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Glycobiology Advance Access published online on July 14, 2004
Glycobiology, doi:10.1093/glycob/cwh128
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Received May 6, 2004
Revised July 6, 2004
Accepted July 7, 2004

ORIGINAL ARTICLES

Isolation and characterization of a heparin with high anticoagulant activity from the clam Tapes phylippinarum. Evidence for the presence of a high content of antithrombin III-binding site

Marina Cesaretti 1, Elisa Luppi 1, Francesca Maccari 1, Nicola Volpi 1*

1 Department of Biologia Animale, University of Modena and Reggio Emilia, Modena, Italy

* To whom correspondence should be addressed. E-mail: volpi{at}unimo.it.


  Abstract

Heparin with high anticoagulant activity (APTT of 350 ± 56 and antiXa activity of 320 ± 48) was isolated from the marine clam species Tapes phylippinarum, in an amount of approx. 2.1 mg/g of dry animals. Agarose-gel electrophoresis showed a high content of the slow moving heparin component (22 ± 6.8%) and 78 ± 5.4% of the fast moving species. An average molecular mass of 13.600 was calculated by PAGE analysis while a number average molecular weight Mn value of 10,700, a weight average molecular weight Mw of 14,900 and a dispersity index Mn/Mw of 1.386 were obtained by HPSEC. Structural analysis of clam heparin, performed by depolymerizing heparin samples with heparinase (EC 4.2.2.7) and then separating the resulting unsaturated oligosaccharides by SAX-HPLC, according to Linhardt et al. (Linhardt, R.J., Wang, H.M., Loganathan, D., and Bae, J.H. (1992) Search for the heparin antithrombin III-binding site precursor. J. Biol. Chem., 267, 2380), revealed the presence of large amounts (more than 130% than standard pharmaceutical heparin obtained from bovine intestine) of the oligosaccharide sequence bearing part of the ATIII-binding region, {Delta}UA2S (1->4)-{alpha}-D-GlcN2S6S (1->4)-{alpha}-L-IdoA (1->4)-{alpha}-D-GlcNAc6S (1->4)-{beta}-D-GlcA (1->4)-{alpha}-D-GlcN2S3S6S in the Tapes phylippinarum heparin, in comparison with bovine mucosal heparin and a sample of porcine mucosal heparin previously published. Furthermore, as expected from the oligosaccharide compositional analysis, due to the presence of a large mol % (80.6%) of the trisulfated disaccharide {Delta}UA2S(1->4)-{alpha}-D-GlcN2S6S, mollusc heparin is a more sulfated polysaccharide than bovine mucosal heparin (73.5%) and a sample of porcine mucosal (72.8%) heparin previously reported.

To our knowledge, this is the first paper describing a clam heparin having the ATIII binding site identical to the one prevalent in human and porcine intestinal mucosal heparins and bovine intestinal mucosal heparin but different from that prevalent in beef lung heparin.

Keywords: Glycosaminoglycans; Heparin; Molluscs; Anticoagulant drug; Tapes phylippinarum.
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