Activation of the kallikrein-kinin system and release of new kinins through alternative cleavage of kininogens by microbial and human cell proteinases
-
Takahisa Imamura
Abstract
Kinins are released from kininogens through the activation of the Hageman factor-prekallikrein system or by tissue kallikrein. These peptides exert various biological activities, such as vascular permeability increase, smooth muscle contraction, pain sensation and induction of hypotension. In many instances kinins are thought to be involved in the pathophysiology of various diseases. Recent studies have revealed that microbial and human cell proteinases activate Hageman factor and/or prekallikrein, or directly release kinin from kininogens. This review discusses the activation of the kinin-release system by mast-cell tryptase and microbial proteinases, including gingipains, which are cysteine proteinases from Porphyromonas gingivalis, the major pathogen of periodontal disease. Each enzyme is evaluated in the context of its association to allergy and infectious diseases, respectively. Furthermore, a novel system of kinin generation directly from kininogens by the concerted action of two proteinases is described. An interesting example of this system with implications to bacterial pathogenicity is the release of kinins from kininogens by neutrophil elastase and a synergistic action of cysteine proteinases from Staphylococcus aureus. This alternative production of kinins by proteinases present in diseased sites indicates a significant contribution of proteinases other than kallikreins in kinin generation. Therefore kinin receptor antagonists and proteinase inhibitors may be useful as therapeutic agents.
References
Akaike, T., Maeda, H., Maruo, K., Sakata, Y., and Sato, K. (1994). Potentiation of infectivity and pathogenesis of influenza A virus by house dust mite protease. J. Infect. Dis.170, 1023–1026.10.1093/infdis/170.4.1023Search in Google Scholar
Alfie, M.E., Alim, S., Mehta, D., Shesely, E.G., and Carretero, O.A. (1999). An enhanced effect of arginine vasopressin in bradykinin B2 receptor null mutant mice. Hypertension33, 1436–1440.10.1161/01.HYP.33.6.1436Search in Google Scholar
Alter, S.C., Lammle, B., Griffin, J.H., and Schwartz LB. (1988). Tryptase from human mast cells does not activate purified human Hageman factor. Clin. Allergy18, 151–156.10.1111/j.1365-2222.1988.tb02854.xSearch in Google Scholar
Barkocy-Gallagher, G.A., Han, N., Patti, J.M., Whitlock J., Progulske-Fox, A., and Lantz, M.S. (1996). Analysis of the prtP gene encoding porphypain, a cysteine proteinase of Porphyromonas gingivalis. J. Bacteriol.178, 2734–2741.10.1128/jb.178.10.2734-2741.1996Search in Google Scholar
Baumgarten, C.R., Nichols, R.C., Naclerio, R.M., Lichtenstein, L.M., Norman, P.S., and Proud, D. (1986). Plasma kallikrein during experimentally induced allergic rhinitis: role in kinin formation and contribution to TAME-esterase activity in nasal secretions. J. Immunol.137, 977–982.10.4049/jimmunol.137.3.977Search in Google Scholar
Beatty, K., Bieth, J., and Travis, J. (1980). Kinetic of association of serine proteinases with native and oxidized α1-proteinase inhibitor and α1-antichymotrypsin. J. Biol. Chem.255, 3931–3934.10.1016/S0021-9258(19)85615-6Search in Google Scholar
Bhoola, K.D., Figueroa, C.D., and Worthy, K. (1992). Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol. Rev.44, 1–80.Search in Google Scholar
Cochrane, C.G., and Griffin, J.H. (1982). The biochemistry and pathophysiology of the contact system of plasma. Adv. Immunol.33, 241–306.10.1016/S0065-2776(08)60837-8Search in Google Scholar
Cochrane, D.E., Carraway, R.E., Feldberg, R.S., Boucher, W., and Gelfand, J.M. (1993). Stimulated rat mast cells generate histamine-releasing peptide from albumin. Peptides14, 117–123.10.1016/0196-9781(93)90018-CSearch in Google Scholar
Colman, R.W., Bagdasarian, A., Talamo, R.C., Scott, C.F., Seavey, M., Guimaraes, J.A., Pierce, J.V., and Kaplan, A.P. (1975). William trait. Human kininogen deficiency with diminished levels of plasminogen proactivator and prekallikrein associated with abnormalities of the Hageman factor-dependent pathways. J. Clin. Invest.56, 1650–1662.Search in Google Scholar
D’Andrea, M.R., Rogahn, C.J., and Andrade-Gordon, P. (2000). Localization of protease-activated receptors-1 and -2 in human mast cells: indications for an amplified mast cell degranulation cascade. Biotech. Histochem.75, 85–90.10.3109/10520290009064152Search in Google Scholar PubMed
Fuller, R.W., Dixon, C.M.S., Cuss, F.M.C., and Barnes, P.J. (1987). Bradykinin-induced bronchoconstriction in humans: mode of action. Am. Rev. Respir. Dis.135, 176–180.Search in Google Scholar
Gordon, J.R., and Galli, S.J. (1990). Mast cells as a source of both preformed and immunologically inducible TNF-α/cahectin. Nature346, 274–276.10.1038/346274a0Search in Google Scholar PubMed
Grenier, D., and Mayrand, D. (1987). Selected characteristics of pathogenic and nonpathogenic strains of Bacteroides gingivalis. J. Clin. Microbiol.25, 738–740.10.1128/jcm.25.4.738-740.1987Search in Google Scholar PubMed PubMed Central
Harvima, I.T., Harvima, R.J., Penttilä, I.M., Eloranta, T.O., Horsmanheimo, M., and Fräki, J.E. (1989). Effect of human mast cell tryptase on human plasma proenzymes. Int. Arch. Allergy Appl. Immunol.90, 104–108.10.1159/000235008Search in Google Scholar
He, S.H., He, Y.S., and Xie, H. (2004). Activation of human colon mast cells through proteinase activated receptor-2. World J. Gastroenterol.10, 327–331.10.3748/wjg.v10.i3.327Search in Google Scholar
Herwald, H., Collin, M., Müller-Ester, W., and Björck, L. (1996). Streptococcal cysteine proteinase releases kinins: a novel virulence mechanism. J. Exp. Med.184, 665–673.10.1084/jem.184.2.665Search in Google Scholar
Hesselvik, J.F., Blomback, M., Brodin, B., and Maller, R. (1989). Coagulation, fibrinolysis, and kallikrein systems in sepsis: relation to outcome. Crit. Care Med.17, 724–733.10.1097/00003246-198908000-00002Search in Google Scholar
Higashiyama, S., Ishiguro H., Ohkubo, I., Fujimoto S., Matsuda, T., and Sasaki, M. (1986). Kinin release from kininogens by calpains. Life Sci.39, 1639–1644.10.1016/0024-3205(86)90160-8Search in Google Scholar
Hinode, D., Nagata, A., Ichimiya, S., Hayashi, H., Morioka, M., and Nakamura, R. (1992) Generation of plasma kinin by three types of protease isolated from Porphyromonas gingivalis 381. Arch. Oral Biol.37, 859–868.10.1016/0003-9969(92)90120-WSearch in Google Scholar
Holt, S.C., Ebersole, J., Fenton, J., Brunsvold, M., and Kornmann, K.S. (1987). Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science239, 55–57.Search in Google Scholar
Imamura, T., Pike, R.N., Potempa, J., and Travis, J. (1994). 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.94, 361–367.10.1172/JCI117330Search in Google Scholar
Imamura, T., Pike, R.N., Potempa, J., and Travis, J. (1995). Dependence of vascular permeability enhancement on cysteine proteinases in vesicles of Porphyromonas gingivalis. Infect. Immun.63, 1999–2003.10.1128/iai.63.5.1999-2003.1995Search in Google Scholar
Imamura, T., Dubin, A., Moore, W., Tanaka, R., and Travis, J. (1996). Induction of vascular permeability enhancement by human tryptase: dependence on activation of prekallikrein and direct release of bradykinin from kininogens. Lab. Invest.74, 861–870.Search in Google Scholar
Imamura, T., Potempa, J., and Travis, J. (2000). Comparison of pathogenic properties between two types of arginine-specific cysteine proteinases (Gingipains-R) from Porphyromonas gingivalis. Microb. Pathol.29, 155–163.10.1006/mpat.2000.0380Search in Google Scholar
Imamura, T., Tanase, S., Hayashi, I., Potempa, J., Kozik, A., and Travis, J. (2002). Release of a new vascular permeability enhancing peptide from kininogens by human neutrophil elastase. Biochem. Biophys. Res. Commun.294, 423–428.10.1016/S0006-291X(02)00490-4Search in Google Scholar
Ipsen, H., Klysner, S., Larsen, J.N., Løwenstein, H., Matthiesen, F., Schou, C., and Sparholt, S.H. (1993). Allergic extracts. In: Allergy, E. Middleton Jr., C.E. Reed, E.F. Ellis, N.F. Adkinson Jr., J.W. Yunginger, and W.W. Busse, eds. (St. Louis, USA: Mosby), pp. 529–553.Search in Google Scholar
Kalter E.S., van Dijk, W.C., Timmerman, A., Verhoef, J., and Bouma, B.N. (1983). Activation of purified human plasma prekallikrein triggered by cell wall fractions of Escherichia coli and Staphylococcus aureus. J. Infect. Dis.148, 682–691.10.1093/infdis/148.4.682Search in Google Scholar
Kalter, E.S., Daha, M.R., ten Carte, J.W., Verhoef, J., and Bouma, B.N. (1985). Activation and inhibition of Hageman factordependent pathways and the complement system in uncomplicated bacteremia or bacterial shock. J. Infect. Dis.151, 1019–1027.10.1093/infdis/151.6.1019Search in Google Scholar
Kaminishi, H., Cho, T., Itoh, T., Iwata, A., Kawasaki, K., Hagiwara, Y., and Maeda, H. (1993). Vascular permeability enhancing activity of Porphyromonas gingivalis protease in guinea pig. FEMS Microbiol. Lett.114, 109–114.10.1111/j.1574-6968.1993.tb06559.xSearch in Google Scholar
Kaplan, A., and Silverberg, M. (1987). The coagulation-kinin pathway of human plasma. Blood70, 1–15.Search in Google Scholar
Kozik, A., Moore, R. B., Potempa, J., Imamura, T., Rapala-Kozik, M., and Travis, J. (1998). A novel mechanism for bradykinin production at inflammatory sites: diverse effects of a mixture of neutrophil elastase and mast cell tryptase versus tissue and plasma kallikreins on native and oxidized kininogens. J. Biol. Chem.273, 33224–33229.10.1074/jbc.273.50.33224Search in Google Scholar
Lee, P.Y., and Pearce, F.L. (1990). Histamine secretion from mast cells stimulated with bradykinin. Agents Actions30, 67–69.10.1007/BF01969000Search in Google Scholar
Lerner, U.H. (1994). Regulation of bone metabolism by the kallikrein-kinin system, the coagulation cascade, and the acutephase reactants. Oral Surg. Oral Med. Oral Pathol.78, 481–493.10.1016/0030-4220(94)90043-4Search in Google Scholar
Macfarlane, S.R., Seatter, M.J., Kanke, T., Hunter, G.D., and Plevin, R. (2001). Proteinase-activated receptors. Pharmacol. Rev.53, 245–282.Search in Google Scholar
Madeddu, P., Varoni, M.V., Palomba, D., Emanueli, C., Demontis, M.P., Glorioso, N., Dessi-Fulgheri, P., Sarzani, R., and Anania, V. (1997). Cardiovascular phenotype of a mouse strain with disruption of bradykinin B2-receptor gene. Circulation96, 3570–3578.10.1161/01.CIR.96.10.3570Search in Google Scholar
Maeda, H., Matsumura, Y., and Kato H. (1988). Purification and identification of [hydroxyprolyl3]bradykinin in ascitic fluid from a patient with gastric cancer. J. Biol. Chem.263, 16051–16054.10.1016/S0021-9258(18)37555-0Search in Google Scholar
Maier, M., Spragg, J., and Schwartz, L.B. (1983). Inactivation of human high molecular weight kininogen by mast cell tryptase. J. Immunol.130, 2352–2356.10.4049/jimmunol.130.5.2352Search in Google Scholar
Maruo, K., Akaike, T., Matsumura Y., Kohmoto, S., Inada, Y., Ono, T., Arao, T., and Maeda, H. (1991). Triggering of the vascular permeability reaction by activation of the Hageman factor-prekallikrein system by house dust mite proteinase. Biochim. Biophys. Acta1074, 62–68.10.1016/0304-4165(91)90040-NSearch in Google Scholar
Maruo, K., Akaike, T., Inada, Y., Ohkubo, I., Ono, T., and Maeda, H. (1993). Effect of microbial and mite proteases on low and high molecular weight kininogens. Generation of kinin and inactivation of thiol protease inhibitory activity. J. Biol. Chem.268, 17711–17715.Search in Google Scholar
Maruo, K., Akaike, T., Ono, T., Okamoto T., and Maeda, H. (1997). Generation of anaphylatoxins through proteolytic processing of C3 and C5 by house dust mite protease. J. Allergy Clin. Immunol.100, 253–260.10.1016/S0091-6749(97)70233-1Search in Google Scholar
Matsumoto, K., Yamamoto, T., Kamata, R., and Maeda H. (1984). Pathogenesis of serratial infection: activation of the Hageman factor-prekallikrein cascade by serratial protease. J. Biochem.96, 739–749.10.1093/oxfordjournals.jbchem.a134892Search in Google Scholar
Matsumura, Y., Maruo, K., Kimura, M., Yamamoto, T., Konno, T., and Maeda, H. (1991). Kinin-generating cascade in advanced cancer patient an in vitro study. Jpn. J. Cancer Res.79, 732–741.10.1111/j.1349-7006.1991.tb01910.xSearch in Google Scholar
Meier, H.L., Kaplan, A.P., Lichtenstein, L.M., Revak, S., Cochrane, C.G., and Newball, H.H. (1983). Anaphylactic release of a prekallikrein activator from human lung in vitro. J. Clin. Invest.72, 574–581.10.1172/JCI111005Search in Google Scholar
Molla, A., Yamamoto, T., Akaike, T., Miyoshi, S., and Maeda, H. (1989). Activation of Hageman factor and prekallikrein and generation of kinin by various microbial proteinases. J. Biol. Chem.264, 10589–10594.10.1016/S0021-9258(18)81661-1Search in Google Scholar
Mori, T., and Imamura, T (1998). Inhibition of guinea pig skin allergic reactions by nonpeptide bradykinin B2 receptor antagonist, FR173657. Int. Arch. Allergy Immunol.116, 278–283.10.1159/000023956Search in Google Scholar
Nakayama, K. (1997). Domain-specific rearrangement between the two Arg-gingipain-encoding genes in Porphyromonas gingivalis: possible involvement of nonreciprocal recombination. Microbiol. Immunol.41, 185–196.10.1111/j.1348-0421.1997.tb01189.xSearch in Google Scholar
Okamoto, K., Kadowaki, T., Nakayama, K., and Yamamoto, K. (1996). Cloning and sequencing of the gene encoding a novel lysine-specific cysteine proteinase (Lys-gingipain) in Porphyromonas gingivalis: structural relationship with the arginine-specific cysteine proteinase (Arg-gingipain). J. Biochem.120, 398–406.10.1093/oxfordjournals.jbchem.a021426Search in Google Scholar
Pavloff, N., Potempa, J., Pike, R.N., Prochazka, V., Kiefer, M.C., Travis, J., and Barr, P. (1995). Molecular cloning and structural characterization of the Arg-gingipain proteinase of Porphyromonas gingivalis. J. Biol. Chem.270, 1007–1010.10.1074/jbc.270.3.1007Search in Google Scholar
Pavloff, N., Pemberton, P.A., Potempa, J., Chen, W.C.A., Pike, R.N., Prochazka, V., Kiefer, M.C., Travis, J., and Barr, P. (1997). Molecular cloning and characterization of Porphyromonas gingivalis Lys-gingipain. A new member of an emerging family of pathogenic bacterial proteinase. J. Biol. Chem.272, 1595–1600.Search in Google Scholar
Pereira, P.J., Bergner, A., Macedo-Ribeiro, S., Huber, R., Matschiner, G., Fritz, H., Sommerhoff, C.P., and Bode, W. (1998). Human β-tryptase is a ring-like tetramer with active sites facing a central pore. Nature392, 306–311.10.1038/32703Search in Google Scholar
Potempa, J., Pavloff, N., and Travis, J. (1995). Porphyromonas gingivalis: a proteinase/gene accounting audit. Trends Microbiol.3, 430–434.10.1016/S0966-842X(00)88996-9Search in Google Scholar
Proud, D., Togias, A., Naclerio, R.M., and Crush, S.A. (1983). Kinins are generated in vivo following nasal airway challenge of allergic individuals with allergen. J. Clin. Invest.72, 1678–1685.10.1172/JCI111127Search in Google Scholar
Proud, D., MacGlashan, D.W.Jr., Newball, H.H., Schulman, E.S., and Lichtenstein, L.M. (1985). Immunoglobulin E-mediated release of a kininogenase from purified human lung mast cells. Am. J. Respir. Dis.132, 405–408.Search in Google Scholar
Proud, D., Reynolds, C.J., Lacapra, S., Kagey-Sobotka, A., Lichtenstein, L.M., and Naclerio, R.M. (1988). Nasal provocation with bradykinin induces symptoms of rhinitis and a sore throat. Am. Rev. Respir. Dis.137, 613–616.10.1164/ajrccm/137.3.613Search in Google Scholar
Proud, D., Sweet, J., Stein, P., Settipane, R.A., Kagey-Sobotka, A., Friedlaender, M.H., and Lichtenstein, L.M. (1990). Inflammatory mediator release on conjunctival provocation of allergic subjects with allergen. J. Allergy Clin. Immunol.85, 896–905.10.1016/0091-6749(90)90075-FSearch in Google Scholar
Proud, D., Baily, G.S., Naclerio, R.M., Retnolds, C.J., Cruz, A.A., Eggleston, P.A., Lichtenstein, L.M., and Togias, A.G. (1992). Tryptase and histamine as markers to evaluate mast cell activation during the responses to nasal challenge with allergen, cold, dry air, and hyperosmolar solutions. J. Allergy Clin. Immunol.89, 1098–1110.10.1016/0091-6749(92)90293-BSearch in Google Scholar
Rahman, S., Bunning, R.A., Dobson, P.R., Evans, D.B., Chapman, K,. Jones, T.H., Brown, B.L., and Russell, R.G. (1992). Bradykinin stimulates the production of prostaglandin E2 and interleukin-6 in human osteoblast-like cells. Biochim. Biophys. Acta1135, 97–102.10.1016/0167-4889(92)90172-8Search in Google Scholar
Ransjo, M., Marklund, M., Persson, M., and Lerner, U.H. (1998). Synergistic interactions of bradykinin, thrombin, interleukin-1 and tumor necrosis factor on prostanoid biosynthesis in human periodontal ligament cells. Arch. Oral Biol.43, 253–260.10.1016/S0003-9969(98)00010-7Search in Google Scholar
Regoli, D., and Barabé, J. (1980). Pharmacology of bradykinin and related kinins. Pharmacol. Rev.32, 1–46.Search in Google Scholar
Salvemini, D., Masini, E., Anggard, E., Mannaioni, P.F., and Vane, J. (1990). Synthesis of a nitric oxide-like factor from L-arginine by rat serosal mast cells: stimulation of guanylate cyclase and inhibition of platelet aggregation. Biochem. Biophys. Res. Commun.169, 596–601.10.1016/0006-291X(90)90372-TSearch in Google Scholar
Sato, F., and Nagasawa, S. (1988). Mechanism of kinin release from human low-molecular-mass-kininogen by the synergistic action of human plasma kallikrein and leukocyte elastase. Biol. Chem. Hoppe-Seyler369, 1009–1017.10.1515/bchm3.1988.369.2.1009Search in Google Scholar
Schwartz, L.B., Lewis, R.A., and Austen, K.F. (1981a). Tryptase from human pulmonary mast cells: purification and characterization. J. Biol. Chem.256, 11939–11943.10.1016/S0021-9258(19)68496-6Search in Google Scholar
Schwartz, L.B., Lewis, R.A., Seldin, D., and Austen, K.F. (1981b). Acid hydrases and tryptase from secretory granules of dispersed human lung mast cells. J. Immunol.126, 1290–1294.10.4049/jimmunol.126.4.1290Search in Google Scholar
Schwartz, L.B., Bradford, T., and Griffin, J.H. (1985). The effect of tryptase from human mast cells on human prekallikrein. Biochem. Biophys. Res. Commun.129, 76–81.10.1016/0006-291X(85)91405-6Search in Google Scholar
Schwartz, L.B., Maier, M., and Spragg, J. (1986). Interaction of human low molecular weight kininogen with human mast cell tryptase. Adv. Exp. Med. Biol.198, 105–111.10.1007/978-1-4684-5143-6_15Search in Google Scholar
Schwartz, L.B., Metcalfe, D.D., Miller, J.S., Earl, H., and Sullivan, T. (1987). Tryptase levels as an indicator of mast-cell activation in systemic anaphylaxis and mastcytosis. N. Engl. J. Med.316, 1622–1626.10.1056/NEJM198706253162603Search in Google Scholar
Schwartz, L.B., Yunginger, J.W., Miller, J.S., Bokhari, R., and Dull, D. (1989). The time course of appearance and disappearance of human mast cell tryptase in the circulation after anaphylaxis. J. Clin. Invest.83, 1551–1555.10.1172/JCI114051Search in Google Scholar
Shalit, M., Schwartz, L.B., Von Allmen. C., Atkins, P.C., Lavker, R.M., and Zweiman, B. (1990). Release of histamine and tryptase during continuous and interrupted cutaneous challenge with allergen in humans. J. Allergy Clin. Immunol.86, 117–125.10.1016/S0091-6749(05)80131-9Search in Google Scholar
Slots, J. (1982). Importance of black-pigmented Bacteroides in human periodontal disease. In: Host-Parasite Interactions in Periodontal Diseases, R.J. Genco and S.E. Mergenhagen, eds. (Washington DC, USA: American Society of Microbiology), pp. 27–45.Search in Google Scholar
Smalley, J.W., Birss, A.J., Kay, H.M., McKee, A.S., and Marsh, P.D. (1989). The distribution of trypsin-like enzyme activity in the cultures of a virulent and an avirulent strain of Bacteroides gingivalis W50. Oral Microbiol. Immunol.4, 178–181.10.1111/j.1399-302X.1989.tb00249.xSearch in Google Scholar
Smith, T.J., Hougland, H.W., and Johnson, D.A. (1984). Human lung tryptase. Purification and characterization. J. Biol. Chem.259, 11046–11051.Search in Google Scholar
Smith-Erichsen, N., Aasen, A.O., Gallimore, M.J., and Amundsen, E. (1982). Studies of components of the coagulation systems in normal individuals and septic shock patients. Circ. Shock9, 491–497.Search in Google Scholar
Svensson, C., Andersson, M., Persson, C.G.A., Venge, P., Alkner, U., and Pipkorn, U. (1990). Albumin, bradykinin, and eosinophil cationic protein on the nasal mucosal surface in patients with hay fever during natural allergen exposure. J. Allergy Clin. Immunol.85, 823–833.10.1016/0091-6749(90)90064-BSearch in Google Scholar
Takagaki, Y., Kitamura, N., and Nakanishi, S. (1985). Cloning and sequence analysis of cDNAs for human high molecular weight and low molecular weight prekininogens: primary structures of two human prekininogens. J. Biol. Chem.260, 8601–8609.10.1016/S0021-9258(17)39515-7Search in Google Scholar
Takahashi, K., Aoki, T., Kohmoto, S., Nishimura, H., Kodera Y., Matsushima, A., and Inada, Y. (1990). Activation of kallikreinkinin system in human plasma with purified serine proteinase from Dermatophagoides farinae. Int. Arch. Allergy Appl. Immunol.91, 80–85.10.1159/000235094Search in Google Scholar PubMed
Van der Linden, P.G., Hack, C.E., Poortman, J., Vivie-Kipp, Y.C., Struyvenberg, A., and Van der Zwan, J.K. (1992). Insect-sting challenge in 138 patients: relation between clinical severity of anaphylaxis and mast cell activation. J. Allergy Clin. Immunol.90, 110–118.Search in Google Scholar
Van der Linden, P.G., Hack, C.E., Eerenberg, A.J.M., Struyvenberg, A., and Van der Zwan, J.K. (1993). Activation of the contact system in insect-sting anaphylaxis: association with the development of angioedema and shock. Blood82, 1732–1739.10.1182/blood.V82.6.1732.1732Search in Google Scholar
Vargaftig, B.B., and Giroux, E.L. (1976). Mechanism of clostripain-induced kinin release from human, rat, and canine plasma. Adv. Exp. Med. Biol.70, 157–175.10.1007/978-1-4684-3267-1_20Search in Google Scholar PubMed
Varonier, H.S., and Panzani, R. (1968). The effect of inhalations of bradykinin on healthy and atopic (asthmatic) children. Int. Arch. Allergy Appl. Immunol.34, 293–296.10.1159/000230120Search in Google Scholar
Vissers, M.C.M., and Winterbourn, C.C. (1987). Myeloperoxidase-dependent oxidative inactivation of neutrophil neutral proteinases and microbial enzymes. Biochem. J.245, 277–280.10.1042/bj2450277Search in Google Scholar
Wachtfogel, Y.T., Cadena, R.A.D., Kunapuli, S.P., Rick, L., Miller, M., Schultze, R.L., Altieri, D.C., Edgington, T.S., and Colman, R.W. (1994). High molecular weight kininogen binds to Mac-1 on neutrophils by its heavy chain (domain 3) and its light chain (domain 5). J. Biol. Chem.269, 19307–19312.10.1016/S0021-9258(17)32168-3Search in Google Scholar
Wenzel, S.A., Fowler, A.A.III, and Schwartz, L.B. (1988). Activation of pulmonary mast cells by bronchoalveolar allergen challenge: in vivo release of histamine and tryptase in atopic subjects with and without asthma. Am. Rev. Respir. Dis.137, 1002–1008.10.1164/ajrccm/137.5.1002Search in Google Scholar PubMed
© Walter de Gruyter
Articles in the same Issue
- Hiroshi Maeda – 40 years of research
- Activation of the kallikrein-kinin system and release of new kinins through alternative cleavage of kininogens by microbial and human cell proteinases
- Molecular mechanism for activation and regulation of matrix metalloproteinases during bacterial infections and respiratory inflammation
- Role of bacterial proteases in pseudomonal and serratial keratitis
- Cysteine cathepsins in human cancer
- Secretory leukoprotease inhibitor and pulmonary surfactant serve as principal defenses against influenza A virus infection in the airway and chemical agents up-regulating their levels may have therapeutic potential
- Design of inhibitors against HIV, HTLV-I, and Plasmodium falciparum aspartic proteases
- Roles of Arg- and Lys-gingipains in coaggregation of Porphyromonas gingivalis: identification of its responsible molecules in translation products of rgpA, kgp, and hagA genes
- Coordinate expression of the Porphyromonas gingivalis lysine-specific gingipain proteinase, Kgp, arginine-specific gingipain proteinase, RgpA, and the heme/hemoglobin receptor, HmuR
- Genetic characterization of staphopain genes in Staphylococcus aureus
- Visualisation of tissue kallikrein, kininogen and kinin receptors in human skin following trauma and in dermal diseases
- Reduction of myocardial infarction by calpain inhibitors A-705239 and A-705253 in isolated perfused rabbit hearts
- A proteinase inhibitor from Caesalpinia echinata (pau-brasil) seeds for plasma kallikrein, plasmin and factor XIIa
- Plasma prekallikrein/kallikrein processing by lysosomal cysteine proteases
- Characteristics of the caspase-like catalytic domain of human paracaspase
- mRNA expression analysis of a variety of apoptosis-related genes, including the novel gene of the BCL2-family, BCL2L12, in HL-60 leukemia cells after treatment with carboplatin and doxorubicin
- Thermoplasma acidophilum TAA43 is an archaeal member of the eukaryotic meiotic branch of AAA ATPases
- Lipopolysaccharide binding of an exchangeable apolipoprotein, apolipophorin III, from Galleria mellonella
Articles in the same Issue
- Hiroshi Maeda – 40 years of research
- Activation of the kallikrein-kinin system and release of new kinins through alternative cleavage of kininogens by microbial and human cell proteinases
- Molecular mechanism for activation and regulation of matrix metalloproteinases during bacterial infections and respiratory inflammation
- Role of bacterial proteases in pseudomonal and serratial keratitis
- Cysteine cathepsins in human cancer
- Secretory leukoprotease inhibitor and pulmonary surfactant serve as principal defenses against influenza A virus infection in the airway and chemical agents up-regulating their levels may have therapeutic potential
- Design of inhibitors against HIV, HTLV-I, and Plasmodium falciparum aspartic proteases
- Roles of Arg- and Lys-gingipains in coaggregation of Porphyromonas gingivalis: identification of its responsible molecules in translation products of rgpA, kgp, and hagA genes
- Coordinate expression of the Porphyromonas gingivalis lysine-specific gingipain proteinase, Kgp, arginine-specific gingipain proteinase, RgpA, and the heme/hemoglobin receptor, HmuR
- Genetic characterization of staphopain genes in Staphylococcus aureus
- Visualisation of tissue kallikrein, kininogen and kinin receptors in human skin following trauma and in dermal diseases
- Reduction of myocardial infarction by calpain inhibitors A-705239 and A-705253 in isolated perfused rabbit hearts
- A proteinase inhibitor from Caesalpinia echinata (pau-brasil) seeds for plasma kallikrein, plasmin and factor XIIa
- Plasma prekallikrein/kallikrein processing by lysosomal cysteine proteases
- Characteristics of the caspase-like catalytic domain of human paracaspase
- mRNA expression analysis of a variety of apoptosis-related genes, including the novel gene of the BCL2-family, BCL2L12, in HL-60 leukemia cells after treatment with carboplatin and doxorubicin
- Thermoplasma acidophilum TAA43 is an archaeal member of the eukaryotic meiotic branch of AAA ATPases
- Lipopolysaccharide binding of an exchangeable apolipoprotein, apolipophorin III, from Galleria mellonella