Activation of the plasma kallikrein-kinin system on human lung epithelial cells

Biological Chemistry

Volumn 391, Issue 9, 2010, Pages 1067-1077

  Della Vergiliana, Julius F Varano ^a   Asokananthan, Nithiananthan ^a   Stewart, Geoffrey A ^a,b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

bradykinin; heat shock protein 90; high molecular weight kininogen; lung epithelium; plasma prekallikrein; prolylcarboxypeptidase

Indexed keywords

ANGIOTENSIN II; ANTIPAIN; BRADYKININ; CAPTOPRIL; CYSTEINE; HEAT SHOCK PROTEIN 90; KININOGEN; LEUPEPTIN; NOVOBIOCIN; PHOSPHORAMIDON; PREKALLIKREIN; PROLINE CARBOXYPEPTIDASE; PROTAMINE; ZINC;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; EPITHELIUM CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; KALLIKREIN KININ SYSTEM; LUNG ALVEOLUS EPITHELIUM; PLASMA; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

BRADYKININ; CARRIER PROTEINS; EPITHELIAL CELLS; FLOW CYTOMETRY; HSP90 HEAT-SHOCK PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; KALLIKREIN-KININ SYSTEM; KININOGENS; LUNG; MITOCHONDRIAL PROTEINS; NOVOBIOCIN; PREKALLIKREIN; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; TUMOR CELLS, CULTURED;

EID: 77957592168     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2010.102     Document Type: Article

References (66)

1. Akbary, A.M., Wirth, KJ., and Schölkens, B.A. (1996). Efficacy and tolerability of Icatibant (Hoe 140) in patients with moder-ately severe chronic bronchial asthma. Immunopharmacology 33, 238-242.
2. Asokananthan, N., Graham, P.T., Fink, J., Knight, D.A., Bakker, AJ., McWilliam, A.S., Thompson, PJ., and Stewart, G.A. (2002). Activation of protease-activated receptor (PAR)-1, PAR-2, and PAR-4 stimulates IL-6, IL-8, and prostaglandin E2 release from human respiratory epithelial cells. J. Immunol. 168, 3577-3585.
3. Barbasz, A. and Kozik, A. (2009). The assembly and activation of kinin-forming systems on the surface of human U-937 macro-phage-like cells. Biol. Chem. 390, 269-275.
4. Barbasz, A., Guevara-Lora, I., Rapala-Kozik, M., and Kozik, A. (2008). Kininogen binding to the surface of macrophages. Int. Immunopharmacol. 8, 211-216.
5. Baumgarten, C.R., Togias, A.G., Naclerio, R.M., Lichtenstein, L.M., Norman, P.S., and Proud, D. (1985). Influx of kininogens into nasal secretions after antigen challenge of allergic individuals. J. Clin. Invest. 76, 191-197.
6. 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 for-mation and contribution to TAME-esterase activity in nasal secretion. J. Immunol. 137, 977-982.
7. 2+ and cell migration. J. Leukoc. Biol. 81, 1445-1154.
8. Brown, NJ., Gainer, J.V., Stein, C.M., and Vaughan, D.E. (1999). Bradykinin stimulates tissue plasminogen activator release in human vasculature. Hypertension 33, 1431-1435.
9. 1 and B2 receptor in lung cancer. Biol. Chem. 389, 1225-1233.
10. Christiansen, S.C., Proud, D., and Cochrane, C.G. (1987). Detection of tissue kallikrein in the bronchoalveolar lavage fluid of asth-matic subjects. J. Clin. Invest. 79, 188-197.
11. Christiansen, S.C., Proud, D., Sarnoff, R.B., Juergens, U., Cochrane, C.G., and Zuraw, B.L. (1992). Elevation oftissue kallikrein and kinin in the airways of asthmatic subjects after endobronchial challenge. Am. Rev. Respir. Dis. 145, 900-905.
12. Chung, D.W., Fujikawa, K., McMullen, B.A., and Davie, E.W (1986). Human plasma prekallikrein, a zymogen to a serine pro-tease that contains four tandem repeats. Biochemistry 25, 2410-2417.
13. Colman, R.W., Pixley, R.A., Najamunnisa, S., Yan, W., Wang, J., Mazar, A., and McCrae, K.R. (1997). Binding ofhigh molecular weight kininogen to human endothelial cells is mediated via a site within domains 2 and 3 of the urokinase receptor. J. Clin. Invest. 100, 1481-1487.
14. Croce, M.V., Colussi, A.G., Price, M.R., and Segal-Eiras, A. (1999). Identification and characterization of different subpopulations in a human lung adenocarcinoma cell line (A549). Pathol. Oncol. Res. 5, 197-204.
15. Eustace, B.K., Sakurai, T., Stewart, J.K., Yimlamai, D., Unger, C., Zehetmeier, C., Lain, C., Torella, C., Henning, S.W., Beste, G., et al. (2004). Functional proteomic screens reveal an essential extracellular role for hsp90α in cancer cell invasiveness. Nat. Cell Biol. 6, 507-514.
16. Fernando, L.P., Natesan, S., Joseph, K., and Kaplan, A.P. (2003). High molecular weight kininogen and factor XII binding to endothelial cells and astrocytes. Thromb. Haemost. 90, 787-95.
17. 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.
18. Fink, E., Bhoola, K.D., Snyman, C., Neth, P., and Figueroa, C.D. (2007). Cellular expression of plasma prekallikrein in human tissues. Biol. Chem. 388, 957-963.
19. Gustafson, E.J., Schutsky, D., Knight, L.C., and Schmaier, A.H. (1986). High molecular weight kininogen binds unstimulated platelets. J. Clin. Invest. 78, 310-318.
20. Gustafson, EJ., Schmaier, A.H., Wachtfogel, Y.T., Kaufman, N., Kucich, U., and Colman, R.W. (1989). Human neutrophils con-tain and bind high molecular weight kininogen. J. Clin. Invest. 84, 28-35.
21. Imamura, T., Pike, R.N., Potempa, J., and Travis, J. (1994). Patho-genesis of periodontitis: a major arginine-specific cysteine pro-teinase from porphyromonas gingivalis induces vascular permeability enhancement through activation of the kallikrein/ kinin pathway J. Clin. Invest. 94, 361-367.
22. 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.
23. Hasan, A.A., Cines, D.B., Zhang, J., and Schmaier, A.H. (1994). The carboxyl terminus of bradykinin and amino terminus of the light chain of kininogen comprise an endothelial cell binding domain. J. Biol. Chem. 269, 31822-31830.
24. Hasan, A.A., Cines, D.B., Herwald, H., Schmaier, A.H., and Müller-Esterl, W. (1995). Mapping the cell binding site on high molec-ular weight kininogen domain 5. J. Biol. Chem. 270, 19256-19261.
25. 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.
26. Hermann, A., Arnhold, M., Kresse, H., Neth, P., and Fink, E. (1999). Expression of plasma prekallikrein mRNA in human non-hepatic tissue and cell lineages suggests special local functions of the enzyme. Biol. Chem. 380, 1097-1102.
27. Herwald, H., Hasan, A.A., Godovac-Zimmermann, J., Schmaier, A.H., and Müller-Esterl, W. (1995). Identification of an endothelial cell binding site on kininogen domain D3. J. Biol. Chem. 270, 14634-14642.
28. Hooley, E., McEwan, P.A., and Emsley, J. (2007). Molecular modeling of the prekallikrein structure provides insights into high-molecular-weight kininogen binding and zymogen activation. J. Thromb. Haemost. 5, 2461-2466.
29. Joseph, K., Ghebrehiwet, B., and Kaplan, A.P. (1999). Cytokeratin I and gC1qR mediate high molecular weight kininogen binding to endothelial cells. Clin. Immunol. 92, 246-255.
30. Joseph, K., Tholanikunnel, B.G., and Kaplan, A.P. (2002). Heat shock protein 90 catalyzes activation of the prekallikrein-kini-nogen complex in the absence of factor FXII. Proc. Natl. Acad. Sci. USA 99, 896-900.
31. Joseph, K., Tholanikunnel, B.G., Ghebrehiwet, B., and Kaplan, A.P. (2004). Interaction of high molecular weight kininogen binding proteins on endothelial cells. Thromb. Haemost. 91, 61-70.
32. Joseph, K., Tholanikunnel, B.G., and Kaplan, A.P. (2009). Factor XII-independent cleavage of high-molecular-weight kininogen by prekallikrein and inhibition by C1 inhibitor. J. Allergy Clin. Immunol. 124, 143-149.
33. Kaplan, A.P., Joseph, K., and Silverberg, M. (2002). Pathways for bradykinin formation and inflammatory disease. J. Allergy Clin. Immunol. 109, 195-209.
34. Kerbiriou, D.M. and Griffin, J.H. (1979). Human high molecular weight kininogen: studies of structure-function relationships and of proteolysis of the molecule occurring during contact activa-tion of plasma. J. Biol. Chem. 254, 12020-12027.
35. Khan, M.M., Bradforf, H.N., Isordia-Salas, I., Liu, Y., Wu, L., Espi-nola, R.G., Ghebrehiwet, B., and Colman, R.W. (2006). High-molecular-weight kininogen fragments stimulate the secretion of cytokines and chemokines through uPAR, Mac-1, and gC1qR in monocytes. Arterioscler. Thromb. Vasc. Biol. 26, 2260-2266.
36. Khor, Y.H., Teoh, A.K.Y., Lam, S.M., Mo, D.C.Q., Weston, S., Reid, D.W., and Walters, E.H. (2009). Increased vascular permeability precedes cellular inflammation as asthma control deteriorates. Clin. Exp. Allergy 39, 1659-1667.
37. Koyama, S., Sato, E., Nomura, H., Kubo, K., Miura, M., Yamashita, T., Nagai, S., and Izumi, T. (1998). Bradykinin stimulates type II alveolar cells to release neutrophil and monocytes chemotactic activity and inflammatory cytokines. Am. J. Pathol. 153, 1885-1893.
38. 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 plas-ma kallikreins on native and oxidized kininogens. J. Biol. Chem. 273, 33224-33229.
39. Kumamoto, K., Stewart, T.A., Johnson, A.R., and Erdös, E.G. (1981). Prolylcarboxypeptidase (angiotensinase C) in human lung and cultured cells. J. Clin. Invest. 7, 210-215.
40. Mahdi, F., Shariat-Madar, Z., Todd, R.F., Figueroa, C.D., and Schmaier, A.H. (2001). Expression and colocalization of cyto-keratin 1 and urokinase plasminogen activator receptor on endo-thelial cells. Blood 97, 2342-2350.
41. Marcu, M.G., Chadli, A., Bouhouche, I., Catelli, M., and Neckers, L. (2000a). The heat shock protein 90 antagonist novobiocin interacts with a previously unrecognized ATP-binding domain in the C-terminus of the chaperone. J. Biol. Chem. 275, 37181-37186.
42. Marcu, M.G., Schulte, T.W., and Neckers, L. (2000b). Novobiocin and related coumarins and depletion of heat shock protein 90-dependent signaling proteins. J. Natl. Cancer Inst. 92, 242-248.
43. Molla, A., Yamamoto, T., Akaike, T., Miyoshi, S., and Maeda, H. (1989). Activation of Hageman factor and prekallikrein and gen-eration of kinin by various microbial proteinases. J. Biol. Chem. 264, 10589-10594.
44. Motta, G., Røjkjaer, R., Hasan, A.A.K., Cines, D.B., and Schmaier, A.H. (1998). High molecular weight kininogen regulates pre-kallikrein assembly and activation on endothelial cells: a novel mechanism for contact activation. Blood 91, 516-528.
45. Page, J.D., You, J.L., Harris, R.B., and Colman, R.W. (1994). Local-ization of the binding site of plasma kallikrein for high-molec-ular- weight kininogen to both apple 1 and apple 4 domains of the heavy chain. Arch. Biochem. Biophys. 314, 159-164.
46. Palmer, R.MJ., Ferrige, A.G., and Moncada, S. (1987). Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327, 524-526.
47. Persson, C. and Uller, L. (2009). Roles of plasma exudation in asth-ma and COPD. Clin. Exp. Allergy 39, 1626-1629.
48. Persson, C.G., Andersson, M., Greiff, L., Svensson, C., Erjefält, J.S., Sundler, F., Wollmer, P., Alkner, U., Erjefält, I., and Gus-tafsson, B. (1995). Airway permeability Clin. Exp. Allergy 25, 807-814.
49. Reddigari, S.R., Kuna, P., Miragliotta, G., Shibayama, Y., Nishika-wa, K., and Kaplan, A.P. (1993a). Human high molecular weight kininogen bind to human umbilical vein endothelial cells via its heavy and light chains. Blood 81, 1306-1311.
50. Reddigari, S.R., Shibayama, Y., Brunnée, T., and Kaplan, A.P. (1993b). Human Hageman factor (Factor XII) and high molec-ular weight kininogen compete for the same binding site on human umbilical vein endothelial cells. J. Biol. Chem. 268, 11982-11987.
51. Renné, T., Dedio, J., David, G., and Müller-Esterl, W. (2000). High molecular weight kininogen utilizes heparan sulphate proteogly-cans for accumulation on endothelial cells. J. Biol. Chem. 275, 33688-33696.
52. Røjkjaer, R., Hasan, A.A., Motta, G., Schousboe, I., and Schmaier, A.H. (1998). Factor XII does not initiate prekallikrein activation on endothelial cells. Thromb. Haemost. 80, 74-81.
53. Roque, B.P., Nobel, F., Daugé, V, Fournié-Zaluski, M.C., and Beau-mont, A. (1993). Neutral endopeptidase 24.11: structure, inhi-bition, and experimental and clinical pharmacology Pharmacol. Rev. 45, 87-146.
54. Safaiyan, F., Kolset, S.O., Prydz, K., Gottfridsson, E., Lindahl, U., and Salmivirta, M. (1999). Selective effects of sodium chlorate treatment on the sulfation of heparan sulfate. J. Biol. Chem. 274, 36367-36273.
55. Schmaier, A.H. (2007). Plasma kallikrein/kinin system: a revised hypothesis for its activation and its physiologic contributions. Curr. Opin. Hematol. 7, 261-265.
56. Schmaier, A.H., Kuo, A., Lundberg, D., Murray, S., and Cines, D.B. (1988). The expression of high molecular weight kininogen on human umbilical vein endothelial cells. J. Biol. Chem. 263, 16327-16333.
57. Shariat-Madar, Z., Mahdi, F., and Schmaier, A.H. (1999). Mapping binding domains of kininogens on endothelial cell cytokeratin 1. J. Biol. Chem. 274, 7137-7145.
58. Shariat-Madar, Z., Mahdi, F., and Schmaier, A.H. (2002). Identifi-cation and characterization of prolylcarboxypeptidase as an endothelial cell prekallikrein activator. J. Biol. Chem. 277, 17962-17969.
59. Shariat-Madar, Z., Mahdi, F., and Schmaier, A.H. (2004). Recom-binant prolylcarboxypeptidase activates plasma prekallikrein. Blood 103, 4554-4561.
60. Sheikh, I.A. and Kaplan, A.P. (1986). Studies of the digestion of bradykinin, lysyl bradykinin, and kinin-degradation products by carboxypeptidase A, B, and N. Biochem. Pharmacol. 35, 1957-1963.
61. Sheikh, I.A. and Kaplan, A.P. (1989). Mechanism of digestion of bradykinin and lysylbradykinin (kallidin) in human serum. Role of carboxypeptidase, angiotensin-converting enzyme and deter-mination of degradation products. Biochem. Pharmacol. 38, 993-1000.
62. Simmons, W.H. and Orawski, A.T. (1992). Membrane-bound ami-nopeptidase P from bovine lung. Its purification, properties, and degradation of bradykinin. J. Biol. Chem. 267, 4897-4903.
63. 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.
64. Wachtfogel, Y.T., DeLa Cadena, R.A., Kunapuli, S.P., Rick, L., Mil-ler, M., Schultze, R.L., Altieri, D.C., Edgington, T.S., and Col-man, 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.
65. 2 synthesis in human vascular endothelial cells. Hypertension 36, 201-207.
66. Zhao, Y., Qiu, Q., Mahdi, F., Shariat-Madar, Z., Røjkjaer, R., and Schmaier, A.H. (2001). Assembly and activation of HK-PK complex on endothelial cells results in bradykinin liberation and NO formation. Am. J. Physiol. 280, H1821-H1829.