Abstract
Aeromonas sobria serine protease (ASP) is secreted from Aeromonas sobria, a pathogen causing gastroenteritis and sepsis. ASP resembles Saccharomyces cerevisiae Kex2, a member of the subtilisin family, and preferentially cleaves peptide bonds at the C-terminal side of paired basic amino acid residues; also accepting unpaired arginine at the P1 site. Unlike Kex2, however, ASP lacks an intramolecular chaperone N-terminal propeptide, instead utilizes the external chaperone ORF2 for proper folding, therefore, ASP and its homologues constitute a new subfamily in the subtilisin family. Through activation of the kallikrein/kinin system, ASP induces vascular leakage, and presumably causes edema and septic shock. ASP accelerates plasma clotting by α-thrombin generation from prothrombin, whereas it impairs plasma clottability by fibrinogen degradation, together bringing about blood coagulation disorder that occurs in disseminated intravascular coagulation, a major complication of sepsis. From complement C5 ASP liberates C5a that induces neutrophil recruitment and superoxide release, and mast cell degranulation, which are associated with pus formation, tissue injury and diarrhea, respectively. Nicked two-chain ASP also secreted from A. sobria is more resistant to inactivation by α2-macroglobulin than single-chain ASP, thereby raising virulence activities. Thus, ASP is a potent virulence factor and may participate in the pathogenesis of A. sobria infection.
Acknowledgments
We thank Dr. T. Yoshimura, Department of Pathology and Experimental Medicine, Okayama University for his critical reading and editing of this manuscript. We also thank Dr. H. Kobayashi, Laboratory of Molecular Microbiological Science, Faculty of Pharmaceutical Sciences, Hiroshima International University for his invaluable comments on ASP properties.
References
Ascencio, F., Aleljung, P., Olusanya, O., and Wadström, T. (1990). Type I and IV collagen and fibrinogen binding to Aeromonas species isolated from various infections. Zentralbl. Bakteriol. 273, 186–194.10.1016/S0934-8840(11)80248-3Search in Google Scholar
Brenner, C. and Fuller, R.S. (1992). Structural and enzymatic characterization of a purified prohormon-processing enzyme: secreted, soluble Kex2 protease. Proc. Natl. Acad. Sci. USA 89, 922–926.10.1073/pnas.89.3.922Search in Google Scholar
Chang, J.-Y. (1986). The structures and proteolytic specificities of autolysed human thrombin. Biochem. J. 240, 797–802.10.1042/bj2400797Search in Google Scholar
Chang, A.K., Kim, H.Y., Park, J.E., Acharya, P., Park, I.-S., Yoon, S.M., You, H.J., Hahm, K.-S., Park, J.K., and Lee, J.S. (2005). Vibrio vulnificus secretes a broad-specificity metalloprotease capable of interfering with blood homeostasis through prothrombin activation and fibrinolysis. J. Bacteriol. 187, 6909–6916.10.1128/JB.187.20.6909-6916.2005Search in Google Scholar
Chung, D.W., Fujikawa, K., MacMullen, B.A., and Davie, E.W. (1986). Human plasma prekallikrein, a zymogen to a serine protease that contains four tandem repeats. Biochemistry 25, 2410–2417.10.1021/bi00357a017Search 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
Coleman, G. and Whitby, P.W. (1993). A comparison of amino acid sequence of the serine protease of the fish pathogen Aeromonas salmonicida with those of other subtilisin-type enzymes relative to their substrate-binding sites. J. Gen. Microbiol. 139, 245–249.10.1099/00221287-139-2-245Search in Google Scholar PubMed
Collet, J.-P., Moen, J.L., Veklich, Y.I., Gorkun, O.V., Lord, S.T., Montalescot, G., and Wiesel, J.W. (2005). The αC domains of fibrinogen affect the structure of the fibrin clot, its physical properties, and its susceptibility to fibrinolysis. Blood 106, 3824–3830.10.1182/blood-2005-05-2150Search in Google Scholar PubMed PubMed Central
Daily, O.P., Joseph, S.W., Coolbaugh, J.C., Walker, R.I., Merrell, B.R., Rollins, D.M., Seidler, R.J., Colwell, R.R., and Lissner, C.R. (1981). Association of Aeromonas sobria with human infection. J. Clin. Microbiol. 13, 769 –777.10.1128/jcm.13.4.769-777.1981Search in Google Scholar PubMed PubMed Central
Degen, S.F.J., MacGillivray, R.T.A., and Davie, E.W. (1983). Characterization of the complementary deoxyribonucleic acid and gene coding for human prothrombin. Biochemistry 22, 2087–2097.10.1021/bi00278a008Search in Google Scholar PubMed
de Bruijn, M.H.L. and Fey, G.H. (1985). Human complement component C3: cDNA coding sequence and derived primary structure. Proc. Natl. Acad. Sci. USA 82, 708–712.10.1073/pnas.82.3.708Search in Google Scholar
Deutsch, S.F. and Wedzina, W. (1997). Aeromonas sobria- associated left-sided segmental colitis. Am. J. Gastroenterol. 92, 2104–2106.Search in Google Scholar
DiScipio, R.G., Smith, C.A., Müller-Eberhard, H.J., and Hugli, T.E. (1983). The activation of human complement component C5 by a fluid phase C5 convertase. J. Biol. Chem. 258, 10629–10636.10.1016/S0021-9258(17)44503-0Search in Google Scholar
DiScipio, R.G., Daffern, P.J., Kawahara, M., Pike, R., Travis, J., and Hugli, T.E. (1996). Cleavage of human complement component C5 by cysteine proteinases from Porphyromonas gingivalis: prior oxidation of C5 augments proteinase digestion of C5. Immunology 87, 660–667.10.1046/j.1365-2567.1996.478594.xSearch in Google Scholar
Doyle, M.F. and Mann, K.G. (1990) Multiple active forms of thrombin. IV. Relative activities of meizothrombins. J. Biol. Chem. 265, 10693–10701.10.1016/S0021-9258(18)87002-8Search in Google Scholar
Duthie, R., Ling, T.W., Cheng, A.F.B., and French, G.L. (1995). Aeromonas septicemia in Hong Kong: species distribution and associated diseases. J. Infect. Dis. 30, 241–244.Search in Google Scholar
Esteve, C. and Birbeck, T.H. (2004). Secretion of haemolysins and proteases by Aeromonas hydrophila EO63: separation and characterization of the serine protease (caseinase) and the metalloprotease (elastase). J. Appl. Microbiol. 96, 994–1001.10.1111/j.1365-2672.2004.02227.xSearch in Google Scholar
Farraye, F.A., Peppercorn, M.A., Ciano, P.S., and Kavesh, W.N. (1989). Segmental colitis associated with Aeromonas hydrophila. Am. J. Gastroenterol. 84, 436–438.Search in Google Scholar
Fernandez, H.N. and Hugli, T.E. (1978). Primary structural analysis of the polypeptide portion of human C5a anaphylatoxin: polypeptide sequence determination and assignment of the oligosaccharide attachment site in C5a. J. Biol. Chem. 253, 6955–6964.10.1016/S0021-9258(17)38013-4Search in Google Scholar
Fernandez, H.N., Henson, P.M., Otani, A., and Hugli, T.E. (1978). Chemotactic response to human C3a and C5a anaphylatoxins. 1. Evaluation of C3a and C5a leukotaxis in vitro and under stimulated in vivo cinditions. J. Immunol. 120, 109–115.10.4049/jimmunol.120.1.109Search in Google Scholar
Fittschen, C., Sandhaus, R.A., Worthen, G.S., and Henson, P.M. (1988). Bacterial lipopolysaccharide enhances chemoattractant-induced elastase secretion by human neutrophils. J. Leukoc. Biol. 43, 547–556.10.1002/jlb.43.6.547Search in Google Scholar PubMed
Goldstein, I.M. and Weissmann, G. (1974). Generation of C5-derived lysosomal enzyme releasing activity (C5a) by lysates of leukocyte lysosomes. J. Immunol. 113, 1583–1588.10.4049/jimmunol.113.5.1583Search in Google Scholar
Grøn, H., Meldal, M., and Breddam, K. (1992). Extensive comparison of the substrate preferences of two subtilisins as determined with peptide substrates which are based on the principle of intramolecular quenching. Biochemistry 31, 6011–6018.10.1021/bi00141a008Search in Google Scholar PubMed
Guo, R.F., Riedemann, N.C., Bernacki, K.D., Sarma, V.J., Laudes, I.J., Reuben, J.S., Younkin, E.M., Neff, T.A., Paulauskis, J.D., Zetoune, F.S., et al. (2003). Neutrophil C5a receptor and the outcome in a rat model of sepsis. FASEB J. 13, 1889–1891.10.1096/fj.03-0009fjeSearch in Google Scholar PubMed
Halkier, T. (1991). Mechanisms in Blood Coagulation, Fibrinolysis and the Complement System (Cambridge, UK: Cambridge University Press).Search in Google Scholar
Harpel, P.C. (1973). Studies on human plasma α2-macroglobulin-enzyme interactions: evidence for proteolytic modification of the subunit chain structure. J. Exp. Med. 138, 508–521.10.1084/jem.138.3.508Search in Google Scholar PubMed PubMed Central
Harris, T.O., Shelver, D.W., Bohnsack, J.F., and Rubens, C.E. (2003). A novel streptococcal surface protease promotes virulence, resistance to opsonophagocytosis, and cleavage of human fibrinogen. J. Clin. Invest. 111, 61–70.10.1172/JCI200316270Search in Google Scholar
Haycox, C.L., Odland, P.D., Coltrera, M.D., and Raugi, G.J. (1995). Indications and complications of medicinal leech therapy. J. Am. Acad. Dermatol. 33, 1053–1055.10.1016/0190-9622(95)90320-8Search in Google Scholar
Herwald, H., Collin, M., Müller-Esterl, W., and Björck, L. (1996). Streptococcal cysteine protease releases kinins: a novel virulence mechanism. J. Exp. Med. 184, 665–673.10.1084/jem.184.2.665Search in Google Scholar PubMed PubMed Central
Hesselvik, J.F., Blombäck, 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 PubMed
Holyoak, T., Wilson, M.A., Fenn, T.D., Kettner, C.A., Petsko, G.A., Fuller, R.S., and Ringe, D. (2003). 2.4 Å resolution crystal structure of the prototypical hormone-processing protease Kex2 in complex with an Ala-Lys-Arg boronic acid inhibitor. Biochemistry 42, 6709–6718.10.1021/bi034434tSearch in Google Scholar PubMed
Huber-Lang, M.S., Younkin, E.M., Sarma, J.V., McGuire, S.R., Lu, K.T., Guo, R.F., Padgaonkar, V.A., Curnutte, J.T., Erickson, R., and Ward, P.A. (2002). Complement-induced impairment of innate immunity during sepsis. J. Immunol. 169, 3223–3231.10.4049/jimmunol.169.6.3223Search in Google Scholar PubMed
Husslein, V., Bergbauer, H., and Chakraborty, T. (1991). Studies on aerolysin and a serine protease from Aeromonas trota sp. nov. Experientia 47, 420 – 421.Search in Google Scholar
Ikeda, K., Nagasawa, K., Horiuchi, T., Tsuru, T., Nishizaka, H., and Niho, Y. (1997). C5a induces tissue factor activity on endothelial cells. Thromb. Haemost. 77, 394–398.10.1055/s-0038-1655974Search in Google Scholar
Imamura, T. (2014). Staphopains in Staphylococcus aureus bacteremia: virulence activities related to the onset of septic shock, coagulation disorders, and infectious endocarditis. J. Oral Biosci. 56, 81–85.10.1016/j.job.2014.04.001Search in Google Scholar
Imamura, T., Yamamoto, T., and Kambara, T. (1984). Guinea pig plasma kallikrein as a vascular permeability enhancement factor: its dependence on kinin generation and regulation mechanisms in vivo. Am. J. Pathol. 115, 92–101.Search in Google Scholar
Imamura, T., Potempa, J., Pike, R.N., and Travis, J. (1995). Effect of free and vesicle-bound cysteine proteinases of Porphyromonas gingivalis on plasma clot formation: implications for bleeding tendency at periodontitis sites. Infect. Immun. 63, 4877–4882.10.1128/iai.63.12.4877-4882.1995Search in Google Scholar PubMed PubMed Central
Imamura, T., Banbula, A., Pereira, P.J.B., Travis, J., and Potempa, J. (2001) Activation of human prothrombin by arginine-specific cysteine proteases (gingipain R) from Porphyromonas gingivalis. J. Biol. Chem. 276, 18984–18991.10.1074/jbc.M006760200Search in Google Scholar PubMed
Imamura, T., Tanase, S., Szmyd, G., Kozik, A, Travis, J., and Potempa, J. (2005). Induction of vascular leakage through release of bradykinin and a novel kinin by cysteine proteinases from Staphylococcus aureus. J. Exp. Med. 201, 1669 –1676.10.1084/jem.20042041Search in Google Scholar PubMed PubMed Central
Imamura, T., Kobayashi, H., Khan, R., Nitta, H., and Okamoto, K. (2006). Induction of vascular leakage and blood pressure lowering through kinin release by a serine protease from Aeromonas sobria. J. Immunol. 177, 8723–8729.10.4049/jimmunol.177.12.8723Search in Google Scholar PubMed
Imamura, T., Nitta, H., Wada, Y., Kobayashi, H., and Okamoto, K. (2008). Impaired plasma clottability induction through fibrinogen degradation byASP, a serine protease released from Aeromonas sobria. FEMS Microbiol. Lett. 284, 35–42.10.1111/j.1574-6968.2008.01184.xSearch in Google Scholar PubMed PubMed Central
Janda, J.M. (1991). Recent advances in the study of the taxonomy, pathogenicity, and infectious syndromes associated with the genus Aeromonas. Clin. Microbiol. Rev. 4, 397–410.10.1128/CMR.4.4.397Search in Google Scholar PubMed PubMed Central
Janda, J.M. and Brenden, R. (1987). Importance of Aeromonas sobria in Aeromonas bacteremia. J. Infect. Dis. 155, 589–591.10.1093/infdis/155.3.589Search in Google Scholar PubMed
Janda, J.M. and Duffey, P.S. (1988). Mesophilic aeromonads in human disease: current taxonomy, laboratory identification, and infectious disease spectrum. Rev. Infect. Dis. 10, 980–997.10.1093/clinids/10.5.980Search in Google Scholar PubMed
Janda, J.M. and Abbott, S.L. (1996). Human pathogens. In: The Genus Aeromonas. B. Austin, M. Altwegg, P.J. Gosling and S. Joseph, eds. (Chichester, UK: John Wiley & Sons), pp. 151–173.Search in Google Scholar
Janda, J.M. and Abbott, S.L. (1998). Evolving concepts regarding the genus Aeromonas: an expanding panorama of species, disease presentations, and unanswered questions. Clin. Infect. Dis. 27, 332–344.10.1086/514652Search in Google Scholar PubMed
Janda, J.M. and Abbott, S.L. (2010). The genus Aeromonas: taxonomy, pathogenicity, and infection. Clin. Microbiol. Rev. 23, 35–73.10.1128/CMR.00039-09Search in Google Scholar PubMed PubMed Central
Janda, J.M., Reitano, M., and Bottone, E.J. (1984). Biotyping of Aeromonas isolates as a correlate to delineating a species-associated disease spectrum. J. Clin. Microbiol. 19, 44–47.10.1128/jcm.19.1.44-47.1984Search in Google Scholar PubMed PubMed Central
Janda, J.M., Guthertz, L.S., Kokka, R.P., and Shimada, T. (1994). Aeromonas species in septicemia: laboratory characteristics and clinical observations. Clin. Infect. Dis. 19, 77–83.10.1093/clinids/19.1.77Search in Google Scholar PubMed
Janda, J.M., Abbott, S.L., Khashe, S., Kellogg, G.H., and Shimada, T. (1996). Further studies on biochemical characteristics and serologic properties of the genus Aeromonas. J. Clin. Microbiol. 34, 1930–1933.10.1128/jcm.34.8.1930-1933.1996Search in Google Scholar PubMed PubMed Central
Jones, B.L. and Wilcox, M.H. (1995). Aeromonas infection and their treatment. J. Antimicrob. Chemother. 35, 453–461.10.1093/jac/35.4.453Search in Google Scholar PubMed
Kalter, E.S., Daha, M.R., ten Cate, 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, 1019–1027.10.1093/infdis/151.6.1019Search in Google Scholar PubMed
Kaminishi, H., Hamatake, H., Cho, T., Tamaki, T., Suenaga, N., Fujii, T., Hagihara, Y., and Maeda, H. (1994). Activation of blood clotting factors by microbial proteases. FEMS Microbiol. Lett. 121, 327–332.10.1111/j.1574-6968.1994.tb07121.xSearch in Google Scholar PubMed
Kikuchi, Y. and Kaplan, A.P. (2002). A role for C5a in augmenting IgG-dependent histamine release from basophils in chronic urticaria. J. Allergy Clin. Immunol. 109, 114–118.10.1067/mai.2002.120954Search in Google Scholar PubMed
Kobayashi, H., Takahashi, E., Oguma, K., Fujii, Y., Yamanaka, H., Negishi, T., Arimoto-Kobayashi, S., Tsuji, T., and Okamoto, K. (2006). Cleavage specificity of the serine protease of Aeromonas sobria, a member of the kexin family of subtilases. FEMS Microbiol. Lett. 256, 165–170.10.1111/j.1574-6968.2006.00134.xSearch in Google Scholar PubMed
Kobayashi, H., Utsunomiya, H, Yamanaka, H., Sei, Y., Katunuma, N., Okamoto, K., and Tsuge, H. (2009a). Structural basis for the kexin-like serine protease from Aeromonas sobria as sepsis-causing factor. J. Biol. Chem. 284, 27655–2763.10.1074/jbc.M109.006114Search in Google Scholar PubMed PubMed Central
Kobayashi, H., Tateishi, A., Tsuge, H., Takahashi, E., Okamoto, K., and Yamanaka, H. (2009b). The carboxy-terminal tail of Aeromonas sobria serine protease is associated with the chaperone. Microbiol. Immunol. 53, 647–657.10.1111/j.1348-0421.2009.00175.xSearch in Google Scholar PubMed
Kobayashi, H., Yoshida, T., Miyakawa, T., Tashiro, M., Okamoto, K., Yamanaka, H., Tanokura, M., and Tsuge, H. (2015). Structural basis for action of the external chaperone for a propeptide-deficient serine protease from Aeromonas sobria. J. Biol. Chem. 290, 11130–11143.10.1074/jbc.M114.622852Search in Google Scholar PubMed PubMed Central
Kollman, J.M., Pandi, L., Sawaya, M.R., Riley, M., and Doolittle, R.F. (2009). Crystal structure of human fibrinogen. Biochemistry 48, 3877–3886.10.1021/bi802205gSearch in Google Scholar PubMed
Konteatis, Z.D., Siciliano, S.J., Riper, G.V., Molineaux, C.J., Pandya, S., Fischer, P., Rosen, H., Mumford, R.A., and Springer, M.S. (1994). Development of C5a receptor antagonists: differential loss of functional responses. J. Immunol. 153, 4200–4205.10.4049/jimmunol.153.9.4200Search in Google Scholar
Kurachi, K. and Davie, E.W. (1982). Isolation and characterization of a cDNA clone for human factor IX. Proc. Natl. Acad. Sci. USA 79, 6461–6464.10.1073/pnas.79.21.6461Search in Google Scholar
Leeb-Lundberg, L.M.F., Marceau, F., Müller-Esterl, W., Pettibone, D.J., and Zuraw. B.L. (2005). International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol. Rev. 57: 27–77.10.1124/pr.57.1.2Search in Google Scholar
Levi, M. (2001). Pathogenesis and treatment of disseminated intravascular coagulation in the septic patient. J. Crit. Care 16, 167–177.10.1053/jcrc.2001.30666Search in Google Scholar
Levi, M. and ten Cate, H. (1999). Disseminated intravascula coagulation. N. Engl. J. Med. 341, 586–592.10.1056/NEJM199908193410807Search in Google Scholar
Leytus, S.P., Chung, D.W., Kisiel, W., Sasagawa, T., Howald, W.N., Kwa, E.Y., and Weinstein, B. (1984). Characterization of a cDNA coding for human blood coagulation factor X. Proc. Natl. Acad. Sci. USA 81, 3699–3702.10.1073/pnas.81.12.3699Search in Google Scholar
Lin, S.-H, Shieh, S.-D., Lin, Y.-F., De Bauer, E., Van Landuyt, H.W., Gordts, B., and Boelaert, J.R. (1996). Fatal Aeromonas hydrophila bacteremia in a hemodialysis patient treated with deferoxamine. Am. J. Kidney Dis. 27, 733–735.10.1016/S0272-6386(96)90112-2Search in Google Scholar
Mann, K.G.R. and Lundblad, L. (1987). Biochemistry of thrombin. In: Hemostasis and Thrombosis: Basic Principles and Clinical Practice, 2nd edition. (R.W. Colman, J. Hirsh and V.J. Marder, eds. (Philadelphia, PA: JB Lippincott), pp. 148–161.Search in Google Scholar
Marder, S.R., Chenoweth, D.E., Goldstein, I.M., and Perez, H.D. (1985). Chemotactic responses of human peripheral blood monocytes to the complement-derived peptides C5a and C5a des Arg. J. Immunol. 134, 3325–3331.10.4049/jimmunol.134.5.3325Search in Google Scholar
Marshall, J.C. (1997). Inflammation, coagulopathy, and the pathogenesis of multiple organ dysfunction and anticoagulant mechanisms in sepsis and endotoxaemia. Eur. J. Clin. Invest. 27, 3–9.Search in Google Scholar
Maruo, K., T. Akaike, T., Inada, Y., Ohkubo, I., Ono, T., and H. Maeda. (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, 17711–17715.10.1016/S0021-9258(17)46762-7Search 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, 253–26010.1016/S0091-6749(97)70233-1Search in Google Scholar
Mollnes, T.E., Brekke, O.L., Fung, M., Fure, H., Christiansen, D., Bergseth, G., Videm, V., Lappegård, K.T., Köhl, J., and Lambris, J.D. (2002). Essential role of the C5a receptor in E. coli induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. Blood 100, 1869–1877.Search in Google Scholar
Muhlfelder, T.W., Niemetz, J., Kreutzer, D., Beebe, D., Ward, P.A., and Rosenfeld, S.I. (1979). C5 chemotactic fragment induces leukocyte production of tissue factor activity: a link between complement and coagulation. J. Clin. Invest. 63, 147–150.10.1172/JCI109269Search in Google Scholar PubMed PubMed Central
Müller-Esterl, W. (1986). Kininogens. In: Methods of Enzymatic Analysis: Proteins and Peptides, Vol. 9, 3rd Ed., H.U. Bergmeyer, J. Bergmeyer and M. Graßl, eds. (Weinheim, Germany: VCH), pp. 304–316.Search in Google Scholar
Murakami, Y., Wada, Y., Kobayashi, H., Hasegawa, M., Okamoto, K., Eto, M., and Imamura, T. (2012a). The tail nick augments Aeromonas sobria serine protease (ASP) activity in plasma through retarding inhibition by α2-macroglobulin. FEBS Lett. 586, 3613–3617.10.1016/j.febslet.2012.08.004Search in Google Scholar PubMed
Murakami, Y., Wada, Y., Kobayashi, H., Irie, A., Hasegawa, M., Yamanaka, H., Okamoto, K., Eto, M., and Imamura, T. (2012b). Inhibition of Aeromonas sobria serine protease (ASP) by α2-macroglobulin. Biol. Chem. 393, 1193–1200.10.1515/hsz-2012-0117Search in Google Scholar
Nakae, H., Endo, S., Inada, K., Takakuwa, T., Kasai, T., and Yoshida, M. (1994). Serum complement levels and severity of sepsis. Res. Commun. Chem. Pathol. Pharmacol. 84, 189–195.Search in Google Scholar
Nemerson, Y. (1988). Tissue factor and hemostasis. Blood 71, 1–8.10.1182/blood.V71.1.1.1Search in Google Scholar
Nitta, H., Kobayashi, H., Irie, A., Baba, H., Okamoto, K., and Imamura, T. (2007). Activation of prothrombin by ASP, a serine protease released from Aeromonas sobria. FEBS Lett. 581, 5935–5939.10.1016/j.febslet.2007.11.076Search in Google Scholar
Nitta, H., Imamura, T., Wada, Y., Irie, A., Kobayashi, H., Okamoto, K., and Baba, H. (2008). Production of C5a by ASP, a Serine Protease Released from Aeromonas sobria. J. Immunol. 181, 3602–3608.10.4049/jimmunol.181.5.3602Search in Google Scholar
Nomura, T., Fujii, Y., Yamanaka, Y., Kobayashi, H., and Okamoto, K. (2002). The protein encoded at the 30 end of the serine protease gene of Aeromonas sobria functions as a chaperone in the production of the protease. J. Bacteriol. 184, 7058–7061.10.1128/JB.184.24.7058-7061.2002Search in Google Scholar
Ohbayashi, T., Irie, A., Murakami, Y., Nowak, M., Potempa, J., Nishimiura, Y., Shinohara, M., and Imamura, T. (2011). Degradation of fibrinogen and collagen by staphopains, cysteine proteases released from Staphylococcus aureus. Microbiology 157, 786–792.10.1099/mic.0.044503-0Search in Google Scholar
Okamoto, K., Nomura, T., Hamada, M., Fukuda, T., Noguchi, Y., and Fujii, Y. (2000). Production of serine protease of Aeromonas sobria is controlled by the protein encoded by the gene lying adjacent to the 3′ end of the protease gene. Microbiol. Immunol. 44, 787–798.10.1111/j.1348-0421.2000.tb02565.xSearch in Google Scholar
Pixley, R.A., DeLa Cadena, R.A., Page, J.D., Kaufman, N., Wyshock, E.G., R. Colman, W., Chang, A., and Taylor, Jr, F.B. (1992). Activation of the contact system in lethal hypotensive bacteremia in a baboon model. Am. J. Pathol. 140, 897–906.Search in Google Scholar
Pixley, R.A., DeLa Cadena, R.A., Page, J.D., Kaufman, N., Wyshock, E.G., Chang, A., Taylor, Jr., F.B., and Colman, R.W. (1993). 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. 91, 61–68.10.1172/JCI116201Search in Google Scholar
Pixley, R.A., Zellis, S., Bankes, P., DeLa Cadena, R.A., Page, J.D., Scott, C.F., Kappelmayer, J., Wyshock, E.G., Kelly, J.J., and Colman, R.W. (1995). Prognostic value of assessing contact system activation and factor V in systemic inflammatory response syndrome. Crit. Care Med. 23, 41–51.10.1097/00003246-199501000-00010Search in Google Scholar
Pizzo, S.V., Schwartz, M.L., Hill, R.L., and McKee, P.A. (1972). The effect of plasmin on the subunit structure of human fibrinogen. J. Biol. Chem. 247, 636–645.10.1016/S0021-9258(19)45656-1Search in Google Scholar
Regoli, D. and Barabé, J. (1980). Pharmacology of bradykinin and related kinins. Pharmacol. Rev. 32, 1–46.Search in Google Scholar
Rhaleb, N.-E., Rouissi, N., Jukic, D., Regoli, D., Henke, S., Breipohl, G., and Knolle, J. (1992). Pharmacological characterization of a new highly potent B2 receptor antagonist (HOE 140: D-Arg-(Hyp3, Thi5, D-Tic7, Oic8)bradykinin). Eur. J. Pharmacol. 210, 115–120.10.1016/0014-2999(92)90661-MSearch in Google Scholar
Rheinnecker, M., Baker, G., Eder, J., and Fersht, A.R. (1993). Engineering a novel spcificity in subtilisin BPN’. Biohemistry 32, 1199–1203.10.1021/bi00056a001Search in Google Scholar
Rockwell, M. and Fuller, R.S. (1998). Interplay between S1 and S4 subsites in kex2 protease: Kex2 exhibits dual specificity for the P4 side chain. Biohemistry 37, 3386–3391.10.1021/bi972534rSearch in Google Scholar
Rockwell, N.C., Krysan, D.J., Komiyama, T., and Fuller, R.S. (2002). Precursor processing by Kex2/Furin proteases. Chem. Rev. 102, 4525–4548.10.1021/cr010168iSearch in Google Scholar
Rosing, J., Zwaal, R.F.A., and Tans, G. (1986). Formation of meizothrombin as intermediate in factor Xa-catalyzed prothrombin activation. J. Biol. Chem. 261, 4224–4228.10.1016/S0021-9258(17)35651-XSearch in Google Scholar
Sacks, T., Moldow, C.F., Craddock, P.R., Bowers, T.K., and Jacob, H.S. (1978). Oxygen radicals mediate endothelial cell damage by complement-stimulated granulocytes: an in vitro model of immune vascular damage. J. Clin. Invest. 61, 1161–1167.10.1172/JCI109031Search in Google Scholar
Schiavano, G.F., Bruscolini, F., Albano, A., and Brandi, G. (1998). Virulence factors in Aeromonas spp. and their association with gastrointestinal disease. New Microbiol. 21, 23–30.Search in Google Scholar
Siezen, R.J. and Leunissen, J.A. (1997). Subtilases: the superfamily of subtilisin-like serine proteases. Protein Sci. 6, 501–523.10.1002/pro.5560060301Search 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. Shock 9, 491–497.Search 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. J. Biol. Chem. 260, 8601–8609.10.1016/S0021-9258(17)39515-7Search in Google Scholar
Wegrzynowicz, Z., Heczko, P.B., Drapeau, G.R., Jeljaszewicz, J., and Pulverer, G. (1981). Prothrombin activation by a metalloprotease from Staphylococcus aureus. J. Clin. Microbiol. 12, 138–139.10.1128/jcm.12.2.138-139.1980Search in Google Scholar PubMed PubMed Central
Wirth, K., Hock, F.J., Albus, U., Linz, W., Alpermann, H.G., Anagnostopoulos, H., Henke, S., Breipohl, G., Knolle, J., and Schölkens, B.A. (1991). Hoe 140 a new potent and long acting bradykinin-antagonist: in vivo studies. Br. J. Pharmacol. 102, 774–777.10.1111/j.1476-5381.1991.tb12249.xSearch in Google Scholar PubMed PubMed Central
Wingrove, J.A., DiScipio, R.G., Chen, Z., Potempa, J., Travis, J., and Hugli, T.E. (1992). Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J. Biol. Chem. 267, 18902–18907.10.1016/S0021-9258(19)37046-2Search in Google Scholar
Wöhrl, S., Hemmer, W., Focke, M., Rappersberger, K., and Jarisch, R. (2004). Histamine intolerance-like symptoms in healthy volunteers after oral provocation with liquid histamine. Allergy Asthma Proc. 25, 305–311.Search in Google Scholar
Wuepper, K.D. and Cochrane, C.G. (1972). Plasma prekallikrein: isolation, characterization, and mechanism of activation. J. Exp. Med. 135, 1–20.10.1084/jem.135.1.1Search in Google Scholar PubMed PubMed Central
Yokoyama, R., Fujii, Y., Noguchi, Y., Nomura, T., Akita, M., Setsu, K., Yamamoto, S., and Okamoto, K. (2002). Physicochemical and biological properties of an extracellular serine protease of Aeromonas sobria. Microbiol. Immunol. 46, 383–390.10.1111/j.1348-0421.2002.tb02710.xSearch in Google Scholar PubMed
Zhu, X.L., Ohta, Y., Jordan, F., and Inouye, M. (1989). Pro-sequence of subtilisin can guide the refolding of denatured subtilisin in an intermolecular process. Nature 339, 483–484.10.1038/339483a0Search in Google Scholar PubMed
©2017 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Reviews
- Aeromonas sobria serine protease (ASP): a subtilisin family endopeptidase with multiple virulence activities
- Targeting and inactivation of bacterial toxins by human defensins
- S100A6 – focus on recent developments
- Catalase, a remarkable enzyme: targeting the oldest antioxidant enzyme to find a new cancer treatment approach
- Research Articles/Short Communications
- Protein Structure and Function
- I36T↑T mutation in South African subtype C (C-SA) HIV-1 protease significantly alters protease-drug interactions
- Cell Biology and Signaling
- Mutation of N-linked glycosylation in EpCAM affected cell adhesion in breast cancer cells
- Galanin suppresses proliferation of human U251 and T98G glioma cells via its subtype 1 receptor
- Role of sigma 1 receptor in high fat diet-induced peripheral neuropathy
- Proteolysis
- Tissue kallikrein-related peptidase 4 (KLK4), a novel biomarker in triple-negative breast cancer
Articles in the same Issue
- Frontmatter
- Reviews
- Aeromonas sobria serine protease (ASP): a subtilisin family endopeptidase with multiple virulence activities
- Targeting and inactivation of bacterial toxins by human defensins
- S100A6 – focus on recent developments
- Catalase, a remarkable enzyme: targeting the oldest antioxidant enzyme to find a new cancer treatment approach
- Research Articles/Short Communications
- Protein Structure and Function
- I36T↑T mutation in South African subtype C (C-SA) HIV-1 protease significantly alters protease-drug interactions
- Cell Biology and Signaling
- Mutation of N-linked glycosylation in EpCAM affected cell adhesion in breast cancer cells
- Galanin suppresses proliferation of human U251 and T98G glioma cells via its subtype 1 receptor
- Role of sigma 1 receptor in high fat diet-induced peripheral neuropathy
- Proteolysis
- Tissue kallikrein-related peptidase 4 (KLK4), a novel biomarker in triple-negative breast cancer