Activation of proteinase-activated receptor 1 stimulates epithelial chloride secretion through a unique MAP kinase- and cyclo-oxygenase-dependent pathway

FASEB Journal

Volumn 16, Issue 12, 2002, Pages 1515-1525

  Buresi, Michelle C ^a   Buret, Andrég ^a   Hollenberg, Morley D ^a   MacNaughton, Wallace K ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

Epidermal growth factor; Inflammatory bowel disease; PAR 1; PCR

Indexed keywords

ALANYL 4 FLUOROPHENYLALANYLARGINYLCYCLOHEXYLALANYLCITRULLINE TYROSINE; CHLORIDE; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; EPIDERMAL GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOPROTEIN; PHOSPHOSERINE; PROSTAGLANDIN SYNTHASE; PROTEIN KINASE P60; PROTEINASE ACTIVATED RECEPTOR 1; THROMBIN; UNCLASSIFIED DRUG;

ARTICLE; CHLORIDE TRANSPORT; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INFLAMMATION; INTESTINE EPITHELIUM CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANDROSTADIENES; BUTADIENES; CELL LINE; CHLORIDES; EPITHELIAL CELLS; HUMANS; IMIDAZOLES; INDOLES; MALEIMIDES; MITOGEN-ACTIVATED PROTEIN KINASES; NITRILES; NITROBENZENES; PHOSPHOLIPASES A; PHOSPHORYLATION; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PROSTAGLANDINS; PYRAZOLES; PYRIDINES; PYRIMIDINES; QUINAZOLINES; RECEPTOR, PAR-1; RECEPTORS, THROMBIN; SIGNAL TRANSDUCTION; SULFONAMIDES; THROMBIN; TYRPHOSTINS;

RICKETTSIA SP. PAR;

EID: 0036793557     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.02-0039com     Document Type: Article

References (60)

1. Macfarlane, S. R., Seatter, M. J., Kanke, T., Hunter, G. D., and Plevin, R. (2001) Proteinase-activated receptors. Pharmacol. Rev. 53, 245-282
2. Vu, T. K., Wheaton, V. I., Hung, D. T., Charo, I., and Coughlin, S. R. (1991) Domains specifying thrombin-receptor interaction. Nature (London) 353, 674-677
3. Vu, T. K., Hung, D. T., Wheaton, V. I., and Coughlin, S. R. (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64, 1057-1068
4. - secretion in human intestinal epithelial cells. Am. J. Physiol. 281, G323-G332
5. Dery, O., and Bunnett, N. W. (1999) Proteinase-activated receptors: a growing family of heptahelical receptors for thrombin, trypsin and tryptase. Biochem. Soc. Trans. 27, 246-254
6. Cirino, G., Cicala, C., Bucci, M. R., Sorrentino, L., Maraganore, J. M., and Stone, S. R. (1996) Thrombin functions as an inflammatory mediator through activation of its receptor. J. Exp. Med. 183, 821-827
7. 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
8. Stadnicki, A., Gonciarz, M., Niewiarowski, T. J., Hartleb, J., Rudnicki, M., Merrell, N. B., DeLa Cadena, R. A., and Colman, R. W. (1997) Activation of plasma contact and coagulation systems and neutrophils in the active phase of ulcerative colitis. Dig, Dis. Sci. 42, 2356-2366
9. Chamouard, P., Grunebaum, L., Wiesel, M. L., Frey, P. L., Wittersheim, C., Sapin, R., Baumann, R., and Cazenave, J. P. (1995) Prothrombin fragment 1 + 2 and thrombin-antithrombin III complex as markers of activation of blood coagulation in inflammatory bowel diseases. Eur. J. Gastroenterol. Hepatol. 7, 1183-1188
10. Ghosh, S., Mackie, M. J., McVerry, B. A., Galloway, M., Ellis, A., and McKay, J. (1983) Chronic inflammatory bowel disease, deep-venous thrombosis and antithrombin activity. Acta Haematol. 70, 50-53
11. de Jong, E., Porte, R. J., Knot, E. A., Verheijen, J. H., and Dees, J. (1989) Disturbed fibrinolysis in patients with inflammatory bowel disease. A study in blood plasma, colon mucosa, and feces. Gut 30, 188-194
12. Wood, J. D. (1993) Neuro-immunophysiology of colon function. Pharmacology 47 Suppl. 1, 7-13
13. Zheng, X. L., Renaux, B., and Hollenberg, M. D. (1998) Parallel contractile signal transduction pathways activated by receptors for thrombin and epidermal growth factor-urogastrone in guinea pig gastric smooth muscle: blockade by inhibitors of mitogen-activated protein kinase-kinase and phosphatidyl inositol 3′-kinase. J Pharmacol. Exp. Ther. 285, 325-334
14. Daub, H., Weiss, F. U., Wallasch, C., and Ullrich, A. (1996) Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature (London) 379, 557-560
15. Keely, S. J., Uribe, J. M., and Barrett, K. E. (1998) Carbachol stimulates transactivation of epidermal growth factor receptor and mitogen-activated protein kinase in T84 cells. Implications for carbachol-stimulated chloride secretion. J. Biol. Chem. 273, 27111-27117
16. Luttrell, L. M., Daaka, Y., and Lefkowitz, R. J. (1999) Regulation of tyrosine kinase cascades by G-protein-coupled receptors. Curr. Opin. Cell Biol. 11, 177-183
17. 2+. PYK-2, and p60(src). J. Biol. Chem. 275, 12619-12625
18. Prenzel, N., Zwick, E., Daub, H., Leserer, M., Abraham, R., Wallasch, C., and Ullrich, A. (1999) EGF receptor transactivation by G-protein-coupled receptors requires metalloproteinase cleavage of proHB-EGF. Nature (London) 402, 884-888
19. Gschwind, A., Zwick, E., Prenzel, N., Leserer, M., and Ullrich, A. (2001) Cell communication networks: epidermal growth factor receptor transactivation as the paradigm for interreceptor signal transmission. Oncogene. 20, 1594-1600
20. Lan, R. S., Knight, D. A., Stewart, G. A., and Henry, P. J. (2001) Role of PGE(2) in protease-activated receptor-1, -2 and -4 mediated relaxation in the mouse isolated trachea. Br. J. Pharmacol. 132, 93-100
21. Tognetto, M., Trevisani, M., Maggiore, B., Navarra, G., Turini, A., Guerrini, R., Bunnett, N. W., Geppetti, P., and Harrison, S. (2000) Evidence that PAR-1 and PAR-2 mediate prostanoid-dependent contraction in isolated guinea-pig gallbladder. Br. J. Pharmacol. 131, 689-694
22. Hinterleitner, T. A., and Powell, D. W. (1991) Immune system control of intestinal ion transport. Proc. Soc. Exp. Biol. Med. 197, 249-260
23. Powell, D. W., Mifflin, R. C., Valentich, J. D., Crowe, S. E., Saada, J. I., and West, A. B. (1999) Myofibroblasts. II. Intestinal subepithelial myofibroblasts. Am. J Physiol. 277, C183-C201
24. Seymour, M. L., Zaidi, N. F., Hollenberg, M. D., and MacNaughton, W. K. (2001) The upregulation of colonic fibroblast cyclooxygenase (COX)-2 expression and PGE2 production by thrombin. FASEBJ. 15, A830 (abstr.)
25. Pang, G., Buret, A., O'Loughlin, E., Smith, A., Batey, R., and Clancy, R. (1996) Immunologic, functional, and morphological characterization of three new human small intestinal epithelial cell lines. Gastroenterology 111, 8-18
26. Teoh, D. A., Kamieniecki, D., Pang, G., and Buret, A. G. (2000) Giardia lamblia rearranges F-actin and alpha-actinin in human colonic and duodenal monolayers and reduces transepithelial electrical resistance. J. Parasitol. 86, 800-806
27. 1- targeted ligands. J. Pharmacol. Exp. Therap. 288, 358-370
28. Waltenberger, J., Uecker, A., Kroll, J., Frank, H., Mayr, U., Bjorge, J. D., Fujita, D., Gazit, A., Hombach, V., Levitzki, A., and Bohmer, F. D. (1999) A dual inhibitor of platelet-derived growth factor beta-receptor and Src kinase activity potently interferes with motogenic and mitogenic responses to PDGF in vascular smooth muscle cells. A novel candidate for prevention of vascular remodeling. Circ. Res. 85, 12-22
29. Bos, M., Mendelsohn, J., Kim, Y. M., Albanell, J., Fry, D. W., and Baselga, J. (1997) PD153035, a tyrosine kinase inhibitor, prevents epidermal growth factor receptor activation and inhibits growth of cancer cells in a receptor number-dependent manner. Clin. Cancer Res. 3, 2099-2106
30. Davies, S. P., Reddy, H., Caivano, M., and Cohen, P. (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105
31. Kovalenko, M., Gazit, A., Bohmer, A., Rorsman, C., Ronnstrand, L., Heldin, C. H., Waltenberger, J., Bohmer, F. D., and Levitzki, A. (1994) Selective platelet-derived growth factor receptor kinase blockers reverse sis-transformation. Cancer Res. 54, 6106-6114
32. Toullec, D., Pianetti, P., Coste, H., Bellevergue, P., Grand-Perret, T., Ajakane, M., Baudet, V., Boissin, P., Boursier, E., and Loriolle, F., (1991) The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266, 15771-15781
33. Parvathy, S., Hussain, I., Karran, E. H., Turner, A. J., and Hooper, N. M. (1998) Alzheimer's amyloid precursor protein alpha-secretase is inhibited by hydroxamic acid-based zinc metalloprotease inhibitors: similarities to the angiotensin converting enzyme secretase. Biochemistry 37, 1680-1685
34. 2+-sensing receptor activates cytosolic phospholipase A2 via a Gqalpha-dependent ERK-independent pathway. J. Biol. Chem. 276, 13941-13948
35. Wong, P. Y., Chan, H. C., Leung, P. S., Chung, Y. W., Wong, Y. L., Lee, W. M., Ng, V., and Dun, N. J. (1999) Regulation of anion secretion by cyclo-oxygenase and prostanoids in cultured epididymal epithelia from the rat. J. Physiol. (London) 514, 809-820
36. Futaki, N., Takahashi, S., Yokoyama, M., Arai, I., Higuchi, S., and Otomo, S. (1994) NS-398, a new anti-inflammatory agent, selectively inhibits prostaglandin G/H synthase/cyclooxygenase (COX-2) activity in vitro. Prostaglandins 47, 55-59
37. Warner, T. D., Giuliano, F., Vojnovic, I., Bukasa, A., Mitchell, J. A., and Vane, J. R. (1999) Nonsteroid drug selectivities for cyclo-oxygenase-1 rather than cyclo-oxygenase-2 are associated with human gastrointestinal toxicity: A full in vitro analysis. Proc. Natl. Acad. Sci. USA 96, 7563-7568
38. Smith, C. J., Zhang, Y., Koboldt, C. M., Muhammad, J., Zweifel, B. S., Shaffer, A., Talley, J. J., Masferrer, J. L., Seibert, K., and Isakson, P. C. (1998) Pharmacological analysis of cyclooxygenase-1 in inflammation. Proc. Natl. Acad. Sci. USA 95, 13313-13318
39. Halushka, P. V., Boehm, A., and Mais, D. E. (1988) Polymyxin B increases TXA2/PGH2 agonist and antagonist affinities in human platelet membranes. Eicosanoids 1, 41-44
40. Kalmes, A., Vesti, B. R., Daum, G., Abraham, J. A., and Clowes, A. W. (2000) Heparin blockade of thrombin-induced smooth muscle cell migration involves inhibition of epidermal growth factor (EGF) receptor transactivation by heparin-binding EGF-like growth factor. Circ. Res. 87, 92-98
41. Ricketts, W. A., Brown, J. H., and Olefsky, J. M. (1999) Pertussis toxin-sensitive and -insensitive thrombin stimulation of Shc phosphorylation and mitogenesis are mediated through distinct pathways. Mol. Endocrinol. 13, 1988-2001
42. - secretion in T84 cells. Am. J. Physiol. 264, C671-C676
43. Barrett, K. E., and Keely, S. J. (2000) Chloride secretion by the intestinal epithelium: molecular basis and regulatory aspects. Annu. Rev. Physiol. 62, 535-572
44. Singer, I. I., Kawka, D. W., Schloemann, S., Tessner, T., Riehl, T., and Stenson, W. F. (1998) Cyclooxygenase 2 is induced in colonic epithelial cells in inflammatory bowel disease. Gastroenterology 115, 297-306
45. Haas, M., Askari, A., and Xie, Z. (2000) Involvement of Src and epidermal growth factor receptor in the signal-transducing function of Na+/K+-ATPase, J. Biol. Chem. 275, 27832-27837
46. Lepple-Wienhues, A., Wieland, U., Laun, T., Heil, L., Stern, M., and Lang, F. (2001) A src-like kinase activates outwardly rectifying chloride channels in CFTR-defective lymphocytes. FASEB J. 15, 927-931
47. Rao, R. K., Lopez, Y., Riviere, P. J. M., Pascaud, X., Junien, J. L., and Porreca, F. (1996) Nitric oxide modulates neuropeptide Y regulation of ion transport in mouse ileum. J. Pharmacol. Exp. Ther. 278, 193-198
48. Eguchi, S., Dempsey, P. J., Frank, G. D., Motley, E. D., and Inagami, T. (2001) Activation of MAPKs by angiotensin II in vascular smooth muscle cells. Metalloprotease-dependent EGF receptor activation is required for activation of ERK and p38 MAPK but not for JNK. J Biol. Chem. 276, 7957-7962
49. Uribe, J. M., Keely, S. J.,Traynor-Kaplan, A. E., and Barrett, K. E. (1996) Phosphatidylinositol 3-kinase mediates the inhibitory effect of epidermal growth factor on calcium-dependent chloride secretion. J. Biol. Chem. 271, 26588-26595
50. Olayioye, M. A., Graus-Porta, D., Beerli, R. R., Rohrer, J., Gay, B., and Hynes, N. E. (1998) ErbB-1 and ErbB-2 acquire distinct signaling properties dependent upon their dimerization partner. Mol. Cell. Biol. 18, 5042-5051
51. Biscardi, J. S., Maa, M. C., Tice, D. A., Cox, M. E., Leu, T. H., and Parsons, S. J. (1999) c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J. Biol. Chem. 274, 8335-8343
52. Wu, W., Graves, L. M., Gill, G. N., Parsons, S. J., and Samet, J. M. (2002) Src-dependent phosphorylation of the epidermal growth factor receptor on tyrosine 845 Is required for zinc-induced Ras activation. J. Biol. Chem. Epub ahead of print. www.jbc.org
53. Kanda, Y., Mizuno, K., Kuroki, Y., and Watanabe, Y. (2001) Thrombin-induced p38 mitogen-activated protein kinase activation is mediated by epidermal growth factor receptor transactivation pathway. Br J. Pharmacol 132, 1657-1664
54. Authi, K. S., Lagarde, M., and Crawford, N. (1985) Diacylglycerol lipase activity in human platelet intracellular and surface membranes. Some kinetic properties and fatty acid specificity. FEBS Lett. 180, 95-101
55. Okazaki, T., Sagawa, N., Okita, J. R., Bleasdale, J. E., MacDonald, P. C., and Johnston, J. M. (1981) Diacylglycerol metabolism and arachidonic acid release in human fetal membranes and decidua vera. J. Biol. Chem. 256, 7316-7321
56. Hazan-Halevy, I., Seger, R., and Levy, R. (2000) The requirement of both extracellular regulated kinase and p38 mitogen-activated protein kinase for stimulation of cytosolic phospholipase A (2) activity by either FcgammaRIIA or FcgammaRIIIB in human neutrophils. A possible role for Pyk2 but not for the Grb2-Sos-Shc complex. J. Biol. Chem. 275, 12416-12423
57. MacNaughton, W. K., and Cushing, K. (2000) Role of constitutive cyclooxygenase-2 in prostaglandin-dependent secretion in mouse colon in vitro. J. Pharmacol. Exp. Ther. 293, 539-544
58. Beubler, E., Schuligoi, R., Chopra, A. K., Ribardo, D. A., and Peskar, B. A. (2001) Cholera toxin induces prostaglandin synthesis via post-transcriptional activation of cyclooxygenase-2 in the rat jejunum. J. Pharmacol. Exp. Ther. 297, 940-945
59. Derian, C. K., and Eckardt, A. J. (1997) Thrombin receptor-dependent prostaglandin E2 synthesis in hamster fibroblasts: synergistic interactions with interleukin-1beta. Exp. Cell Res. 232, 1-7
60. Samokhin, G. P., Jirousek, M. R., Ways, D. K., and Henriksen, R. A. (1999) Effects of protein kinase C inhibitors on thromboxane production by thrombin-stimulated platelets. Eur. J. Pharmacol. 386, 297-303