Vascular dermatan sulfate and heparin cofactor II

Progress in Molecular Biology and Translational Science

Volumn 93, Issue C, 2010, Pages 351-372

  Tollefsen, Douglas M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Artery; Atherosclerosis; Coagulation; Dermatan sulfate; Heparin cofactor II; Neointima; Serpin; Thrombin; Thrombosis

Indexed keywords

ANTICOAGULANT AGENT; DERMATAN SULFATE; HEPARIN COFACTOR II; SERINE PROTEINASE INHIBITOR;

ANIMAL; ATHEROSCLEROSIS; BLOOD VESSEL; CAROTID ARTERY THROMBOSIS; DRUG EFFECT; HUMAN; METABOLISM; MOUSE; MOUSE MUTANT; PATHOLOGY; PHYSIOLOGY; REVIEW;

ANIMALS; ANTICOAGULANTS; ATHEROSCLEROSIS; BLOOD VESSELS; CAROTID ARTERY THROMBOSIS; DERMATAN SULFATE; HEPARIN COFACTOR II; HUMANS; MICE; MICE, KNOCKOUT; SERINE PROTEINASE INHIBITORS;

EID: 77958169319     PISSN: 18771173     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1877-1173(10)93015-9     Document Type: Chapter

References (99)

1. J.M. Trowbridge, and R.L. Gallo Dermatan sulfate: new functions from an old glycosaminoglycan Glycobiology 12 2002 117R 125R
2. D.M. Tollefsen Heparin cofactor II modulates the response to vascular injury Arterioscler Thromb Vasc Biol 27 2007 454 460
3. J.A. Huntington Mechanisms of glycosaminoglycan activation of the serpins in hemostasis J Thromb Haemost 1 2003 1535 1549
4. K.M. Brinkhous, H.P. Smith, E.D. Warner, and W.H. Seegers The inhibition of blood clotting: an unidentified substance which acts in conjunction with heparin to prevent the conversion of prothrombin into thrombin Am J Physiol 125 1939 683
5. U. Abildgaard Highly purified antithrombin 3 with heparin cofactor activity prepared by disc electrophoresis Scand J Clin Lab Invest 21 1968 89 91
6. J.S. Rosenberg, P.W. McKenna, and R.D. Rosenberg Inhibition of human factor IXa by human antithrombin J Biol Chem 250 1975 8883 8888
7. R.D. Rosenberg, and P.S. Damus The purification and mechanism of action of human antithrombin-heparin cofactor J Biol Chem 248 1973 6490 6505
8. G.F. Briginshaw, and J.N. Shanberge Identification of two distinct heparin cofactors in human plasma. Separation and partial purification Arch Biochem Biophys 161 1974 683 690
9. G.F. Briginshaw, and J.N. Shanberge Identification of two distinct heparin cofactors in human plasma II. Inhibition of thrombin and activated factor X Thromb Res 4 1974 463 477
10. D.M. Tollefsen, and M.K. Blank Detection of a new heparin-dependent inhibitor of thrombin in human plasma J Clin Invest 68 1981 589 596
11. P. Friberger, N. Egberg, E. Holmer, M. Hellgren, and M. Blombck Antithrombin assaythe use of human or bovine thrombin and the observation of a "second" heparin cofactor Thromb Res 25 1982 433 436
12. M.J. Griffith, T. Carraway, G.C. White, and F.A. Dombrose Heparin cofactor activities in a family with hereditary antithrombin III deficiency: evidence for a second heparin cofactor in human plasma Blood 61 1983 111 118
13. D.M. Tollefsen, D.W. Majerus, and M.K. Blank Heparin cofactor II. Purification and properties of a heparin-dependent inhibitor of thrombin in human plasma J Biol Chem 257 1982 2162 2169
14. M.A. Blinder, J.C. Marasa, C.H. Reynolds, L.L. Deaven, and D.M. Tollefsen Heparin cofactor II: cDNA sequence, chromosome localization, restriction fragment length polymorphism, and expression in Escherichia coli Biochemistry 27 1988 752 759
15. H. Ragg A new member of the plasma protease inhibitor gene family Nucleic Acids Res 14 1986 1073 1088
16. G.S. Zhang, J.H. Mehringer, V.M. Van Deerlin, C.A. Kozak, and D.M. Tollefsen Murine heparin cofactor II: purification, cDNA sequence, expression, and gene structure Biochemistry 33 1994 3632 3642
17. P. Kamp, A. Strathmann, and H. Ragg Heparin cofactor II, antithrombin-beta and their complexes with thrombin in human tissues Thromb Res 101 2001 483 491
18. D.M. Tollefsen, and C.A. Pestka Heparin cofactor II activity in patients with disseminated intravascular coagulation and hepatic failure Blood 66 1985 769 774
19. M.Z. Kounnas, F.C. Church, W.S. Argraves, and D.K. Strickland 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 271 1996 6523 6529
20. P.G. Gettins Serpin structure, mechanism, and function Chem Rev 102 2002 4751 4804
21. J.A. Huntington Shape-shifting serpinsadvantages of a mobile mechanism Trends Biochem Sci 31 2006 427 435
22. J.A. Huntington, R.J. Read, and R.W. Carrell Structure of a serpin-protease complex shows inhibition by deformation Nature 407 2000 923 926
23. M.J. Griffith, C.M. Noyes, J.A. Tyndall, and F.C. Church Structural evidence for leucine at the reactive site of heparin cofactor II Biochemistry 24 1985 6777 6782
24. K.A. Parker, and D.M. Tollefsen The protease specificity of heparin cofactor II. Inhibition of thrombin generated during coagulation J Biol Chem 260 1985 3501 3505
25. F.C. Church, C.M. Noyes, and M.J. Griffith Inhibition of chymotrypsin by heparin cofactor II Proc Natl Acad Sci USA 82 1985 6431 6434
26. V.M. Derechin, M.A. Blinder, and D.M. Tollefsen Substitution of arginine for Leu444 in the reactive site of heparin cofactor II enhances the rate of thrombin inhibition J Biol Chem 265 1990 5623 5628
27. D.M. Tollefsen, C.A. Pestka, and W.J. Monafo Activation of heparin cofactor II by dermatan sulfate J Biol Chem 258 1983 6713 6716
28. G.L. Hortin, D.M. Tollefsen, and B.M. Benutto Antithrombin activity of a peptide corresponding to residues 5475 of heparin cofactor II J Biol Chem 264 1989 13979 13982
29. H. Ragg, T. Ulshfer, and J. Gerewitz On the activation of human leuserpin-2, a thrombin inhibitor, by glycosaminoglycans J Biol Chem 265 1990 5211 5218
30. H. Ragg, T. Ulshfer, and J. Gerewitz Glycosaminoglycan-mediated leuserpin-2/thrombin interaction. Structurefunction relationships J Biol Chem 265 1990 22386 22391
31. V.M. Van Deerlin, and D.M. Tollefsen The N-terminal acidic domain of heparin cofactor II mediates the inhibition of alpha-thrombin in the presence of glycosaminoglycans J Biol Chem 266 1991 20223 20231
32. Y.M. Fortenberry, H.C. Whinna, H.R. Gentry, T. Myles, L.L. Leung, and F.C. Church Molecular mapping of the thrombin-heparin cofactor II complex J Biol Chem 279 2004 43237 43244
33. J.P. Sheehan, D.M. Tollefsen, and J.E. Sadler Heparin cofactor II is regulated allosterically and not primarily by template effects. Studies with mutant thrombins and glycosaminoglycans J Biol Chem 269 1994 32747 32751
34. J.P. Sheehan, Q. Wu, D.M. Tollefsen, and J.E. Sadler 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 268 1993 3639 3645
35. S. Brinkmeyer, R. Eckert, and H. Ragg Reformable intramolecular cross-linking of the N-terminal domain of heparin cofactor II: effects on enzyme inhibition Eur J Biochem 271 2004 4275 4283
36. T.P. Baglin, R.W. Carrell, F.C. Church, C.T. Esmon, and J.A. Huntington Crystal structures of native and thrombin-complexed heparin cofactor II reveal a multistep allosteric mechanism Proc Natl Acad Sci USA 99 2002 11079 11084
37. I.M. Verhamme, P.E. Bock, and C.M. Jackson The preferred pathway of glycosaminoglycan-accelerated inactivation of thrombin by heparin cofactor II J Biol Chem 279 2004 9785 9795
38. D. O'Keeffe, S.T. Olson, N. Gasiunas, J. Gallagher, T.P. Baglin, and J.A. Huntington The heparin binding properties of heparin cofactor II suggest an antithrombin-like activation mechanism J Biol Chem 279 2004 50267 50273
39. M.A. Blinder, T.R. Andersson, U. Abildgaard, and D.M. Tollefsen Heparin cofactor IIOslo. Mutation of Arg-189 to His decreases the affinity for dermatan sulfate J Biol Chem 264 1989 5128 5133
40. M.A. Blinder, and D.M. Tollefsen Site-directed mutagenesis of arginine 103 and lysine 185 in the proposed glycosaminoglycan-binding site of heparin cofactor II J Biol Chem 265 1990 286 291
41. H.C. Whinna, M.A. Blinder, M. Szewczyk, D.M. Tollefsen, and F.C. Church Role of lysine 173 in heparin binding to heparin cofactor II J Biol Chem 266 1991 8129 8135
42. M.M. Maimone Characterization of heparin and dermatan sulfate molecules that bind and activate heparin cofactor II 1990 Washington University St. Louis, MO Ph.D. thesis
43. M.M. Maimone, and D.M. Tollefsen Activation of heparin cofactor II by heparin oligosaccharides Biochem Biophys Res Commun 152 1988 1056 1061
44. N.S. Colwell, M.J. Grupe, and D.M. Tollefsen Amino acid residues of heparin cofactor II required for stimulation of thrombin inhibition by sulphated polyanions Biochim Biophys Acta 1431 1999 148 156
45. M.M. Maimone, and D.M. Tollefsen Structure of a dermatan sulfate hexasaccharide that binds to heparin cofactor II with high affinity J Biol Chem 265 1990 18263 18271
46. M.S.G. Pavo, K.R. Aiello, C.C. Werneck, L.C. Silva, A.-P. Valente, and B. Mulloy Highly sulfated dermatan sulfates from Ascidians. Structure versus anticoagulant activity of these glycosaminoglycans J Biol Chem 273 1998 27848 27857
47. M.S.G. Pavo, P.A.S. Mouro, B. Mulloy, and D.M. Tollefsen A unique dermatan sulfate-like glycosaminoglycan from ascidian. Its structure and the effect of its unusual sulfation pattern on anticoagulant activity J Biol Chem 270 1995 31027 31036
48. A.M. Halldrsdttir, L. Zhang, and D.M. Tollefsen N-Acetylgalactosamine 4, 6-O-sulfate residues mediate binding and activation of heparin cofactor II by porcine mucosal dermatan sulfate Glycobiology 16 2006 693 701
49. M.W. Hatton, H. Hoogendoorn, S.M. Southward, B. Ross, and M.A. Blajchman Comparative metabolism and distribution of rabbit heparin cofactor II and rabbit antithrombin in rabbits Am J Physiol 272 1997 E824 E831
50. P. Si, D. Dupouy, J. Pichon, and B. Boneu Turnover study of heparin cofactor II in healthy man Thromb Haemost 54 1985 635 638
51. P. Si, J. Lansen, F. Lacheretz, B. Verschuere, and B. Boneu Comparative turn-over of heparin cofactor II and antithrombin III in baboons. Influence of heparin and pentosan polysulfate administration Thromb Haemost 56 1986 302 307
52. D.T. Le, P. Borgs, T.W. Toneff, M.H. Witte, and S.I. Rapaport Hemostatic factors in rabbit limb lymph: relationship to mechanisms regulating extravascular coagulation Am J Physiol 274 1998 H769 H776
53. P.L. Tuma, and A.L. Hubbard Transcytosis: crossing cellular barriers Physiol Rev 83 2003 871 932
54. S.T. Cooper, L.L. Neese, M.N. DiCuccio, D.K. Liles, M. Hoffman, and F.C. Church Vascular localization of the heparin-binding serpins antithrombin, heparin cofactor II, and protein C inhibitor Clin Appl Thromb Hemost 2 1996 185 191
55. A.M.F. Tovar, D.A. de Mattos, M.P. Stelling, B.S.L. Sarcinelli-Luz, R.A. Nazareth, and P.A.S. Mouro Dermatan sulfate is the predominant antithrombotic glycosaminoglycan in vessel walls: implications for a possible physiological function of heparin cofactor II Biochim Biophys Acta 1740 2005 45 53
56. P. Si, F. Ofosu, F. Fernandez, M.R. Buchanan, M. Petitou, and B. Boneu Respective role of antithrombin III and heparin cofactor II in the in vitro anticoagulant effect of heparin and of various sulphated polysaccharides Br J Haematol 64 1986 707 714
57. E.A. McGuire, and D.M. Tollefsen Activation of heparin cofactor II by fibroblasts and vascular smooth muscle cells J Biol Chem 262 1987 169 175
58. H.C. Whinna, H.U. Choi, L.C. Rosenberg, and F.C. Church Interaction of heparin cofactor II with biglycan and decorin J Biol Chem 268 1993 3920 3924
59. L. He, C.P. Vicente, R.J. Westrick, D.T. Eitzman, and D.M. Tollefsen Heparin cofactor II inhibits arterial thrombosis after endothelial injury J Clin Invest 109 2002 213 219
60. K. Aihara, H. Azuma, M. Akaike, Y. Ikeda, M. Sata, and N. Takamori Strain-dependent embryonic lethality and exaggerated vascular remodeling in heparin cofactor II-deficient mice J Clin Invest 117 2007 1514 1526
61. A.R. Saniabadi, K. Umemura, N. Matsumoto, S. Sakuma, and M. Nakashima Vessel wall injury and arterial thrombosis induced by a photochemical reaction Thromb Haemost 73 1995 868 872
62. J.N. Wilcox, K.M. Smith, S.M. Schwartz, and D. Gordon Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque Proc Natl Acad Sci USA 86 1989 2839 2843
63. K.G. Mann, S. Butenas, and K. Brummel The dynamics of thrombin formation Arterioscler Thromb Vasc Biol 23 2003 17 25
64. S.R. Coughlin Protease-activated receptors in the cardiovascular system Cold Spring Harb Symp Quant Biol 67 2002 197 208
65. L. He, T.K. Giri, C.P. Vicente, and D.M. Tollefsen Vascular dermatan sulfate regulates the antithrombotic activity of heparin cofactor II Blood 111 2008 4118 4125
66. C.P. Vicente, L. He, M.S. Pavao, and D.M. Tollefsen Antithrombotic activity of dermatan sulfate in heparin cofactor II-deficient mice Blood 104 2004 3965 3970
67. M. Abbadini, G.J. Zhu, A. Maggi, J. Pangrazzi, M.B. Donati, and L. Mussoni Dermatan sulphate induces plasminogen activator release in the perfused rat hindquarters Blood 70 1987 1858 1860
68. M. Barbanti, F. Calanni, E. Marchi, N. Semeraro, and M. Colucci Desmin 370, a low molecular weight dermatan sulfate, reduces the weight of preformed thrombi in rats made afibrinogenemic by ancrod Thromb Haemost 73 1995 287 290
69. C.P. Vicente, L. He, and D.M. Tollefsen Accelerated atherogenesis and neointima formation in heparin cofactor II deficient mice Blood 110 2007 4261 4267
70. J.E. Leidenfrost, M.F. Khan, K.P. Boc, B.R. Villa, E.T. Collins, and W.C. Parks A model of primary atherosclerosis and post-angioplasty restenosis in mice Am J Pathol 163 2003 773 778
71. A. Farb, G. Sangiorgi, A.J. Carter, V.M. Walley, W.D. Edwards, and R.S. Schwartz Pathology of acute and chronic coronary stenting in humans Circulation 99 1999 44 52 (Pubitemid 29035956)
72. W.M. Cheung, M.R. D'Andrea, P. Andrade-Gordon, and B.P. Damiano Altered vascular injury responses in mice deficient in protease-activated receptor-1 Arterioscler Thromb Vasc Biol 19 1999 3014 3024
73. P. Andrade-Gordon, C.K. Derian, B.E. Maryanoff, H.C. Zhang, M.F. Addo, and W. Cheung Administration of a potent antagonist of protease-activated receptor-1 (PAR-1) attenuates vascular restenosis following balloon angioplasty in rats J Pharmacol Exp Ther 298 2001 34 42
74. X. Chen, S. Ren, M.G. Ma, S. Dharmalingam, L. Lu, and M. Xue Hirulog-like peptide reduces restenosis and expression of tissue factor and transforming growth factor-beta in carotid artery of atherosclerotic rabbits Atherosclerosis 169 2003 31 40
75. M.R. Buchanan, and S.J. Brister Inhibition of chronic vessel wall intimal hyperplasia following acute anticoagulant treatment: relative effects of heparin and dermatan sulphate Thromb Res 91 1998 157 167
76. P.C. Liaw, D.L. Becker, A.R. Stafford, J.C. Fredenburgh, and J.I. Weitz 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 276 2001 20959 20965
77. J.I. Borissoff, H.M. Spronk, S. Heeneman, and H. ten Cate Is thrombin a key player in the 'coagulation-atherogenesis' maze? Cardiovasc Res 82 2009 392 403
78. A.A. Stoop, F. Lupu, and H. Pannekoek 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 20 2000 1143 1149
79. R.J. Westrick, P.F. Bodary, Z. Xu, Y.C. Shen, G.J. Broze, and D.T. Eitzman Deficiency of tissue factor pathway inhibitor promotes atherosclerosis and thrombosis in mice Circulation 103 2001 3044 3046
80. J.C. Rau, C. Deans, M.R. Hoffman, D.B. Thomas, G.T. Malcom, and A.W. Zieske Heparin cofactor II in atherosclerotic lesions from the Pathobiological Determinants of Atherosclerosis in Youth (PDAY) study Exp Mol Pathol 87 2009 178 183
81. R.A. Shirk, N. Parthasarathy, J.D. San Antonio, F.C. Church, and W.D. Wagner Altered dermatan sulfate structure and reduced heparin cofactor II-stimulating activity of biglycan and decorin from human atherosclerotic plaque J Biol Chem 275 2000 18085 18092
82. J.R. Couchman, B. Caterson, J.E. Christner, and J.R. Baker Mapping by monoclonal antibody detection of glycosaminoglycans in connective tissues Nature 307 1984 650 652
83. G. David, X.M. Bai, B. Van der Schueren, J.J. Cassiman, and H. Van den Berghe Developmental changes in heparan sulfate expression: in situ detection with mAbs J Cell Biol 119 1992 961 975
84. F. Rodeghiero, and A. Tosetto The VITA Project: population-based distributions of protein C, antithrombin III, heparin-cofactor II and plasminogen-relationship with physiological variables and establishment of reference ranges Thromb Haemost 76 1996 226 233
85. D.M. Tollefsen Heparin cofactor II deficiency Arch Pathol Lab Med 126 2002 1394 1400
86. L. Liu, L. Dewar, Y. Song, M. Kulczycky, M.A. Blajchman, and J.W. Fenton 2nd Inhibition of thrombin by antithrombin III and heparin cofactor II in vivo Thromb Haemost 73 1995 405 412
87. M. Massouh, A. Jatoi, E.M. Gordon, and O.D. Ratnoff Heparin cofactor II activity in plasma during pregnancy and oral contraceptive use J Lab Clin Med 114 1989 697 699
88. J. Bellart, R. Gilabert, L. Cabero, J. Fontcuberta, J. Monasterio, and R.M. Miralles Heparin cofactor II: a new marker for pre-eclampsia Blood Coagul Fibrinolysis 9 1998 205 208
89. M. Andrew, L. Mitchell, L. Berry, B. Paes, M. Delorme, and F. Ofosu An anticoagulant dermatan sulfate proteoglycan circulates in the pregnant woman and her fetus J Clin Invest 89 1992 321 326
90. T.K. Giri, and D.M. Tollefsen Placental dermatan sulfate: isolation, anticoagulant activity, and association with heparin cofactor II Blood 107 2006 2753 2758
91. P. Villa, J. Aznar, A. Vaya, F. Espaa, F. Ferrando, and Y. Mira Hereditary homozygous heparin cofactor II deficiency and the risk of developing venous thrombosis Thromb Haemost 82 1999 1011 1014
92. K. Aihara, H. Azuma, N. Takamori, Y. Kanagawa, M. Akaike, and M. Fujimura Heparin cofactor II is a novel protective factor against carotid atherosclerosis in elderly individuals Circulation 109 2004 2761 2765
93. S.S. Huang, P.H. Huang, Y.H. Chen, S.H. Sung, K.H. Chiang, and J.W. Chen Plasma heparin cofactor II activity is an independent predictor of future cardiovascular events in patients after acute myocardial infarction Coron Artery Dis 19 2008 597 602
94. K. Aihara, H. Azuma, M. Akaike, H. Kurobe, N. Takamori, and Y. Ikeda Heparin cofactor II is an independent protective factor against peripheral arterial disease in elderly subjects with cardiovascular risk factors J Atheroscler Thromb 16 2009 127 134
95. T.K. Giri, C.W. Ahn, K.K. Wu, and D.M. Tollefsen Heparin cofactor II levels do not predict the development of coronary heart disease: the Atherosclerosis Risk in Communities (ARIC) study Arterioscler Thromb Vasc Biol 25 2005 2689 2690
96. N. Takamori, H. Azuma, M. Kato, S. Hashizume, K. Aihara, and M. Akaike High plasma heparin cofactor II activity is associated with reduced incidence of in-stent restenosis after percutaneous coronary intervention Circulation 109 2004 481 486
97. M. Schillinger, M. Exner, S. Sabeti, W. Mlekusch, J. Amighi, and S. Handler High plasma heparin cofactor II activity protects from restenosis after femoropopliteal stenting Thromb Haemost 92 2004 1108 1113
98. K. Langford-Smith, M. Arasaradnam, J.E. Wraith, R. Wynn, and B.W. Bigger Evaluation of heparin cofactor II-thrombin complex as a biomarker on blood spots from mucopolysaccharidosis I, IIIA and IIIB mice Mol Genet Metab 99 2010 269 274
99. D.R. Randall, K.E. Colobong, H. Hemmelgarn, G.B. Sinclair, E. Hetty, and A. Thomas Heparin cofactor II-thrombin complex: a biomarker of MPS disease Mol Genet Metab 94 2008 456 461