Activation of the kallikrein-kinin system and release of new kinins through alternative cleavage of kininogens by microbial and human cell proteinases

Biological Chemistry

Volumn 385, Issue 11, 2004, Pages 989-996

  Imamura, Takahisa ^a   Potempa, Jan ^b,c   Travis, James ^c  

^a KUMAMOTO UNIVERSITY   (Japan)

^b JAGIELLONIAN UNIVERSITY   (Poland)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

Allergy; Elastase; Gingipain; Infection; Mite; Tryptase

Indexed keywords

ARGININE; BACTERIAL PROTEIN; BLOOD CLOTTING FACTOR 12; CELL PROTEIN; CLOSTRIPAIN; CYSTEINE PROTEINASE; ENZYME INHIBITOR; GINGIPAIN R; KALLIKREIN; KININ DERIVATIVE; KININOGEN; LEUKOCYTE ELASTASE; METALLOPROTEINASE; PREKALLIKREIN; PROTEINASE; PROTEINASE INHIBITOR; SOYBEAN TRYPSIN INHIBITOR; SUBTILISIN; TISSUE KALLIKREIN; TRYPTASE;

ALLERGIC RHINITIS; BACTERIAL INFECTION; BACTERIAL VIRULENCE; DERMATOPHAGOIDES FARINAE; DRUG POTENCY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME RELEASE; ENZYME SYNTHESIS; HUMAN; KALLIKREIN KININ SYSTEM; NONHUMAN; PATHOGENESIS; PERIODONTAL DISEASE; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; REVIEW; STAPHYLOCOCCUS AUREUS;

BACTERIAL PHYSIOLOGY; HUMANS; HYDROLYSIS; KALLIKREIN-KININ SYSTEM; KININOGENS;

ACARI; BACTERIA (MICROORGANISMS); PORPHYROMONAS; PORPHYROMONAS GINGIVALIS; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS;

EID: 10044233762     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/BC.2004.129     Document Type: Review

References (83)

1. 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.
2. 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. Hypertension 33, 1436-1440.
3. 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. Allergy 18, 151-156.
4. 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.
5. 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.
6. 1-antichymotrypsin. J. Biol. Chem. 255, 3931-3934.
7. Bhoola, K.D., Figueroa, C.D., and Worthy, K. (1992). Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol. Rev. 44, 1-80.
8. Cochrane, C.G., and Griffin, J.H. (1982). The biochemistry and pathophysiology of the contact system of plasma. Adv. Immunol. 33 241-306.
9. 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. Peptides 14, 117-123.
10. 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.
11. 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.
12. 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.
13. Gordon, J.R., and Galli, S.J. (1990). Mast cells as a source of both preformed and immunologically inducible TNF-α/cahectin. Nature 346, 274-276.
14. Grenier, D., and Mayrand, D. (1987). Selected characteristics of pathogenic and nonpathogenic strains of Bacteroides gingivalis. J. Clin. Microbiol. 25, 738-740.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. 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.
21. 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. Science 239 55-57.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. 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.
29. Kalter, E.S., Daha, M.R., ten Carte, J.W., Verhoef, J., and Bouma, B.N. (1985). Activation and inhibition of Hageman factor-dependent pathways and the complement system in uncomplicated bacteremia or bacterial shock. J. Infect. Dis. 151, 1019-1027.
30. 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.
31. Kaplan, A., and Silverberg, M. (1987). The coagulation-kinin pathway of human plasma. Blood 70, 1-15.
32. 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.
33. Lee, P.Y., and Pearce, F.L. (1990). Histamine secretion from mast cells stimulated with bradykinin. Agents Actions 30, 67-69.
34. Lerner, U.H. (1994). Regulation of bone metabolism by the kallikrein-kinin system, the coagulation cascade, and the acute-phase reactants. Oral Surg. Oral Med. Oral Pathol. 78, 481-493.
35. Macfarlane, S.R., Seatter, M.J., Kanke, T., Hunter, G.D., and Plevin, R. (2001). Proteinase-activated receptors. Pharmacol. Rev. 53 245-282.
36. 2-receptor gene. Circulation 96, 3570-3578.
37. 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.
38. 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.
39. 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. Acta 1074, 62-68.
40. 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.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 2 receptor antagonist, FR173657. Int. Arch. Allergy Immunol. 116, 278-283.
47. 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.
48. 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.
49. 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.
50. 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.
51. 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. Nature 392, 306-311.
52. Potempa, J., Pavloff, N., and Travis, J. (1995). Porphyromonas gingivalis: a proteinase/gene accounting audit. Trends Microbiol. 3, 430-434.
53. 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. 2 and interleukin-6 in human osteoblast-like cells. Biochim. Biophys. Acta 1135, 97-102.
59. 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.
60. Regoli, D., and Barabé, J. (1980). Pharmacology of bradykinin and related kinins. Pharmacol. Rev. 32, 1-46.
61. 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.
62. 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-Seyler 369, 1009-1017.
63. 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.
64. 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.
65. 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.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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.
71. 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.
72. Smith, T.J., Hougland, H.W., and Johnson, D.A. (1984). Human lung tryptase. Purification and characterization. J. Biol. Chem. 259 11046-11051.
73. 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. Shock 9, 491-497.
74. 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.
75. 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.
76. 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.
77. 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.
78. 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. Blood 82, 1732-1739.
79. 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.
80. 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.
81. 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.
82. 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 Mac1 on neutrophils by its heavy chain (domain 3) and its light chain (domain 5). J. Biol. Chem. 269, 19307-19312.
83. 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.