Induction of intracellular signalling in human endothelial cells by the hyaluronan-binding protease involves two distinct pathways
-
Julia Anne Kreß
Abstract
Recently a novel plasma serine protease with high affinity to hyaluronic acid and glycosaminoglycans, such as heparin and heparan sulfate, has been described and termed hyaluronan-binding protease (HABP). HABP cleaves kininogen in vitro, releasing the vasoactive peptide bradykinin, and activates plasminogen activators, suggesting a vascular cell-directed physiological function of this novel plasma protease. Here we show that HABP stimulates human umbilical vein endothelial cells (HUVECs) by activating two distinct cell-surface receptors. On the one hand, HABP releases bradykinin from cell surface-bound or soluble kininogen and triggers a bradykinin B2-receptor-dependent mobilisation of intracellular Ca2+. On the other hand, HABP activates the p44/42-dependent MAPK (ERK1/2) signalling cascade independent of the B2-receptor, but involving the fibroblast growth factor receptor-1 and basic fibroblast growth factor. This signalling pathway leads to phosphorylation of the kinases Raf, MEK1/2 and ERK1/2. The extracellular activity of HABP also affects the gene expression level through phosphorylation of two transcription factors, the cAMP-responsive element binding protein CREB and the proto-oncogene c-Myc. Our results indicate a proangiogenic potential of HABP, which, in combination with a profibrinolytic activity, directs the physiological function of this plasma protease to processes in which clot lysis, cell motility and neovascularisation are pivotal processes, e.g., in wound healing, tissue repair and tumour progession.
References
Bashkin, P., Klagsbrun, M., Doctrow, S., Shvan, C.M., Folkman, J., and Vlodavsky, I. (1989). Basic fibroblast growth factor binds to subendothelial extracellular matrix and is released by heparanase and heparin-like molecules. Biochemistry28, 1737–1743.10.1021/bi00430a047Search in Google Scholar PubMed
Benezra, M., Vlodavsky, I., Ishai-Michaeli, R., Neufeld, G., and Bar-Shavit, R. (1993). Thrombin-induced release of active basic fibroblast growth factor-heparan sulfate complexes from subendothelial extracellular matrix. Blood81, 3324–3331.10.1182/blood.V81.12.3324.3324Search in Google Scholar
Bernier, S.G., Haldar, S., and Michel, T. (2000). Bradykinin-regulated interactions of the mitogen-activated protein kinase pathway with the endothelial nitric-oxide synthase. J. Biol. Chem.275, 30707–30715.10.1074/jbc.M005116200Search in Google Scholar PubMed
Boyd, K.E. and Farnham, P.J. (1999). Identification of target genes of oncogenic transcription factors. Proc. Soc. Exp. Biol. Med.222, 9–28.Search in Google Scholar
Busse, R. and Fleming, I. (1996). Molecular responses of endothelial tissue to kinins. Diabetes45, S8–S13.10.2337/diab.45.1.S8Search in Google Scholar PubMed
Busse, R. and Lamontagne, D. (1991). Endothelium-derived bradykinin is responsible for the increase in calcium produced by angiotensin-converting enzyme inhibitors in human endothelial cells. Naunyn-Schmiedeberg's Arch. Pharmacol.344, 126–129.10.1007/BF00167392Search in Google Scholar PubMed
Camerer, E., Rottingen, J.-A., Iversen, J.-G., and Prydz, H. (1996). Coagulation factors VII and X induce Ca2+ oscillations in Madin-Darby canine kidney cells only when proteolytically active. J. Biol. Chem.271, 29034–29042.10.1074/jbc.271.46.29034Search in Google Scholar PubMed
Choi-Miura, N.H., Tobe, T., Sumiya, J., Nakano, Y., Sano, Y., Mazda, T., and Tomita, M. (1996). Purification and characterization of a novel hyaluronan-binding protein (PHBP) from human plasma: it has three EGF, a kringle and a serine protease domain, similar to hepatocyte growth factor activator. J. Biochem.119, 1157–1165.10.1093/oxfordjournals.jbchem.a021362Search in Google Scholar PubMed
Cines, D.B., Pollak, E.S., Buck, C.A., Loscalzo, J., Zimmerman, G.A., McEver, R.P., Pober, J.S., Wick, T.M., Konkle, B.A., Schwartz, B.S., et al. (1998). Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood91, 3527–3561.Search in Google Scholar
Colman, R.W. and Schmaier, A.H. (1997). Contact system: a vascular biology modulator with anticoagulant, profibrinolytic, antiadhesive, and proinflammatory attributes. Blood90, 3819–3843.10.1182/blood.V90.10.3819Search in Google Scholar
Colman, R.W., Pixley, R.A., Najamunnissa, S, Yan, W., Wang, J., Mazar, A., and McCrae, K.R. (1997). Binding of high 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, 1481–1487.10.1172/JCI119669Search in Google Scholar PubMed PubMed Central
Costa, M., Shen, Y., Maurer, F., and Medcalf, R.L. (1998). Transcriptional regulation of the tissue-type plasminogen-activator gene in human endothelial cells: identification of nuclear factors that recognise functional elements in the tissue-type plasminogen-activator gene promoter. Eur. J. Biochem.258, 123–131.10.1046/j.1432-1327.1998.2580123.xSearch in Google Scholar PubMed
Coughlin, S.R. (2001). Protease-activated receptors in vascular biology. Thromb. Haemost.86, 298–307.10.1055/s-0037-1616227Search in Google Scholar
Dery, O., Corvera, C.U., Steinhoff, M., and Bunnett, N.W. (1998). Proteinase-activated receptors: novel mechanisms of signaling by serine proteases. Am. J. Physiol.274, C1429–C1452.10.1152/ajpcell.1998.274.6.C1429Search in Google Scholar PubMed
Etscheid, M., Hunfeld, A., König, H., Seitz, R., and Dodt, J. (2000). Activation of proPHBSP, the zymogen of a plasma hyaluronan binding serine protease, by an intermolecular autocatalytical mechanism. Biol. Chem.381, 1223–1231.Search in Google Scholar
Etscheid, M., Beer, N., Fink, E., Seitz, R., and Dodt, J. (2002). The hyaluronan-binding serine protease from human plasma cleaves HMW and LMW kininogen and releases bradykinin. Biol. Chem.383, 1633–1643.10.1515/BC.2002.184Search in Google Scholar PubMed
Etscheid, M., Beer, N., Kreß, J.A., Seitz, R., and Dodt, J. (2004). Inhibition of bFGF/EGF-dependent endothelial cell proliferation by the hyaluronan-binding protease from human plasma. Eur. J. Cell Biol.82, 597–604.10.1078/0171-9335-00349Search in Google Scholar PubMed
Etscheid, M., Beer, N., and Dodt, J. (2005). The hyaluronan-binding protease upregulates ERK1/2 and PI3K/Akt signalling pathways in fibroblasts and stimulates cell proliferation and migration. Cell. Signal.17, 1486–1494.10.1016/j.cellsig.2005.03.007Search in Google Scholar PubMed
Fernando, L.P., Fernando, A.N., Joseph, K., and Kaplan, A.P. (2003). Assessment of the role of heparan sulfate in high molecular weight kininogen binding to human umbilical vein endothelial cells. J. Thromb. Haemost.1, 2444–2449.10.1046/j.1538-7836.2003.00438.xSearch in Google Scholar PubMed
Fink, E., Schill, W.-B., Fiedler, F., Krassnigg, F., Geiger, R., and Shimamoto, K. (1985). Tissue kallikrein of human seminal plasma is secreted by the prostate gland. Biol. Chem. Hoppe-Seyler366, 917–924.10.1515/bchm3.1985.366.2.917Search in Google Scholar PubMed
Fleming, I., Fisslthaler, B., and Busse, R. (1995). Calcium signalling in endothelial cells involves activation of tyrosine kinases and leads to activation of mitogen-activated protein kinases. Circ. Res.76, 522–529.10.1161/01.RES.76.4.522Search in Google Scholar
Freay, A., Johns, A., Adams, D.J., Ryan, U.S., and van Breemen, C. (1989). Bradykinin and inositol 1,4,5-triphosphate-stimulated calcium release from intracellular stores in cultured bovine endothelial cells. Pflüger's Arch.414, 377–384.10.1007/BF00585046Search in Google Scholar PubMed
Grewal, S.S., Fass, D.M., Yao, H., Ellig, C.L., Goodman, R.H., and Stork, P.J.S. (2000). Calcium and cAMP signals differentially regulate cAMP-responsive element-binding protein function via a Rap1-extracellular signal-regulated kinase pathway. J. Biol. Chem.275, 34433–34441.10.1074/jbc.M004728200Search in Google Scholar PubMed
Gryglewski, R.J., Botting, R.M., and Vane, J.R. (1988). Mediators produced by the endothelial cell. Hypertension12, 530–548.10.1161/01.HYP.12.6.530Search in Google Scholar
Grynkiewicz, G., Poenie, M., and Tsien, R.Y. (1985). A new generation of Ca2+-chelators with greatly improved fluorescent properties. J. Biol. Chem.260, 3340–3350.Search in Google Scholar
Hasan, A.A.K., Zisman, T., and Schmaier, A.H. (1998). Identification of cytokeratin 1 as a binding protein and presentation receptor for kininogens on endothelial cells. Proc. Natl. Acad. Sci. USA95, 3615–3620.10.1073/pnas.95.7.3615Search in Google Scholar
Herbert, J.M., Bono, F., Hérault, J.P., Avril, C., Dol, F., Mares, A.M., and Schaeffner, P. (1998). Effector protease receptor 1 mediates the mitogenic activity of factor Xa for vascular smooth muscle cells in vitro and in vivo. J. Clin. Invest.101, 993–1000.10.1172/JCI1833Search in Google Scholar
Hunfeld, A., Etscheid, M., König, H., Seitz, R., and Dodt, J. (1999). Detection of a novel plasma serine protease during purification of vitamin K-dependent coagulation factors. FEBS Lett.456, 290–294.10.1016/S0014-5793(99)00959-XSearch in Google Scholar
Ishai-Michaeli, R., Eldor, A., and Vlodavsky, I. (1990). Heparanase activity expressed by platelets, neutrophils and lymphoma cells releases active fibroblast growth factor from extracellular matrix. Cell Regul.1, 833–842.10.1091/mbc.1.11.833Search in Google Scholar PubMed PubMed Central
Jaffe, E.A., Nachman, R.L., Becker, C.G., and Minick, C.R. (1973). Culture of human endothelial cells derived from umbilical veins. Identification by morphologic and immunologic criteria. J. Clin. Invest.52, 2745–2756.Search in Google Scholar
Joseph, K., Ghebrehiwet, B., Peerschke, E.I., Reid, K.B., and Kaplan, A.P. (1996). Identification of the zinc-dependent endothelial cell binding protein for high molecular weight kininogen and factor XII: identity with the receptor that binds to the globular ‘heads’ of C1q (gC1q-R). Proc. Natl. Acad. Sci. USA93, 8552–8557.10.1073/pnas.93.16.8552Search in Google Scholar PubMed PubMed Central
Kannemeier, C., Al-Fakhri, N., Preissner, K.T., and Kanse, S.M. (2004). Factor VII-activating protease (FSAP) inhibits growth factor-mediated cell proliferation and migration of vascular smooth muscle cells. FASEB J.18, 728–730.10.1096/fj.03-0898fjeSearch in Google Scholar PubMed
Ko, F.N., Yang, Y.C., Huang, S.C., and Ou, J.T. (1996). Coagulation factor Xa stimulates platelet-derived growth factor release and mitogenesis in cultured vascular smooth muscle cells of rat. J. Clin. Invest.98, 1493–1501.10.1172/JCI118938Search in Google Scholar PubMed PubMed Central
Kooistra, T., Schrauwen, Y., Arts, J., and Emeis, J.J. (1994). Regulation of endothelial cell t-PA synthesis and release. Int. J. Hematol.59, 233–255.Search in Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of the bacteriophage T4. Nature227, 680–685.10.1038/227680a0Search in Google Scholar PubMed
Lobb, R.R. (1988). Thrombin inactivates acidic fibroblast growth factor but not basic fibroblast growth factor. Biochemistry27, 2572–2578.10.1021/bi00407a045Search in Google Scholar PubMed
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
Marceau, F. (1995). Kinin B1 receptors: a review. Immunopharmacology30, 1–26.10.1016/0162-3109(95)00011-HSearch in Google Scholar
Mayadas, T., Wagner, D.D., and Simpson, P.J. (1989). von Willebrand factor biosynthesis and partitioning between constitutive and regulated pathways of secretion after thrombin stimulation. Blood73, 706–711.10.1182/blood.V73.3.706.706Search in Google Scholar
Mignatti, P., Morimoto, T., and Rifkin, D.B. (1992). Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J. Cell Physiol.151, 81–93.10.1002/jcp.1041510113Search in Google Scholar
Molloy, C., Pawlowski, J.E., Taylor, D.S., Turner, C.E., Weber, H., and Peluso, M. (1996). Thrombin receptor activation elicits rapid protein tyrosine phosphorylation and stimulation of the Raf-1/MAP kinase pathway preceding delayed mitogenesis in cultured aortic smooth muscle cells. J. Clin. Invest.97, 1173–1183.10.1172/JCI118531Search in Google Scholar
Morgan-Boyd, R., Stewart, J.M., Vavrek, R.J., Hassid, A. (1987). Effects of bradykinin and angiotensin II on intracellular Ca2+ dynamics in endothelial cells. Am. J. Physiol253, C588–C598.10.1152/ajpcell.1987.253.4.C588Search in Google Scholar
Nakazawa, F., Kannemeier, C., Shibamiya, A., Song, Y., Tzima, E., Schubert, U., Koyama, T., Niepmann, M., Trusheim, H., Engelmann, B., and Preissner, K.T. (2005). Extracellular RNA is a natural cofactor for the (auto-)activation of factor VII-activating protease (FSAP). Biochem. J.385, 831–838.10.1042/BJ20041021Search in Google Scholar
Nawroth, P., Kisiel, W., and Stern, D. (1985). The role of endothelium in the homeostatic balance of haemostasis. Clin. Haematol.14, 531–546.10.1016/S0308-2261(21)00487-2Search in Google Scholar
Poulsen, L.K., Jacobsen, N., Sorensen, B.B., Bergenhem, N.C.H., Kelly, J.D., Forster, D.C., Thastrup, O., Ezban, M., and Petersen, L.C. (1998). Signal transduction in the mitogen-activated protein kinase pathway induced by binding of factor VIIa to tissue factor. J. Biol. Chem.273, 6228–6232.10.1074/jbc.273.11.6228Search in Google Scholar
Quinn, P.G. (2002). Mechanisms of basal and kinase-inducible transcription activation by CREB. Prog.72, 269–305.10.1016/S0079-6603(02)72072-2Search in Google Scholar
Renné, T., Dedio, J., David, G., and Müller-Esterl, W. (2000). High molecular weight kininogen utilizes heparan sulfate proteoglycans for accumulation on endothelial cells. J. Biol. Chem.275, 33688–33696.10.1074/jbc.M000313200Search in Google Scholar PubMed
Renné, T., Schuh, K., and Müller-Esterl, W. (2005). Local bradykinin formation is controlled by glycosaminoglycans. J. Immunol.175, 3377–3385.10.4049/jimmunol.175.5.3377Search in Google Scholar
Römisch, J., Feußner, A., Vermöhlen, S., and Stöhr, H.-A. (1999). A protease isolated from human plasma activating factor VII independent of tissue factor. Blood Coagul. Fibrinol.10, 471–479.10.1097/00001721-199912000-00004Search in Google Scholar
Römisch, J., Vermöhlen, S., Feußner, A., and Stöhr, H.-A. (2000). The FVII activating protease cleaves single-chain plasminogen activators. Haemostasis29, 292–299.Search in Google Scholar
Rottingen, J.-A., Enden, T., Camerer, E., Iversen, J.-G., and Prydz, H. (1995). Binding of human factor VIIa to tissue factor induces cytosolic Ca2+ signals in J82 cells, transfected COS-1 cells, Madin-Darby canine kidney cells and in human endothelial cells induced to synthesize tissue factor. J. Biol. Chem.270, 4650–4660.10.1074/jbc.270.9.4650Search in Google Scholar
Saksela, O., Moscatelli, D., Sommer, A., and Rifkin, D.B. (1988). Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J. Cell Biol.107, 743–751.10.1083/jcb.107.2.743Search in Google Scholar
Schmaier, A.H., Kuo, A., Lundberg, D., Murray, S., and Cines, D.B. (1988). Expression of high molecular weight kininogen on human umbilical vein endothelial cells. J. Biol. Chem.263, 16327.10.1016/S0021-9258(18)37596-3Search in Google Scholar
Schmaier, A.H. (2000). Plasma kallikrein/kinin system: a revised hypothesis for its activation and its physiologic contributions. Curr. Opin. Hematol.7, 261–265.10.1097/00062752-200009000-00001Search in Google Scholar PubMed
Shariat-Madar, Z., Mahdi, F., and Schmaier, A.H. (2001). Factor XI assembly and activation on human umbilical vein endothelial cells in culture. Thromb. Haemost.85, 544–551.10.1055/s-0037-1615619Search in Google Scholar
Sommer, A. and Rifkin, D.B. (1989). Interaction of heparin with human basic fibroblast growth factor: protection of the angiogenic protein from proteolytic degradation by a glycosaminoglycan. J. Cell Physiol.138, 215–220.10.1002/jcp.1041380129Search in Google Scholar PubMed
Sorensen, B.B., Freskgard, P.O., Nielsen, L.S., Rao, L.V., Ezban, M., and Petersen, L.C. (1999). Factor VIIa-induced p44/42 mitogen-activated protein kinase activation requires the proteolytic activity of factor VIIa and is independent of the tissue factor cytoplasmic domain. J. Biol. Chem.274, 21349–21354.10.1074/jbc.274.30.21349Search in Google Scholar PubMed
Sung, C.P., Arleth, A.J., Shikano, K., Berkowitz, B.A. (1988). Characterization and function of bradykinin receptors in vascular endothelial cells. J. Pharmacol. Exp. Ther.247, 8–13.Search in Google Scholar
Towbin, H., Staehelin, T., and Gordon, T. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA76, 4350–4354.10.1073/pnas.76.9.4350Search in Google Scholar PubMed PubMed Central
Whitelock, J.M., Murdoch, A.D., Iozzo, R.V., and Underwood, P.A. (1996). The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin, and heparanase. J. Biol. Chem.271, 10079–10086.10.1074/jbc.271.17.10079Search in Google Scholar PubMed
©2006 by Walter de Gruyter Berlin New York
Articles in the same Issue
- The arylhydrocarbon receptor: more than a tox story
- The aryl hydrocarbon receptor and light
- The impact of aryl hydrocarbon receptor signaling on matrix metabolism: implications for development and disease
- A role for the aryl hydrocarbon receptor in mammary gland tumorigenesis
- Evidence supporting the hypothesis that one of the main functions of the aryl hydrocarbon receptor is mediation of cell stress responses
- The arylhydrocarbon receptor repressor (AhRR): structure, expression, and function
- Impact of the arylhydrocarbon receptor on eugenol- and isoeugenol-induced cell cycle arrest in human immortalized keratinocytes (HaCaT)
- Aryl hydrocarbon receptor agonists directly activate estrogen receptor α in MCF-7 breast cancer cells
- Identifying target genes of the aryl hydrocarbon receptor nuclear translocator (Arnt) using DNA microarray analysis
- Transcriptional signatures of immune cells in aryl hydrocarbon receptor (AHR)-proficient and AHR-deficient mice
- 14-3-3 proteins in membrane protein transport
- The K+ channel gene, Kcnb1: genomic structure and characterization of its 5′-regulatory region as part of an overlapping gene group
- Structure-based specificity mapping of secreted aspartic proteases of Candida parapsilosis, Candida albicans, and Candida tropicalis using peptidomimetic inhibitors and homology modeling
- The solution structure of the membrane-proximal cytokine receptor domain of the human interleukin-6 receptor
- Sequence determination of lychnin, a type 1 ribosome-inactivating protein from Lychnis chalcedonica seeds
- Paired helical filaments contain small amounts of cholesterol, phosphatidylcholine and sphingolipids
- Induction of intracellular signalling in human endothelial cells by the hyaluronan-binding protease involves two distinct pathways
- A novel proteolytically processed CDP/Cux isoform of 90 kDa is generated by cathepsin L
- Degradation of apolipoprotein B-100 by lysosomal cysteine cathepsins
- Identification of trypsin I as a candidate for influenza A virus and Sendai virus envelope glycoprotein processing protease in rat brain
Articles in the same Issue
- The arylhydrocarbon receptor: more than a tox story
- The aryl hydrocarbon receptor and light
- The impact of aryl hydrocarbon receptor signaling on matrix metabolism: implications for development and disease
- A role for the aryl hydrocarbon receptor in mammary gland tumorigenesis
- Evidence supporting the hypothesis that one of the main functions of the aryl hydrocarbon receptor is mediation of cell stress responses
- The arylhydrocarbon receptor repressor (AhRR): structure, expression, and function
- Impact of the arylhydrocarbon receptor on eugenol- and isoeugenol-induced cell cycle arrest in human immortalized keratinocytes (HaCaT)
- Aryl hydrocarbon receptor agonists directly activate estrogen receptor α in MCF-7 breast cancer cells
- Identifying target genes of the aryl hydrocarbon receptor nuclear translocator (Arnt) using DNA microarray analysis
- Transcriptional signatures of immune cells in aryl hydrocarbon receptor (AHR)-proficient and AHR-deficient mice
- 14-3-3 proteins in membrane protein transport
- The K+ channel gene, Kcnb1: genomic structure and characterization of its 5′-regulatory region as part of an overlapping gene group
- Structure-based specificity mapping of secreted aspartic proteases of Candida parapsilosis, Candida albicans, and Candida tropicalis using peptidomimetic inhibitors and homology modeling
- The solution structure of the membrane-proximal cytokine receptor domain of the human interleukin-6 receptor
- Sequence determination of lychnin, a type 1 ribosome-inactivating protein from Lychnis chalcedonica seeds
- Paired helical filaments contain small amounts of cholesterol, phosphatidylcholine and sphingolipids
- Induction of intracellular signalling in human endothelial cells by the hyaluronan-binding protease involves two distinct pathways
- A novel proteolytically processed CDP/Cux isoform of 90 kDa is generated by cathepsin L
- Degradation of apolipoprotein B-100 by lysosomal cysteine cathepsins
- Identification of trypsin I as a candidate for influenza A virus and Sendai virus envelope glycoprotein processing protease in rat brain