Isolation of Frog and Chicken cDNAs Encoding Heparin Cofactor II

Niall S. Colwell; Douglas M. Tollefsen

doi:10.1055/s-0037-1615359

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 1998; 80(05): 784-790
DOI: 10.1055/s-0037-1615359

Review Article

Schattauer GmbH

Isolation of Frog and Chicken cDNAs Encoding Heparin Cofactor II

Niall S. Colwell

¹From the Division of Hematology, Department of Internal Medicine, Washington University School of Medicine, St. Louis, Missouri, USA

,

Douglas M. Tollefsen

¹From the Division of Hematology, Department of Internal Medicine, Washington University School of Medicine, St. Louis, Missouri, USA

› Author Affiliations

Abstract

Summary

Heparin cofactor II (HCII) is a serpin that inhibits thrombin rapidly in the presence of heparin or dermatan sulfate. HCII activity has been detected in human, rabbit, and mouse plasma, and cDNA clones for HCII have been isolated previously from human, rabbit, rat, and mouse liver libraries, suggesting a conserved physiologic role for HCII among mammals. In this report, we show that both frog and chicken plasma contain a dermatan sulfate-dependent inhibitor that forms a 118-kDa complex with human ¹²⁵I-thrombin. Screening of frog and chicken liver cDNA libraries in bacteriophage λ with a human HCII cDNA probe yielded nearly full-length clones with inserts of 1.8 and 1.7 kb, respectively. The amino acid sequences deduced from the frog and chicken HCII cDNAs are ~60% identical to one another and to each of the mammalian sequences. In particular, the N-terminal acidic domain, the glycosaminoglycan-binding site, and the reactive site sequences are highly conserved. Our results indicate that HCII is widely distributed among vertebrates and may have a common function in birds, amphibians, and mammals.

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References

References
1 Tollefsen DM. Insight into the mechanism of action of heparin cofactor II. Thromb Haemost 1995; 74: 1209-14.
2 Gettins PGW, Patston PA, Olson ST. Serpins: Structure, Function and Biology. Austin: TX: R. G. Landes Company; 1996
3 Chemistry and Biology of Serpins.. Church FC, Cunningham DD, Ginsburg D, Hoffman M, Stone SR, Tollefsen DM. eds. New York: Plenum Press 1997
4 Griffith MJ, Noyes CM, Tyndall JA, Church FC. Structural evidence for leucine at the reactive site of heparin cofactor II. Biochemistry 1985; 24: 6777-82.
5 Ragg H. A new member of the plasma protease inhibitor gene family. Nucleic Acids Res 1986; 14: 1073-88.
6 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: 752-9.
7 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: 13979-82.
8 Van Deerlin VMD, Tollefsen DM. The N-terminal acidic domain of heparin cofactor II mediates the inhibition of a-thrombin in the presence of glycosaminoglycans. J Biol Chem 1991; 266: 20223-31.
9 Ragg H, Ulshöfer T, Gerewitz J. On the activation of human leuserpin-2, a thrombin inhibitor, by glycosaminoglycans. J Biol Chem 1990; 265: 5211-8.
10 Rogers SJ, Pratt CW, Whinna HC, Church FC. Role of thrombin exosites in inhibition by heparin cofactor II. J Biol Chem 1992; 267: 3613-7.
11 Sheehan JP, Wu Q, Tollefsen DM, Sadler JE. Mutagenesis of thrombin selectively modulates inhibition by serpins heparin cofactor II and anti-thrombin III. Interaction with the anion-binding exosite determines heparin cofactor II specificity. J Biol Chem 1993; 268: 3639-45.
12 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: 32747-51.
13 Tollefsen DM, Blank MK. Detection of a new heparin-dependent inhibitor of thrombin in human plasma. J Clin Invest 1981; 68: 589-96.
14 Tollefsen DM, Pestka CA, Monafo WJ. Activation of heparin cofactor II by dermatan sulfate. J Biol Chem 1983; 258: 6713-6.
15 McGuire EA, Tollefsen DM. Activation of heparin cofactor II by fibro-blasts and vascular smooth muscle cells. J Biol Chem 1987; 262: 169-75.
16 Whinna HC, Choi HU, Rosenberg LC, Church FC. Interaction of heparin cofactor II with biglycan and decorin. J Biol Chem 1993; 268: 3920-4.
17 Shirk RA, Church FC, Wagner WD. Arterial smooth muscle cell heparan sulfate proteoglycans accelerate thrombin inhibition by heparin cofactor II. Arterioscler Thromb Vasc Biol 1996; 16: 1138-46.
18 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: 321-6.
19 Sheffield WP, Schuyler PD, Blajchman MA. Molecular cloning and expression of rabbit heparin cofactor II: a plasma thrombin inhibitor highly conserved between species. Thromb Haemost 1994; 71: 778-82.
20 Westrup D, Ragg H. Secondary thrombin-binding site, glycosaminoglycan binding domain and reactive center region of leuserpin-2 are strongly conserved in mammalian species. Biochim Biophys Acta 1994; 1217: 93-6.
21 Zhang GS, Mehringer JH, Van Deerlin VMD, Kozak CA, Tollefsen DM. Murine heparin cofactor II: purification, cDNA sequence, expression, and gene structure. Biochemistry 1994; 33: 3632-42.
22 Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-5.
23 Sambrook J, Fritsch EF, Maniatis T. Molecular Cloning: a Laboratory Manual (2nd Edition). Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 1989
24 Bajaj SP, Birktoft JJ. Human factor IX and factor IXa. Methods Enzymol 1993; 222: 96-128.
25 Sié P, Ofosu F, Fernandez F, Buchanan MR, Petitou M, Boneu B. 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 1986; 64: 707-14.
26 Tejada ML, Deeley RG. Cloning of an avian antithrombin: developmental and hormonal regulation of expression. Thromb Haemost 1995; 73: 654-61.
27 Kozak M. An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol 1991; 115: 887-903.
28 von Heijne G. Signal sequences. The limits of variation. J Mol Biol 1985; 184: 99-105.
29 Parker KA, Tollefsen DM. The protease specificity of heparin cofactor II. Inhibition of thrombin generated during coagulation. J Biol Chem 1985; 260: 3501-5.
30 Church FC, Noyes CM, Griffith MJ. Inhibition of chymotrypsin by heparin cofactor II. Proc Natl Acad Sci U S A 1985; 82: 6431-4.
31 Pratt CW, Tobin RB, Church FC. Interaction of heparin cofactor II with neutrophil elastase and cathepsin G. J Biol Chem 1990; 265: 6092-7.
32 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: 5623-8.
33 Sheffield WP, Blajchman MA. Deletion mutagenesis of heparin cofactor II: defining the minimum size of a thrombin inhibiting serpin. FEBS Lett 1995; 365: 189-92.
34 Hortin G, Tollefsen DM, Strauss AW. Identification of two sites of sulfation of human heparin cofactor II. J Biol Chem 1986; 261: 15827-30.
35 Church FC, Pratt CW, Hoffman M. Leukocyte chemoattractant peptides from the serpin heparin cofactor II. J Biol Chem 1991; 266: 704-9.
36 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: 5128-33.
37 Blinder MA, Tollefsen DM. Site-directed mutagenesis of arginine 103 and lysine 185 in the proposed glycosaminoglycan-binding site of heparin cofactor II. J Biol Chem 1990; 265: 286-91.
38 Ragg H, Ulshöfer T, Gerewitz J. Glycosaminoglycan-mediated leuserpin-2/ thrombin interaction. Structure-function relationships. J Biol Chem 1990; 265: 22386-91.
39 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: 8129-35.
40 Church FC, Meade JB, Pratt CW. Structure-function relationships in heparin cofactor II: spectral analysis of aromatic residues and absence of a role for sulfhydryl groups in thrombin inhibition. Arch Biochem Biophys 1987; 259: 331-40.
41 Huber R, Carrell RW. Implications of the three-dimensional structure of α1-antitrypsin for structure and function of serpins. Biochemistry 1989; 28: 8951-66.
42 Ciaccia AV, Monroe DM, Church FC. Arginine 200 of heparin cofactor II promotes intramolecular interactions of the acidic domain. Implication for thrombin inhibition. J Biol Chem 1997; 272: 14074-9.
43 Banfield DK, MacGillivray RTA. Partial characterization of vertebrate prothrombin cDNAs: amplification and sequence analysis of the B chain of thrombin from nine different species. Proc Natl Acad Sci U S A 1992; 89: 2779-83.
44 Andersson TR, Larsen ML, Handeland GF, Abildgaard U. Heparin cofactor II activity in plasma: application of an automated assay method to the study of a normal adult population. Scand J Haematol 1986; 36: 96-102.
45 Bertina RM, van der Linden IK, Engesser L, Muller HP, Brommer EJP. Hereditary heparin cofactor II deficiency and the risk of development of thrombosis. Thromb Haemost 1987; 57: 196-200.
46 Awidi AS, Abu-Khalaf M, Herzallah U, Abu-Rajab A, Shannak MM, Abu-Obeid T, Al-Taher I, Anshasi B. Hereditary thrombophilia among 217 consecutive patients with thromboembolic disease in Jordan. Am J Hematol 1993; 44: 95-100.
47 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: 697-9.
48 Liu L, Dewar L, Song Y, Kulczycky M, Blajchman MA, Fenton II JW, 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: 405-12.
49 Andersson T, Lorentzen B, Hogdahl H, Clausen T, Mowinckel MC, Abildgaard U. Thrombin-inhibitor complexes in the blood during and after delivery. Thromb Res 1996; 82: 109-17.
50 Coughlin SR. Sol Sherry lecture in thrombosis: how thrombin ‘talks’ to cells, molecular mechanisms and roles in vivo. Arterioscler Thromb Vasc Biol 1998; 18: 514-8.
51 Han J-H, Côté HFC, Tollefsen DM. Inhibition of meizothrombin and meizothrombin(desF1) by heparin cofactor II. J Biol Chem 1997; 272: 28660-5.