Angiotensin I-converting enzyme inhibitor peptides derived from the endostatin-containing NC1 fragment of human collagen XVIII
-
Shirley L. Farias
Abstract
Extracellular matrix and soluble plasma proteins generate peptides that regulate biological activities such as cell growth, differentiation and migration. Bradykinin, a peptide released from kininogen by kallikreins, stimulates vasodilatation and endothelial cell proliferation. Various classes of substances can potentiate these biological actions of bradykinin. Among them, the best studied are bradykinin potentiating peptides (BPPs) derived from snake venom, which can also strongly inhibit angiotensin I-converting enzyme (ACE) activity. We identified and synthesized sequences resembling BPPs in the vicinity of potential proteolytic cleavage sites in the collagen XVIII molecule, close to endostatin. These peptides were screened as inhibitors of human recombinant wild-type ACE containing two intact functional domains; two full-length ACE mutants containing only a functional C- or N-domain catalytic site; and human testicular ACE, a natural form of the enzyme that only contains the C-domain. The BPP-like peptides inhibited ACE in the micromolar range and interacted preferentially with the C-domain. The proteolytic activity involved in the release of BPP-like peptides was studied in human serum and human umbilical-vein endothelial cells. The presence of enzymes able to release these peptides in blood led us to speculate on a physiological mechanism for the control of ACE activities.
References
Akchumov, A.A., Golubenko, Z., and Sosnina, N. (1992). Isolation and characterization of biological properties of inhibitors of angiotensin-converting-enzyme from the spider venom Latrodectus tredecimguttatus. Agents Actions (Suppl.) 38, 469–474.Search in Google Scholar
Araujo, M.C., Melo, R.L., Cesari, M.H., Juliano, M.A., Juliano, L., and Carmona, A.K. (2000). Peptidase specificity characterization of C- and N-terminal catalytic sites of angiotensin I-converting enzyme. Biochemistry39, 8519–8525.10.1021/bi9928905Search in Google Scholar
Barrett, A.J. and Kirschke, H. (1981). Cathepsin B, cathepsin H, and cathepsin L. Methods Enzymol.80, 535–561.10.1016/S0076-6879(81)80043-2Search in Google Scholar
Carmona, E., Dufour, E., Plouffe, C., Takebe, S., Mason, P., Mort, J.S., and Menard, R. (1996). Potency and selectivity of the cathepsin L propeptide as an inhibitor of cysteine proteases. Biochemistry35, 8149–8157.10.1021/bi952736sSearch in Google Scholar
Cintra, A.C., Vieira, C.A, and Giglio, J.R. (1990). Primary structure and biological activity of bradykinin potentiating peptide from Bothrops insularis snake venom. J. Protein Chem.9, 221–227.10.1007/BF01025312Search in Google Scholar
Cotton, J., Hayashi, M.A., Cuniasse, P., Vazeux, G., Ianzer, D., Camargo, A.C.M., and Dive, V. (2002). Selective inhibition of the C-domain of angiotensin I converting enzyme by bradykinin potentiating peptides. Biochemistry41, 6065–6071.10.1021/bi012121xSearch in Google Scholar
Cushman, D.W. and Ondetti, M.A. (1980). Inhibitors of angiotensin-converting enzyme. Prog. Med. Chem.17, 41–104.10.1016/S0079-6468(08)70157-7Search in Google Scholar
Ehlers, M.R. and Riordan, J.F. (1991). Angiotensin-converting enzyme: zinc- and inhibitor-binding stoichiometries of the somatic and testis isozymes. Biochemistry30, 7118–7126.10.1021/bi00243a012Search in Google Scholar PubMed
Emanueli, C., Salis, M.B., Stacca, T., Pintus, G., Kirchmair, R., Isner, J.M., Pinna, A., Gaspa, L., Regoli, D., Cayla, C., et al. (2002). Targeting kinin B1 receptor for therapeutic neovascularization. Circulation105, 360–366.10.1161/hc0302.102142Search in Google Scholar PubMed
Erdös, E.G. and Marcic, B.M. (2001). Kinins, receptors, kininases and inhibitors – where did they lead us? Biol. Chem.382, 43–47.Search in Google Scholar
Fabre, J.E., Rivard, A., Magner, M., Silver, M., and Isner, J.M. (1999). Tissue inhibition of angiotensin-converting enzyme activity stimulates angiogenesis in vivo. Circulation99, 3043–3049.10.1161/01.CIR.99.23.3043Search in Google Scholar PubMed
Felbor, U., Dreier, L., Bryant, R.A., Ploegh, H.L., Olsen, B.R., and Mothes, W. (2000). Secreted cathepsin L generates endostatin from collagen XVIII. EMBO J.19, 1187–1194.10.1093/emboj/19.6.1187Search in Google Scholar PubMed PubMed Central
Ferreira, L.A, Henriques, O.B., Lebrun, I, Batista, M.B., Prezoto, B.C, Andreoni, A.S., Zelnic, R., and Habermehl, G. (1992). A new bradykinin-potentiating peptide (peptide P) isolated from the venom of Bothrops jararacussu (jararacucu tapete, urutu dourado). Toxicon30, 33–40.10.1016/0041-0101(92)90499-USearch in Google Scholar
Ferreira, L.A., Alves, W.E., and Henriques, O.B. (1993). Peptide T, a novel bradykinin potentiator isolated from Tityus serrulatus scorpion venom. Toxicon31, 941–947.10.1016/0041-0101(93)90253-FSearch in Google Scholar
Ferreira, S.H. (1965). A bradykinin-potentiating factor (BPF) present in the venom of Bothrops jararaca. Br. J. Pharmacol. Chemother.24, 163–169.10.1111/j.1476-5381.1965.tb02091.xSearch in Google Scholar
Ferreira, S.H., Bartelt, D.C., and Greene, L.J. (1970). Isolation of bradykinin potentiating peptides from Bothrops jararaca venom. Biochemistry9, 2583–2593.10.1021/bi00815a005Search in Google Scholar
Ferreras, M., Felbor, U., Lenhard, T., Olsen, B.R., and Delaissé, J. (2000). Generation and degradation of human endostatin proteins by various proteinases. FEBS Lett.486, 247–251.10.1016/S0014-5793(00)02249-3Search in Google Scholar
Freer, R.J. and Stewart, J.M. (1971). Synthetic bradykinin-potentiating peptides related to those isolated from snake venom. Ciencia Cultura23, 539–542.Search in Google Scholar
Fujita, M., Hayashi, I., Yamashina, S., Itoman, M., and Majima, M. (2002). Blockade of angiotensin AT1a receptor signaling reduces tumor growth, angiogenesis and metastasis. Biochem. Biophys. Res. Commun.294, 1450–1456.10.1016/S0006-291X(02)00496-5Search in Google Scholar
Heljasvaara, R., Nyberg, P., Luostarinen, J., Parikka, M., Heikkila, P., Rehn, M., Sorsa, T., Salo, T., and Pihlajaniemi, T. (2005). Generation of biologically active endostatin fragments from human collagen XVIII by distinct matrix metalloproteases. Exp. Cell Res.307, 292–304.10.1016/j.yexcr.2005.03.021Search in Google Scholar
Henriques, O.B., de Jesus, R.B., and Santos, R.A. (1987). Bradykinin potentiating peptides isolated from α-casein tryptic hydrolysate. Biochem. Pharmacol.36, 182–184.10.1016/0006-2952(87)90398-4Search in Google Scholar
Hii, S.-I., Nicol, D.L., Gotley, D.C., Thompson, L.C. Green, M.K., and Jonsson, J.R. (1998). Captopril inhibits tumour growth in a xenograft model of human renal cell carcinoma. Br. J. Cancer77, 880–883.10.1038/bjc.1998.145Search in Google Scholar PubMed PubMed Central
Hirata, I.Y, Cezari, M.H.C., Nakaie, C.R., Boshcov, P., Ito, A.S., Juliano, M.A., and Juliano, L. (1994). Internally quenched fluorogenic protease substrates: Solid-phase synthesis and fluorescent spectroscopy of peptides containing ortho-aminobenzoyl-dinitrophenyl groups as donor-acceptor pairs. Lett. Pept. Sci.1, 299–308.Search in Google Scholar
Ianzer, D., Konno, K., Marques-Porto, R., Portaro, F.C., Stocklin, R., Camargo, A.C.M., and Pimenta, D.C. (2004). Identification of five new bradykinin potentiating peptides (BPPs) from Bothrops jararaca crude venom by using electrospray ionization tandem mass spectrometry after a two-step liquid chromatography. Peptides25, 1085–1092.10.1016/j.peptides.2004.04.006Search in Google Scholar PubMed
Iozzo, R.V. (2005). Basement membrane proteoglycans: from cellar to ceiling. Nat. Rev. Mol. Cell. Biol.6, 646–656.10.1038/nrm1702Search in Google Scholar
Ivanov, V.T., Karelin, A.A., Philippova, M.M., Nazimov, I.V., and Pletnev, V.Z. (1997). Hemoglobin as a source of endogenous bioactive peptides: the concept of tissue-specific peptide pool. Biopolymers43, 171–178.10.1002/(SICI)1097-0282(1997)43:2<171::AID-BIP10>3.0.CO;2-OSearch in Google Scholar
Kato, H. and Suzuki, T. (1971). Bradykinin-potentiating peptides from the venom of Agkistrodom halys blomhoffi. Isolation of five bradykinin potentiators and the amino acid sequences of two of them, potentiators B and C. Biochemistry10, 972–980.Search in Google Scholar
Lebrun, I., Lebrun, F.L.A.S., Henriques, O.B., Carmona, A.K., Juliano, L., and Camargo, A.C.M. (1995). Isolation and characterization of a new bradykinin potentiating octapeptide from γ-casein. Can. J. Physiol. Pharmacol.73, 85–91.10.1139/y95-012Search in Google Scholar
Lin, H.C., Chang, J.H., Jain, S., Gabison, E.E., Kure, T., Kato, T., Fukai, N., and Azar, D.T. (2001). Matrilysin cleavage of corneal collagen type XVIII NC1 domain and generation of a 28-kDa fragment. Invest. Ophthalmol. Vis. Sci.42, 2517–2524.Search in Google Scholar
Lindberg, H., Nielsen, D., Jensen, B.V., Eriksen, J., and Skovsgaard, T. (2004). Angiotensin-converting enzyme inhibitors for cancer treatment? Acta Oncol.43, 142–152.Search in Google Scholar
Lorell, B.H. (1999). Role of angiotensin AT1, and AT2 receptors in cardiac hypertrophy and disease. Am. J. Cardiol.83, 48H–52H.10.1016/S0002-9149(99)00258-1Search in Google Scholar
Marneros, A.G. and Olsen, B.R. (2001). The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol.20, 337–345.10.1016/S0945-053X(01)00151-2Search in Google Scholar
Mueller, S., Gothe, R., Siems, W.D., Vietinghoff, G., Paegelow, I., and Reissmann, S. (2005). Potentiation of bradykinin actions by analogues of the bradykinin potentiating nonapeptide BPP9a. Peptides26, 1235–1247.10.1016/j.peptides.2005.03.046Search in Google Scholar
Nagler, D.K., Storer, A.C., Portaro, F.C., Carmona, E., Juliano, L., and Menard, R. (1997). Major increase in endopeptidase activity of human cathepsin B upon removal of occluding loop contacts. Biochemistry36, 12608–12615.10.1021/bi971264+Search in Google Scholar
O'Reilly, M.S., Boehm, T., Shing, Y., Fukai, N., Vasios, G., Lane, W.S., Flynn, E., Birkhead, J.R., Olsen, B.R., and Folkman, J. (1997). Endostatin: an endogenous inhibitor of angiogenesis and tumor growth. Cell88, 277–285.10.1016/S0092-8674(00)81848-6Search in Google Scholar
Parenti, A., Morbidelli, L., Ledda, F., Granger, H.J., and Ziche, M. (2001). The bradykinin/B1 receptor promotes angiogenesis by up-regulation of endogenous FGF-2 in endothelium via the nitric oxide synthase pathway. FASEB J.15, 1487–1489.10.1096/fj.00-0503fjeSearch in Google Scholar
Piot, J.M, Zhao, Q., Guillochon, D., Ricart, G., and Thomas, D. (1992). Isolation and characterization of a bradykinin-potentiating peptide from a bovine peptic hemoglobin hydrolysate. FEBS Lett.299, 75–79.10.1016/0014-5793(92)80104-OSearch in Google Scholar
Pupilli, C., Lasagni, L., Romagnani, P., Bellini, F., Mannelli, M., Misciglia, N., Mavilia, C., Vellei U., Villari, D., and Serio, M. (1999). Angiotensin II stimulates the synthesis and secretion of vascular permeability factor/vascular endothelial growth factor in human mesangial cells. J. Am. Soc. Nephrol.10, 245–255.10.1681/ASN.V102245Search in Google Scholar
Regoli, D. and Barabe, J. (1980). Pharmacology of bradykinin and related kinins. Pharmacol. Rev.32, 1–46.Search in Google Scholar
Sasaki, T., Fukai, N., Mann, K., Göhring, W., Olsen, B.R., and Timpl, R. (1998). Structure, function and tissue forms of the C-terminal globular domain of collagen XVIII containing the angiogenesis inhibitor endostatin. EMBO J.17, 4249–4256.10.1093/emboj/17.15.4249Search in Google Scholar
Silvestre, J., Bergaya, S., Tamarat, R., Duriez, M., Boulanger, C.M., and Levy, B.I. (2001). Proangiogenic effect of angiotensin-converting enzyme inhibition is mediated by the bradykinin B2 receptor pathway. Circ. Res.89, 678–683.10.1161/hh2001.097691Search in Google Scholar
Small, W., Molteni, A., Kim, Y.T., Taylor, J.M., Chen, Z., and Ward, W.F. (1997). Captopril modulates hormone receptor concentration and inhibits proliferation of human mammary ductal carcinoma cells in culture. Breast Cancer Res. Treat.44, 217–224.10.1023/A:1005827119296Search in Google Scholar
Volpert, O.V., Ward, W.F., Lingen, M.W., Chesler, L., Solt, D.B., Johnson, M.D., Molteni, A., Polverini, P.J., and Bouck, N.P. (1996). Captopril inhibits angiogenesis and slows the growth of experimental tumors in rats. J. Clin. Invest.98, 671–679.10.1172/JCI118838Search in Google Scholar
Wei, L., Alhenc-Gelas, F., Corvol, P., and Clauser, E. (1991). The two homologous domains of human angiotensin I-converting enzyme are both catalytically active. J. Biol. Chem.266, 9002–9008.10.1016/S0021-9258(18)31543-6Search in Google Scholar
Wen, W., Moses, M.A., Wiederschain, D., Arbiser, J.L., and Folkman, J. (1999). The generation of endostatin is mediated by elastase. Cancer Res.59, 6052–6056.Search in Google Scholar
Williams, B., Baker A.Q., Gallacher B., and Lodwick, D. (1995). Angiotensin II increases vascular permeability factor gene expression by human vascular smooth muscle cells. Hypertension25, 913–917.10.1161/01.HYP.25.5.913Search in Google Scholar
Woodman, Z.L., Oppong, S.Y., Cook, S., Hooper, N.M., Schwager, S.L., Brandt, W.F., Ehlers, M.R., and Sturrock, E.D. (2000). Shedding of somatic angiotensin-converting enzyme (ACE) is inefficient compared with testis ACE despite cleavage at identical stalk sites. Biochem. J.347, 711–718.10.1042/bj3470711Search in Google Scholar
Yamafuji, K., Taniguchi, Y, and Sakamoto, E. (1996). The thiol enzyme from rat spleen that produces bradykinin potentiating peptide from rat plasma. Immunopharmacology32, 157–159.10.1016/0162-3109(95)00080-1Search in Google Scholar
Yoshiji, H., Kuriyama, S., Kawata, M., Yoshii, J., Ikenaka, Y., Noguchi, R., Nakatani, T., Tsujinoue H., and Fukui, H. (2001). The angiotensin I-converting enzyme inhibitor perindopril suppresses tumor growth and angiogenesis: possible role of the vascular endothelial growth factor. Clin. Cancer Res.7, 1073–1078.Search in Google Scholar
©2006 by Walter de Gruyter Berlin New York
Articles in the same Issue
- Protein aggregation in crowded environments
- Nitrite, a naturally occurring precursor of nitric oxide that acts like a ‘prodrug’
- Functional studies of the small subunit of EcoHK31I DNA methyltransferase
- Functional analysis of amino acid residues at the dimerisation interface of KpnI DNA methyltransferase
- Conformation and stability of the Streptococcus pyogenes pSM19035-encoded site-specific β recombinase, and identification of a folding intermediate
- Tyr-48, a conserved residue in ribotoxins, is involved in the RNA-degrading activity of α-sarcin
- Pathogenicity of catalytic antibodies: catalytic activity of Bence Jones proteins from myeloma patients with renal impairment can elicit cytotoxic effects
- Transgenic expression of gallerimycin, a novel antifungal insect defensin from the greater wax moth Galleria mellonella, confers resistance to pathogenic fungi in tobacco
- Catalytic pathways of Euphorbia characias peroxidase reacting with hydrogen peroxide
- Biochemical and pharmacological characterization of the human bradykinin subtype 2 receptor produced in mammalian cells using the Semliki Forest virus system
- A spectroscopic analysis of the interaction between the human regulatory proteins RACK1 and Ki-1/57
- Subcellular localisation of human inositol 1,4,5-trisphosphate 3-kinase C: species-specific use of alternative export sites for nucleo-cytoplasmic shuttling indicates divergent roles of the catalytic and N-terminal domains
- The gating effect of calmodulin and calcium on the connexin50 hemichannel
- C-Terminal fusion of eGFP to the bradykinin B2 receptor strongly affects down-regulation but not receptor internalization or signaling
- Angiotensin I-converting enzyme inhibitor peptides derived from the endostatin-containing NC1 fragment of human collagen XVIII
- μ-Calpain binds to lipid bilayers via the exposed hydrophobic surface of its Ca2+-activated conformation
- Cathepsin L splice variants in human breast cell lines
Articles in the same Issue
- Protein aggregation in crowded environments
- Nitrite, a naturally occurring precursor of nitric oxide that acts like a ‘prodrug’
- Functional studies of the small subunit of EcoHK31I DNA methyltransferase
- Functional analysis of amino acid residues at the dimerisation interface of KpnI DNA methyltransferase
- Conformation and stability of the Streptococcus pyogenes pSM19035-encoded site-specific β recombinase, and identification of a folding intermediate
- Tyr-48, a conserved residue in ribotoxins, is involved in the RNA-degrading activity of α-sarcin
- Pathogenicity of catalytic antibodies: catalytic activity of Bence Jones proteins from myeloma patients with renal impairment can elicit cytotoxic effects
- Transgenic expression of gallerimycin, a novel antifungal insect defensin from the greater wax moth Galleria mellonella, confers resistance to pathogenic fungi in tobacco
- Catalytic pathways of Euphorbia characias peroxidase reacting with hydrogen peroxide
- Biochemical and pharmacological characterization of the human bradykinin subtype 2 receptor produced in mammalian cells using the Semliki Forest virus system
- A spectroscopic analysis of the interaction between the human regulatory proteins RACK1 and Ki-1/57
- Subcellular localisation of human inositol 1,4,5-trisphosphate 3-kinase C: species-specific use of alternative export sites for nucleo-cytoplasmic shuttling indicates divergent roles of the catalytic and N-terminal domains
- The gating effect of calmodulin and calcium on the connexin50 hemichannel
- C-Terminal fusion of eGFP to the bradykinin B2 receptor strongly affects down-regulation but not receptor internalization or signaling
- Angiotensin I-converting enzyme inhibitor peptides derived from the endostatin-containing NC1 fragment of human collagen XVIII
- μ-Calpain binds to lipid bilayers via the exposed hydrophobic surface of its Ca2+-activated conformation
- Cathepsin L splice variants in human breast cell lines