A heparin-like compound isolated from a marine crab rich in glucuronic acid 2-O-sulfate presents low anticoagulant activity

Carbohydrate Polymers

Volumn 94, Issue 1, 2013, Pages 647-654

  Andrade, Giulianna P V ^a   Lima, Marcelo A ^b,c   De Souza, Airton A ^b,d   Fareed, Jawed ^e   Hoppensteadt, Debra A ^e   Santos, Elizeu A ^a   Chavante, Suely F ^a   Oliveira, Fernanda W ^a   Rocha, Hugo A O ^a   Nader, Helena B ^b  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO NORTE   (Brazil)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF LIVERPOOL   (United Kingdom)

^d Centro Federal de Educacao Tecnologica do Rio Grande do Norte   (Brazil)

^e LOYOLA UNIVERSITY CHICAGO   (United States)

Author keywords

Anticoagulant activity; Hemorrhagic effect; Heparan sulfate; Heparin; Heparinases; Nuclear magnetic resonance

Indexed keywords

ANTICOAGULANT ACTIVITIES; HEMORRHAGIC EFFECT; HEPARAN SULFATES; HEPARIN; HEPARINASES;

GLUCOSE; MAMMALS; NUCLEAR MAGNETIC RESONANCE; SHELLFISH;

POLYSACCHARIDES;

ANTICOAGULANT AGENT; DISACCHARIDE; GLUCOSAMINE; GLUCURONIC ACID; GLUCURONIC ACID 2 SULFATE; GLUCURONIC ACID 2-SULFATE; HEPARAN SULFATE; HEPARIN; URONIC ACID;

ANIMAL; ARTICLE; BRACHYURA; CARBOHYDRATE ANALYSIS; CATTLE; CHEMISTRY; CONFORMATION; ISOLATION AND PURIFICATION; MALE; MOLECULAR WEIGHT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PARTIAL THROMBOPLASTIN TIME; RAT;

ANIMALS; ANTICOAGULANTS; BRACHYURA; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CATTLE; DISACCHARIDES; GLUCOSAMINE; GLUCURONATES; HEPARIN; HEPARITIN SULFATE; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MOLECULAR WEIGHT; PARTIAL THROMBOPLASTIN TIME; RATS; URONIC ACIDS;

DECAPODA (CRUSTACEA); GONIOPSIS CRUENTATA; MAMMALIA;

EID: 84874397016     PISSN: 01448617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.carbpol.2013.01.069     Document Type: Article

References (42)

1. P. Bianchini, H.B. Nader, H.K. Takahashi, B. Osima, A.H. Straus, and C.P. Dietrich Fractionation and identification of heparin and other acidic mucopolysaccharide by a new discontinuous eletroforetic method Journal of Chromatography 196 1980 455 462
2. R.I. Boucas, T.R. Jarrouge-Boucas, M.A. Lima, E.S. Trindade, F.A. Moraes, and R.P. Cavalheiro Glycosaminoglycan backbone is not required for the modulation of hemostasis: Effect of different heparin derivatives and non-glycosaminoglycan analogs Matrix Biology 31 5 2012 308 316
3. R.I. Boucas, L.O. Sampaio, G.P.V. Andrade, C.C. Lopes, F.D. Nascimento, and I.L.S. Tersariol Heparin and heparin derivatives and their effect on hemostasis H. Verli, Insights into carbohydrate structure and biological function 2006 Transworld Research Network Kerala, India 25 50
4. A.S. Brito, D.S. Arimateia, L.R. Souza, M.A. Lima, V.O. Santos, and V.P. Medeiros Anti-inflammatory properties of a heparin-like glycosaminoglycan with reduced anti-coagulant activity isolated from a marine shrimp Bioorganic and Medicinal Chemistry 16 21 2008 9588 9595
5. C.M. Cassaro, and C.P. Dietrich Distribution of sulfated mucopolysaccharides in invertebrates Journal of Biological Chemistry 252 7 1977 2254 2261
6. B. Casu, G. Grazioli, N. Razi, M. Guerrini, A. Naggi, and G. Torri Heparin-like compounds prepared by chemical modification of capsular polysaccharide from E. coli K5 Carbohydrate Research 263 2 1994 271 284
7. B. Casu, M. Guerrini, A. Naggi, G. Torri, L. De-Ambrosi, and G. Boveri Characterization of sulfation patterns of beef and pig mucosal heparins by nuclear magnetic resonance spectroscopy Arzneimittel-Forschung 46 5 1996 472 477
8. B. Casu, A. Naggi, and G. Torri Heparin-derived heparan sulfate mimics to modulate heparan sulfate-protein interaction in inflammation and cancer Matrix Biology 29 6 2010 442 452
9. M.C. Cavalcante, S. Allodi, A.P. Valente, A.H. Straus, H.K. Takahashi, and P.A. Mourao Occurrence of heparin in the invertebrate styela plicata (Tunicata) is restricted to cell layers facing the outside environment. An ancient role in defense? Journal of Biological Chemistry 275 46 2000 36186 36189
10. S.F. Chavante, E.A. Santos, F.W. Oliveira, M. Guerrini, G. Torri, and B. Casu A novel heparan sulphate with high degree of N-sulphation and high heparin cofactor-II activity from the brine shrimp Artemia franciscana International Journal of Biological Macromolecules 27 1 2000 49 57
11. U.R. Desai, H.M. Wang, and R.J. Linhardt Specificity studies on the heparin lyases from Flavobacterium heparinum Biochemistry 32 32 1993 8140 8145
12. C.P. Dietrich, J.F. de Paiva, C.T. Moraes, H.K. Takahashi, M.A. Porcionatto, and H.B. Nader Isolation and characterization of a heparin with high anticoagulant activity from Anomalocardia brasiliana Biochimica et Biophysica Acta 843 1-2 1985 1 7
13. C.P. Dietrich, and H.B. Nader Fractionation and properties of four heparitin sulfates from beef lung tissue. Isolation and partial characterization of a hemogeneous species of heparitin sulfate Biochimica et Biophysica Acta 343 1 1974 34 44
14. C.P. Dietrich, J.F. Paiva, R.A. Castro, S.F. Chavante, W. Jeske, and J. Fareed Structural features and anticoagulant activities of a novel natural low molecular weight heparin from the shrimp Penaeus brasiliensis Biochimica et Biophysica Acta 1428 2-3 1999 273 283
15. C.P. Dietrich, S.K. Shinjo, F.A. Moraes, R.A. Castro, A. Mendes, and T.C. Gouvea Structural features and bleeding activity of commercial low molecular weight heparins: Neutralization by ATP and protamine Seminars in Thrombosis and Hemostasis 25 Suppl 3 1999 43 50
16. C.P. Dietrich, I.L. Tersariol, R.G. Da Silva, P. Bianchini, and H.B. Nader Dependence of the C-6 sulfate of the glucosamine moiety and 1-4 glycosidic linkage of heparin disaccharides for production of hemorrhage: Reversal of the antihemostatic activity of heparin and their fragments by adenosine triphosphate and myosin Seminars in Thrombosis and Hemostasis 17 Suppl 1 1991 65 73
17. C.P. Dietrich, I.L. Tersariol, L. Toma, C.T. Moraes, M.A. Porcionatto, and F.W. Oliveira Structure of heparan sulfate: Identification of variable and constant oligosaccharide domains in eight heparan sulfates of different origins Cell and Molecular Biology (Noisy-le-grand) 44 3 1998 417 429
18. Z.A. Dische A new specific color reaction of hexuronic acid Journal of Biological Chemistry 167 1947 189 193
19. K.S. Dodgson, and R.G. Price A note on the determination of the ester sulphate content of sulphated polysaccharides Biochemical Journal 84 1962 106 110
20. J.L. Dreyfuss, C.V. Regatieri, M.A. Lima, E.J. Paredes-Gamero, A.S. Brito, and S.F. Chavante A heparin mimetic isolated from a marine shrimp suppresses neovascularization Journal of Thrombosis and Haemostasis 8 8 2010 1828 1837
21. M. Guerrini, A. Naggi, S. Guglieri, R. Santarsiero, and G. Torri Complex glycosaminoglycans: Profiling substitution patterns by two-dimensional nuclear magnetic resonance spectroscopy Analytical Biochemistry 337 1 2005 35 47
22. B. Kaiser, J. Fareed, D. Hoppensteadt, B. Birdsong, J.M. Walenga, and F. Markwardt Influence of recombinant hirudin and unfractionated heparin on thrombin and factor Xa generation in extrinsic and intrinsic activated systems Thrombosis Research 65 2 1992 157 164
23. M. Kusche, G. Torri, B. Casu, and U. Lindahl Biosynthesis of heparin. Availability of glucosaminyl 3-O-sulfation sites Journal of Biological Chemistry 265 13 1990 7292 7300
24. U. Lindahl, J.P. Li, M. Kusche-Gullberg, M. Salmivirta, S. Alaranta, and T. Veromaa Generation of "neoheparin" from E. coli K5 capsular polysaccharide Journal of Medicinal Chemistry 48 2 2005 349 352
25. E. Luppi, M. Cesaretti, and N. Volpi Purification and characterization of heparin from the Italian clam Callista chione Biomacromolecules 6 3 2005 1672 1678
26. G.F. Medeiros, A. Mendes, R.A. Castro, E.C. Bau, H.B. Nader, and C.P. Dietrich Distribution of sulfated glycosaminoglycans in the animal kingdom: Widespread occurrence of heparin-like compounds in invertebrates Biochimica et Biophysica Acta 1475 3 2000 287 294
27. B. Mulloy, M.J. Forster, C. Jones, A.F. Drake, E.A. Johnson, and D.B. Davies The effect of variation of substitution on the solution conformation of heparin: A spectroscopic and molecular modelling study Carbohydrate Research 255 1994 1 26
28. H.B. Nader, E.Y. Kobayashi, S.F. Chavante, I.L. Tersariol, R.A. Castro, and S.K. Shinjo New insights on the specificity of heparin and heparan sulfate lyases from Flavobacterium heparinum revealed by the use of synthetic derivatives of K5 polysaccharide from E. coli and 2-O-desulfated heparin Glycoconjugate Journal 16 6 1999 265 270
29. H.B. Nader, C.C. Lopes, H.A. Rocha, E.A. Santos, and C.P. Dietrich Heparins and heparinoids: Occurrence, structure and mechanism of antithrombotic and hemorrhagic activities Current Pharmaceutical Design 10 9 2004 951 966
30. H.B. Nader, M.A. Porcionatto, I.L. Tersariol, M.A. Pinhal, F.W. Oliveira, and C.T. Moraes Purification and substrate specificity of heparitinase I and heparitinase II from Flavobacterium heparinum. Analyses of the heparin and heparan sulfate degradation products by 13C NMR spectroscopy Journal of Biological Chemistry 265 28 1990 16807 16813
31. H.B. Nader, I.L. Tersariol, and C.P. Dietrich Antihemostatic activity of heparin disaccharides and oligosaccharides obtained by chemical and enzymatic fragmentation: Reversal of the hemorrhagic activity by ATP and myosin Thrombosis Research 54 3 1989 207 214
32. E.J. Paredes-Gamero, V.P. Medeiros, E.H. Farias, G.Z. Justo, E.S. Trindade, and A.L. Andrade-Lopes Heparin induces rat aorta relaxation via integrin-dependent activation of muscarinic M3 receptors Hypertension 56 4 2010 713 721
33. G. Pejler, A. Danielsson, I. Bjork, U. Lindahl, H.B. Nader, and C.P. Dietrich Structure and antithrombin-binding properties of heparin isolated from the clams Anomalocardia brasiliana and Tivela mactroides Journal of Biological Chemistry 262 24 1987 11413 11421
34. C.J. Rondle, and W.T. Morgan The determination of glucosamine and galactosamine Biochemical Journal 61 4 1955 586 589
35. L.O. Sampaio, I.L.S. Tersariol, C.C. Lopes, R.I. Bouças, F.D. Nascimento, and H.A. Rocha Heparin and heparan sulfates. Structure distribution and protein interactions H. Verli, Insights into carbohydrate structure and biological function 2006 Transworld Research Network Kerala, India 1 24
36. J.C. Santos, J.M. Mesquita, C.L. Belmiro, C.B. da Silveira, C. Viskov, and P.A. Mourier Isolation and characterization of a heparin with low antithrombin activity from the body of Styela plicata (Chordata-Tunicata). Distinct effects on venous and arterial models of thrombosis Thrombosis Research 121 2 2007 213 223
37. P. Sie, M. Petitou, J.C. Lormeau, D. Dupouy, B. Boneu, and J. Choay Studies on the structural requirements of heparin for the catalysis of thrombin inhibition by heparin cofactor II Biochimica et Biophysica Acta 966 2 1988 188 195
38. M.E. Silva, and C.P. Dietrich Isolation and partial characterization of three induced enzymes from Flavobacterium heparinum involved in the degradation of heparin and heparitin sulfates Biochemical and Biophysical Research Communications 56 4 1974 965 972
39. O.M. Toledo, and C.P. Dietrich Tissue specific distribution of sulfated mucopolysaccharides in mammals Biochimica et Biophysica Acta 498 1 1977 114 122
40. S. Yamada, T. Murakami, H. Tsuda, K. Yoshida, and K. Sugahara Isolation of the porcine heparin tetrasaccharides with glucuronate 2-O-sulfate. Heparinase cleaves glucuronate 2-O-sulfate-containing disaccharides in highly sulfated blocks in heparin Journal of Biological Chemistry 270 15 1995 8696 8705
41. E.A. Yates, F. Santini, M. Guerrini, A. Naggi, G. Torri, and B. Casu 1H and 13C NMR spectral assignments of the major sequences of twelve systematically modified heparin derivatives Carbohydrate Research 294 1996 15 27
42. Z. Zhang, J. Xie, H. Liu, J. Liu, and R.J. Linhardt Quantification of heparan sulfate disaccharides using ion-pairing reversed-phase microflow high-performance liquid chromatography with electrospray ionization trap mass spectrometry Analytical Chemistry 81 11 2009 4349 4355