Thrombin regulates vascular smooth muscle cell proteoglycan synthesis via PAR-1 and multiple downstream signalling pathways

Thrombosis Research

Volumn 123, Issue 2, 2008, Pages 288-297

  Ivey, Melanie E ^a,b   Little, Peter J ^a,b  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b Central and Eastern Clinical School   (Australia)

Author keywords

Protease activated Receptors; Proteoglycans; Thrombin; Vascular smooth muscle

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; BIGLYCAN; CHONDROITIN; DECORIN; DERMATAN SULFATE; DISACCHARIDE; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; GLUCOSAMINE; GLYCOSAMINOGLYCAN; PROTEIN KINASE C; PROTEINASE ACTIVATED RECEPTOR 1; PROTEOGLYCAN; SULFATE; SULFUR 35; THROMBIN; TRITIUM;

ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; DOSE RESPONSE; ENZYME INHIBITION; GEL PERMEATION CHROMATOGRAPHY; HUMAN; HUMAN CELL; IN VIVO STUDY; INTERNAL MAMMARY ARTERY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEOGLYCAN SYNTHESIS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; SULFATION; VASCULAR SMOOTH MUSCLE;

HUMANS; MUSCLE, SMOOTH, VASCULAR; ORGAN CULTURE TECHNIQUES; PROTEOGLYCANS; RECEPTOR, PAR-1; SIGNAL TRANSDUCTION; THROMBIN;

EID: 55549147505     PISSN: 00493848     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.thromres.2008.04.019     Document Type: Article

References (47)

1. Coughlin S.R. Thrombin signalling and protease-activated receptors. Nature 407 (2000) 258-264
2. Vu T.K., Hung D.T., Wheaton V.I., and Coughlin S.R. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64 (1991) 1057-1068
3. Bretschneider E., Kaufmann R., Braun M., Nowak G., Glusa E., and Schror K. Evidence for functionally active protease-activated receptor-4 (PAR-4) in human vascular smooth muscle cells. Br J Pharmacol 132 (2001) 1441-1446
4. Bretschneider E., Spanbroek R., Lotzer K., Habenicht A.J., and Schror K. Evidence for functionally active protease-activated receptor-3 (PAR-3) in human vascular smooth muscle cells. Thromb Haemost 90 (2003) 704-709
5. Walker T.R., Cadwallader K.A., MacKinnon A., and Chilvers E.R. Thrombin induces DNA synthesis and phosphoinositide hydrolysis in airway smooth muscle by activation of distinct receptors. Biochem Pharmacol 70 (2005) 959-967
6. Seasholtz T.M., Majumdar M., Kaplan D.D., and Brown J.H. Rho and Rho kinase mediate thrombin-stimulated vascular smooth muscle cell DNA synthesis and migration. Circ Res 84 (1999) 1186-1193
7. Ayoub M.A., Maurel D., Binet V., Fink M., Prezeau L., Ansanay H., et al. Real-time analysis of agonist-induced activation of protease-activated receptor 1/Galphai1 protein complex measured by bioluminescence resonance energy transfer in living cells. Mol Pharmacol 71 (2007) 1329-1340
8. Andrade-Gordon P., Maryanoff B.E., Derian C.K., Zhang H.C., Addo M.F., Darrow A.L., et al. Design, synthesis, and biological characterization of a peptide-mimetic antagonist for a tethered-ligand receptor. Proc Natl Acad Sci U S A 96 (1999) 12257-12262
9. Damiano B.P., Derian C.K., Maryanoff B.E., Zhang H.C., and Gordon P.A. RWJ-58259: a selective antagonist of protease activated receptor-1. Cardiovasc Drug Rev 21 (2003) 313-326
10. Janssens W.J., and Verhaeghe R.H. Effect of thrombin on isolated canine blood vessels. Blood Vessels 19 (1982) 126-134
11. Dabbagh K., Laurent G.J., McAnulty R.J., and Chambers R.C. Thrombin stimulates smooth muscle cell procollagen synthesis and mRNA levels via a PAR-1 mediated mechanism. Thromb Haemost 79 (1998) 405-409
12. Wight T.N. Cell biology of arterial proteoglycans. Arteriosclerosis 9 (1989) 1-20
13. O'Brien K.D., Olin K.L., Alpers C.E., Chiu W., Ferguson M., Hudkins K., et al. Comparison of apolipoprotein and proteoglycan deposits in human coronary atherosclerotic plaques: colocalization of biglycan with apolipoproteins. Circulation 98 (1998) 519-527
14. Nakashima Y., Fujii H., Sumiyoshi S., Wight T.N., and Sueishi K. Early human atherosclerosis: accumulation of lipid and proteoglycans in intimal thickenings followed by macrophage infiltration. Arterioscler Thromb Vasc Biol 27 (2007) 1159-1165
15. McDonald T.O., Gerrity R.G., Jen C., Chen H.J., Wark K., Wight T.N., et al. Diabetes and Arterial Extracellular Matrix Changes in a Porcine Model of Atherosclerosis. J Histochem Cytochem 55 (2007) 1149-1157
16. Figueroa J.E., and Vijayagopal P. Angiotensin II stimulates synthesis of vascular smooth muscle cell proteoglycans with enhanced low density lipoprotein binding properties. Atherosclerosis 162 (2002) 261-268
17. Little P.J., Tannock L., Olin K.L., Chait A., and Wight T.N. Proteoglycans synthesized by arterial smooth muscle cells in the presence of transforming growth factor-beta1 exhibit increased binding to LDLs. Arterioscler Thromb Vasc Biol 22 (2002) 55-60
18. Schonherr E., Jarvelainen H.T., Kinsella M.G., Sandell L.J., and Wight T.N. Platelet-derived growth factor and transforming growth factor-beta 1 differentially affect the synthesis of biglycan and decorin by monkey arterial smooth muscle cells. Arterioscler Thromb 13 (1993) 1026-1036
19. Figueroa J.E., and Vijayagopal P. Angiotensin II stimulates synthesis of vascular smooth muscle cell proteoglycans with enhanced low density lipoprotein binding properties. Atherosclerosis 162 (2002) 261-268
20. Shimizu-Hirota R., Sasamura H., Mifune M., Nakaya H., Kuroda M., Hayashi M., et al. Regulation of vascular proteoglycan synthesis by angiotensin II type 1 and type 2 receptors. J Am Soc Nephrol 12 (2001) 2609-2615
21. Olsson U., Ostergren-Lunden G., and Moses J. Glycosaminoglycan-lipoprotein interaction. Glycoconj J 18 (2001) 789-797
22. Yamamoto C., Wakata T., Fujiwara Y., and Kaji T. Induction of synthesis of a large heparan sulfate proteoglycan, perlecan, by thrombin in cultured human coronary smooth muscle cells. Biochim Biophys Acta 1722 (2005) 92-102
23. Neylon C.B., Little P.J., Cragoe Jr. E.J., and Bobik A. Intracellular pH in human arterial smooth muscle. Regulation by Na+/H+ exchange and a novel 5-(N-ethyl-N-isopropyl)amiloride-sensitive Na(+)- and HCO3(-)-dependent mechanism. Circ Res 67 (1990) 814-825
24. Nigro J., Dilley R.J., and Little P.J. Differential effects of gemfibrozil on migration, proliferation and proteoglycan production in human vascular smooth muscle cells. Atherosclerosis 162 (2002) 119-129
25. Wasteson A. A method for the determination of the molecular weight and molecular-weight distribution of chondroitin sulphate. J Chromatogr 59 (1971) 87-97
26. Toullec D., Pianetti P., Coste H., Bellevergue P., Grand-Perret T., Ajakane M., et al. The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem 266 (1991) 15771-15781
27. Salamanca D.A., and Khalil R.A. Protein kinase C isoforms as specific targets for modulation of vascular smooth muscle function in hypertension. Biochem Pharmacol 70 (2005) 1537-1547
28. Daub H., Weiss F.U., Wallasch C., and Ullrich A. Role of transactivation of the EGF receptor in signalling by G-protein-coupled receptors. Nature 379 (1996) 557-560
29. Kalmes A., Vesti B.R., Daum G., Abraham J.A., and Clowes A.W. 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 (2000) 92-98
30. Ballinger M.L., Nigro J., Frontanilla K.V., Dart A.M., and Little P.J. Regulation of glycosaminoglycan structure and atherogenesis. Cell Mol Life Sci 61 (2004) 1296-1306
31. Little P.J., Ballinger M.L., and Osman N. Vascular wall proteoglycan synthesis and structure as a target for the prevention of atherosclerosis. Vasc Health Risk Manage 3 (2007) 1-8
32. Calabro A., Hascall V.C., and Midura R.J. Adaptation of FACE methodology for microanalysis of total hyaluronan and chondroitin sulfate composition from cartilage. Glycobiology 10 (2000) 283-293
33. Hirano K. The roles of proteinase-activated receptors in the vascular physiology and pathophysiology. Arterioscler Thromb Vasc Biol 27 (2007) 27-36
34. Camejo G., Hurt-Camejo E., Olsson U., and Bondjers G. Proteoglycans and lipoproteins in atherosclerosis. Curr Opin Lipidol 4 (1993) 385-391
35. Cardoso L.E., and Mourao P.A. Glycosaminoglycan fractions from human arteries presenting diverse susceptibilities to atherosclerosis have different binding affinities to plasma LDL. Arterioscler Thromb 14 (1994) 115-124
36. Camejo G., Olofsson S.O., Lopez F., Carlsson P., and Bondjers G. Identification of Apo B-100 segments mediating the interaction of low density lipoproteins with arterial proteoglycans. Arteriosclerosis 8 (1988) 368-377
37. Molino M., Raghunath P.N., Kuo A., Ahuja M., Hoxie J.A., Brass L.F., et al. Differential expression of functional protease-activated receptor-2 (PAR-2) in human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 18 (1998) 825-832
38. Nakanishi-Matsui M., Zheng Y.W., Sulciner D.J., Weiss E.J., Ludeman M.J., and Coughlin S.R. PAR3 is a cofactor for PAR4 activation by thrombin. Nature 404 (2000) 609-613
39. Kanda Y., Mizuno K., Kuroki Y., and Watanabe Y. Thrombin-induced p38 mitogen-activated protein kinase activation is mediated by epidermal growth factor receptor transactivation pathway. Br J Pharmacol 132 (2001) 1657-1664
40. Schmidt A., Echtermeyer F., Alozie A., Brands K., and Buddecke E. Plasmin- and thrombin-accelerated shedding of syndecan-4 ectodomain generates cleavage sites at Lys(114)-Arg(115) and Lys(129)-Val(130) bonds. J Biol Chem 280 (2005) 34441-34446
41. Subramanian S.V., Fitzgerald M.L., and Bernfield M. Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. J Biol Chem 272 (1997) 14713-14720
42. Rodriguez-Lee M., Ostergren-Lunden G., Wallin B., Moses J., Bondjers G., and Camejo G. Fatty acids cause alterations of human arterial smooth muscle cell proteoglycans that increase the affinity for low-density lipoprotein. Arterioscler Thromb Vasc Biol 26 (2006) 130-135
43. Poleni P.E., Bianchi A., Etienne S., Koufany M., Sebillaud S., Netter P., et al. Agonists of peroxisome proliferators-activated receptors (PPAR) alpha, beta/delta or gamma reduce transforming growth factor (TGF)-beta-induced proteoglycans' production in chondrocytes. Osteoarthritis Cartilage 15 (2007) 493-505
44. Tiedemann K., Olander B., Eklund E., Todorova L., Bengtsson M., Maccarana M., et al. Regulation of the chondroitin/dermatan fine structure by transforming growth factor-beta1 through effects on polymer-modifying enzymes. Glycobiology 15 (2005) 1277-1285
45. Kanda Y., Nishio E., Kuroki Y., Mizuno K., and Watanabe Y. Thrombin activates p38 mitogen-activated protein kinase in vascular smooth muscle cells. Life Sci 68 (2001) 1989-2000
46. Ungefroren H., Groth S., Ruhnke M., Kalthoff H., and Fandrich F. Transforming growth factor-beta (TGF-beta) type I receptor/ALK5-dependent activation of the GADD45beta gene mediates the induction of biglycan expression by TGF-beta. J Biol Chem 280 (2005) 2644-2652
47. Dadlani H., Ballinger M.L., Osman N., Getachew R., and Little P.J. Smad and p38 MAP kinase mediated signalling of proteoglycan synthesis in vascular smooth muscle. J Biol Chem 283 (2008) 7844-7852