Sulfated galactan is a catalyst of antithrombin-mediated inactivation of α-thrombin

Biochimica et Biophysica Acta - General Subjects

Volumn 1780, Issue 9, 2008, Pages 1047-1053

  Melo, Fábio R ^a   Pereira, Mariana S ^a   Monteiro, Robson Q ^a   Foguel, Débora ^a   Mourão, Paulo A S ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

Algal polysaccharide; Anticoagulant activity; Antithrombotic agent; Exosite II of thrombin

Indexed keywords

ANTITHROMBIN; GALACTAN; HEPARIN; POLYSACCHARIDE; THROMBIN;

ANTICOAGULATION; ARTICLE; BINDING AFFINITY; CATALYST; CONCENTRATION (PARAMETERS); MOLECULAR SIZE; PRIORITY JOURNAL;

ANTITHROMBINS; BINDING SITES; CATALYSIS; CHROMATOGRAPHY, AFFINITY; CHROMATOGRAPHY, GEL; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ENZYME ACTIVATION; GALACTANS; HIRUDINS; HUMANS; PEPTIDE FRAGMENTS; SULFURIC ACID ESTERS; THROMBIN;

ALGAE;

EID: 47049103979     PISSN: 03044165     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbagen.2008.05.006     Document Type: Article

References (34)

1. Kakkar V.V., and Hedges A.R. Use of heparin as a profilatic agent against venous thromboembolism. In: Lane D.A., and Lindahl U. (Eds). Heparin: Chemical and Biological Properties, Clinical Applications (1989), Edward Arnold, London 455-473
2. Béguin S., Lindhout T., and Hemker H.C. The mode of action of heparin in plasma. Thromb. Haemostas. 60 (1988) 457-462
3. Thunberg L., Bäckström G., and Lindahl U. Further characterization of the antithrombin-binding sequence in heparin. Carbohydr. Res. 100 (1982) 393-410
4. Lindahl U., Backström G., and Thumberg L. The antithrombin-binding sequence in heparin. Identification of an essential 6-O-sulfate group. J. Biol. Chem. 258 (1983) 9826-9830
5. Streusand V.J., Björk I., Gettins P.G.W., Petitou M., and Olson S.T. Mechanism of acceleration of antithrombin-proteinase reactions by low-affinity heparin. J. Biol. Chem. 270 (1995) 9043-9051
6. Church F.C., Pratt C.W., Noyes C.M., Kalayanamit T., Sherrill G.B., Tobin R.B., and Meade J.B. Structural and functional-properties of human alpha-thrombin, phosphopyridoxylated alpha-thrombin, and gamma-T-thrombin - identification of lysyl residues in alpha-thrombin that are critical for heparin and fibrin(ogen) interactions. J. Biol. Chem. 264 (1989) 18419-18425
7. Colliec S., Fischer A.M., Tapon-Bretaudière J., Boisson C., Durand P., and Jozefonvicz J. Anticoagulant properties of a fucoidan fraction. Thromb. Res. 64 (1991) 143-154
8. Mourão P.A.S., Pereira M.S., Pavão M.S., Mulloy B., Tollefsen D.M., Mowinckel M.C., and Abildgaard U. Structure and anticoagulant activity of a fucosylated chondroitin sulfate from echinoderm - sulfated fucose branches on the polysaccharide account for its high anticoagulant action. J. Biol. Chem. 271 (1996) 23973-23984
9. Pereira M.S., Mulloy B., and Mourão P.A.S. Structure and anticoagulant activity of sulfated fucans - comparison between the regular, repetitive, and linear fucans from echinoderms with the more heterogeneous and branched polymers from brown algae. J. Biol. Chem. 274 (1999) 7656-7667
10. Pereira M.S., Melo F.R., and Mourão P.A.S. Is there a correlation between structure and anticoagulant action of sulfated galactans and sulfated fucans?. Glycobiology 12 (2002) 573-580
11. Pereira M.S., Vilela-Silva A.C.E.S., Valente A.P., and Mourão P.A.S. A 2-sulfated, 3-linked alpha-L-galactan is an anticoagulant polysaccharide. Carbohydr. Res. 337 (2002) 2231-2238
12. Melo F.R., Pereira M.S., Foguel D., and Mourão P.A.S. Antithrombin-mediated anticoagulant activity of sulfated polysaccharides - different mechanisms for heparin and sulfated galactans. J. Biol. Chem. 279 (2004) 20824-20835
13. Shipp E.L., and Hsieh-Wilson L.C. Profiling the sulfation specificities of glycosaminoglycans interactions with growth factor and chemotactic proteins using microarrays. Chem. Biol. 14 (2007) 195-208
14. Gama C.I., Tully S.E., Sotogaku N., Clark P.M., Rawat M., Vaidehi N., Goddard W.A., Nishi A., and Hsieh-Wilson L.C. Sulfation patterns of glycosaminoglycans encode molecular recognition and activity. Nat. Chem. Biol. 2 (2006) 467-473
15. Farias W.R.L., Valente A.P., Pereira M.S., and Mourão P.A.S. Structure and anticoagulant activity of sulfated galactans - isolation of a unique sulfated galactan from the red algae Botryocladia occidentalis and comparison of its anticoagulant action with that of sulfated galactans from invertebrates. J. Biol. Chem. 275 (2000) 29299-29307
16. Farias W.R.L., Nazareth R.A., and Mourão P.A.S. Dual effects of sulfated D-galactans from the red algae Botryocladia occidentalis preventing thrombosis and inducing platelet aggregation. Thromb. Haemostasis 86 (2001) 1540-1546
17. Melo F.R., and Mourão P.A.E. An algal sulfated galactan has unusual dual effect on venous thrombosis due to activation of factor XII and inhibition of the coagulation proteases. Thromb. Haemostasis 99 (2008) 531-538
18. Pereira M.G., Benevides N.M.B., Melo M.R.S., Valente A.P., Melo F.R., and Mourão P.A.S. Structure and anticoagulant activity of a sulfated galactan from the red alga, Gelidium crinale. Is there a specific structural requirement for the anticoagulant action?. Carbohydr. Res. 340 (2005) 2015-2023
19. Monteiro R.Q., Bock P.E., Bianconi M.L., and Zingali R.B. Characterization of bothrojaracin interaction with human prothrombin. Protein Sci. 10 (2001) 1897-1904
20. Olson S.T., and Björk I. Predominant contribution of surface approximation to the mechanism of heparin acceleration of the antithrombin-thrombin reaction - elucidation from salt concentration effects. J. Biol. Chem. 266 (1991) 6353-6364
21. Verhamme I.M., Bock P.E., and Jackson C.M. The preferred pathway of glycosaminoglycan-accelerated inactivation of thrombin by heparin cofactor II. J. Biol. Chem. 279 (2004) 9785-9795
22. Winzor D.J., Munro P.D., and Jackson C.M. Study of high-affinity interactions by quantitative affinity-chromatography-analytical expressions in terms of total ligand concentration. J. Chromatogr. 597 (1992) 57-66
23. Laemmli U.K. Cleavage of structural proteins during assembly of head of bacteriophage-t4. Nature 227 (1970) 680-685
24. Merril C.R., Harrington M., and Alley V. A photodevelopment silver stain for the rapid visualization of proteins separated on polyacrylamide gels. Electrophoresis 5 (1984) 289-297
25. Olson S.T., Halvorson H.R., and Björk I. Quantitative characterization of the thrombin-heparin interaction discrimination between specific and nonspecific-binding models. J. Biol. Chem. 266 (1991) 6342-6352
26. Myles T., Church F.C., Whinna H.C., Monard D., and Stone S.R. Role of thrombin anion-binding exosite-I in the formation of thrombin-serpin complexes. J. Biol. Chem. 273 (1998) 31203-31208
27. Liaw P.C.Y., Fredenburgh J.C., Stafford A.R., Tulinsky A., Austin R.C., and Weitz J.I. Localization of the thrombin-binding domain on prothrombin fragment 2. J. Biol. Chem. 273 (1998) 8932-8939
28. Rydel T.J., Yin M.L., Padmanabhan K.P., Blankenship D.T., Cardin A.D., Correa P.E., Fenton J.W., and Tulinsky A. Crystallographic structure of human gamma-thrombin. J. Biol. Chem. 269 (1994) 22000-22006
29. Lewis S.D., Lorand L., Fenton II J.W., and Shafer J.A. Catalytic competence of human α- and γ-thrombin in the activation of fibrinogen and factor XIII. Biochemistry 26 (1987) 7597-7603
30. Lottenberg R., Hall J.A., Fenton J.W., and Jackson C.M. The action of thrombin on peptide p-nitroanilide substrates - hydrolysis of tos-gly-pro-arg-pna and d-phe-pip-arg-pna by human alpha-thrombin and human gamma-thrombin and bovine-alpha-thrombin and bovine beta-thrombin. Thromb. Res. 28 (1982) 313-332
31. Danielsson A., and Björk I. Spontaneous dissociation of the antithrombin-thrombin complex produces a proteolytically modified form of the inhibitor. FEBS Lett. 119 (1980) 241-244
32. Chang J.Y., and Tran T.H. Antithrombin-III basel - identification of a pro-leu substitution in a hereditary abnormal antithrombin with impaired heparin-cofactor activity. J. Biol. Chem. 261 (1986) 1174-1176
33. Koide T., Odani S., Takahashi K., Ono T., and Sakuragawa N. Antithrombin-III toyama - replacement of arginine-47 by cysteine in hereditary abnormal antithrombin-III that lacks heparin-binding ability. Proc. Natl. Acad. Sci. U.S.A. 81 (1984) 289-293
34. Owen M.C., Borg J.Y., Soria C., Soria J., Caen J., and Carrel R.W. Heparin binding defect in a new anti-thrombin-iii variant - Rouen, 47 Arg to His. Blood 69 (1987) 1275-1279