wilson V, Jokiranta S, Smith RJ, Noris M, Goodship T, Atkinson JP, Fremeaux-Bacchi V, (2015) Mapping interactions between complement C3 and regulators using mutations in atypical hemolytic uremic syndrome. Blood 194: 5129-5138
188. Seddon JM, Yu Y, Miller EC, Reynolds R, Tan PL, Gowrisankar S, Goldstein JI, Triebwasser M, Anderson HE, Zerbib J, Kavanagh D, Souied E, Katsanis N, Daly MJ, Atkinson JP, Raychaudhuri S, (2013) Rare variants in CFI, C3 and C9 are associated with high risk of advanced age-related macular degeneration. Nat Genet 45: 1366-1370
189. Selman L, Hansen S, (2012) Structure and function of collectin liver 1 (CL-L1) and collectin 11 (CL-11, CL-K1). Immunobiology 217: 851-863
190. Shinjyo N, Stahlberg A, Dragunow M, Pekny M, Pekna M, (2009) Complement-derived anaphylatoxin C3a regulates in vitro differentiation and migration of neural progenitor cells. Stem Cells 27: 2824-2832
191. Sirmaci A, Walsh T, Akay H, Spiliopoulos M, Sakalar YB, Hasanefendioglu-Bayrak A, Duman D, Farooq A, King MC, Tekin M, (2010) MASP1 mutations in patients with facial, umbilical, coccygeal, and auditory findings of Carnevale, Malpuech, OSA, and Michels syndromes. Am J Hum Genet 87: 679-686
192. Skjoedt MO, Hummelshoj T, Palarasah Y, Honore C, Koch C, Skjodt K, Garred P, (2010) A novel mannose-binding lectin/ficolin-associated protein is highly expressed in heart and skeletal muscle tissues and inhibits complement activation. J Biol Chem 285: 8234-8243
193. Son M, Santiago-Schwarz F, Al-Abed Y, Diamond B, (2012) C1q limits dendritic cell differentiation and activation by engaging LAIR-1. Proc Natl Acad Sci USA 109: E3160-E3167
194. Stephan AH, Barres BA, Stevens B, (2012) The complement system: an unexpected role in synaptic pruning during development and disease. Annu Rev Neurosci 35: 369-389
195. Strey CW, Markiewski M, Mastellos D, Tudoran R, Spruce LA, Greenbaum LE, Lambris JD, (2003) The proinflammatory mediators C3a and C5a are essential for liver regeneration. J Exp Med 198: 913-923
196. Sugimoto R, Yae Y, Akaiwa M, Kitajima S, Shibata Y, Sato H, Hirata J, Okochi K, Izuhara K, Hamasaki N, (1998) Cloning and characterization of the Hakata antigen, a member of the ficolin/opsonin p35 lectin family. J Biol Chem 273: 20721-20727
197. Swierzko A, Lukasiewicz J, Cedzynski M, Maciejewska A, Jachymek W, Niedziela T, Matsushita M, Lugowski C, (2012) New functional ligands for ficolin-3 among lipopolysaccharides of Hafnia alvei. Glycobiology 22: 267-280
198. Szalai AJ, Agrawal A, Greenhough TJ, Volanakis JE, (1999) C-reactive protein: structural biology and host defense function. Clin Chem Lab Med 37: 265-270
199. Takahashi M, Ishida Y, Iwaki D, Kanno K, Suzuki T, Endo Y, Homma Y, Fujita T, (2010) Essential role of mannose-binding lectin-associated serine protease-1 in activation of the complement factor D. J Exp Med 207: 29-37
200. Takahashi K, Chang WC, Takahashi M, Pavlov V, Ishida Y, La Bonte L, Shi L, Fujita T, Stahl GL, Van Cott EM, (2011) Mannose-binding lectin and its associated proteases (MASPs) mediate coagulation and its deficiency is a risk factor in developing complications from infection, including disseminated intravascular coagulation. Immunobiology 216: 96-102
201. Takata Y, Kinoshita T, Kozono H, Takeda J, Tanaka E, Hong K, Inoue K, (1987) Covalent association of C3b with C4b within C5 convertase of the classical complement pathway. J Exp Med 165: 1494-1507
202. Tam JC, Bidgood SR, McEwan WA, James LC, (2014) Intracellular sensing of complement C3 activates cell autonomous immunity. Science 345: 1256070
203. Tedder TF, Fearon DT, Gartland GL, Cooper MD, (1983) Expression of C3b receptors on human be cells and myelomonocytic cells but not natural killer cells. J Immunol 130: 1668-1673
204. Tegla CA, Cudrici C, Patel S, Trippe R III, Rus V, Niculescu F, Rus H, (2011) Membrane attack by complement: the assembly and biology of terminal complement complexes. Immunol Res 51: 45-60
205. Teillet F, Dublet B, Andrieu JP, Gaboriaud C, Arlaud GJ, Thielens NM, (2005) The two major oligomeric forms of human mannan-binding lectin: chemical characterization, carbohydrate-binding properties, and interaction with MBL-associated serine proteases. J Immunol 174: 2870-2877
206. Teillet F, Gaboriaud C, Lacroix M, Martin L, Arlaud GJ, Thielens NM, (2008) Crystal structure of the CUB1-EGF-CUB2 domain of human MASP-1/3 and identification of its interaction sites with mannan-binding lectin and ficolins. J Biol Chem 283: 25715-25724
207. Timmann C, Leippe M, Horstmann RD, (1991) Two major serum components antigenically related to complement factor H are different glycosylation forms of a single protein with no factor H-like complement regulatory functions. J Immunol 146: 1265-1270
208. Torreira E, Tortajada A, Montes T, Rodriguez de Cordoba S, Llorca O, (2009) 3D structure of the C3bB complex provides insights into the activation and regulation of the complement alternative pathway convertase. Proc Natl Acad Sci USA 106: 882-887
209. Triantafilou K, Hughes TR, Triantafilou M, Morgan BP, (2013) The complement membrane attack complex triggers intracellular Ca2+ fluxes leading to NLRP3 inflammasome activation. J Cell Sci 126: 2903-2913
210. Tschopp J, French LE, (1994) Clusterin: modulation of complement function. Clin Exp Immunol 97 (Suppl 2): 11-14
211. Tsujimura M, Ishida C, Sagara Y, Miyazaki T, Murakami K, Shiraki H, Okochi K, Maeda Y, (2001) Detection of serum thermolabile beta-2 macroglycoprotein (Hakata antigen) by enzyme-linked immunosorbent assay using polysaccharide produced by Aerococcus viridans. Clin Diagn Lab Immunol 8: 454-459
212. Venkatraman Girija U, Gingras AR, Marshall JE, Panchal R, Sheikh MA, Gal P, Schwaeble WJ, Mitchell DA, Moody PC, Wallis R, (2013) Structural basis of the C1q/C1s interaction and its central role in assembly of the C1 complex of complement activation. Proc Natl Acad Sci USA 110: 13916-13920
213. Wallis R, Mitchell DA, Schmid R, Schwaeble WJ, Keeble AH, (2010) Paths reunited: Initiation of the classical and lectin pathways of complement activation. Immunobiology 215: 1-11
214. Weber M, Blair E, Simpson CV, O'Hara M, Blackburn PE, Rot A, Graham GJ, Nibbs RJ, (2004) The chemokine receptor D6 constitutively traffics to and from the cell surface to internalize and degrade chemokines. Mol Biol Cell 15: 2492-2508
215. Weiler JM, (1989) Regulation of C5 convertase activity by properdin, factors B and H. Immunol Res 8: 305-315
216. Weismann D, Hartvigsen K, Lauer N, Bennett KL, Scholl HP, Charbel Issa P, Cano M, Brandstatter H, Tsimikas S, Skerka C, Superti-Furga G, Handa JT, Zipfel PF, Witztum JL, Binder CJ, (2011) Complement factor H binds malondialdehyde epitopes and protects from oxidative stress. Nature 478: 76-81
217. Wieme RJ, Demeulenaere L, (1967) Genetically determined electrophoretic variant of the human complement component C'3. Nature 214: 1042-1043
218. Wiesmann C, Katschke KJ, Yin J, Helmy KY, Steffek M, Fairbrother WJ, McCallum SA, Embuscado L, DeForge L, Hass PE, van Lookeren Campagne M, (2006) Structure of C3b in complex with CRIg gives insights into regulation of complement activation. Nature 444: 217-220
219. Wilken HC, Gotze O, Werfel T, Zwirner J, (1999) C3a(desArg) does not bind to and signal through the human C3a receptor. Immunol Lett 67: 141-145
220. Woodruff TM, Arumugam TV, Shiels IA, Reid RC, Fairlie DP, Taylor SM, (2003) A potent human C5a receptor antagonist protects against disease pathology in a rat model of inflammatory bowel disease. J Immunol 171: 5514-5520
221. Wu J, Wu YQ, Ricklin D, Janssen BJ, Lambris JD, Gros P, (2009) Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Nat Immunol 10: 728-733
222. Yongqing T, Wilmann PG, Reeve SB, Coetzer TH, Smith AI, Whisstock JC, Pike RN, Wijeyewickrema LC, (2013) The x-ray crystal structure of mannose-binding lectin-associated serine proteinase-3 reveals the structural basis for enzyme inactivity associated with the Carnevale, Mingarelli, Malpuech, and Michels (3MC) syndrome. J Biol Chem 288: 22399-22407
223. Yoshizawa S, Nagasawa K, Yae Y, Niho Y, Okochi K, (1997) A thermolabile beta 2-macroglycoprotein (TMG) and the antibody against TMG in patients with systemic lupus erythematosus. Clin Chim Acta 264: 219-225
224. Zaferani A, Vives RR, van der Pol P, Navis GJ, Daha MR, van Kooten C, Lortat-Jacob H, Seelen MA, van den Born J, (2012) Factor h and properdin recognize different epitopes on renal tubular epithelial heparan sulfate. J Biol Chem 287: 31471-31481
225. Zarbin MA, (2004) Current concepts in the pathogenesis of age-related macular degeneration. Arch Ophthalmol 122: 598-614
226. Zhan X, Larson DE, Wang C, Koboldt DC, Sergeev YV, Fulton RS, Fulton LL, Fronick CC, Branham KE, Bragg-Gresham J, Jun G, Hu Y, Kang HM, Liu D, Othman M, Brooks M, Ratnapriya R, Boleda A, Grassmann F, von Strachwitz C, et al, (2013) Identification of a rare coding variant in complement 3 associated with age-related macular degeneration. Nat Genet 45: 1375-1379
227. Zhang M, Takahashi K, Alicot EM, Vorup-Jensen T, Kessler B, Thiel S, Jensenius JC, Ezekowitz RA, Moore FD, Carroll MC, (2006) Activation of the lectin pathway by natural IgM in a model of ischemia/reperfusion injury. J Immunol 177: 4727-4734
228. Zipfel PF, Lauer N, Skerka C, (2010) The role of complement in AMD. Adv Exp Med Biol 703: 9-24