Proteinase-mediated cell signalling: Targeting proteinase-activated receptors (PARs) by kallikreins and more

Biological Chemistry

Volumn 387, Issue 6, 2006, Pages 677-685

  Oikonomopoulou, Katerina ^a   Hansen, Kristina K ^b   Saifeddine, Mahmoud ^b   Vergnolle, Nathalie ^b   Tea, Illa ^b   Diamandis, Eleftherios P ^a   Hollenberg, Morley D ^b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

Hormone action; Inflammation; Kallikreins; Protease activated receptors; Proteases; Proteinases; Receptors; Signal transduction; Trypsin

Indexed keywords

G PROTEIN COUPLED RECEPTOR; GROWTH FACTOR RECEPTOR; INSULIN RECEPTOR; KALLIKREIN; PROTEINASE; PROTEINASE ACTIVATED RECEPTOR; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; THROMBIN; TISSUE KALLIKREIN; TRYPSIN;

AMINO TERMINAL SEQUENCE; BLOOD VESSEL REACTIVITY; CATALYSIS; CELL GROWTH; CONFERENCE PAPER; ENZYME ANALYSIS; HORMONAL REGULATION; HORMONE DETERMINATION; HUMAN; INFLAMMATION; KALLIKREIN KININ SYSTEM; NOCICEPTION; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; PEPTIDE FRAGMENTS; PEPTIDE HYDROLASES; RECEPTORS, THROMBIN; SIGNAL TRANSDUCTION; TISSUE KALLIKREINS;

EID: 33745673593     PISSN: 14316730     EISSN: 14374315     Source Type: Journal    
DOI: 10.1515/BC.2006.086     Document Type: Conference Paper

References (66)

1. Ahlquist, R.P. (1948). A study of the adrenotropic receptors. Am. J. Physiol. 153, 586-600.
2. al-Ani, B., Saifeddine., M., and Hollenberg, M.D. (1995). Detection of functional receptors for the proteinase-activated-receptor-2-activating polypeptide, SLIGRL-NH2, in rat vascular and gastric smooth muscle. Can. J. Physiol. Pharmacol. 73, 1203-1207.
3. Asfaha, S., Brussee, V., Chapman, K., Zochodne, D.W., and Vergnolle, N. (2002). Proteinase-activated receptor-1 agonists attenuate nociception in response to noxious stimuli. Br. J. Pharmacol. 135, 1101-1106.
4. Bar-Shavit, P., Kahn, A., Mudd, M.S., Wilner, G.D., Mann, K.G., and Fenton, J.W. II (1984). Localization of a chemotactic domain in human thrombin. Biochemistry 23, 397-400.
5. Bar-Shavit, P., Kahn, A.J., Mann, K.G., and Wilner, G.D. (1986). Identification of a thrombin sequence with growth factor activity on macrophages. Proc. Natl. Acad. Sci. USA 83, 976-980.
6. Blaber, S.I., Scarisbrick, I.A., Bernett, M.J., Dhanarajan, P., Seavy, M.A., Jin, Y., Schwartz, M.A., Rodriguez, M., and Blaber, M. (2002). Enzymatic properties of rat myelencephalon-specific protease. Biochemistry 41, 1165-1173.
7. Blaber, S.I., Ciric, B., Christophi, G.P., Bernett, M.J., Blaber, M., Rodriguez, M., and Scarisbrick, I.A. (2004). Targeting kallikrein 6 proteolysis attenuates CNS inflammatory disease. FASEB J. 18, 920-922.
8. Borgono, C.A. and Diamandis, E.P. (2004). The emerging roles of human tissue kallikreins in cancer. Nat. Rev. Cancer 4, 876-890.
9. Borgono, C.A., Grass, L., Soosaipillai, A., Yousef, G.M., Petraki, C.D., Howarth, D.H., Fracchioli, S., Katsaros, D., and Diamandis, E.P. (2003). Human kallikrein 14: a new potential biomarker for ovarian and breast cancer. Cancer Res. 63, 9032-9041.
10. Borgono, C.A., Michael, I.P., and Diamandis, E.P. (2004). Human tissue kallikreins: physiologic roles and applications in cancer. Mol. Cancer Res. 2, 257-280.
11. Boven, L.A., Vergnolle, N., Henry, S.D., Silva, C., Imai, Y., Holden, J., Warren, K., Hollenberg, M.D., and Power, C. (2003). Up-regulation of proteinase-activated receptor 1 expression in astrocytes during HIV encephalitis. J. Immunol. 170, 2638-2646.
12. Cenac, N., Coelho, A.M., Nguyen, C., Compton, S., Andrade-Gordon, P., MacNaughton, W.K., Wallace, J.L., Hollenberg, M.D., Bunnett, N.W., Garcia-Villar, R., et al. (2002). Induction of intestinal inflammation in mouse by activation of proteinase-activated receptor-2. Am. J. Pathol. 161, 1903-1915.
13. Choong, P.F. and Nadesapillai, A.P. (2003). Urokinase plasminogen activator system: a multifunctional role in tumor progression and metastasis. Clin. Orthop. Relat. Res. 415, S46-58.
14. Compton, S.J., McGuire, J.J., Saifeddine, M., and Hollenberg, M.D. (2002a). Restricted ability of human mast cell tryptase to activate proteinase-activated receptor-2 in rat aorta. Can. J. Physiol. Pharmacol. 80, 987-992.
15. Compton, S.J., Sandhu, S., Wijesuriya, S.J., and Hollenberg, M.D. (2002b). Glycosylation of human proteinase-activated receptor-2 (hPAR2): role in cell surface expression and signalling. Biochem. J. 368, 495-505.
16. Corvera, C.U., Dery, O., McConalogue, K., Gamp, P., Thoma, M., al-Ani, B., Caughey, G.H., Hollenberg, M.D., and Bunnett, N.W. (1999). Thrombin and mast cell tryptase regulate guinea-pig myenteric neurons through proteinase-activated receptors-1 and -2. J. Physiol. 517, 741-756.
17. Coughlin, S.R. (2000). Thrombin signalling and protease-activated receptors. Nature 407, 258-264.
18. Cuatrecasas, P. (1971). Perturbation of the insulin receptor of isolated fat cells with proteolytic enzymes. J. Biol. Chem. 246, 6522-6531.
19. de Garavilla, L., Vergnolle, N., Young, S.H., Ennes, H., Steinhoff, M., Ossovskaya, V.S., D'Andrea, M.R., Mayer, E.A., Wallace, J.L., Hollenberg, M.D., et al. (2001). Agonists of proteinase-activated receptor 1 induce plasma extravasation by a neurogenic mechanism. Br. J. Pharmacol. 133, 975-987.
20. Diamandis, E.P., Yousef, G.M., Soosaipillai, A.R., and Bunting, P. (2000). Human kallikrein 6 (zyme/protease M/neurosin): a new serum biomarker of ovarian carcinoma. Clin. Biochem. 33, 579-583.
21. Ferrell, W.R., Lockhart, J.C., Kelso, E.B., Dunning, L., Plevin, R., Meek, S.E., Smith, A.J., Hunter, G.D., McLean, J.S., McGarry, F., et al. (2003). Essential role for proteinase-activated receptor-2 in arthritis. J. Clin. Invest. 111, 35-41.
22. Frenette, G., Tremblay, R.R., Lazure, C., and Dube, J.Y. (1997). Prostatic kallikrein hK2, but not prostate-specific antigen (hK3), activates single-chain urokinase-type plasminogen activator. Int. J. Cancer 71, 897-899.
23. Glenn, K.C., Frost, G.H., Bergmann, J.S., and Carney, D.H. (1988). Synthetic peptides bind to high-affinity thrombin receptors and modulate thrombin mitogenesis. Pept. Res. 1, 65-73.
24. Hollenberg, M.D. and Compton, S.J. (2002). International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol. Rev. 54, 203-217.
25. Hollenberg, M.D. and Houle, S. (2005). Proteinases as hormone-like signal messengers. Swiss Med. Wkly. 135, 425-432.
26. Hollenberg, M.D. and Saifeddine, M. (2001). Proteinase-activated receptor 4 (PAR4): activation and inhibition of rat platelet aggregation by PAR4-derived peptides. Can. J. Physiol. Pharmacol. 79, 439-442.
27. Hollenberg, M.D., Laniyonu, A.A., Saifeddine, M., and Moore, G.J. (1993). Role of the amino- and carboxyl-terminal domains of thrombin receptor-derived polypeptides in biological activity in vascular endothelium and gastric smooth muscle: evidence for receptor subtypes. Mol. Pharmacol. 43, 921-930.
28. Hollenberg, M.D., Saifeddine, M., and al-Ani, B. (1996). Proteinase-activated receptor-2 in rat aorta: structural requirements for agonist activity of receptor-activating peptides. Mol. Pharmacol. 49, 229-233.
29. Hollenberg, M.D., Saifeddine, M., al-Ani, B., and Kawabata, A. (1997). Proteinase-activated receptors: structural requirements for activity, receptor cross-reactivity, and receptor selectivity of receptor-activating peptides. Can. J. Physiol. Pharmacol. 75, 832-841.
30. Hollenberg, M.D., Saifeddine, M., Sandhu, S., Houle, S., and Vergnolle, N. (2004). Proteinase-activated receptor-4: evaluation of tethered ligand-derived peptides as probes for receptor function and as inflammatory agonists in vivo. Br. J. Pharmacol. 143, 443-454.
31. Kawabata, A., Saifeddine, M., Al-Ani, B., Leblond, L., and Hollenberg, M.D. (1999). Evaluation of proteinase-activated receptor-1 (PAR1) agonists and antagonists using a cultured cell receptor desensitization assay: activation of PAR2 by PAR1-targeted ligands. J. Pharmacol. Exp. Ther. 288, 358-370.
32. Kim, H., Scorilas, A., Katsaros, D., Yousef, G.M., Massobrio, M., Fracchioli, S., Piccinno, R., Gordini, G., and Diamandis, E.P. (2001). Human kallikrein gene 5 (KLK5) expression is an indicator of poor prognosis in ovarian cancer. Br. J. Cancer 84, 643-650.
33. Kinlough-Rathbone, R.L., Rand, M.L., and Packham, M.A. (1993). Rabbit and rat platelets do not respond to thrombin receptor peptides that activate human platelets. Blood 82, 103-106.
34. Kong, W., McConalogue, K., Khitin, L.M., Hollenberg, M.D., Payan, D.G., Bohm, S.K., and Bunnett, N.W. (1997). Luminal trypsin may regulate enterocytes through proteinase-activated receptor 2. Proc. Natl. Acad. Sci. USA 94, 8884-8889.
35. Kono, T. and Barham, F.W. (1971). Insulin-like effects of trypsin on fat cells. Localization of the metabolic steps and the cellular site affected by the enzyme. J. Biol. Chem. 246, 6204-6209.
36. Lafleur, M.A., Hollenberg, M.D., Atkinson, S.J., Knauper, V., Murphy, G., and Edwards, D.R. (2001). Activation of pro-(matrix metalloproteinase-2) (pro-MMP-2) by thrombin is membrane-type-MMP-dependent in human umbilical vein endothelial cells and generates a distinct 63 kDa active species. Biochem. J. 357, 107-115.
37. Macfarlane, S.R., Seatter, M.J., Kanke, T., Hunter, G.D., and Plevin, R. (2001). Proteinase-activated receptors. Pharmacol. Rev. 53, 245-282.
38. Mirza, H., Schmidt, V.A., Derian, C.K., Jesty, J., and Bahou, W.F. (1997). Mitogenic responses mediated through the proteinase-activated receptor-2 are induced by expressed forms of mast cell α- or β-tryptases. Blood 90, 3914-3922.
39. Molino, M., Barnathan, E.S., Numerof, R., Clark, J., Dreyer, M., Cumashi, A., Hoxie, J.A., Schechter, N., Woolkalis, M., and Brass, L.F. (1997). Interactions of mast cell tryptase with thrombin receptors and PAR-2. J. Biol. Chem. 272, 4043-4049.
40. Nguyen, C., Coelho, A.M., Grady, E., Compton, S.J., Wallace, J.L., Hollenberg, M.D., Cenac, N., Garcia-Villar, R., Bueno, L., Steinhoff, M., et al. (2003). Colitis induced by proteinase-activated receptor-2 agonists is mediated by a neurogenic mechanism. Can. J. Physiol. Pharmacol. 81, 920-927.
41. Nicholson, D.W., Ali, A., Thornberry, N.A., Vaillancourt, J.P., Ding, C.K., Gallant, M., Gareau, Y., Griffin, P.R., Labelle, M., Lazebnik, Y.A., et al. (1995). Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376, 37-43.
42. Noorbakhsh, F., Vergnolle, N., Hollenberg, M.D., and Power, C. (2003). Proteinase-activated receptors in the nervous system. Nat. Rev. Neurosci. 4, 981-990.
43. Noorbakhsh, F., Vergnolle, N., McArthur, J.C., Silva, C., Vodjgani, M., Andrade-Gordon, P., Hollenberg, M.D., and Power, C. (2005). Proteinase-activated receptor-2 induction by neuroinflammation prevents neuronal death during HIV infection. J. Immunol. 174, 7320-7329.
44. Noorbakhsh, F., Tsutsui, S., Vergnolle, N., Boven, L.A., Shariat, N., Vodjgani, M., Warren, K.G., Andrade-Gordon, P., Hollenberg, M.D., and Power, C. (2006). Proteinase-activated receptor 2 modulates neuroinflammation in experimental autoimmune encephalomyelitis and multiple sclerosis. J. Exp. Med. 20, 203, 425-435.
45. Nystedt, S., Emilsson, K., Wahlestedt, C., and Sundelin, J. (1994). Molecular cloning of a potential proteinase activated receptor. Proc. Natl. Acad. Sci. USA 91, 9208-9212.
46. Oikonomopoulou, K., Hansen, K.K., Saifeddine, M., Vergnolle, N., Tea, I., Blaber, M., Blaber, S.I., Scarisbrick, I., Diamandis, E.P., and Hollenberg, M.D. (2006). Kallikrein-mediated cell signaling: targeting proteinase-activated receptors (PARs). Biol. Chem. 387, 817-824.
47. Ossovskaya, VS. and Bunnett, N.W. (2004). Protease-activated receptors: contribution to physiology and disease. Physiol. Rev. 84, 579-621.
48. 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 402, 884-888.
49. 2+ mobilization. FEBS Lett. 288, 123-128.
50. Rieser, P. (1967). The insulin-like action of pepsin and pepsinogen. Acta Endocrinol. (Copenh.) 54, 375-379.
51. Rieser, P. and Rieser, C.H. (1964). Anabolic responses of diaphragm muscle to insulin and to other pancreatic proteins. Proc. Soc. Exp. Biol. Med. 116, 669-671.
52. Ruf, W., Dorfleutner, A., and Riewald, M. (2003). Specificity of coagulation factor signaling. J. Thromb. Haemost. 1, 1495-1503.
53. Saifeddine, M., al-Ani, B., Cheng, C.H., Wang, L., and Hollenberg, M.D. (1996). Rat proteinase-activated receptor-2 (PAR2): cDNA sequence and activity of receptor-derived peptides in gastric and vascular tissue. Br. J. Pharmacol. 118, 521-530.
54. Scarisbrick, I.A., Blaber, S.I., Lucchinetti, C.F., Genain, C.P., Blaber, M., and Rodriguez, M. (2002). Activity of a newly identified serine protease in CNS demyelination. Brain 125, 1283-1296.
55. Shoelson, S.E., White, M.F., and Kahn, C.R. (1988). Tryptic activation of the insulin receptor. Proteolytic truncation of the α-subunit releases the β-subunit from inhibitory control. J. Biol. Chem. 263, 4852-4860.
56. Steinhoff, M., Vergnolle, N., Young, S.H., Tognetto, M., Amadesi, S., Ennes, H.S., Trevisani, M., Hollenberg, M.D., Wallace, J.L., Caughey, G.H., et al. (2000). Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat. Med. 6, 151-158.
57. Steinhoff, M., Buddenkotte, J., Shpacovitch, V., Rattenholl, A., Moormann, C., Vergnolle, N., Luger, T.A., and Hollenberg, M.D. (2005). Proteinase-activated receptors: transducers of proteinase-mediated signaling in inflammation and immune response. Endocr. Rev. 26, 1-43.
58. Takayama, T.K., McMullen, B.A., Nelson, P.S., Matsumura, M., and Fujikawa, K. (2001). Characterization of hK4 (prostase), a prostate-specific serine protease: activation of the precursor of prostate specific antigen (pro-PSA) and single-chain urokinase-type plasminogen activator and degradation of prostatic acid phosphatase. Biochemistry 40, 15341-15348.
59. Tanimoto, H., Underwood, L.J., Shigemasa, K., Parmley, T.H., and O'Brien, T.J. (2001). Increased expression of protease M in ovarian tumors. Tumour Biol. 22, 11-18.
60. Vergnolle, N. (2004). Modulation of visceral pain and inflammation by protease-activated receptors. Br. J. Pharmacol. 141, 1264-1274.
61. Vergnolle, N., Hollenberg, M.D., and Wallace, J.L. (1999a). Pro-and anti-inflammatory actions of thrombin: a distinct role for proteinase-activated receptor-1 (PAR1). Br. J. Pharmacol. 126, 1262-1268.
62. Vergnolle, N., Hollenberg, M.D., Sharkey, K.A., and Wallace, J.L. (1999b). Characterization of the inflammatory response to proteinase-activated receptor-2 (PAR2)-activating peptides in the rat paw. Br. J. Pharmacol. 127, 1083-1090.
63. Vergnolle, N., Bunnett, N.W., Sharkey, K.A., Brussee, V., Compton, S.J., Grady, E.F., Cirino, G., Gerard, N., Basbaum, A.I., Andrade-Gordon, P., Hollenberg, M.D., and Wallace, J.L. (2001a). Proteinase-activated receptor-2 and hyperalgesia: a novel pain pathway. Nat. Med. 7, 821-826.
64. Vergnolle, N., Wallace, J.L., Bunnett, N.W., and Hollenberg, M.D. (2001b). Protease-activated receptors in inflammation, neuronal signaling and pain. Trends Pharmacol. Sci. 22, 146-152.
65. 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.
66. Yousef, G.M., Polymeris, M.E., Grass, L., Soosaipillai, A., Chan, P.C., Scorilas, A., Borgono, C., Harbeck, N., Schmalfeldt, B., Dorn, J., et al. (2003). Human kallikrein 5: a potential novel serum biomarker for breast and ovarian cancer. Cancer Res. 63, 3958-3965.