Arterial smooth muscle cell heparan sulfate proteoglycans accelerate thrombin inhibition by heparin cofactor II

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 16, Issue 9, 1996, Pages 1138-1146

  Shirk, Rebecca A ^a   Church, Frank C ^b   Wagner, William D ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

heparin cofactor II; proteoglycans; serpin; smooth muscle cells; thrombin

Indexed keywords

ANTITHROMBIN; DERMATAN SULFATE; GLUCAN SYNTHASE; GLYCOSAMINOGLYCAN; HEPARIN COFACTOR II; N ACETYLGALACTOSAMINE 4 SULFATASE; PROTEOCHONDROITIN SULFATE; PROTEOGLYCAN; PROTEOHEPARAN SULFATE; SERINE PROTEINASE INHIBITOR; THROMBIN;

ANIMAL CELL; AORTA; ARTERY WALL; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; EXTRACELLULAR MATRIX; MONKEY; MONOLAYER CULTURE; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; THROMBOSIS; VASCULAR SMOOTH MUSCLE;

EID: 0029761974     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.16.9.1138     Document Type: Article

References (85)

1. Melzig M, Harms C, Teuscher E, Voigt B, Wagner G. Influence of inhibitors of thrombin on porcine aortic smooth muscle cells in primary culture. Biomed Biochim Acta. 1986;45:1199-1202.
2. Graham DJ, Alexander JJ. The effects of thrombin on bovine aortic endothelial and smooth muscle cells. J Vasc Surg. 1990;11:307-313.
3. McNamara CA, Sarembock IJ, Gimple LW, Fenton JW II, Coughlin SR, Owens GK. Thrombin stimulates proliferation of cultured rat aortic smooth muscle cells by a proteolytically activated receptor. J Clin invest. 1993;91:94-98.
4. Chen LB, Buchanan JM. Mitogenic activity of blood components, I: thrombin and prothrombin. Proc Natl Acad Sci U S A. 1975;72:131-135.
5. Glenn KC, Carney DH, Fenton JW II, Cunningham DD. Thrombin active site regions required for fibroblast receptor binding and initiation of cell division. J Biol Chem. 1980;255:6609-6616.
6. Hung DT, Vu TH, Nelken NA, Coughlin SR. Thrombin-induced events in non-platelet cells are mediated by the unique proteolytic mechanism established for the cloned platelet thrombin receptor. J Cell Biol. 1992;116:827-832.
7. Bar-Shavit R, Kahn A, Wilner GD, Fenton JW II. Monocyte chemotaxis: stimulation by specific exosite region in thrombin. Science. 1983;220:728-731.
8. Crago AM, Wu HF, Hoffman M, Church FC. Monocyte chemoattractant activity of Ser195→Ala active site mutant recombinant alpha-thrombin. Exp Cell Res. 1995;219:650-656.
9. Libby P, Warner SJ, Friedman GB. Interleukin 1: a mitogen for human vascular smooth muscle cells that induces the release of growth-inhibitory prostanoids. J Clin Invest. 1988;81:487-498.
10. Daniel TO, Gibbs VC, Milfay DF, Garovoy MR, Williams LT. Thrombin stimulates c-sis gene expression in microvascular endothelial cells. J Biol Chem. 1986;261:9579-9582.
11. Prescott SM, Zimmerman GA, McIntyre TM. Human endothelial cells in culture produce platelet-activating factor (1-alkyl-2-acetyl-sn-glycero-3-phosphocholine) when stimulated with thrombin. Proc Natl Acad Sci USA. 1984;81:3534-3538.
12. Wilcox JN, Smith KM, Schwartz SM, Gordon D. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. P roc Natl Acad Sci USA. 1989;86:2839-2843.
13. Drake TA, Morrissey JH, Edgington TS. Selective cellular expression of tissue factor in human tissues: implications for disorders of hemostasis and thrombosis. Am J Pathol. 1989;134:1087-1097.
14. Vu TK, Hung DT, Wheaton VI, Coughlin SR. Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell. 1991;64:1057-1068.
15. Nelken NA, Soifer SJ, O'Keefe J, Vu TK, Charo IF, Coughlin SR. Thrombin receptor expression in normal and atherosclerotic human arteries. J Clin Invest. 1992;90:1614-1621.
16. Sarembock IJ, Gertz SD, Gimple LW, Owen RM, Powers ER, Roberts WC. Effectiveness of recombinant desulfatohirudin in reducing restenosis after balloon angioplasty of atherosclerotic femoral arteries in rabbits. Circulation. 1991;84:232-243.
17. Walters TK, Gorog DA, Wood RF. Thrombin generation following arterial injury is a critical initiating event in the pathogenesis of the proliferative stages of the atherosclerotic process. J Vase Res. 1994;31:173-177.
18. Brinkhous KM, Smith HP, Warner ED, Seegers WH. The inhibition of blood clotting: an unidentified substance which acts in conjunction with heparin to prevent conversion of prothrombin to thrombin. Am J Physiol. 1939;125:683-687.
19. Abildgaard U. Highly purified antithrombin III with heparin cofactor activity prepared by disc electrophoresis. Scand J Clin Lab Invest. 1968;21:89-91.
20. Rosenberg RD, Damus PS. The purification and mechanism of action of human antithrombin-heparin cofactor. J Biol Chem. 1973;248:6490-6505.
21. Olson ST, Bjork I. Regulation of thrombin activity by antithrombin and heparin. Semin Thromb Hemost. 1994;20:373-409.
22. Machovich R, Borsodi A, Blasko G, Orakzai SA. Inactivation of alpha- and beta-thrombin by antithrombin-III, alpha 2-macroglobulin and alpha 1-proteinase inhibitor. Biochem J. 1977;167:393-398.
23. Andrew M, Mitchell L, Vegh P, Ofosu F. Thrombin regulation in children differs from adults in the absence and presence of heparin. Thromb Haemost. 1994;72:836-842.
24. Briginshaw GF, Shanberge JN. Identification of two distinct heparin cofactors in human plasma, II: inhibition of thrombin and activated factor X. Thromb Res. 1974;4:463-477.
25. Tollefsen DM, Majerus DW, Blank MK. Heparin cofactor II: purification and properties of a heparin-dependent inhibitor of thrombin in human plasma. J Biol Chem. 1982;257:2162-2169.
26. Learned LA, Bloom JW, Hunter MJ. The antithrombin activity of alpha-1-protease inhibitor: the antitrypsin activity of antithrombin III. Thromb Res. 1976;8:99-109.
27. Matheson NR, Travis J. Inactivation of human thrombin in the presence of human alpha1-proteinase inhibitor. Biochem J. 1976;159:495-502.
28. Bar-Shavit R, Eldor A, Vlodavsky I. Binding of thrombin to subendothelial extracellular matrix: protection and expression of functional properties. J Clin Invest. 1989;84:1096-1104.
29. Tollefsen DM, Pestka CA, Monafo WJ. Activation of heparin cofactor II by dermatan sulfate. J Biol Chem. 1983;258:6713-6716.
30. McGuire EA, Tollefsen DM. Activation of heparin cofactor II by fibroblasts and vascular smooth muscle cells. J Biol Chem. 1987;262:169-175.
31. Pratt CW, Whinna HC, Meade JB, Treanor RE, Church FC. Physicochemical aspects of heparin cofactor II. Ann N Y Acad Sci. 1989;556:104-115.
32. Whinna HC, Choi HU, Rosenberg LC, Church FC. Interaction of heparin cofactor II with biglycan and decorin. J Biol Chem. 1993;268:3920-3924.
33. Huber R, Carrell RW. Implications of the three-dimensional structure of alpha 1-antitrypsin for structure and function of serpins. Biochemistry. 1989;28:8951-8966.
34. Pratt CW, Church FC. Antithrombin: structure and function. Semin Hematol. 1991;28:3-9.
35. Busch C, Owen WG. Identification in vitro of an endothelial cell surface cofactor for antithrombin III: parallel studies with isolated perfused rat hearts and microcarrier cultures of bovine endothelium. J Clin Invent. 1982;69:726-729.
36. Marcum JA, McKenney JB, Rosenberg RD. Acceleration of thrombin-antithrombin complex formation in rat hindquarters via heparin-like molecules bound to the endothelium. J Clin invest. 1984;74:341-350.
37. Marcum JA, Rosenberg RD. Anticoagulantly active heparin-like molecules from vascular tissue. Biochemistry. 1984;23:1730-1737.
38. de Agostini AI, Watkins SC, Slayter HS, Youssoufian H, Rosenberg RD. Localization of anticoagulantly active heparan sulfate proteoglycans in vascular endothelium: antithrombin binding on cultured endothelial cells and perfused rat aorta. J Cell Biol. 1990;111:1293-1304.
39. Wight TN, Ross R. Proteoglycans in primate arteries, II: synthesis and secretion of glycosaminoglycans by arterial smooth muscle cells in culture. J Cell Biol. 1975;67:675-686.
40. Wight TN, Ross R. Proteoglycans in primate arteries, I: ultrastructural localization and distribution in the intima. J Cell Biol. 1975;67:660-674.
41. Salisbury BG, Wagner WD. Isolation and preliminary characterization of proteoglycans dissociatively extracted from human aorta. J Biol Chem. 1981;256:8050-8057.
42. Register TC, Wagner WD. Heterogeneity in glycosylation of dermatan sulfate proteoglycan core proteins isolated from human aorta. Connect Tissue Res. 1990;25:35-48.
43. Choi HU, Johnson TL, Pal S, Tang LH, Rosenberg L, Neame PJ. Characterization of the dermatan sulfate proteoglycans, DS-PGI and DS-PGII, from bovine articular cartilage and skin isolated by octyl-Sepharose chromatography. J Biol Chem. 1989;264:2876-2884.
44. Rosenberg LC, Choi HU, Tang LH, Johnson TL, Pal S, Webber C, Reiner, A, Poole AR. Isolation of dermatan sulfate proteoglycans from mature bovine articular cartilages. J Biol Chem. 1985;260:6304-6313.
45. Fisher LW, Termine JD, Dejter SW Jr, Whitson SW, Yanagishita M, Kimura JH, Hascall VC, Kleinman HK, Hassell JR, Nilsson B. Proteoglycans of developing bone. J Biol Chem. 1983;258:6588-6594.
46. Fisher LW, Hawkins GR, Tuross N, Termine JD. Purification and partial characterization of small proteoglycans I and II, bone sialo-proteins I and II, and osteonectin from the mineral compartment of developing human bone. J Biol Chem. 1987;262:9702-9708.
47. Griffith MJ, Noyes CM, Church FC. Reactive site peptide structural similarity between heparin cofactor II and antithrombin III. J Biol Chem. 1985;260:2218-2225.
48. Church FC, Whinna HC. Rapid sulfopropyl-disk Chromatographic purification of bovine and human thrombin. Anal Biochem. 1986;157:77-83.
49. Ross R. The smooth muscle cell, II: growth of smooth muscle in culture and formation of elastic fibers. J Cell Biol. 1971;50:172-186.
50. Edwards IJ, Xu H, Wright MJ, Wagner WD. Interleukin-1 upregulates decorin production by arterial smooth muscle cells. Arterioscler Thromb. 1994;14:1032-1039.
51. Oike Y, Kimata K, Shinomura T, Suzuki S. Proteinase activity in chondroitin lyase (chondroitinase) and endo-beta-D-galactosidase (keratanase) preparations and a method to abolish their proteolytic effect on proteoglycan. Biochem J. 1980;191:203-207.
52. Lowry OH, Rosebrough NJ, Farr AL, RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193:265-275.
53. Pratt CW, Whinna HC, Church FC. A comparison of three heparin-binding serine proteinase inhibitors. J Biol Chem. 1992;267:8795-8801.
54. Phillips JE, Shirk RA, Whinna HC, Henriksen RA, Church FC. Inhibition of dysthrombins Quick I and II by heparin cofactor II and antithrombin. J Biol Chem. 1993;268:3321-3327.
55. Heyderman RS, Klein NJ, Shennan GI, Levin M. Reduction of the anticoagulant activity of glycosaminoglycans on the surface of the vascular endothelium by endotoxin and neutrophils: evaluation by an amidolytic assay. Thromb Res. 1992;67:677-685.
56. Blumenkrantz N, Asboe-Hansen G. New method for quantitative determination of uronic acids. Anal Biochem. 1973;54:484-489.
57. Wight TN, Hascall VC. Proteoglycans in primate arteries, III: characterization of the proteoglycans synthesized by arterial smooth muscle cells in culture. J Cell Biol. 1983;96:167-176.
58. Rauch U, Glossl J, Kresse H. Comparison of small proteoglycans from skin fibroblasts and vascular smooth-muscle cells. Biochem J. 1986;238:465-474.
59. Lark MW, Wight TN. Modulation of proteoglycan metabolism by aortic smooth muscle cells grown on collagen gels. Arteriosclerosis. 1986;6:638-650.
60. Schonherr E, Jarvelainen HT, Sandell LJ, Wight TN. Effects of platelet-derived growth factor and transforming growth factor-beta 1 on the synthesis of a large versican-like chondroitin sulfate proteoglycan by arterial smooth muscle cells. J Biol Chem. 1991;266:17640-17647.
61. Schonherr E, Jarvelainen HT, Kinsella MG, Sandell LJ, Wight TN. 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. 1993;13:1026-1036.
62. Maimone MM, Tollefsen DM. Structure of a dermatan sulfate hexasaccharide that binds to heparin cofactor II with high affinity. J Biol Chem. 1990;265:18263-18271.
63. Tollefsen DM. The interaction of glycosaminogiycans with heparin cofactor II. Ann N Y Acad Sci. 1994;714:21-31.
64. Bernfield M, Kokenyesi R, Kato M, Hinkes MT, Spring J, Gallo RL, Lose EJ. Biology of the syndecans: a family of transmembrane heparan sulfate proteoglycans. Annu Rev Cell Biol. 1992;8:365-393.
65. Gallagher JT. The extended family of proteoglycans: social residents of the pericellular zone. Curr Opin Cell Biol. 1989;1:1201-1218.
66. Roden L, Ananth S, Campbell P, Curenton T, Ekborg G, Manzella S, Pillion D, Meezan E. Heparin: an introduction. In: Lane DA, Bjork I, Lindahl U, eds. Heparin and Related Polysaccharides. New York, NY: Plenum Press; 1992:1-20.
67. Lindahl U, Lidholt K, Spillmann D, Kjellen L. More to "heparin" than anticoagulation. Thromb Res. 1994;75:1-32.
68. Schmidt A, Lemming G, Yoshida K, Buddecke E, Molecular organization and antiproliferative domains of arterial tissue heparan sulfate. Eur J Cell Biol. 1992;59:322-328.
69. Lindblom A, Bengtsson-Olivecrona G, Fransson LA. Domain structure of endothelial heparan sulphate. Biochem J. 1991;279:821-829.
70. Turnbull JE, Gallagher JT. Molecular organization of heparan sulphate from human skin fibroblasts. Biochem J. 1990;265:715-724.
71. Marcum JA, Atha DH, Fritze LM, Nawroth P, Stern D, Rosenberg RD. Cloned bovine aortic endothelial cells synthesize anticoagulantly active heparan sulfate proteoglycan. J Biol Chem. 1986;261:7507-7517.
72. Turnbull JE, Fernig DG, Ke Y, Wilkinson MC, Gallagher JT. Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J Biol Chem. 1992;267:10337-10341.
73. Parthasarathy N, Goldberg U, Sivaram P, Mulloy B, Flory DM, Wagner WD. Oligosaccharide sequences of endothelial cell surface heparan sulfate proteoglycan with affinity for lipoprotein lipase. J Biol Chem. 1994;269:22391-22396.
74. Kim YS, Linhardt RJ. Structural features of heparin and their effect on heparin cofactor II mediated inhibition of thrombin. Thromb Res. 1989;53:55-71.
75. Rogers SJ, Pratt CW, Whinna HC, Church FC. Role of thrombin exosites in inhibition by heparin cofactor II. J Biol Chem. 1992;267:3613-3617.
76. Kjellen L, Oldberg A, Hook M. Cell-surface heparan sulfate: mechanisms of proteoglycan-cell association. J Biol Chem. 1980;255:10407-10413.
77. Farrell DH, Cunningham DD. Glycosaminoglycans on fibroblasts accelerate thrombin inhibition by protease nexin-1. Biochem J. 1987;245:543-550.
78. Choi BH, Suzuki M, Kim T, Wagner SL, Cunningham DD. Protease nexin-1 : localization in the human brain suggests a protective role against extravasated serine proteases. Am J Pathol. 1990;137:741-747.
79. Cunningham DD, Pulliam L, Vaughan PJ. Protease nexin-1 and thrombin: injury-related processes in the brain. Thromb Haemost. 1993;70:168-171.
80. Priglinger U, Geiger M, Bielek E, Vanyek E, Binder BR. Binding of urinary protein C inhibitor to cultured human epithelial kidney tumor cells (TCL-598): the role of glycosaminoglycans present on the luminal cell surface. J Biol Chem. 1994;269:14705-14710.
81. Cooper ST, Neese LL, DiCuccio MN, Liles DK, Huffman M, Church FC. Vascular localization of the heparin-binding serpins antithrombin, heparin cofactor II, and protein C inhibitor. Clin Appl Thromb Hemost. In press.
82. Snow AD, Bolender RP, Wight TN, Clowes AW. Heparin modulates the composition of the extracellular matrix domain surrounding arterial smooth muscle cells. Am J Pathol. 1990;137:313-330.
83. Riessen R, Isner JM, Blessing E, Loushin C, Nikol S, Wight TN. Regional differences in the distribution of the proteoglycans biglycan and decorin in the extracellular matrix of atherosclerotic and restenotic human coronary arteries. Am J Pathol. 1994;144:962-974.
84. Stevens RL, Colombo M, Gonzales JJ, Hollander W, Schmid K. The glycosaminoglycans of the human artery and their changes in atherosclerosis. J Clin Invest. 1976;58:470-481.
85. Tammi M, Seppala PO, Lehtonen A, Mottonen M. Connective tissue components in normal and atherosclerotic human coronary arteries. Atherosclerosis. 1978;29:191-194.