The second laminin G-type domain of protein S is indispensable for expression of full cofactor activity in activated protein C-catalysed inactivation of factor vet and factor VIIIa

Thrombosis and Haemostasis

Volumn 84, Issue 2, 2000, Pages 271-277

  Evenäs, Petra ^a   Garcia De Frutos, Pablo ^a,b   Nicolaes, Gerry A F ^a   Dahlbäck, Björn ^a  

^a LUND UNIVERSITY   (Sweden)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

Author keywords

APC cofactor activity; Factor V; G domains; Protein S; SHBG like region

Indexed keywords

ACTIVATED PROTEIN C; ANTICOAGULANT AGENT; BLOOD CLOTTING FACTOR 5A; BLOOD CLOTTING FACTOR 8A; LAMININ; PROTEIN S; VITAMIN K GROUP;

ARTICLE; CONTROLLED STUDY; HUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN;

EID: 0033854083     PISSN: 03406245     EISSN: None     Source Type: Journal    
DOI: 10.1055/s-0037-1614007     Document Type: Article

References (50)

1. Tans G, Nicolaes GAF, Rosing J. Regulation of thrombin formation by activated protein C: effect of the factor V Leiden mutation. Semin Hematol 1997; 34: 244-55.
2. Dahlbäck B, Stenflo J. The Protein C anticoagulant system. In: Stammatoyannopoulos G, Majerus PW, Perlmutter RM, Varmus H, eds. WB Saunders company. Molecular Basis of Blood Disease. Third ed. Philadelphia: 2000: in press.
3. Rosing J, Hoekema L, Nicolaes GAF, Thomassen MCLGD, Hemker HC, Váradi K, Schwarz HP, Tans G, Effects of protein S and factor Xa on peptide bond cleavages during inactivation of factor Va and factor VaR506Q by activated protein C J Biol Chem 1995; 270: 27852-8.
4. Shen L, Dahlbäck B. Factor V and protein S as synergistic cofactors to activated protein C in degradation of factor VIIIa. J Biol Chem 1994; 269: 18735-8.
5. Lu D, Kalafatis M, Mann KG, Long GL. Comparison of activated protein C/protein S-mediated inactivation of human factor VIII and factor V. Blood 1996; 87: 4708-17.
6. Walker FJ, Chavin SI, Fay PJ. Inactivation of FVIIIa by activated protein C and protein S. Arch Biochem Biophys 1987; 252: 322-8.
7. Váradi K, Rosing J, Tans G, Pahinger I, Keil B, Schwarz HP. Factor V enhances the cofactor function of protein S in the APC-mediated inactivation of FVIII: Influence of the Factor VR506Q mutation. Thromb Haemost 1996; 76: 208-14.
8. Kalafatis M, Rand MD, Mann KG. The mechanism of inactivation of human factor V and human factor Va by activated protein C. J Biol Chem 1994; 269: 31869-80.
9. Nicolaes GAF, Tans G, Thomassen MCLGD, Hemker HC. Pabinger I, Váradi K, Schwarz HP, Rosing J. Peptide bond cleavages and loss of functional activity during inactivation of factor Va and factor VaR506Q by activated protein C. J Biol Chem 1995; 270: 21158-66.
10. Lundwall Å, Dackowski W, Cohen E, Shaffer M, Mahr A, Dahlbäck B, Stenflo J, Wydro R. Isolation and sequence of the cDNA for human protein S, a regulator of blood coagulation. Proc Natl Acad Sci U.S.A. 1986; 83: 6716-20.
11. Gershagen S, Fernlund P, Lundwall Å. A cDNA coding for human sex hormone binding globulin. Homology to vitamin K-dependent protein S. FEBS Letters 1987; 220: 129-35.
12. Joseph DR, Baker ME. Sex hormone-binding globulin, androgen-binding protein, and vitamin K-dependent protein S are homologous to laminin A, merosin, and Drosophila crumbs protein. FASEB 1992; 6: 2477-81.
13. Villoutreix BO, García de Frutos P. Lövenklev M, Linse S, Fernlund P, Dahlbäck B. SHBG region of the anticoagulant cofactor protein S: secondary structure prediction, circular dichroism, spectroscopy, and analysis of naturally occurring mutations. Proteins 1997; 29: 478-91.
14. Talts JF, Mann K, Yamada Y, Timpl R. Structural analysis and proteolytic processing of recombinant G domain of mouse laminin α2 chain. FEBS Letters 1998; 426: 71-6.
15. Aiach M, Borgel D, Gaussem P, Emmerich J, Alhenc-Gelas M, Gandrille S. Protein C and protein S deficiencies. Semin Hematol 1997; 34: 205-17.
16. Walker FJ. Regulation of protein C by protein S: The role of phospholipid in FVa inactivation. J Biol Chem 1981; 256: 11128-31.
17. Yegneswaran S, Wood GM, Esmon CT, Johnson AE. Protein S alters the active site location of activated protein C above the membrane. J Biol Chem 1997; 272: 25013-21.
18. Dahlbäck B, Hildebrand B, Malm J. Characterization of functionally important domains in human vitamin K-dependent protein S using monoclonal antibodies. J Biol Chem 1990; 265: 8127-35.
19. He X, Shen L, Dahlbäck B. Expression and functional characterization of chimeras between human and bovine vitamin-K-dependent protein S-defining modules important for the species specificity of the activated protein C cofactor activity. Eur J Biochem 1995; 227: 433-40.
20. He X, Shen L, Villoutreix BO, Dahlbäck B. Amino acid residues in thrombin-sensitive region and first epidermal growth factor domain of vitamin K-dependent protein S determining specificity of the activated protein C cofactor function. J Biol Chem 1998; 273: 27449-58.
21. Nyberg P. Dahlbäck B, García de Frutos P. The SHBG-like region of protein S is crucial for factor V-dependent APC-cofactor function. FEBS Letters 1998; 433: 28-32.
22. Koppelman SJ, van't Veer C, Sixma JJ, Bouma BN. Inhibition of the intrinsic factor X activation by protein S: Evidence for a specific binding of protein S to factor VIII. Blood 1995; 86: 2653-60.
23. Mitchell CA, Kelemen SM, Salem HH. The anticoagulant properties of a modified form of protein S. Thromb. Haemost 1988; 60: 298-304.
24. Schneider C, King RM, Philipson L. Genes specifically expressed at growth arrest of mammalian cells. Cell 1988; 54: 787-93.
25. Manfioletti G, Brancolini C, Avanzi G, Schneider C. The protein encoded by a growth arrest-specific gene (gas6) is a new memher of the vitamin K-dependent proteins related to protein S, a negative coregulator in the blood coagulation cascade. Mol Cell Biol 1993; 13: 4976-85.
26. Goruppi S, Ruaro E, Schneider C. Gas6, the ligand of Axl tyrosine kinase receptor, has mitogenic and survival activities for serum starved NIH3T3 fibroblasts. Oncogene 1996; 12: 471-80.
27. McCloskey P, Friedell Y-W, Attar E, Villa J, Jin Y, Varnum B, Liu ET. Gas6 mediates adhesion of cells expressing the receptor tyrosine kinase Axl. J Biol Chem 1997; 272: 23285-91.
28. Varnum BC, Young C, Elliott G, Garcia A, Bartley TD, Fridell YW, Hunt RW, Trail G, Clogson C, Toso RJ, Yanagihara D, Bennett L, Sylber M, Merewether LA, Tseng A, Escobar E, Liu ET, Yamane HK. Axl receptor tyrosine kinase stimulated by the vitamin K-dependent protein encoded by growth-arrest-specific gene 6. Nature 1995; 373: 623-6.
29. Godowski PJ, Mark MR, Chen J, Sadick MD, Raab H, Hammonds RG. Reevaluation of the roles of protein S and Gas6 as ligands for the receptor tyrosine kinase Rse/Tyro 3. Cell 1995; 82: 355-8.
30. Chen J, Carey K, Godowski PJ. Identification of Gas6 as a ligand for Mer, a neural cell adhesion molecule related receptor tyrosine kinase implicated in cellular transformation. Oncogene 1997; 14: 2033-9.
31. Rosing J, Bakker HM, Thomassen MCLGD, Hemker HC, Tans G. Characterization of two forms of human FVa with different cofactor activities. J Biol Chem 1993; 268: 21130-6.
32. Persson E, Hogg PJ, Stenflo J. Effects of Ca2+ binding on the protease module of factor Xa and its interaction with factor Va. Evidence for two Gla-independent Ca(2+)-binding sites in factor Xa. J Biol Chem 1993; 268: 22531-9.
33. Evenäs P, García de Frutos P, Linse S, Dahlbäck B. Both G-type domains of protein S are required for the high-affinity interaction with C4b-binding protein. Eur J Biochem 1999; 266: 935-42.
34. Thorelli E, Kaufman RJ, Dahlbäck B. Cleavage of factor V at Arg506 by activated protein C and the expression of anticoagulant activity of factor V. Blood 1999; 93: 2552-8.
35. Kaufman RJ. Vectors used for expression in mammalian cells. Methods Enzymol 1990; 185:487-511.
36. Dahlbäck B. Inhibition of protein Ca cofactor function of human and bovine protein S by C4b-binding protein. J Biol Chem 1986; 261: 12022-7.
37. Tans G, Rosing J, Thomassen MCLGD, Heeb MJ, Zwaal RFA, Griffin JH. Comparison of anticoagulant and procoagulant activities of stimulated platelets and platelet-derived microparticles. Blood 1991; 77: 2641-8.
38. Rosing J, Tans G, Govers-Riemslag JWP, Zwaal RFA, Hemker HC. The role of phospholipids and factor Va in the prothrombinase complex. J Biol Chem 1980; 255: 274-83.
39. Malm J, Cohen E, Dackowski W, Dahlbäck B, Wydro R. Expression of completely -γ-carboxylated and β-hydroxylated recombinant human vitamin K-dependent protein S with full biological activity. Eur J Biochem 1990; 187: 737-43.
40. Walker FJ. Regulation of activated protein C by a new protein. A possible function for bovine protein S. J Biol Chem 1980; 255: 5521-4.
41. Egan JO, Kalafatis M, Mann KG. The effect of Arg306 Ala and Arg506 Gln substitutions in the inactivation of recombinant human factor Va by activated protein C and protein S. Protein Sci 1997; 6: 2016-27.
42. Heeb MJ, Rehemtulla A, Moussali M, Kojima Y, Kaufman RJ. Importance of individual activated protein C cleavage site regions in coagulation factor V for factor Va inactivation and for factor Xa activation. Eur J Biochem 1999; 260: 64-75.
43. Deutzmann R, Huber H, Schmelz KA, Oberbäumer I. Hatl L. Structural study of long arm fragments of laminin. Evidence for repetitive C-terminal sequences in the A-chain, not present in the B-chains. Eur J Biochem 1988; 177: 35-45.
44. Noonan DM, Fulle A, Valente P, Cai S, Horigan E, Sasaki M, Yamada Y, Hassel JR. The complement sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin A chain, LDL-receptor and N-CAM. J Biol Chem 1991; 266: 22939-47.
45. Rothberg JM, Artavanis-Tsakonas S. Modularity of the slit protein. Characterization of a conserved carboxy-terminal sequence in secreted proteins and a motif implicated in extracellular protein interactions. J Mol Biol 1992; 227: 367-70.
46. Ushkaryov YA, Petrenko AG, Geppert M, Südhof TC. Neurexins: Synaptic cell surface proteins related to the α-lactrotoxin receptor and laminin. Science 1992; 257: 50-6.
47. Beckmann G, Hanke J, Bork P, Reich, J. G. Merging extracellular domains: Fold prediction for laminin G-like amino-terminal thrombospundin-like modules based on homology to pentraxins. J Mol Biol 1998; 275: 725-30.
48. He X, Shen L, Malmborg A-C, Smith KJ, Dahlbäck B, Linse S. Binding site for C4b-binding protein in vitamin K-dependent protein S fully contained in carboxy-terminal laminin G-type-repeats. A study using recombinant factor IX-protein S chimeras and surface plasmon resonance. Biochemistry 1997; 36: 3745-54.
49. Evena's P, Dahlbäck B, García de Frutos P. The first laminin G-type domain in the SHBG-like region of protein S contains residues essential for activation of the receptor tyrosine kinase Sky. Biol Chem 2000: 381: 199-209.
50. Rudenko G, Nguyen T, Chelliah Y, Südhof TC, Deisenhofer J. The structure of the ligand-binding domain of Neurexin Ib: Regulation of LNS domain function by alternative splicing. Cell 1999; 99: 93-101.