Mitogenic Activity and Signaling Mechanism of 2-(14,15- Epoxyeicosatrienoyl)Glycerol, a Novel Cytochrome P450 Arachidonate Metabolite

REFERENCES

• Amsler, K., and J. S. Cook. 1982. Development of Na+-dependent hexose transport in a cultured line of porcine kidney cells. Am. J. Physiol. 242:C94–C101.
   PubMedGoogle Scholar
• Asakura, M., M. Kitakaze, S. Takashima, Y. Liao, F. Ishikura, T. Yoshinaka, H. Ohmoto, K. Node, K. Yoshino, H. Ishiguro, H. Asanuma, S. Sanada, Y. Matsumura, H. Takeda, S. Beppu, M. Tada, M. Hori, and S. Higashiyama. 2002. Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-EGF: metalloproteinase inhibitors as a new therapy. Nat. Med. 8:35–40.
   PubMed Web of Science ®Google Scholar
• Blobel, C. P. 2005. ADAMs: key components in EGFR signalling and development. Nat. Rev. Mol. Cell. Biol. 6:32–43.
   PubMed Web of Science ®Google Scholar
• Bonvalet, J. P., P. Pradelles, and N. Farman. 1987. Segmental synthesis and actions of prostaglandins along the nephron. Am. J. Physiol. 253:F377–F387.
   PubMed Web of Science ®Google Scholar
• Brachmann, R., P. B. Lindquist, M. Nagashima, W. Kohr, T. Lipari, M. Napier, and R. Derynck. 1989. Transmembrane TGF-alpha precursors activate EGF/TGF-alpha receptors. Cell 56:691–700.
   PubMed Web of Science ®Google Scholar
• Burns, K. D., J. Capdevila, S. Wei, M. D. Breyer, T. Homma, and R. C. Harris. 1995. Role of cytochrome P-450 epoxygenase metabolites in EGF signaling in renal proximal tubule. Am. J. Physiol. 269:C831—C340.
   Google Scholar
• Campbell, W. B., D. Gebremedhin, P. F. Pratt, and D. R. Harder. 1996. Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors. Circ. Res. 78:415–423.
   PubMed Web of Science ®Google Scholar
• Capdevila, J., N. Chacos, J. Werringloer, R. A. Prough, and R. W. Estabrook. 1981. Liver microsomal cytochrome P-450 and the oxidative metabolism of arachidonic acid. Proc. Natl. Acad. Sci. USA 78:5362–5366.
   PubMed Web of Science ®Google Scholar
• Capdevila, J. H., J. R. Falck, E. Dishman, and A. Karara. 1990. Cytochrome P-450 arachidonate oxygenase. Methods Enzymol. 187:385–394.
   PubMedGoogle Scholar
• Capdevila, J. H., J. R. Falck, and R. C. Harris. 2000. Cytochrome P450 and arachidonic acid bioactivation. Molecular and functional properties of the arachidonate monooxygenase. J. Lipid Res. 41:163–181.
   PubMed Web of Science ®Google Scholar
• Carpenter, G., and S. Cohen. 1990. Epidermal growth factor. J. Biol. Chem. 265:7709–7712.
   PubMed Web of Science ®Google Scholar
• Chen, J. K., J. Capdevila, and R. C. Harris. 2002. Heparin-binding EGF-like growth factor mediates the biological effects of P450 arachidonate epoxygenase metabolites in epithelial cells. Proc. Natl. Acad. Sci. USA 99:6029–6034.
   PubMed Web of Science ®Google Scholar
• Chen, J. K., J. Capdevila, and R. C. Harris. 2000. Overexpression of C-terminal Src kinase blocks 14, 15-epoxyeicosatrienoic acid-induced tyrosine phosphorylation and mitogenesis. J. Biol. Chem. 275:13789–13792.
   PubMedGoogle Scholar
• Chen, J. K., J. Chen, J. D. Imig, S. Wei, D. L. Hachey, S. G. Jagadeesh, J. R. Falck, J. H. Capdevila, and R. C. Harris. Identification of novel endogenous cytochrome P450 arachidonate metabolites with high affinity for cannabinoid receptors, in press.
   Google Scholar
• Chen, J. K., J. R. Falck, K. M. Reddy, J. Capdevila, and R. C. Harris. 1998. Epoxyeicosatrienoic acids and their sulfonimide derivatives stimulate tyrosine phosphorylation and induce mitogenesis in renal epithelial cells. J. Biol. Chem. 273:29254–29261.
   PubMed Web of Science ®Google Scholar
• Chen, J. K., D. W. Wang, J. R. Falck, J. Capdevila, and R. C. Harris. 1999. Transfection of an active cytochrome P450 arachidonic acid epoxygenase indicates that 14,15-epoxyeicosatrienoic acid functions as an intracellular second messenger in response to epidermal growth factor. J. Biol. Chem. 274:4764–4769.
   PubMed Web of Science ®Google Scholar
• Corey, E. J., N. Haruki, and J. R. Falck. 1979. Selective epoxidation of eicosa-cis-5,8,11,14-tetraenoic (arachidonic) acid and eicosa-cis-8,11,14-trienoic acid. J. Am. Chem. Soc. 101:1586–1587.
   Web of Science ®Google Scholar
• Derynck, R. 1992. The physiology of transforming growth factor-alpha. Adv. Cancer Res. 58:27–52.
   PubMed Web of Science ®Google Scholar
• Dethlefsen, S. M., G. Raab, M. A. Moses, R. M. Adam, M. Klagsbrun, and M. R. Freeman. 1998. Extracellular calcium influx stimulates metalloproteinase cleavage and secretion of heparin-binding EGF-like growth factor independently of protein kinase C. J. Cell Biochem. 69:143–153.
   PubMedGoogle Scholar
• Di Marzo, V. 1995. Arachidonic acid and eicosanoids as targets and effectors in second messenger interactions. Prostaglandins Leukot. Essent. Fatty Acids 53:239–254.
   PubMedGoogle Scholar
• Dong, J., and H. S. Wiley. 2000. Trafficking and proteolytic release of epidermal growth factor receptor ligands are modulated by their membrane-anchoring domains. J. Biol. Chem. 275:557–564.
   PubMedGoogle Scholar
• Endou, H. 1983. Cytochrome P-450 monooxygenase system in the rabbit kidney: its intranephron localization and its induction. Jpn. J. Pharmacol. 33:423–433.
   PubMedGoogle Scholar
• Escalante, B. A., R. Staudinger, M. Schwartzman, and N. Abraham. 1995. Amiloride-sensitive ion transport inhibition by epoxyeicosatrienoic acids in renal epithelial cells. Adv. Prostaglandin Thromboxane Leukot. Res. 23:207–209.
   PubMedGoogle Scholar
• Fischer, O. M., S. Hart, A. Gschwind, N. Prenzel, and A. Ullrich. 2004. Oxidative and osmotic stress signaling in tumor cells is mediated by ADAM proteases and heparin-binding epidermal growth factor. Mol. Cell. Biol. 24:5172–5183.
   PubMed Web of Science ®Google Scholar
• Fisslthaler, B., R. Popp, L. Kiss, M. Potente, D. R. Harder, I. Fleming, and R. Busse. 1999. Cytochrome P450 2C is an EDHF synthase in coronary arteries. Nature 401:493–497.
   PubMed Web of Science ®Google Scholar
• Graier, W. F., S. Simecek, and M. Sturek. 1995. Cytochrome P450 mono-oxygenase-regulated signalling of Ca2+ entry in human and bovine endothelial cells. J. Physiol. 482:259–274.
   PubMed Web of Science ®Google Scholar
• Groenen, L. C., E. C. Nice, and A. W. Burgess. 1994. Structure-function relationships for the EGF/TGF-alpha family of mitogens. Growth Factors 11:235–257.
   PubMed Web of Science ®Google Scholar
• Han, L., and R. K. Razdan. 1999. Total synthesis of 2-arachidonylglycerol (2-ara-Gl). Tetrahedron Lett. 40:1631–1634.
   Google Scholar
• Harris, R. C., E. Chung, and R. J. Coffey. 2003. EGF receptor ligands. Exp. Cell Res. 284:2–13.
   PubMed Web of Science ®Google Scholar
• Harris, R. C., T. Homma, H. R. Jacobson, and J. Capdevila. 1990. Epoxyeicosatrienoic acids activate Na+/H+ exchange and are mitogenic in cultured rat glomerular mesangial cells. J. Cell Physiol. 144:429–437.
   PubMed Web of Science ®Google Scholar
• Higashiyama, S., J. A. Abraham, J. Miller, J. C. Fiddes, and M. Klagsbrun. 1991. A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 251:936–939.
   PubMed Web of Science ®Google Scholar
• Higashiyama, S., R. Iwamoto, K. Goishi, G. Raab, N. Taniguchi, M. Klagsbrun, and E. Mekada. 1995. The membrane protein CD9/DRAP 27 potentiates the juxtacrine growth factor activity of the membrane-anchored heparin-binding EGF-like growth factor. J. Cell Biol. 128:929–938.
   PubMed Web of Science ®Google Scholar
• Hinkle, C. L., S. W. Sunnarborg, D. Loiselle, C. E. Parker, M. Stevenson, W. E. Russell, and D. C. Lee. 2004. Selective roles for tumor necrosis factor alpha-converting enzyme/ADAM17 in the shedding of the epidermal growth factor receptor ligand family: the juxtamembrane stalk determines cleavage efficiency. J. Biol. Chem. 279:24179–24188.
   PubMed Web of Science ®Google Scholar
• Hise, M. K., M. Salmanullah, L. Liu, C. I. Drachenberg, J. C. Papadimitriou, and R. M. Rohan. 2001. Control of the epidermal growth factor receptor and its ligands during renal injury. Nephron 88:71–79.
   PubMed Web of Science ®Google Scholar
• Hoebel, B. G., E. Steyrer, and W. F. Graier. 1998. Origin and function of epoxyeicosatrienoic acids in vascular endothelial cells: more than just endothelium-derived hyperpolarizing factor? Clin. Exp. Pharmacol. Physiol. 25:826–830.
   PubMed Web of Science ®Google Scholar
• Homma, T., M. Sakai, H. F. Cheng, T. Yasuda, R. J. Coffey, Jr., and R. C. Harris. 1995. Induction of heparin-binding epidermal growth factor-like growth factor mRNA in rat kidney after acute injury. J. Clin. Investig. 96:1018–1025.
   PubMed Web of Science ®Google Scholar
• Imig, J. D. 2000. Epoxygenase metabolites. Epithelial and vascular actions. Mol. Biotechnol. 16:233–251.
   PubMed Web of Science ®Google Scholar
• Izumi, Y., M. Hirata, H. Hasuwa, R. Iwamoto, T. Umata, K. Miyado, Y. Tamai, T. Kurisaki, A. Sehara-Fujisawa, S. Ohno, and E. Mekada. 1998. A metalloprotease-disintegrin, MDC9/meltrin-gamma/ADAM9 and PKCδ are involved in TPA-induced ectodomain shedding of membrane-anchored heparin-binding EGF-like growth factor. EMBO J. 17:7260–7272.
   PubMed Web of Science ®Google Scholar
• Kurisaki, T., A. Masuda, K. Sudo, J. Sakagami, S. Higashiyama, Y. Matsuda, A. Nagabukuro, A. Tsuji, Y. Nabeshima, M. Asano, Y. Iwakura, and A. Sehara-Fujisawa. 2003. Phenotypic analysis of Meltrin α (ADAM12)-deficient mice: involvement of Meltrin α in adipogenesis and myogenesis. Mol. Cell. Biol. 23:55–61.
   PubMed Web of Science ®Google Scholar
• Lemjabbar, H., and C. Basbaum. 2002. Platelet-activating factor receptor and ADAM10 mediate responses to Staphylococcus aureus in epithelial cells. Nat. Med. 8:41–46.
   PubMed Web of Science ®Google Scholar
• Makita, K., J. R. Falck, and J. H. Capdevila. 1996. Cytochrome P450, the arachidonic acid cascade, and hypertension: new vistas for an old enzyme system. FASEB J. 10:1456–1463.
   PubMed Web of Science ®Google Scholar
• Massague, J., and A. Pandiella. 1993. Membrane-anchored growth factors. Annu. Rev. Biochem. 62:515–541.
   PubMed Web of Science ®Google Scholar
• Matsuda, L. A., S. J. Lolait, M. J. Brownstein, A. C. Young, and T. I. Bonner. 1990. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561–564.
   PubMed Web of Science ®Google Scholar
• McCole, D. F., S. J. Keely, R. J. Coffey, and K. E. Barrett. 2002. Transactivation of the epidermal growth factor receptor in colonic epithelial cells by carbachol requires extracellular release of transforming growth factor-alpha. J. Biol. Chem. 277:42603–42612.
   PubMedGoogle Scholar
• Mechoulam, R., S. Ben-Shabat, L. Hanus, M. Ligumsky, N. E. Kaminski, A. R. Schatz, A. Gopher, S. Almog, B. R. Martin, D. R. Compton, and et al. 1995. Identification of an endogenous 2-monoglyceride, present in canine gut, that binds to cannabinoid receptors. Biochem. Pharmacol. 50:83–90.
   PubMed Web of Science ®Google Scholar
• Mifune, M., H. Ohtsu, H. Suzuki, H. Nakashima, E. Brailoiu, N. J. Dun, G. D. Frank, T. Inagami, S. Higashiyama, W. G. Thomas, A. D. Eckhart, P. J. Dempsey, and S. Eguchi. 2005. G protein coupling and second messenger generation are indispensable for metalloprotease-dependent, heparin-binding epidermal growth factor shedding through angiotensin II type-1 receptor. J. Biol. Chem. 280:26592–26599.
   PubMed Web of Science ®Google Scholar
• Morrison, A. R., and N. Pascoe. 1981. Metabolism of arachidonate through NADPH-dependent oxygenase of renal cortex. Proc. Natl. Acad. Sci. USA 78:7375–7378.
   PubMed Web of Science ®Google Scholar
• Munro, S., K. L. Thomas, and M. Abu-Shaar. 1993. Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61–65.
   PubMed Web of Science ®Google Scholar
• Munzenmaier, D. H., and D. R. Harder. 2000. Cerebral microvascular endothelial cell tube formation: role of astrocytic epoxyeicosatrienoic acid release. Am. J. Physiol. Heart Circ. Physiol. 278:H1163–H1167.
   PubMedGoogle Scholar
• Murai, T., Y. Miyazaki, H. Nishinakamura, K. N. Sugahara, T. Miyauchi, Y. Sako, T. Yanagida, and M. Miyasaka. 2004. Engagement of CD44 promotes Rac activation and CD44 cleavage during tumor cell migration. J. Biol. Chem. 279:4541–4550.
   PubMed Web of Science ®Google Scholar
• Needleman, P., J. Turk, B. A. Jakschik, A. R. Morrison, and J. B. Lefkowith. 1986. Arachidonic acid metabolism. Annu. Rev. Biochem. 55:69–102.
   PubMed Web of Science ®Google Scholar
• Node, K., Y. Huo, X. Ruan, B. Yang, M. Spiecker, K. Ley, D. C. Zeldin, and J. K. Liao. 1999. Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science 285:1276–1279.
   PubMed Web of Science ®Google Scholar
• Ohtsu, H., P. J. Dempsey, and S. Eguchi. 2006. ADAMs as mediators of EGF receptor transactivation by G protein-coupled receptors. Am. J. Physiol. Cell Physiol. 291:C1–10.
   PubMedGoogle Scholar
• Oliw, E. H., J. A. Lawson, A. R. Brash, and J. A. Oates. 1981. Arachidonic acid metabolism in rabbit renal cortex. Formation of two novel dihydroxyeicosatrienoic acids. J. Biol. Chem. 256:9924–9931.
   PubMed Web of Science ®Google Scholar
• Pierce, K. L., A. Tohgo, S. Ahn, M. E. Field, L. M. Luttrell, and R. J. Lefkowitz. 2001. Epidermal growth factor (EGF) receptor-dependent ERK activation by G protein-coupled receptors: a co-culture system for identifying intermediates upstream and downstream of heparin-binding EGF shedding. J. Biol. Chem. 276:23155–23160.
   PubMedGoogle Scholar
• Potente, M., U. R. Michaelis, B. Fisslthaler, R. Busse, and I. Fleming. 2002. Cytochrome P450 2C9-induced endothelial cell proliferation involves induction of mitogen-activated protein (MAP) kinase phosphatase-1, inhibition of the c-Jun N-terminal kinase, and up-regulation of cyclin D1. J. Biol. Chem. 277:15671–15676.
   PubMed Web of Science ®Google Scholar
• Prenzel, N., E. Zwick, H. Daub, M. Leserer, R. Abraham, C. Wallasch, and A. Ullrich. 1999. EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature 402:884–888.
   PubMed Web of Science ®Google Scholar
• Roghani, M., J. D. Becherer, M. L. Moss, R. E. Atherton, H. Erdjument-Bromage, J. Arribas, R. K. Blackburn, G. Weskamp, P. Tempst, and C. P. Blobel. 1999. Metalloprotease-disintegrin MDC9: intracellular maturation and catalytic activity. J. Biol. Chem. 274:3531–3540.
   PubMed Web of Science ®Google Scholar
• Sahin, U., G. Weskamp, K. Kelly, H. M. Zhou, S. Higashiyama, J. Peschon, D. Hartmann, P. Saftig, and C. P. Blobel. 2004. Distinct roles for ADAM10 and ADAM17 in ectodomain shedding of six EGFR ligands. J. Cell Biol. 164:769–779.
   PubMed Web of Science ®Google Scholar
• Sakai, M., M. Zhang, T. Homma, B. Garrick, J. A. Abraham, J. A. McKanna, and R. C. Harris. 1997. Production of heparin binding epidermal growth factor-like growth factor in the early phase of regeneration after acute renal injury. Isolation and localization of bioactive molecules. J. Clin. Investig. 99:2128–2138.
   PubMed Web of Science ®Google Scholar
• Seals, D. F., and S. A. Courtneidge. 2003. The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 17:7–30.
   PubMed Web of Science ®Google Scholar
• Shing, Y., G. Christofori, D. Hanahan, Y. Ono, R. Sasada, K. Igarashi, and J. Folkman. 1993. Betacellulin: a mitogen from pancreatic beta cell tumors. Science 259:1604–1607.
   PubMed Web of Science ®Google Scholar
• Shoyab, M., G. D. Plowman, V. L. McDonald, J. G. Bradley, and G. J. Todaro. 1989. Structure and function of human amphiregulin: a member of the epidermal growth factor family. Science 243:1074–1076.
   PubMed Web of Science ®Google Scholar
• Staudinger, R., B. Escalante, M. L. Schwartzman, and N. G. Abraham. 1994. Effects of epoxyeicosatrienoic acids on 86Rb uptake in renal epithelial cells. J. Cell Physiol. 160:69–74.
   PubMedGoogle Scholar
• Strachan, L., J. G. Murison, R. L. Prestidge, M. A. Sleeman, J. D. Watson, and K. D. Kumble. 2001. Cloning and biological activity of epigen, a novel member of the epidermal growth factor superfamily. J. Biol. Chem. 276:18265–18271.
   PubMed Web of Science ®Google Scholar
• Sugiura, T., S. Kondo, A. Sukagawa, S. Nakane, A. Shinoda, K. Itoh, A. Yamashita, and K. Waku. 1995. 2-Arachidonoylglycerol: a possible endogenous cannabinoid receptor ligand in brain. Biochem. Biophys. Res. Commun. 215:89–97.
   PubMed Web of Science ®Google Scholar
• Sunnarborg, S. W., C. L. Hinkle, M. Stevenson, W. E. Russell, C. S. Raska, J. J. Peschon, B. J. Castner, M. J. Gerhart, R. J. Paxton, R. A. Black, and D. C. Lee. 2002. Tumor necrosis factor-alpha converting enzyme (TACE) regulates epidermal growth factor receptor ligand availability. J. Biol. Chem. 277:12838–12845.
   PubMed Web of Science ®Google Scholar
• Suzuki, M., G. Raab, M. A. Moses, C. A. Fernandez, and M. Klagsbrun. 1997. Matrix metalloproteinase-3 releases active heparin-binding EGF-like growth factor by cleavage at a specific juxtamembrane site. J. Biol. Chem. 272:31730–31737.
   PubMedGoogle Scholar
• Toyoda, H., T. Komurasaki, D. Uchida, Y. Takayama, T. Isobe, T. Okuyama, and K. Hanada. 1995. Epiregulin: a novel epidermal growth factor with mitogenic activity for rat primary hepatocytes. J. Biol. Chem. 270:7495–7500.
   PubMed Web of Science ®Google Scholar
• Wong, S. T., L. F. Winchell, B. K. McCune, H. S. Earp, J. Teixido, J. Massague, B. Herman, and D. C. Lee. 1989. The TGF-alpha precursor expressed on the cell surface binds to the EGF receptor on adjacent cells, leading to signal transduction. Cell 56:495–506.
   PubMed Web of Science ®Google Scholar