Heparin cofactor II modulates the response to vascular injury

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 27, Issue 3, 2007, Pages 454-460

  Tollefsen, Douglas M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atherogenesis; Heparin cofactor II; Restenosis; Thrombin; Thrombosis

Indexed keywords

ANTICOAGULANT AGENT; DERMATAN SULFATE; HEPARIN; HEPARIN COFACTOR II; HIRUDIN; ORAL CONTRACEPTIVE AGENT; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 3; PROTEINASE ACTIVATED RECEPTOR 4; RECOMBINANT HEPARIN COFACTOR II; THROMBIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANTICOAGULATION; ARTERY THROMBOSIS; ATHEROGENESIS; ATHEROSCLEROSIS; BINDING SITE; BLOOD VESSEL INJURY; CARBOXY TERMINAL SEQUENCE; CARDIOVASCULAR RISK; CORONARY RISK; DRUG MECHANISM; DRUG PROTEIN BINDING; GENE; GENE DELETION; GENE MUTATION; HUMAN; HUMAN VERSUS ANIMAL COMPARISON; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RESTENOSIS; REVIEW; STENT; SYMPTOMATOLOGY; THROMBOSIS; VEIN THROMBOSIS; VENOUS THROMBOEMBOLISM;

ANIMALS; ATHEROSCLEROSIS; CORONARY RESTENOSIS; DERMATAN SULFATE; DISEASE MODELS, ANIMAL; FEMALE; HEPARIN COFACTOR II; HUMANS; MALE; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; PREGNANCY; SENSITIVITY AND SPECIFICITY; STRUCTURE-ACTIVITY RELATIONSHIP; THROMBIN; THROMBOSIS; TUNICA INTIMA;

EID: 33847010204     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000256471.22437.88     Document Type: Review

References (68)

1. Briginshaw GF, Shanberge JN. Identification of two distinct heparin cofactors in human plasma. Separation and partial purification. Arch Biochem Biophys. 1974;161:683-690.
2. 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.
3. Tollefsen DM, Blank MK. Detection of a new heparin-dependent inhibitor of thrombin in human plasma. J Clin Invest. 1981;68:589-596.
4. Friberger P, Egberg N, Holmer E, Hellgren M, Blombäck M. Antithrombin assay - the use of human or bovine thrombin and the observation of a "second" heparin cofactor. Thromb Res. 1982;25:433-436.
5. Griffith MJ, Carraway T, White GC, Dombrose FA. Heparin cofactor activities in a family with hereditary antithrombin III deficiency: evidence for a second heparin cofactor in human plasma. Blood. 1983;61:111-118.
6. 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.
7. Zhang GS, Mehringer JH, Van Deerlin VM, Kozak CA, Tollefsen DM. Murine heparin cofactor II: purification, cDNA sequence, expression, and gene structure. Biochemistry. 1994;33:3632-3642.
8. Kamp P, Strathmann A, Ragg H. Heparin cofactor II, antithrombin-beta and their complexes with thrombin in human tissues. Thromb Res. 2001;101:483-491.
9. Sié P, Dupouy D, Pichon J, Boneu B. Turnover study of heparin cofactor II in healthy man. Thromb Haemost. 1985;54:635-638.
10. Tollefsen DM, Pestka CA. Heparin cofactor II activity in patients with disseminated intravascular coagulation and hepatic failure. Blood. 1985;66:769-774.
11. Kounnas MZ, Church FC, Argraves WS, Strickland DK. Cellular internalization and degradation of antithrombin III-thrombin, heparin cofactor II-thrombin, and alpha 1-antitrypsin-trypsin complexes is mediated by the low density lipoprotein receptor-related protein. J Biol Chem. 1996;271:6523-6529.
12. Blinder MA, Marasa JC, Reynolds CH, Deaven LL, Tollefsen DM. Heparin cofactor II: cDNA sequence, chromosome localization, restriction fragment length polymorphism, and expression in Escherichia coli. Biochemistry. 1988;27:752-759.
13. Ragg H. A new member of the plasma protease inhibitor gene family. Nucleic Acids Res. 1986;14:1073-1088.
14. Parker KA, Tollefsen DM. The protease specificity of heparin cofactor II. Inhibition of thrombin generated during coagulation. J Biol Chem. 1985;260:3501-3505.
15. Tollefsen DM, Pestka CA, Monafo WJ. Activation of heparin cofactor II by dermatan sulfate. J Biol Chem. 1983;258:6713-6716.
16. Colwell NS, Grupe MJ, Tollefsen DM. Amino acid residues of heparin cofactor II required for stimulation of thrombin inhibition by sulphated polyanions. Biochim Biophys Acta. 1999;1431:148-156.
17. Maimone MM, Tollefsen DM. Activation of heparin cofactor II by heparin oligosaccharides. Biochem Biophys Res Commun. 1988;152:1056-1061.
18. Trowbridge JM, Gallo RL Dermatan sulfate: new functions from an old glycosaminoglycan. Glycobiology. 2002;12:117R-125R.
19. 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.
20. Pavão MSG, Aiello KR, Werneck CC, Silva LC, Valente A-P, Mulloy B, Colwell NS, Tollefsen DM, Mourão PAS. Highly sulfated dermatan sulfates from Ascidians. Structure versus anticoagulant activity of these glycosaminoglycans. J Biol Chem. 1998;273:27848-27857.
21. Pavão MSG, Mourão PAS, Mulloy B, Tollefsen DM. A unique dermatan sulfate-like glycosaminoglycan from ascidian. Its structure and the effect of its unusual sulfation pattern on anticoagulant activity. J Biol Chem. 1995;270:31027-31036.
22. Halldórsdóttir AM, Zhang L, Tollefsen DM. N-Acetylgalactosamine 4,6-O-sulfate residues mediate binding and activation of heparin cofactor II by porcine mucosal dermatan sulfate. Glycobiology. 2006;16:693-701.
23. Huntington JA. Shape-shifting serpins - advantages of a mobile mechanism. Trends Biochem Sci. 2006;31:427-435.
24. Church FC, Noyes CM, Griffith MJ. Inhibition of chymotrypsin by heparin cofactor II. Proc Natl Acad Sci U S A. 1985;82:6431-6434.
25. Derechin VM, Blinder MA, Tollefsen DM. Substitution of arginine for Leu444 in the reactive site of heparin cofactor II enhances the rate of thrombin inhibition. J Biol Chem. 1990;265:5623-5628.
26. Van Deerlin VM, Tollefsen DM. The N-terminal acidic domain of heparin cofactor II mediates the inhibition of alpha-thrombin in the presence of glycosaminoglycans. J Biol Chem. 1991;266:20223-20231.
27. Hortin GL, Tollefsen DM, Benutto BM. Antithrombin activity of a peptide corresponding to residues 54-75 of heparin cofactor II. J Biol Chem. 1989;264:13979-13982.
28. Ragg H, Ulshöfer T, Gerewitz J. On the activation of human leuserpin-2, a thrombin inhibitor, by glycosaminoglycans. J Biol Chem. 1990;265:5211-5218.
29. Ragg H, Ulshöfer T, Gerewitz J. Glycosaminoglycan-mediated leuserpin-2/thrombin interaction. Structure-function relationships. J Biol Chem. 1990;265:22386-22391.
30. Brinkmeyer S, Eckert R, Ragg H. Reformable intramolecular cross-linking of the N-terminal domain of heparin cofactor II: effects on enzyme inhibition. Eur J Biochem. 2004;271:4275-4283.
31. Fortenberry YM, Whinna HC, Gentry HR, Myles T, Leung LL, Church FC. Molecular mapping of the thrombin-heparin cofactor II complex. J Biol Chem. 2004;279:43237-43244.
32. Sheehan JP, Tollefsen DM, Sadler JE. Heparin cofactor II is regulated allosterically and not primarily by template effects. Studies with mutant thrombins and glycosaminoglycans. J Biol Chem. 1994;269:32747-32751.
33. Sheehan JP, Wu Q, Tollefsen DM, Sadler JE. Mutagenesis of thrombin selectively modulates inhibition by serpins heparin cofactor II and antithrombin III. Interaction with the anion-binding exosite determines heparin cofactor II specificity. J Biol Chem. 1993;268:3639-3645.
34. Baglin TP, Carrell RW, Church FC, Esmon CT, Huntington JA. Crystal structures of native and thrombin-complexed heparin cofactor II reveal a multistep allosteric mechanism. Proc Natl Acad Sci U S A. 2002;99:11079-11084.
35. Verhamme IM, Bock PE, Jackson CM. The preferred pathway of glycosaminoglycan-accelerated inactivation of thrombin by heparin cofactor II. J Biol Chem. 2004;279:9785-9795.
36. Liu L, Dewar L, Song Y, Kulczycky M, Blajchman MA, Fenton JW, 2nd, Andrew M, Delorme M, Ginsberg J, Preissner KT, Ofosu FA. Inhibition of thrombin by antithrombin III and heparin cofactor II in vivo. Thromb Haemost. 1995;73:405-412.
37. Hiramoto SA, Cunningham DD. Effects of fibroblasts and endothelial cells on inactivation of target proteases by protease nexin-1, heparin cofactor II, and C1-inhibitor. J Cell Biochem. 1988;36:199-207.
38. McGuire EA, Tollefsen DM. Activation of heparin cofactor II by fibroblasts and vascular smooth muscle cells. J Biol Chem. 1987;262:169-175.
39. Whinna HC, Choi HU, Rosenberg LC, Church FC. Interaction of heparin cofactor II with biglycan and decorin. J Biol Chem. 1993;268:3920-3924.
40. Tovar AMF, de Mattos DA, Stelling MP, Sarcinelli-Luz BSL, Nazareth RA, Mourão PAS. Dermatan sulfate is the predominant antithrombotic glycosaminoglycan in vessel walls: implications for a possible physiological function of heparin cofactor II. Biochim Biophys Acta. 2005;1740:45-53.
41. Tollefsen DM. Heparin cofactor II deficiency. Arch Pathol Lab Med. 2002;126:1394-1400.
42. Villa P, Aznar J, Vaya A, España F, Ferrando F, Mira Y, Estellés A. Hereditary homozygous heparin cofactor II deficiency and the risk of developing venous thrombosis. Thromb Haemost. 1999;82:1011-1014.
43. Massouh M, Jatoi A, Gordon EM, Ratnoff OD. Heparin cofactor II activity in plasma during pregnancy and oral contraceptive use. J Lab Clin Med. 1989;114:697-699.
44. Bellart J, Gilabert R, Cabero L, Fontcuberta J, Monasterio J, Miralles RM. Heparin cofactor II: a new marker for pre-eclampsia. Blood Coagul Fibrinolysis. 1998;9:205-208.
45. Andrew M, Mitchell L, Berry L, Paes B, Delorme M, Ofosu F, Burrows R, Khambalia B. An anticoagulant dermatan sulfate proteoglycan circulates in the pregnant woman and her fetus. J Clin Invest. 1992;89:321-326.
46. Giri TK, Tollefsen DM. Placental dermatan sulfate: isolation, anticoagulant activity, and association with heparin cofactor II. Blood. 2006;107:2753-2758.
47. Takamori N, Azuma H, Kato M, Hashizume S, Aihara K, Akaike M, Tamura K, Matsumoto T. High plasma heparin cofactor II activity is associated with reduced incidence of in-stent restenosis after percutaneous coronary intervention. Circulation. 2004;109:481-486.
48. Schillinger M, Exner M, Sabeti S, Mlekusch W, Amighi J, Handler S, Quehenberger P, Kalifeh N, Wagner O, Minar E. High plasma heparin cofactor II activity protects from restenosis after femoropopliteal stenting. Thromb Haemost. 2004;92:1108-1113.
49. Aihara K, Azuma H, Takamori N, Kanagawa Y, Akaike M, Fujimura M, Yoshida T, Hashizume S, Kato M, Yamaguchi H, Kato S, Ikeda Y, Arase T, Kondo A, Matsumoto T. Heparin cofactor II is a novel protective factor against carotid atherosclerosis in elderly individuals. Circulation. 2004;109:2761-2765.
50. Giri TK, Ahn CW, Wu KK, Tollefsen DM. Heparin cofactor II levels do not predict the development of coronary heart disease: the Atherosclerosis Risk in Communities (ARIC) study. Arterioscler Thromb Vasc Biol. 2005;25:2689-2690.
51. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-874.
52. Tracy RP. Thrombin, inflammation, and cardiovascular disease: an epidemiologic perspective. Chest. 2003;124:49S-57S.
53. Coughlin SR. Protease-activated receptors in the cardiovascular system. Cold Spring Harb Symp Quant Biol. 2002;67:197-208.
54. Farb A, Sangiorgi G, Carter AJ, Walley VM, Edwards WD, Schwartz RS, Virmani R. Pathology of acute and chronic coronary stenting in humans. Circulation. 1999;99:44-52.
55. Cheung WM, D'Andrea MR, Andrade-Gordon P, Damiano BP. Altered vascular injury responses in mice deficient in protease-activated receptor-1. Arterioscler Thromb Vasc Biol. 1999;19:3014-3024.
56. Andrade-Gordon P, Derian CK, Maryanoff BE, Zhang HC, Addo MF, Cheung W, Damiano BP, D'Andrea MR, Darrow AL, de Garavilla L, Eckardt AJ, Giardino EC, Haertlein BJ, McComsey DF. Administration of a potent antagonist of protease-activated receptor-1 (PAR-1) attenuates vascular restenosis following balloon angioplasty in rats. J Pharmacol Exp Ther. 2001;298:34-42.
57. Chen X, Ren S, Ma MG, Dharmalingam S, Lu L, Xue M, Ducas J, Shen GX. Hirulog-like peptide reduces restenosis and expression of tissue factor and transforming growth factor-beta in carotid artery of atherosclerotic rabbits. Atherosclerosis. 2003;169:31-40.
58. Liaw PC, Becker DL, Stafford AR, Fredenburgh JC, Weitz JI. Molecular basis for the susceptibility of fibrin-bound thrombin to inactivation by heparin cofactor ii in the presence of dermatan sulfate but not heparin. J Biol Chem. 2001;276:20959-20965.
59. Buchanan MR, Brister SJ. Inhibition of chronic vessel wall intimal hyperplasia following acute anticoagulant treatment: relative effects of heparin and dermatan sulphate. Thromb Res. 1998;91:157-167.
60. Stoop AA, Lupu F, Pannekoek H. Colocalization of thrombin, PAI-1, and vitronectin in the atherosclerotic vessel wall: A potential regulatory mechanism of thrombin activity by PAI-1/vitronectin complexes. Arterioscler Thromb Vasc Biol. 2000;20:1143-1149.
61. Westrick RJ, Bodary PF, Xu Z, Shen YC, Broze GJ, Eitzman DT. Deficiency of tissue factor pathway inhibitor promotes atherosclerosis and thrombosis in mice. Circulation. 2001;103:3044-3046.
62. Cooper ST, Neese LL, DiCuccio MN, Liles DK, Hoffman M, Church FC. Vascular localization of the heparin-binding serpins antithrombin, heparin cofactor II, and protein C inhibitor. Clin Appl Thrombosis/Hemostasis. 1996;2:185-191.
63. Shirk RA, Parthasarathy N, San Antonio JD, Church FC, Wagner WD. Altered dermatan sulfate structure and reduced heparin cofactor II-stimulating activity of biglycan and decorin from human atherosclerotic plaque. J Biol Chem. 2000;275:18085-18092.
64. He L, Vicente CP, Westrick RJ, Eitzman DT, Tollefsen DM. Heparin cofactor II inhibits arterial thrombosis after endothelial injury. J Clin Invest. 2002;109:213-219.
65. Blinder MA, Andersson TR, Abildgaard U, Tollefsen DM. Heparin cofactor IIOslo. Mutation of Arg-189 to His decreases the affinity for dermatan sulfate. J Biol Chem. 1989;264:5128-5133.
66. Whinna HC, Blinder MA, Szewczyk M, Tollefsen DM, Church FC. Role of lysine 173 in heparin binding to heparin cofactor II. J Biol Chem. 1991;266:8129-8135.
67. Vicente CP, He L, Pavão MSG, Tollefsen DM. Antithrombotic activity of dermatan sulfate in heparin cofactor II-deficient mice. Blood. 2004;104:3965-3970.
68. Leidenfrost JE, Khan MF, Boc KP, Villa BR, Collins ET, Parks WC, Abendschein DR, Choi ET. A model of primary atherosclerosis and postangioplasty restenosis in mice. Am J Pathol. 2003;163:773-778.