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Licensed Unlicensed Requires Authentication Published by De Gruyter June 7, 2018

Functional interrelationships between the kallikrein-related peptidases family and the classical kinin system in the human neutrophil

  • Pamela Ehrenfeld , Kanti D. Bhoola , Carola E. Matus and Carlos D. Figueroa EMAIL logo
From the journal Biological Chemistry

Abstract

In the human neutrophil, kallikrein-related peptidases (KLKs) have a significant functional relationship with the classical kinin system as a kinin B1 receptor agonist induces secretion of KLK1, KLK6, KLK10, KLK13 and KLK14 into the medium. Secretion of KLK1, the kinin-forming enzyme, may perpetuate formation of kinin in the inflammatory milieu by hydrolyzing extravasated kininogens present in tissue edema. Secretion of KLKs into the inflammatory milieu, induced by kinins or other proinflammatory mediators, provides the human neutrophil with a wide range of molecular interactions to hydrolyze different cellular and extracellular matrix components, which may be of critical relevance in different mechanisms involving inflammation.

Award Identifier / Grant number: S-2015-61

Funding statement: The authors wish to thank Dirección de Investigación y Desarrollo from Universidad Austral de Chile, Funder Id: 10.13039/501100007159 (Grant No. S-2015-61 to P.E.) for its continuous support.

References

Araujo, R.C., Kettritz, R., Fichtner, I., Paiva, A.C.M., Pesquero, J.B., and Bader, M. (2001). Altered neutrophil homeostasis in kinin B1 receptor-deficient mice. Biol. Chem. 382, 91–95.10.1515/BC.2001.014Search in Google Scholar

Bertram, C., Misso, N.L., Fogel-Petrovik, M., Figueroa, C.D., Thompson, P.J., and Bhoola, K.D. (2007). Comparison of kinin B1 and B2 receptor expression in neutrophils of asthmatic and non-asthmatic subjects. Int. Immunopharmacol. 7, 1862–1868.10.1016/j.intimp.2007.07.012Search in Google Scholar

Bhoola, K.D., Figueroa, C.D., and Whorthy, K. (1992). Bioregulation of kinins: kallikreins, kininogens, and kininases. Pharmacol. Rev. 44, 1–80.Search in Google Scholar

Böckmann, S. and Paegelow, I. (2000). Kinins and kinin receptors: importance for the activation of leukocytes. J. Leukoc. Biol. 68, 587–592.10.1189/jlb.68.5.587Search in Google Scholar

Campos, M.M., Leal, P.C., Yunes, R.A., and Calixto, J.B. (2006). Non-peptide antagonists for kinin B1 receptors: new insights into their therapeutic potential for the management of inflammation and pain. Trends Pharmacol. Sci. 27, 646–651.10.1016/j.tips.2006.10.007Search in Google Scholar

Carl, V.S., Moore, E.E., Moore, F.A., and Whalley, E.T. (1996). Involvement of bradykinin B1 and B2 receptors in human PMN elastase release and increase in endothelial cell monolayer permeability. Immunopharmacology 33, 325–329.10.1016/0162-3109(96)00055-0Search in Google Scholar

Cassim, B., Shaw, O.M., Mazur, M., Misso, N.L., Naran, A., Langlands, D.R., Thompson, P.J., and Bhoola, K.D. (2009). Kallikreins, kininogens and kinin receptors on circulating and synovial fluid neutrophils: role in kinin generation in rheumatoid arthritis. Rheumatology 48, 490–496.10.1093/rheumatology/kep016Search in Google Scholar PubMed

Charlesworth, M.C., Young, C.Y., Miller, V.M., and Tindall, D.J. (1999). Kininogenase activity of prostate-derived human glandular kallikrein (hK2) purified from seminal fluid. J. Androl. 20, 220–229.Search in Google Scholar

Christiansen, S.C., Proud, D., and Cochrane, C.G. (1987). Detection of tissue kallikrein in the bronchoalveolar lavage fluid of asthmatic subjects. J. Clin. Invest. 79, 188–197.10.1172/JCI112782Search in Google Scholar PubMed PubMed Central

Da Silva, B., Morais, R.L., Pesquero, J.B., Bader, M., Otuki, M.F., and Cabrini, D.A. (2016). Kinin receptors in skin wound healing. J. Dermatol. Sci. 82, 95–105.10.1016/j.jdermsci.2016.01.007Search in Google Scholar PubMed

Dos Santos, A.C., Roffe, E., Arantes, R.M.E., Juliano, L., Pesquero, J.L., Pesquero, J.B., Bader, M., Teixeira, M., and Carvalho-Tavares, J. (2008). Kinin B2 receptor regulates chemokines CCL2 and Ccl5 expression and modulates leukocyte recruitment and pathology in experimental autoimmune encephalomyelitis (EAE) in mice. J. Neuroinflamm. 5, 49.10.1186/1742-2094-5-49Search in Google Scholar PubMed PubMed Central

Duchene, J., Lecomte, F., Ahmed, S., Cayla, C., Pesquero, J., Bader, M., Perretti, M., and Ahluwalia, A. (2007). A novel inflammatory pathway involved in leukocyte recruitment: role for the kinin B1 receptor and the chemokine CXCL5. J. Immunol. 179, 4849–4856.10.4049/jimmunol.179.7.4849Search in Google Scholar PubMed PubMed Central

Ehrenfeld, P., Millan, C., Matus, C.E., Figueroa, J., Burgos, R., Nualart, F., Bhoola, K.D., and Figueroa, C.D. (2006). Activation of kinin B1 receptors induces chemotaxis of human neutrophils J. Leukoc. Biol. 80, 117–124.10.1189/jlb.1205744Search in Google Scholar PubMed

Ehrenfeld, P., Matus, C.E., Pavicic, F., Toledo, C., Nualart, F., Gonzalez, C.B., Burgos, R.A., Bhoola, K.D., and Figueroa, C.D. (2009). Kinin B1 receptor activation turns on exocytosis of matrix metalloprotease-9 and myeloperoxidase in human neutrophils: involvement of mitogen-activated protein kinase family. J. Leukoc. Biol. 86, 1179–1189.10.1189/jlb.0109012Search in Google Scholar PubMed

Figueroa, C.D. and Bhoola, K.D. (1989). Leucocyte tissue kallikrein: an acute phase signal for inflammation. In: The Kallikrein Kinin System in Health and Disease, H. Fritz, I. Schimdt and G. Dietze, eds. (Braunschweig, Germany: Limbach-Verlag), pp. 311–320.Search in Google Scholar

Figueroa, C.D., MacIver, A.G., and Bhoola, K.D. (1989). Identification of a tissue kallikrein in human polymorphonuclear leucocytes. Br. J. Haematol. 72, 321–328.10.1111/j.1365-2141.1989.tb07711.xSearch in Google Scholar PubMed

Figueroa, C.D., Henderson, L.M., Kaufmann, J., De la Cadena, R.A., Colman, R.W., Müller-Esterl, W., and Bhoola, K.D. (1992). Immunovisualization of high (HK) and low (LK) molecular weight kininogens on isolated human neutrophils. Blood 79, 754–759.10.1182/blood.V79.3.754.754Search in Google Scholar

Figueroa, C.D., Matus, C.E., Pavicic, F., Sarmiento, J., Hidalgo, M.A., Burgos, R.A., Gonzalez, C.B., Bhoola, K.D., and Ehrenfeld, P. (2015). Kinin B1 receptor regulates interactions between neutrophils and endothelial cells by modulating the levels of Mac-1, LFA-1 and ICAM-1. Innate Immun. 21, 289–304.10.1177/1753425914529169Search in Google Scholar PubMed

Fox, A., Kaur, S., Li, B., Pansenar, M., Saha, U., Davis, C., Dragoni, I., Colley, S., Ritchie, T., Bevan, S., et al. (2005). Anti-hyperalgesic activity of a novel non-peptide bradykinin B1 receptor antagonist in transgenic mice expressing the human B1 receptor. Br. J. Pharmacol. 144, 889–899.10.1038/sj.bjp.0706139Search in Google Scholar PubMed PubMed Central

Gao, L., Chao, L., and Chao, J. (2009). A novel signaling pathway of tissue kallikrein in promoting keratinocyte migration: activation of proteinase-activated receptor 1 and epidermal growth factor receptor. Exp. Cell Res. 316, 376–389.10.1016/j.yexcr.2009.10.022Search in Google Scholar PubMed PubMed Central

Göbel, K., Pankratz, S., Schneider-Hohendorf, T., Bittner, S., Schuhmann, M.K., Langer, H.F., Stoll, G., Wiendl, H., Kleinschnitz, C., and Meuth, S.G. (2011). Blockade of the kinin receptor B1 protects from autoimmune CNS disease by reducing leukocyte trafficking. J. Autoimmun. 36, 106–114.10.1016/j.jaut.2010.11.004Search in Google Scholar PubMed

Gustafson, E.J., Schmaier, A.H., Wachtfogel, Y.T., Kaufmann, N., Kucich, U., and Colman, R.W. (1989). Human neutrophils contain and bind high molecular weight kininogen. J. Clin. Invest. 84, 28–35.10.1172/JCI114151Search in Google Scholar PubMed PubMed Central

Haddad, E.B., Fox, A.J., Rousell, J., Burgess, G., McIntyre, P., Barnes, P.J., and Chung, K.F. (2000). Post-transcriptional regulation of bradykinin B1 and B2 receptor gene expression in human lung fibroblasts by tumor necrosis factor-α: modulation by dexamethasone. Mol. Pharmacol. 57, 1123–1131.Search in Google Scholar

Hara, D.B., Leite, D.F.P., Fernandes, E.S., Passos, G.F., Guimaraes, A.O., Pesquero, J.B., Campos, M.M., and Calixto, J.B. (2008). The relevance of kinin B1 receptor upregulation in a mouse model of colitis. Br. J. Pharmacol. 154, 1276–1286.10.1038/bjp.2008.212Search in Google Scholar PubMed PubMed Central

Henderson, L.M., Figueroa, C.D., Müller-Esterl, W., and Bhoola, K.D. (1994). Assembly of contact phase factors on the surface of the human neutrophil membrane. Blood 84, 474–482.10.1182/blood.V84.2.474.474Search 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

Kahn, R., Hellmark, T., Leeb-Lundberg, L.M.F., Akbari, N., Todiras, M., Olofsson, T., Wieslander, J., Christensson, A., Westman, K., Bader, M., et al. (2009). Neutrophil-derived proteinase 3 induces kallikrein-independent release of a novel vasoactive kinin. J. Immunol. 182, 7906–7915.10.4049/jimmunol.0803624Search in Google Scholar PubMed

Kemme, M., Podlich, D., Raidoo, D.M., Snyman, C., Naidoo, S., and Bhoola, K.D. (1999). Identification of immunoreactive tissue prokallikrein on the surface membrane of human neutrophils. Biol. Chem. 380, 1321–1328.10.1515/BC.1999.168Search in Google Scholar PubMed

Kleniewski, J. and Donaldson, V. (1988). Granulocyte elastase cleaves human high molecular weight kininogen and destroys its clot-promoting activity. J. Exp. Med. 167, 1895–1907.10.1084/jem.167.6.1895Search in Google Scholar PubMed PubMed Central

Kotz, K., Xiao, W., Miller-Graziano, C., Qian, W.J., Russom, A., Warner, E.A., Moldawer, L.L., De, A., Bankey, P.E., Petritis, B.O., et al. (2010). Clinical microfluidics for neutrophil genomics and proteomics. Nat. Med. 16, 1042–1047.10.1038/nm.2205Search in Google Scholar PubMed PubMed Central

Leeb-Lundberg, L.M., 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 PubMed

Lizama, A., Andrade, Y., Colivoro, P., Sarmiento, J., Matus, C.E., Gonzalez, C.B., Bhoola, K.D., Ehrenfeld, P., and Figueroa, C.D. (2015). Expression and bioregulation of the kallikrein-related peptidases family in the human neutrophil. Innate Immun. 21, 575–586.10.1177/1753425914566083Search in Google Scholar PubMed

Marquez-Curtis, L., Jalili, A., Deiteren, K., Shirvaikar, N., Lambeir, A.M., and Janowska-Wieczorek, A. (2008). Carboxypeptidase M expressed by human bone marrow cells cleaves the C-terminal lysine of stromal cell-derived factor-1α: another player in hematopoietic stem/progenitor cell mobilization? Stem Cells 26, 1211–1220.10.1634/stemcells.2007-0725Search in Google Scholar PubMed

Moran, C.S., Rush, C.M., Dougan, T., Jose, R.J., Biros, E., Norman, P.E., Gera, L., and Golledge, J. (2016). Modulation of kinin B2 receptor signaling controls aortic dilatation and rupture in the angiotensin II-infused apolipoprotein E-deficient mouse. Arterioscler. Thromb. Vasc. Biol. 36, 898–907.10.1161/ATVBAHA.115.306945Search in Google Scholar PubMed

Naidoo, Y., Snyman, C., Raidoo, D.M., Bhoola, K.D., Kemme, M., and Müller-Esterl, W. (1999). Cellular visualization of tissue prokallikrein in human neutrophils and myelocytes. Br. J. Haematol. 105, 599–612.10.1046/j.1365-2141.1999.01391.xSearch in Google Scholar PubMed

Oliveira, C.R., Paredes-Gamero, E.J., Barbosa, C.M.V., Nascimento, F.D., Batista, E.C., Reis, F.C.G., Martins, A.H.B., Ferreira, A.T., Carmona, A.K., Pesquero, J.B., et al. (2010). Myelopoiesis modulation by ACE hyperfunction in kinin B1 receptor knockout mice: Relationship with AcSDKP levels. Chem.-Biol. Interact. 184, 388–395.10.1016/j.cbi.2010.01.015Search in Google Scholar

Paegelow, I., Trzeczak, S., Böckmann, S., and Vietinghoff, G. (2002). Migratory responses of polymorphonuclear leukocytes to kinin peptides. Pharmacology 66, 153–161.10.1159/000063797Search in Google Scholar

Petraki, C.D., Papanastasiou, P.A., Karavana, V.N., and Diamandis, E.P. (2006). Cellular distribution of human tissue kallikreins: immunohistochemical localization. Biol. Chem. 387, 653–663.10.1515/BC.2006.084Search in Google Scholar

Qadri, F. and Bader, M. (2018). Kinin B1 receptors as a therapeutic target for inflammation. Expert Opin. Ther. Targets 22, 31–44.10.1080/14728222.2018.1409724Search in Google Scholar

Raab, A. and Kemme, M. (2000). High-molecular-weight kininogen is a binding protein for tissue prokallikrein. FEBS Lett. 467, 165–168.10.1016/S0014-5793(00)01141-8Search 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. 369, 1009–1017.10.1515/bchm3.1988.369.2.1009Search in Google Scholar PubMed

Shaw, O.M. and Harper, J.L. (2011). Bradykinin receptor 2 extends inflammatory cell recruitment in a model of acute gouty arthritis. Biochem. Biophys. Res. Commun. 416, 266–269.10.1016/j.bbrc.2011.10.137Search in Google Scholar PubMed

Simon, M., Jonca, N., Guerrin, M., Haftek, M., Bernard, D., Caubet, C., Egelrud, T., Schmidt, R., and Serre, G. (2001). Refined characterization of corneodesmosin proteolysis during terminal differentiation of human epidermis and its relationship to desquamation. J. Biol. Chem. 276, 20292–20299.10.1074/jbc.M100201200Search in Google Scholar PubMed

Sotiropoulou, G. and Pampalakis, G. (2010). Kallikrein-related peptidases: bridges between immune functions and extracellular matrix degradation. Biol. Chem. 391, 321–331.10.1515/bc.2010.036Search in Google Scholar

Sotiropoulou, G., Pampalakis, G., and Diamandis, E.P. (2009). Functional roles of human kallikrein-related peptidases. J. Biol. Chem. 284, 32989–32994.10.1074/jbc.R109.027946Search in Google Scholar PubMed PubMed Central

Stuardo, M., Gonzalez, C.B., Nualart, F., Boric, M., Corthorn, J., Bhoola, K.D., and Figueroa, C.D. (2004). Stimulated human neutrophils form biologically active kinin peptides from high and low molecular weight kininogens. J. Leukoc. Biol. 75, 631–640.10.1189/jlb.1103546Search in Google Scholar PubMed

Wedmore, C.V. and Williams, T.J. (1981). Control of vascular permeability by polymorphonuclear leukocytes in inflammation. Nature 289, 646–650.10.1038/289646a0Search in Google Scholar PubMed

Weidmann, H., Heikaus, L., Long, A.T., Naudin, C., Schlüter, H., and Renné, T. (2017). The plasma contact system, a protease cascade at the nexus of inflammation, coagulation and immunity. Biochim Biophys. Acta 1864, 2118–2127.10.1016/j.bbamcr.2017.07.009Search in Google Scholar PubMed

Williams, R.J., Henderson, L.M., Naidoo, Y., Cassim, B., Elson, C.J., and Bhoola, K.D. (1997). Immunocytochemical analysis of tissue kallikrein and the kinin moiety in rheumatoid synovial fluid neutrophils. Br. J. Rheumatol. 36, 420–425.10.1093/rheumatology/36.4.420Search in Google Scholar PubMed

Wu, H.F., Venezie, R.D., Cohen, W.M., Jenzano, J.W., Featherstone, G.L., and Lundblad, R.L. (1993). Identification of tissue kallikrein messenger RNA in human neutrophils. Agents Actions 38, 27–31.10.1007/BF02027209Search in Google Scholar PubMed

Yousef, G.M., Chang, A., Scorilas, A., and Diamandis, E.P. (2000). Genomic organization of the human kallikrein gene family on chromosome 19q13.3-q13.4. Biochem. Biophys. Res. Commun. 276, 125–133.10.1006/bbrc.2000.3448Search in Google Scholar PubMed

Zhang, X., Tan, F., and Skidgel, R.A. (2013). Carboxypeptidase M is a positive allosteric modulator of the kinin B1 receptor. J. Biol. Chem. 288, 33226–33240.10.1074/jbc.M113.520791Search in Google Scholar PubMed PubMed Central

Received: 2017-12-28
Accepted: 2018-04-15
Published Online: 2018-06-07
Published in Print: 2018-09-25

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