Subscribe to RSS
Please copy the URL and add it into your RSS Feed Reader.
https://www.thieme-connect.de/rss/thieme/en/10.1055-s-00000077.xml
Download PDF
Semin Thromb Hemost 2011; 37(4): 362-374
DOI: 10.1055/s-0031-1276585
© Thieme Medical PublishersDOI: 10.1055/s-0031-1276585
C1-Inhibitor: More Than a Serine Protease Inhibitor
Further Information
Publication History
Publication Date:
30 July 2011 (online)
ABSTRACT
C1-inhibitor (C1-inh) is a crucial regulator of the activation of plasmatic cascade systems involved in inflammation contributing to the homeostasis in the generation of proinflammatory mediators. The importance of C1-inh is illustrated by patients with hereditary angioedema where decreased levels of C1-inh lead to an uncontrolled generation of vasoactive peptides resulting in potential life-threatening subcutaneous edema. Recent publications, however, suggest that the anti-inflammatory properties of C1-inh do not strictly depend on its capacity to regulate the complement and contact phase system. This review summarizes the biochemical characteristics of C1-inh and its role in the regulation of plasmatic cascade systems as well as the role of the nonserpin domain.
KEYWORDS
C1-inhibitor - hereditary angioedema - serpin - contact phase - complement - sepsis
REFERENCES
- 1 Caliezi C, Wuillemin W A, Zeerleder S, Redondo M, Eisele B, Hack C E. C1-Esterase inhibitor: an anti-inflammatory agent and its potential use in the treatment of diseases other than hereditary angioedema. Pharmacol Rev. 2000; 52 (1) 91-112
- 2 Schapira M, de Agostini A, Schifferli J A, Colman R W. Biochemistry and pathophysiology of human C1 inhibitor: current issues. Complement. 1985; 2 (2–3) 111-126
- 3 Nuijens J H, Eerenberg-Belmer A JM, Huijbregts C C et al.. Proteolytic inactivation of plasma C1-inhibitor in sepsis. J Clin Invest. 1989; 84 (2) 443-450
- 4 Travis J, Salvesen G S. Human plasma proteinase inhibitors. Annu Rev Biochem. 1983; 52 655-709
- 5 Carrell R W, Boswell D R. Serpins: the superfamily of plasma proteinase inhibitors. In: Barrett A J, Salvesen G, eds. Proteinase Inhibitors. Amsterdam, The Netherlands: Elsevier; 1990: 403-420
- 6 Carrell R W, Travis J. α1-antitrypsin and the serpins: variation and countervariation. Trends Biochem Sci. 1985; 10 20-24
- 7 Carter P E, Dunbar B, Fothergill J E. Genomic and cDNA cloning of the human C1 inhibitor. Intron-exon junctions and comparison with other serpins. Eur J Biochem. 1988; 173 (1) 163-169
- 8 Coutinho M, Aulak K S, Davis III A E. Functional analysis of the serpin domain of C1 inhibitor. J Immunol. 1994; 153 (8) 3648-3654
- 9 Wagenaar-Bos I G, Hack C E. Structure and function of C1-inhibitor. Immunol Allergy Clin North Am. 2006; 26 (4) 615-632
- 10 Bock S C, Skriver K, Nielsen E et al.. Human C1 inhibitor: primary structure, cDNA cloning, and chromosomal localization. Biochemistry. 1986; 25 (15) 4292-4301
- 11 Bos I G, Lubbers Y T, Roem D, Abrahams J P, Hack C E, Eldering E. The functional integrity of the serpin domain of C1-inhibitor depends on the unique N-terminal domain, as revealed by a pathological mutant. J Biol Chem. 2003; 278 (32) 29463-29470
- 12 Huntington J A, Read R J, Carrell R W. Structure of a serpin-protease complex shows inhibition by deformation. Nature. 2000; 407 (6806) 923-926
- 13 Schapira M, de Agostini A, Colman R W. C1 inhibitor: the predominant inhibitor of plasma kallikrein. Methods Enzymol. 1988; 163 179-185
- 14 Ravindran S, Grys T E, Welch R A, Schapira M, Patston P A. Inhibition of plasma kallikrein by C1-inhibitor: role of endothelial cells and the amino-terminal domain of C1-inhibitor. Thromb Haemost. 2004; 92 (6) 1277-1283
- 15 Minta J O. The role of sialic acid in the functional activity and the hepatic clearance of C1-INH. J Immunol. 1981; 126 (1) 245-249
- 16 Reboul A, Prandini M H, Colomb M G. Proteolysis and deglycosylation of human C1 inhibitor. Effect on functional properties. Biochem J. 1987; 244 (1) 117-121
- 17 van Doorn M B, Burggraaf J, van Dam T et al.. A phase I study of recombinant human C1 inhibitor in asymptomatic patients with hereditary angioedema. J Allergy Clin Immunol. 2005; 116 (4) 876-883
- 18 Bos I G, de Bruin E C, Karuntu Y A, Modderman P W, Eldering E, Hack C E. Recombinant human C1-inhibitor produced in Pichia pastoris has the same inhibitory capacity as plasma C1-inhibitor. Biochim Biophys Acta. 2003; 1648 (1–2) 75-83
- 19 Bensa J C, Reboul A, Colomb M G. Biosynthesis in vitro of complement subcomponents C1q, C1s and C1 inhibitor by resting and stimulated human monocytes. Biochem J. 1983; 216 (2) 385-392
- 20 Yeung Laiwah A C, Jones L, Hamilton A O, Whaley K. Complement-subcomponent-C1-inhibitor synthesis by human monocytes. Biochem J. 1985; 226 (1) 199-205
- 21 Katz Y, Strunk R C. Synthesis and regulation of C1 inhibitor in human skin fibroblasts. J Immunol. 1989; 142 (6) 2041-2045
- 22 Katz Y, Gur S, Aladjem M, Strunk R C. Synthesis of complement proteins in amnion. J Clin Endocrinol Metab. 1995; 80 (7) 2027-2032
- 23 Walker D G, Yasuhara O, Patston P A, McGeer E G, McGeer P L. Complement C1 inhibitor is produced by brain tissue and is cleaved in Alzheimer disease. Brain Res. 1995; 675 (1–2) 75-82
- 24 Lotz M, Zuraw B L. Interferon-gamma is a major regulator of C1-inhibitor synthesis by human blood monocytes. J Immunol. 1987; 139 (10) 3382-3387
- 25 Zuraw B L, Lotz M. Regulation of the hepatic synthesis of C1 inhibitor by the hepatocyte stimulating factors interleukin 6 and interferon gamma. J Biol Chem. 1990; 265 (21) 12664-12670
- 26 Schmidt B, Gyapay G, Válay M, Füst G. Human recombinant macrophage colony-stimulating factor (M-CSF) increases Cl-esterase inhibitor (Cl-INH) synthesis by human monocytes. Immunology. 1991; 74 (4) 677-679
- 27 Heda G D, Mardente S, Weiner L, Schmaier A H. Interferon γ increases in vitro and in vivo expression of C1 inhibitor. Blood. 1990; 75 (12) 2401-2407
- 28 Heda G D, Kehoe K J, Mahdi F, Schmaier A H. Phosphatase 2A participates in interferon-γ's induced upregulation of C1 inhibitor mRNA expression. Blood. 1996; 87 (7) 2831-2838
- 29 Zahedi K, Prada A E, Prada J A, Davis III A E. Characterization of the IFN-γ-responsive element in the 5′ flanking region of the C1 inhibitor gene. J Immunol. 1997; 159 (12) 6091-6096
- 30 Schmaier A H, Amenta S, Xiong T, Heda G D, Gewirtz A M. Expression of platelet C1 inhibitor. Blood. 1993; 82 (2) 465-474
- 31 Woo P, Lachmann P JL, Harrison R A, Amos N, Cooper C, Rosen F S. Simultaneous turnover of normal and dysfunctional C1 inhibitor as a probe of in vivo activation of C1 and contact activatable proteases. Clin Exp Immunol. 1985; 61 (1) 1-8
- 32 Quastel M, Harrison R, Cicardi M, Alper C A, Rosen F S. Behavior in vivo of normal and dysfunctional C1 inhibitor in normal subjects and patients with hereditary angioneurotic edema. J Clin Invest. 1983; 71 (4) 1041-1046
- 33 de Smet BJGL, de Boer J P, Agterberg J, Rigter G, Bleeker W K, Hack C E. Clearance of human native, proteinase-complexed, and proteolytically inactivated C1-inhibitor in rats. Blood. 1993; 81 (1) 56-61
- 34 Pappalardo E, Zingale L C, Cicardi M. C1 inhibitor gene expression in patients with hereditary angioedema: quantitative evaluation by means of real-time RT-PCR. J Allergy Clin Immunol. 2004; 114 (3) 638-644
- 35 Wuillemin W A, Bleeker W K, Agterberg J, Rigter G, ten Cate H, Hack C E. Clearance of human factor XIa-inhibitor complexes in rats. Br J Haematol. 1996; 93 (4) 950-954
- 36 Nuijens J H, Huijbregts C C, Eerenberg-Belmer A JM et al.. Quantification of plasma factor XIIa-Cl(-)-inhibitor and kallikrein-Cl(-)-inhibitor complexes in sepsis. Blood. 1988; 72 (6) 1841-1848
- 37 Perlmutter D H, Glover G I, Rivetna M, Schasteen C S, Fallon R J. Identification of a serpin-enzyme complex receptor on human hepatoma cells and human monocytes. Proc Natl Acad Sci U S A. 1990; 87 (10) 3753-3757
- 38 Pizzo S V, Mast A E, Feldman S R, Salvesen G. In vivo catabolism of α 1-antichymotrypsin is mediated by the Serpin receptor which binds α 1-proteinase inhibitor, antithrombin III and heparin cofactor II. Biochim Biophys Acta. 1988; 967 (2) 158-162
- 39 Kalter E S, Daha M R, ten Cate J W, Verhoef J, Bouma B N. Activation and inhibition of Hageman factor-dependent pathways and the complement system in uncomplicated bacteremia or bacterial shock. J Infect Dis. 1985; 151 (6) 1019-1027
- 40 Falus A, Rokita H, Walcz E, Brozik M, Hidvégi T, Merétey K. Hormonal regulation of complement biosynthesis in human cell lines—II. Upregulation of the biosynthesis of complement components C3, factor B and C1 inhibitor by interleukin-6 and interleukin-1 in human hepatoma cell line. Mol Immunol. 1990; 27 (2) 197-201
- 41 Brower M S, Harpel P C. Proteolytic cleavage and inactivation of α 2-plasmin inhibitor and C1 inactivator by human polymorphonuclear leukocyte elastase. J Biol Chem. 1982; 257 (16) 9849-9854
- 42 Eldering E, Huijbregts C CM, Nuijens J H, Verhoeven A J, Hack C E. Recombinant C1 inhibitor P5/P3 variants display resistance to catalytic inactivation by stimulated neutrophils. J Clin Invest. 1993; 91 (3) 1035-1043
- 43 Leid R W, Ballieux BEPB, van der Heijden I et al.. Cleavage and inactivation of human C1 inhibitor by the human leukocyte proteinase, proteinase 3. Eur J Immunol. 1993; 23 (11) 2939-2944
- 44 Wallace E M, Perkins S J, Sim R B, Willis A C, Feighery C, Jackson J. Degradation of C1-inhibitor by plasmin: implications for the control of inflammatory processes. Mol Med. 1997; 3 (6) 385-396
- 45 Catanese J, Kress L F. Enzymatic inactivation of human plasma C1-inhibitor and α 1-antichymotrypsin by Pseudomonas aeruginosa proteinase and elastase. Biochim Biophys Acta. 1984; 789 (1) 37-43
- 46 Zhang F, Bries A D, Lang S C et al.. Metabolic alteration of the N-glycan structure of a protein from patients with a heterozygous protein deficiency. Biochim Biophys Acta. 2004; 1739 (1) 43-49
- 47 Doekes G, van Es L A, Daha M R. C1- inactivator: its efficiency as a regulator of classical complement pathway activation by soluble IgG aggregates. Immunology. 1983; 49 (2) 215-222
- 48 Tenner A J, Frank M M. Activator-bound C1 is less susceptible to inactivation by C1 inhibition than is fluid-phase C1. J Immunol. 1986; 137 (2) 625-630
- 49 Turner M W. Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol Today. 1996; 17 (11) 532-540
- 50 Thiel S, Vorup-Jensen T, Stover C M et al.. A second serine protease associated with mannan-binding lectin that activates complement. Nature. 1997; 386 (6624) 506-510
- 51 Matsushita M, Fujita T. Activation of the classical complement pathway by mannose-binding protein in association with a novel C1s-like serine protease. J Exp Med. 1992; 176 (6) 1497-1502
- 52 Matsushita M, Thiel S, Jensenius J C, Terai I, Fujita T. Proteolytic activities of two types of mannose-binding lectin-associated serine protease. J Immunol. 2000; 165 (5) 2637-2642
- 53 Makrides S C. Therapeutic inhibition of the complement system. Pharmacol Rev. 1998; 50 (1) 59-87
- 54 Podack E R, Kolb W P, Müller-Eberhard H J. The SC5b-7 complex: formation, isolation, properties, and subunit composition. J Immunol. 1977; 119 (6) 2024-2029
- 55 Tschopp J, Müller-Eberhard H J, Podack E R. Formation of transmembrane tubules by spontaneous polymerization of the hydrophilic complement protein C9. Nature. 1982; 298 (5874) 534-538
- 56 Hugli T E, Müller-Eberhard H J. Anaphylatoxins: C3a and C5a. Adv Immunol. 1978; 26 1-53
- 57 Morgan E L. Modulation of the immune response by anaphylatoxins. Complement. 1986; 3 (3) 128-136
- 58 Hartmann K, Henz B M, Krüger-Krasagakes S et al.. C3a and C5a stimulate chemotaxis of human mast cells. Blood. 1997; 89 (8) 2863-2870
- 59 Gerard C, Gerard N P. C5A anaphylatoxin and its seven transmembrane-segment receptor. Annu Rev Immunol. 1994; 12 775-808
- 60 Sim R B, Reboul A, Arlaud G J, Villiers C L, Colomb M G. Interaction of 125I-labelled complement subcomponents C-1r and C-1s with protease inhibitors in plasma. FEBS Lett. 1979; 97 (1) 111-115
- 61 Liszewski M K, Farries T C, Lublin D M, Rooney I A, Atkinson J P. Control of the complement system. Adv Immunol. 1996; 61 201-283
- 62 Bianchino A C, Poon P H, Schumaker V N. A mechanism for the spontaneous activation of the first component of complement, C1, and its regulation by C1-inhibitor. J Immunol. 1988; 141 (11) 3930-3936
- 63 Harpel P C, Cooper N R. Studies on human plasma C1 inactivator-enzyme interactions. I. Mechanisms of interaction with C1s, plasmin, and trypsin. J Clin Invest. 1975; 55 (3) 593-604
- 64 Reboul A, Arlaud G J, Sim R B, Colomb M G. A simplified procedure for the purification of C1-inactivator from human plasma. Interaction with complement subcomponents C1r and C1s. FEBS Lett. 1977; 79 (1) 45-50
- 65 Salvesen G S, Catanese J J, Kress L F, Travis J. Primary structure of the reactive site of human C1-inhibitor. J Biol Chem. 1985; 260 (4) 2432-2436
- 66 Arlaud G J, Reboul A, Sim R B, Colomb M G. Interaction of C1-inhibitor with the C1r and C1s subcomponents in human C1. Biochim Biophys Acta. 1979; 576 (1) 151-162
- 67 Ziccardi R J, Cooper N R. Active disassembly of the first complement component, C-1, by C-1 inactivator. J Immunol. 1979; 123 (2) 788-792
- 68 Chesne S, Villiers C L, Arlaud G J, Lacroix M B, Colomb M G. Fluid-phase interaction of C1 inhibitor (C1 Inh) and the subcomponents C1r and C1s of the first component of complement, C1. Biochem J. 1982; 201 (1) 61-70
- 69 Sim R B, Arlaud G J, Colomb M G. Kinetics of reaction of human C1-inhibitor with the human complement system proteases C1r and C1s. Biochim Biophys Acta. 1980; 612 (2) 433-449
- 70 Jiang H, Wagner E, Zhang H, Frank M M. Complement 1 inhibitor is a regulator of the alternative complement pathway. J Exp Med. 2001; 194 (11) 1609-1616
- 71 Kaplan A P, Silverberg M. The coagulation-kinin pathway of human plasma. Blood. 1987; 70 (1) 1-15
- 72 Colman R W. Surface-mediated defense reactions. The plasma contact activation system. J Clin Invest. 1984; 73 (5) 1249-1253
- 73 Cochrane C G, Griffin J H. The biochemistry and pathophysiology of the contact system of plasma. Adv Immunol. 1982; 33 241-306
- 74 Hojima Y, Cochrane C G, Wiggins R C, Austen K F, Stevens R L. In vitro activation of the contact (Hageman factor) system of plasma by heparin and chondroitin sulfate E. Blood. 1984; 63 (6) 1453-1459
- 75 Kannemeier C, Shibamiya A, Nakazawa F et al.. Extracellular RNA constitutes a natural procoagulant cofactor in blood coagulation. Proc Natl Acad Sci U S A. 2007; 104 (15) 6388-6393
- 76 Maas C, Govers-Riemslag J W, Bouma B et al.. Misfolded proteins activate factor XII in humans, leading to kallikrein formation without initiating coagulation. J Clin Invest. 2008; 118 (9) 3208-3218
- 77 Müller F, Mutch N J, Schenk W A et al.. Platelet polyphosphates are proinflammatory and procoagulant mediators in vivo. Cell. 2009; 139 (6) 1143-1156
- 78 Herwald H, Mörgelin M, Olsén A et al.. Activation of the contact-phase system on bacterial surfaces—a clue to serious complications in infectious diseases. Nat Med. 1998; 4 (3) 298-302
- 79 Colman R W, Bagdasarian A, Talamo R C et al.. Williams trait. Human kininogen deficiency with diminished levels of plasminogen proactivator and prekallikrein associated with abnormalities of the Hageman factor-dependent pathways. J Clin Invest. 1975; 56 (6) 1650-1662
- 80 Ghebrehiwet B, Randazzo B P, Dunn J T, Silverberg M, Kaplan A P. Mechanisms of activation of the classical pathway of complement by Hageman factor fragment. J Clin Invest. 1983; 71 (5) 1450-1456
- 81 Schousboe I. Binding of activated factor XII to endothelial cells affects its inactivation by the C1-esterase inhibitor. Eur J Biochem. 2003; 270 (1) 111-118
- 82 Lämmle B, Wuillemin W A, Huber I et al.. Thromboembolism and bleeding tendency in congenital factor XII deficiency—a study on 74 subjects from 14 Swiss families. Thromb Haemost. 1991; 65 (2) 117-121
- 83 Pixley R A, De La Cadena R, Page J D et al.. The contact system contributes to hypotension but not disseminated intravascular coagulation in lethal bacteremia. In vivo use of a monoclonal anti-factor XII antibody to block contact activation in baboons. J Clin Invest. 1993; 91 (1) 61-68
- 84 Gailani D, Broze Jr G J. Factor XI activation in a revised model of blood coagulation. Science. 1991; 253 (5022) 909-912
- 85 Naito K, Fujikawa K. Activation of human blood coagulation factor XI independent of factor XII. Factor XI is activated by thrombin and factor XIa in the presence of negatively charged surfaces. J Biol Chem. 1991; 266 (12) 7353-7358
- 86 Renné T, Pozgajová M, Grüner S et al.. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med. 2005; 202 (2) 271-281
- 87 Wuillemin W A, Minnema M, Meijers J C et al.. Inactivation of factor XIa in human plasma assessed by measuring factor XIa-protease inhibitor complexes: major role for C1-inhibitor. Blood. 1995; 85 (6) 1517-1526
- 88 Wuillemin W A, Hack C E, Bleeker W K, Biemond B J, Levi M, ten Cate H. Inactivation of factor Xia in vivo: studies in chimpanzees and in humans. Thromb Haemost. 1996; 76 (4) 549-555
- 89 Nielsen E W, Morrissey J, Olsen J O, Osterud B. Factor VIIa in patients with C1-inhibitor deficiency. Thromb Haemost. 1995; 74 (4) 1103-1106
- 90 Nielsen E W, Johansen H T, Høgåsen K, Wuillemin W A, Hack C E, Mollnes T E. Activation of the complement, coagulation, fibrinolytic and kallikrein-kinin systems during attacks of hereditary angioedema. Scand J Immunol. 1996; 44 (2) 185-192
- 91 Husain S S, Hasan A AK, Budzynski A Z. Differences between binding of one-chain and two-chain tissue plasminogen activators to non-cross-linked and cross-linked fibrin clots. Blood. 1989; 74 (3) 999-1006
- 92 Vassalli J D, Sappino A P, Belin D. The plasminogen activator/plasmin system. J Clin Invest. 1991; 88 (4) 1067-1072
- 93 Zamarron C, Lijnen H R, Van Hoef B, Collen D. Biological and thrombolytic properties of proenzyme and active forms of human urokinase—I. Fibrinolytic and fibrinogenolytic properties in human plasma in vitro of urokinases obtained from human urine or by recombinant DNA technology. Thromb Haemost. 1984; 52 (1) 19-23
- 94 Schmaier A H. Contact activation: a revision. Thromb Haemost. 1997; 78 (1) 101-107
- 95 Schousboe I. Factor XIIa activation of plasminogen is enhanced by contact activating surfaces and Zn2+. Blood Coagul Fibrinolysis. 1997; 8 (2) 97-104
- 96 Levi M, Hack C E, de Boer J P, Brandjes D P, Büller H R, ten Cate J W. Reduction of contact activation related fibrinolytic activity in factor XII deficient patients. Further evidence for the role of the contact system in fibrinolysis in vivo. J Clin Invest. 1991; 88 (4) 1155-1160
- 97 Zeerleder S, Schloesser M, Redondo M et al.. Reevaluation of the incidence of thromboembolic complications in congenital factor XII deficiency—a study on 73 subjects from 14 Swiss families. Thromb Haemost. 1999; 82 (4) 1240-1246
- 98 Huisman L GM, van Griensven J MT, Kluft C. On the role of C1-inhibitor as inhibitor of tissue-type plasminogen activator in human plasma. Thromb Haemost. 1995; 73 (3) 466-471
- 99 Levi M, Roem D, Kamp A M, de Boer J P, Hack C E, ten Cate J W. Assessment of the relative contribution of different protease inhibitors to the inhibition of plasmin in vivo. Thromb Haemost. 1993; 69 (2) 141-146
- 100 Römisch J, Feussner A, Vermöhlen S, Stöhr H A. A protease isolated from human plasma activating factor VII independent of tissue factor. Blood Coagul Fibrinolysis. 1999; 10 (8) 471-479
- 101 Römisch J, Vermöhlen S, Feussner A, Stöhr H. The FVII activating protease cleaves single-chain plasminogen activators. Haemostasis. 1999; 29 (5) 292-299
- 102 Etscheid M, Hunfeld A, König H, Seitz R, Dodt J. Activation of proPHBSP, the zymogen of a plasma hyaluronan binding serine protease, by an intermolecular autocatalytic mechanism. Biol Chem. 2000; 381 (12) 1223-1231
- 103 Muhl L, Galuska S P, Oörni K et al.. High negative charge-to-size ratio in polyphosphates and heparin regulates factor VII-activating protease. FEBS J. 2009; 276 (17) 4828-4839
- 104 Nakazawa F, Kannemeier C, Shibamiya A et al.. Extracellular RNA is a natural cofactor for the (auto-)activation of factor VII-activating protease (FSAP). Biochem J. 2005; 385 (Pt 3) 831-838
- 105 Yamamichi S, Nishitani M, Nishimura N, Matsushita Y, Hasumi K. Polyamine-promoted autoactivation of plasma hyaluronan-binding protein. J Thromb Haemost. 2010; 8 (3) 559-566
- 106 Kannemeier C, Feussner A, Stöhr H A, Weisse J, Preissner K T, Römisch J. Factor VII and single-chain plasminogen activator-activating protease: activation and autoactivation of the proenzyme. Eur J Biochem. 2001; 268 (13) 3789-3796
- 107 Etscheid M, Beer N, Fink E, Seitz R, Johannes D. The hyaluronan-binding serine protease from human plasma cleaves HMW and LMW kininogen and releases bradykinin. Biol Chem. 2002; 383 (10) 1633-1643
- 108 Zeerleder S, Zwart B, te Velthuis H et al.. A plasma nucleosome releasing factor (NRF) with serine protease activity is instrumental in removal of nucleosomes from secondary necrotic cells. FEBS Lett. 2007; 581 (28) 5382-5388
- 109 Zeerleder S, Zwart B, te Velthuis H et al.. Nucleosome-releasing factor: a new role for factor VII-activating protease (FSAP). FASEB J. 2008; 22 (12) 4077-4084
- 110 Kannemeier C, Al-Fakhri N, Preissner K T, Kanse S M. Factor VII-activating protease (FSAP) inhibits growth factor-mediated cell proliferation and migration of vascular smooth muscle cells. FASEB J. 2004; 18 (6) 728-730
- 111 Sedding D, Daniel J M, Muhl L et al.. The G534E polymorphism of the gene encoding the factor VII-activating protease is associated with cardiovascular risk due to increased neointima formation. J Exp Med. 2006; 203 (13) 2801-2807
- 112 Choi-Miura N H, Takahashi K, Yoda M, Saito K, Mazda T, Tomita M. Proteolytic activation and inactivation of the serine protease activity of plasma hyaluronan binding protein. Biol Pharm Bull. 2001; 24 (5) 448-452
- 113 Potempa J, Korzus E, Travis J. The serpin superfamily of proteinase inhibitors: structure, function, and regulation. J Biol Chem. 1994; 269 (23) 15957-15960
- 114 Caughman G B, Boackle R J, Vesely J. A postulated mechanism for heparin's potentiation of C1 inhibitor function. Mol Immunol. 1982; 19 (2) 287-295
- 115 Lennick M, Brew S A, Ingham K C. Kinetics of interaction of C1 inhibitor with complement C1s. Biochemistry. 1986; 25 (13) 3890-3898
- 116 Nilsson T, Wiman B. Kinetics of the reaction between human C1-esterase inhibitor and C1r or C1s. Eur J Biochem. 1983; 129 (3) 663-667
- 117 Pixley R A, Schmaier A, Colman R W. Effect of negatively charged activating compounds on inactivation of factor XIIa by Cl inhibitor. Arch Biochem Biophys. 1987; 256 (2) 490-498
- 118 Rent R, Myhrman R, Fiedel B A, Gewurz H. Potentiation of C1 esterase inhibitor activity by heparin. Clin Exp Immunol. 1976; 23 264-271
- 119 Wuillemin W A, te Velthuis H, Lubbers Y T, de Ruig C P, Eldering E, Hack C E. Potentiation of C1 inhibitor by glycosaminoglycans: dextran sulfate species are effective inhibitors of in vitro complement activation in plasma. J Immunol. 1997; 159 (4) 1953-1960
- 120 Bos I G, van Mierlo G J, Bleeker W K et al.. The potentiation of human C1-inhibitor by dextran sulphate is transient in vivo: studies in a rat model. Int Immunopharmacol. 2001; 1 (8) 1583-1595
- 121 Caldwell E E, Andreasen A M, Blietz M A et al.. Heparin binding and augmentation of C1 inhibitor activity. Arch Biochem Biophys. 1999; 361 (2) 215-222
- 122 Wuillemin W A, Eldering E, Citarella F, de Ruig C P, ten Cate H, Hack C E. Modulation of contact system proteases by glycosaminoglycans. Selective enhancement of the inhibition of factor XIa. J Biol Chem. 1996; 271 (22) 12913-12918
- 123 Mauron T, Lämmle B, Wuillemin W A. Influence of low molecular weight heparin and low molecular weight dextran sulfate on the inhibition of coagulation factor XIa by serpins. Thromb Haemost. 1998; 80 (1) 82-86
- 124 Zeerleder S, Caliezi C, van Mierlo G et al.. Administration of C1 inhibitor reduces neutrophil activation in patients with sepsis. Clin Diagn Lab Immunol. 2003; 10 (4) 529-535
- 125 Jansen P M, Eisele B, de Jong I W et al.. Effect of C1 inhibitor on inflammatory and physiologic response patterns in primates suffering from lethal septic shock. J Immunol. 1998; 160 (1) 475-484
- 126 Caliezi C, Zeerleder S, Redondo M et al.. C1-inhibitor in patients with severe sepsis and septic shock: beneficial effect on renal dysfunction. Crit Care Med. 2002; 30 (8) 1722-1728
- 127 Cai S, Dole V S, Bergmeier W et al.. A direct role for C1 inhibitor in regulation of leukocyte adhesion. J Immunol. 2005; 174 (10) 6462-6466
- 128 Liu D, Cai S, Gu X, Scafidi J, Wu X, Davis III A E. C1 inhibitor prevents endotoxin shock via a direct interaction with lipopolysaccharide. J Immunol. 2003; 171 (5) 2594-2601
- 129 Liu D, Lu F, Qin G, Fernandes S M, Li J, Davis III A E. C1 inhibitor-mediated protection from sepsis. J Immunol. 2007; 179 (6) 3966-3972
- 130 Zhang H, Li J, Barrington R A, Liang G, Qin G, Liu D X. An anti-endotoxin peptide that generates from the amino-terminal domain of complement regulatory protein C1 inhibitor. Biochem Biophys Res Commun. 2007; 359 (2) 285-291
- 131 Liu D, Gu X, Scafidi J, Davis III A E. N-linked glycosylation is required for c1 inhibitor-mediated protection from endotoxin shock in mice. Infect Immun. 2004; 72 (4) 1946-1955
- 132 Liu D, Cramer C C, Scafidi J, Davis III A E. N-linked glycosylation at Asn3 and the positively charged residues within the amino-terminal domain of the c1 inhibitor are required for interaction of the C1 Inhibitor with Salmonella enterica serovar typhimurium lipopolysaccharide and lipid A. Infect Immun. 2005; 73 (8) 4478-4487
- 133 Liu D, Zhang D, Scafidi J, Wu X, Cramer C C, Davis III A E. C1 inhibitor prevents gram-negative bacterial lipopolysaccharide-induced vascular permeability. Blood. 2005; 105 (6) 2350-2355
- 134 Horstick G, Heimann A, Götze O et al.. Intracoronary application of C1 esterase inhibitor improves cardiac function and reduces myocardial necrosis in an experimental model of ischemia and reperfusion. Circulation. 1997; 95 (3) 701-708
- 135 de Zwaan C, Kleine A H, Diris J H et al.. Continuous 48-h C1-inhibitor treatment, following reperfusion therapy, in patients with acute myocardial infarction. Eur Heart J. 2002; 23 (21) 1670-1677
- 136 Wouters D, Wagenaar-Bos I, van Ham M, Zeerleder S. C1 inhibitor: just a serine protease inhibitor? New and old considerations on therapeutic applications of C1 inhibitor. Expert Opin Biol Ther. 2008; 8 (8) 1225-1240
- 137 Cichon S, Martin L, Hennies H C et al.. Increased activity of coagulation factor XII (Hageman factor) causes hereditary angioedema type III. Am J Hum Genet. 2006; 79 (6) 1098-1104
- 138 Bork K, Schneiders V. Danazol-induced hepatocellular adenoma in patients with hereditary angio-oedema. J Hepatol. 2002; 36 (5) 707-709
- 139 Cugno M, Nuijens J, Hack E et al.. Plasma levels of C1-inhibitor complexes and cleaved C1-inhibitor in patients with hereditary angioneurotic edema. J Clin Invest. 1990; 85 (4) 1215-1220
- 140 Davis III A E. The pathophysiology of hereditary angioedema. Clin Immunol. 2005; 114 (1) 3-9
- 141 Noga O, Brunnée T, Schäper C, Kunkel G. Heparin, derived from the mast cells of human lungs, is responsible for the generation of kinins in allergic reactions due to the activation of the contact system. Int Arch Allergy Immunol. 1999; 120 (4) 310-316
- 142 Brunnée T, Reddigari S R, Shibayama Y, Kaplan A P, Silverberg M. Mast cell derived heparin activates the contact system: a link to kinin generation in allergic reactions. Clin Exp Allergy. 1997; 27 (6) 653-663
- 143 Iwaki T, Castellino F J. Plasma levels of bradykinin are suppressed in factor XII-deficient mice. Thromb Haemost. 2006; 95 (6) 1003-1010
- 144 Shariat-Madar Z, Mahdi F, Schmaier A H. Identification and characterization of prolylcarboxypeptidase as an endothelial cell prekallikrein activator. J Biol Chem. 2002; 277 (20) 17962-17969
- 145 Bork K, Siedlecki K, Bosch S, Schopf R E, Kreuz W. Asphyxiation by laryngeal edema in patients with hereditary angioedema. Mayo Clin Proc. 2000; 75 (4) 349-354
- 146 Bork K, Barnstedt S E. Treatment of 193 episodes of laryngeal edema with C1 inhibitor concentrate in patients with hereditary angioedema. Arch Intern Med. 2001; 161 (5) 714-718
- 147 Bork K, Meng G, Staubach P, Hardt J. Hereditary angioedema: new findings concerning symptoms, affected organs, and course. Am J Med. 2006; 119 (3) 267-274
- 148 Castro-Magana M, Cheruvanky T, Collipp P J, Ghavami-Maibodi Z, Angulo M, Stewart C. Transient adrenogenital syndrome due to exposure to danazol in utero. Am J Dis Child. 1981; 135 (11) 1032-1034
- 149 Agostoni A, Bergamaschini L, Martignoni G, Cicardi M, Marasini B. Treatment of acute attacks of hereditary angioedema with C1-inhibitor concentrate. Ann Allergy. 1980; 44 (5) 299-301
- 150 Agostoni A, Cicardi M. Hereditary and acquired C1-inhibitor deficiency: biological and clinical characteristics in 235 patients. Medicine (Baltimore). 1992; 71 (4) 206-215
- 151 Bork K, Witzke G. Long-term prophylaxis with C1-inhibitor (C1 INH) concentrate in patients with recurrent angioedema caused by hereditary and acquired C1-inhibitor deficiency. J Allergy Clin Immunol. 1989; 83 (3) 677-682
- 152 Cicardi M, Bergamaschini L, Marasini B, Boccassini G, Tucci A, Agostoni A. Hereditary angioedema: an appraisal of 104 cases. Am J Med Sci. 1982; 284 (1) 2-9
- 153 Waytes A T, Rosen F S, Frank M M. Treatment of hereditary angioedema with a vapor-heated C1 inhibitor concentrate. N Engl J Med. 1996; 334 (25) 1630-1634
- 154 Prematta M, Gibbs J G, Pratt E L, Stoughton T R, Craig T J. Fresh frozen plasma for the treatment of hereditary angioedema. Ann Allergy Asthma Immunol. 2007; 98 (4) 383-388
- 155 Bork K, Frank J, Grundt B, Schlattmann P, Nussberger J, Kreuz W. Treatment of acute edema attacks in hereditary angioedema with a bradykinin receptor-2 antagonist (Icatibant). J Allergy Clin Immunol. 2007; 119 (6) 1497-1503
- 156 Kunschak M, Engl W, Maritsch F et al.. A randomized, controlled trial to study the efficacy and safety of C1 inhibitor concentrate in treating hereditary angioedema. Transfusion. 1998; 38 (6) 540-549
- 157 Bork K, Meng G, Staubach P, Hardt J. Treatment with C1 inhibitor concentrate in abdominal pain attacks of patients with hereditary angioedema. Transfusion. 2005; 45 (11) 1774-1784
- 158 Zuraw B L, Busse P J, White M et al.. Nanofiltered C1 inhibitor concentrate for treatment of hereditary angioedema. N Engl J Med. 2010; 363 (6) 513-522
- 159 Craig T J, Levy R J, Wasserman R L et al.. Efficacy of human C1 esterase inhibitor concentrate compared with placebo in acute hereditary angioedema attacks. J Allergy Clin Immunol. 2009; 124 (4) 801-808
- 160 Choi G, Soeters M R, Farkas H et al.. Recombinant human C1-inhibitor in the treatment of acute angioedema attacks. Transfusion. 2007; 47 (6) 1028-1032
- 161 Zuraw B, Cicardi M, Levy R J, Nuijens J H et al.. Recombinant human C1-inhibitor for the treatment of acute angioedema attacks in patients with hereditary angioedema. J Allergy Clin Immunol. 2010; 126 (4) 821-827
Sacha ZeerlederM.D. Ph.D.
Department of Immunopathology, Sanquin Research, Plesmanlaan 125
1066 CX Amsterdam, The Netherlands
Email: s.zeerleder@sanquin.nl