The dual role of the contact system in bacterial infectious disease

Summary

Hemostasis is a sensitive and tightly regulated process, involving the vascular endothelium and blood cells as well as factors of the coagulation and fibrinolytic cascades. Over the last four decades evidence has accumulated that during infection, inflammatory mediators from the microbe and/or host are capable to modulate the equilibrium between the procoagulant and anticoagulant status of the host. Dependent on the mode of activation, these changes can cause either local or systemic inflammatory reactions that may be beneficial or deleterious to the human host. The present review aims to present the state of the art with respect to the role of the contact system (also known as the intrinsic pathway of coagulation or the kallikrein/kinin system) in innate immunity and systemic inflammatory reactions.

Keywords

Coagulation - contact system - inflammation - infectious diseases - innate immunity

• References

• 1 Roberts HR. Oscar Ratnoff: his contributions to the golden era of coagulation research. Br J Haematol 2003; 122: 180-192.
• 2 Peerschke EI, Petrovan RJ, Ghebrehiwet B. et al. Tissue factor pathway inhibitor-2 (TFPI-2) recognizes the complement and kininogen binding protein gC1qR/p33 (gC1qR): implications for vascular inflammation. Thromb Haemost 2004; 92: 811-819.
• 3 Bhoola KD, Figueroa CD, Worthy K. Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol Rev 1992; 44: 1-80.
• 4 Colman RW, Schmaier AH. Contact system: a vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes. Blood 1997; 90: 3819-3843.
• 5 Renné T, Pozgajová M, Grüner S. et al. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med 2005; 202: 271-281.
• 6 Iwaki T, Castellino FJ. Plasma levels of bradykinin are suppressed in factor XII-deficient mice. Thromb Haemost 2006; 95: 1003-1010.
• 7 Bolton-Maggs PH. Factor XI deficiency and its management. Haemophilia 2000; 6 (Suppl. 01) 100-109.
• 8 Campbell DJ. The kallikrein-kinin system in humans. Clin Exp Pharmacol Physiol 2001; 28: 1060-1065.
• 9 Mahabeer R, Bhoola KD. Kallikrein and kinin receptor genes. Pharmacol Ther 2000; 88: 77-89.
• 10 Leeb-Lundberg LM, Marceau F, Müller-Esterl W. et al. International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol Rev 2005; 57: 27-77.
• 11 Marceau F, Sabourin T, Houle S. et al. Kinin receptors: functional aspects. Int Immunopharmacol 2002; 13–14: 1729-1739.
• 12 Hecquet C, Tan F, Marcic BM. et al. Human bradykinin B(2) receptor is activated by kallikrein and other serine proteases. Mol Pharmacol 2000; 58: 828-836.
• 13 Marceau F, Houle S, Molinaro G. et al. Does the bradykinin B2 receptor function as a protease-activated receptor?. Hypertension 2003; 42: E1-E2.
• 14 Blais Jr., C, Marceau F, Rouleau JL. et al. The kallikrein- kininogen-kinin system: lessons from the quantification of endogenous kinins. Peptides 2000; 21: 1903-1940.
• 15 Kahn R, Herwald H, Müller-Esterl W. et al. Contact- system activation in children with vasculitis. Lancet 2002; 360: 535-541.
• 16 Cassim B, Mody G, Bhoola K. Kallikrein cascade and cytokines in inflamed joints. Pharmacol Ther 2002; 94: 1-34.
• 17 Zasloff M. Antimicrobial peptides of multicellular organisms. Nature 2002; 415: 389-395.
• 18 Bevins CL. Antimicrobial peptides as effector molecules of mammalian host defense. Contrib Microbiol 2003; 10: 106-148.
• 19 Boman HG. Antibacterial peptides: basic facts and emerging concepts. J Intern Med 2003; 254: 197-215.
• 20 Peschel A, Sahl HG. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat Rev Microbiol 2006; 4: 529-536.
• 21 Opal SM, Esmon CT. Bench-to-bedside review: Functional relationships between coagulation and the innate immune response and their respective roles in the pathogenesis of sepsis. Crit Care 2003; 7: 23-38.
• 22 Frick IM, Åkesson P, Herwald H. et al. The contact system--a novel branch of innate immunity generating antibacterial peptides. Embo J 2006; 25: 5569-5578.
• 23 Andersson E, Rydengård V, Sonesson A. et al. Antimicrobial activities of heparin-binding peptides. Eur J Biochem 2004; 271: 1219-1226.
• 24 Nordahl EA, Rydengård V, Mörgelin M. et al. Domain 5 of high molecular weight kininogen is antibacterial. J Biol Chem 2005; 280: 34832-34839.
• 25 Kowalska K, Carr DB, Lipkowski AW. Direct antimicrobial properties of substance P. Life Sci 2002; 71: 747-750.
• 26 Sato E, Koyama S, Nomura H. et al. Bradykinin stimulates alveolar macrophages to release neutrophil, monocyte, and eosinophil chemotactic activity. J Immunol 1996; 157: 3122-3129.
• 27 Paegelow I, Trzeczak S, Bockmann S. et al. Migratory responses of polymorphonuclear leukocytes to kinin peptides. Pharmacology 2002; 66: 153-161.
• 28 Araújo RC, Kettritz R, Fichtner I. et al. Altered neutrophil homeostasis in kinin B1 receptor-deficient mice. Biol Chem 2001; 382: 91-95.
• 29 Herwald H, Mörgelin M, Björck L. Contact activation by pathogenic bacteria: a virulence mechanism contributing to the pathophysiology of sepsis. Scand J Infect Dis 2003; 35: 604-607.
• 30 Kalter ES, van Dijk WC, Timmerman A. et al. Activation of purified human plasma prekallikrein triggered by cell wall fractions of Escherichia coli and Staphylococcus aureus . J Infect Dis 1983; 148: 682-691.
• 31 Ben Nasr AB, Herwald H, Müller-Esterl W. et al. Human kininogens interact with M protein, a bacterial surface protein and virulence determinant. Biochem J 1995; 305: 173-180.
• 32 Ben Nasr AB, Olsén A, Sjöbring U. et al. Assembly of human contact phase factors and release of bradykinin at the surface of curli-expressing Escherichia coli . Mol Microbiol 1996; 20: 927-935.
• 33 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: 298-302.
• 34 Persson K, Mörgelin M, Lindbom L. et al. Severe lung lesions caused by Salmonella are prevented by inhibition of the contact system. J Exp Med 2000; 192: 1415-1424.
• 35 Lottenberg R. Contact activation proteins and the bacterial surface. Trends Microbiol 1996; 4: 413-414.
• 36 Mason JW, Kleeberg U, Dolan P. et al. Plasma kallikrein and Hageman factor in Gram-negative bacteremia. Ann Intern Med 1970; 73: 545-551.
• 37 Pixley RA, Colman RW. The kallikrein-kinin system in sepsis syndrome. Handbook of Immunopharmacology – The Kinin System. New York:: Academic Press; 1997: 173-186.
• 38 Wuillemin WA, Fijnvandraat K, Derkx BH. et al. Activation of the intrinsic pathway of coagulation in children with meningococcal septic shock. Thromb Haemost 1995; 74: 1436-1441.
• 39 van Deuren M, Brandtzaeg P, van der Meer JW. Update on meningococcal disease with emphasis on pathogenesis and clinical management. Clin Microbiol Rev 2000; 13: 144-166.
• 40 Sriskandan S, Cohen J. Kallikrein-kinin system activation in streptococcal toxic shock syndrome. Clin Infect Dis 2000; 30: 961-962.
• 41 Pixley RA, De La Cadena R, Page JD. 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: 61-68.
• 42 Mattsson E, Herwald H, Cramer H. et al. Staphylococcus aureus induces release of bradykinin in human plasma. Infect Immun 2001; 69: 3877-3882.
• 43 Phagoo SB, Reddi K, Silvallana BJ. et al. Infectioninduced kinin B1 receptors in human pulmonary fibroblasts: role of intact pathogens and p38 mitogen-activated protein kinase-dependent signaling. J Pharmacol Exp Ther 2005; 313: 1231-1238.
• 44 Bengtson SH, Phagoo SB, Norrby-Teglund A. et al. Kinin receptor expression during Staphylococcus aureus infection. Blood 2006; 108: 2055-2063.
• 45 Bachar O, Adner M, Uddman R. et al. Toll-like receptor stimulation induces airway hyper-responsiveness to bradykinin, an effect mediated by JNK and NFkappa B signaling pathways. Eur J Immunol 2004; 34: 1196-1207.
• 46 Marceau F, Regoli D. Bradykinin receptor ligands: therapeutic perspectives. Nat Rev Drug Discov 2004; 3: 845-852.
• 47 Moreau ME, Garbacki N, Molinaro G. et al. The kallikrein-kinin system: current and future pharmacological targets. J Pharmacol Sci 2005; 99: 6-38.
• 48 Akbary AM, Wirth KJ, Schölkens BA. Efficacy and tolerability of Icatibant (Hoe 140) in patients with moderately severe chronic bronchial asthma. Immunopharmacology 1996; 33: 238-242.
• 49 Austin CE, Foreman JC. A study of the action of bradykinin and bradykinin analogues in the human nasal airway. J Physiol 1994; 478: 351-356.
• 50 Ueno A, Tokumasu T, Naraba H. et al. The mediators involved in endotoxin-induced vascular permeability increase in the rat skin and their interactions. Jpn J Pharmacol 1996; 70: 285-290.
• 51 Abraham WM, Scuri M, Farmer SG. Peptide and non-peptide bradykinin receptor antagonists: role in allergic airway disease. Eur J Pharmacol 2006; 533: 215-221.
• 52 Fein AM, Bernard GR, Criner GJ. et al. Treatment of severe systemic inflammatory response syndrome and sepsis with a novel bradykinin antagonist, deltibant (CP-0127). Results of a randomized, double-blind, placebo-controlled trial. CP-0127 SIRS and Sepsis Study Group. J Am Med Assoc 1997; 277: 482-487.
• 53 Campos MM, Leal PC, Yunes RA. et al. Non-peptide antagonists for kinin B1 receptors: new insights into their therapeutic potential for the management of inflammation and pain. Trends Pharmacol Sci 2006; 27: 646-651.
• 54 Wuillemin WA, Minnema M, Meijers JC. 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: 1517-1526.
• 55 Schapira M, de Agostini A, Colman RW. C1 inhibitor: the predominant inhibitor of plasma kallikrein. Methods Enzymol 1988; 163: 179-185.
• 56 Levy JH, O’Donnell PS. The therapeutic potential of a kallikrein inhibitor for treating hereditary angioedema. Expert Opin Investig Drugs 2006; 15: 1077-1090.
• 57 Nuijens JH, Eerenberg-Belmer AJ, Huijbregts CC. et al. Proteolytic inactivation of plasma C1– inhibitor in sepsis. J Clin Invest 1989; 84: 443-450.
• 58 Hack CE, Ogilvie AC, Eisele B. et al. C1-inhibitor substitution therapy in septic shock and in the vascular leak syndrome induced by high doses of interleukin-2. Intensive Care Med 1993; 19 (Suppl. 01) S19-28.
• 59 Caliezi C, Wuillemin WA, Zeerleder S. et al. C1-esterase inhibitor: An anti-inflammatory agent and its potential use in the treatment of diseases other than hereditary angioedema. Pharmacol Rev 2000; 52: 91-112.
• 60 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: 1722-1728.
• 61 Liu D, Zhang D, Scafidi J. et al. C1 inhibitor prevents Gram-negative bacterial lipopolysaccharide-induced vascular permeability. Blood 2005; 105: 2350-2355.
• 62 Scott CF, Whitaker EJ, Hammond BF. et al. Purification and characterization of a potent 70-kDa thiol lysyl-proteinase (Lys-gingivain) from Porphyromonas gingivalis that cleaves kininogens and fibrinogen. J Biol Chem 1993; 268: 7935-7942.
• 63 Imamura T, Tanase S, Szmyd G. et al. Induction of vascular leakage through release of bradykinin and a novel kinin by cysteine proteinases from Staphylococcus aureus . J Exp Med 2005; 201: 1669-1676.
• 64 Herwald H, Collin M, Müller-Esterl W. et al. Streptococcal cysteine proteinase releases kinins: a novel virulence mechanism. J Exp Med 1996; 184: 665-673.
• 65 Molla A, Yamamoto T, Akaike T. et al. Activation of Hageman factor and prekallikrein and generation of kinin by various microbial proteinases. J Biol Chem 1989; 264: 10589-10594.
• 66 Imamura T, Pike RN, Potempa J. et al. Pathogenesis of periodontitis: a major arginine-specific cysteine proteinase from Porphyromonas gingivalis induces vascular permeability enhancement through activation of the kallikrein/kinin pathway. J Clin Invest 1994; 94: 361-367.
• 67 Imamura T, Potempa J, Pike RN. et al. Dependence of vascular permeability enhancement on cysteine proteinases in vesicles of Porphyromonas gingivalis . Infect Immun 1995; 63: 1999-2003.
• 68 Sakata Y, Akaike T, Suga M. et al. Bradykinin generation triggered by Pseudomonas proteases facilitates invasion of the systemic circulation by Pseudomonas aeruginosa . Microbiol Immunol 1996; 40: 415-423.
• 69 Sakata Y, Akaike T, Khan MM. et al. Activation of bradykinin generating cascade by Vibrio cholerae protease. Immunopharmacology 1996; 33: 377-379.
• 70 Miyoshi S, Watanabe H, Kawase T. et al. Generation of active fragments from human zymogens in the bradykinin-generating cascade by extracellular proteases from Vibrio vulnificus and V. parahaemolyticus . Toxicon 2004; 44: 887-893.