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J. Biol. Chem., Vol. 282, Issue 3, 1615-1626, January 19, 2007

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The Hemolymph of the Ascidian Styela plicata (Chordata-Tunicata) Contains Heparin inside Basophil-like Cells and a Unique Sulfated Galactoglucan in the Plasma^*

Cintia M. de Barros, Leonardo R. Andrade^¶, Silvana Allodi^¶, Christian Viskov^||, Pierre A. Mourier^||, Moisés C. M. Cavalcante, Anita H. Straus^**1, Helio K. Takahashi^**1, Vitor H. Pomin, Vinicius F. Carvalho, Marco A. Martins¹, and Mauro S. G. Pavão¹²

From the Laboratório de Tecido Conjuntivo, Hospital Universitário Clementino Fraga Filho and Instituto de Bioquímica Médica, Programa de Pós-Graduação em Ciências Morfológicas, Instituto de Ciências Biomédicas, and ^¶Departamento de Histologia e Embriologia, Instituto de Ciências Biomédicas, Universidade Federal do Rio de Janeiro, Cidade Universitária, Rio de Janeiro, RJ, CEP 21941-590, Brasil, ^||Sanofi-aventis, Centre de Recherche de Paris, Unité de Glycochimie, Batiment Lavoisier 13, Quai Jules Guesde 94400 Vitry-sur Seine, France, ^**Departamento de Bioquímica, Escola Paulista de Medicina, Universidade Federal de São Paulo, São Paulo, 04023-900 SP, Brasil, and Laboratório de Inflamação, Instituto Oswaldo Cruz, Fundação Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, RJ, CEP 21045-900, Brasil

The hemolymph of ascidians (Chordata-Tunicata) contains different types of hemocytes embedded in a liquid plasma. In the present study, heparin and a sulfated heteropolysaccharide were purified from the hemolymph of the ascidian Styela plicata. The heteropolysaccharide occurs free in the plasma, is composed of glucose (60%) and galactose (40%), and is highly sulfated. Heparin, on the other hand, occurs in the hemocytes, and high performance liquid chromatography of the products formed by degradation with specific lyases revealed that it is composed mainly by the disaccharides UA(2SO₄)-14--D-GlcN(SO₄) (39.7%) and UA(2SO₄)-14--D-GlcN(SO₄)(6SO₄) (38.2%). Small amounts of the 3-O-sulfated disaccharides UA(2SO₄)-14--D-GlcN(SO₄)(3SO₄) (9.8%) and UA(2SO₄)-14--D-GlcN(SO₄)(3SO₄)(6SO₄) (3.8%) were also detected. These 3-O-sulfated disaccharides were demonstrated to be essential for the binding of the hemocyte heparin to antithrombin III. Electron microscopy techniques were used to characterize the ultrastructure of the hemocytes and to localize heparin and histamine in these cells. At least five cell types were recognized and classified as univacuolated and multivacuolated cells, amebocytes, hemoblasts, and granulocytes. Immunocytochemistry showed that heparin and histamine co-localize in intracellular granules of only one type of hemocyte, the granulocyte. These results show for the first time that in ascidians, a sulfated galactoglucan circulates free in the plasma, and heparin occurs as an intracellular product of a circulating basophil-like cell.

Received for publication, April 27, 2006 , and in revised form, November 16, 2006.

^* This work was supported by grants from Conselho Nacional de Desenvolvimento Cientifico e Tecnológico (CNPq) and Fundação de Amparo a Pesquisa do Rio de Janeiro and by National Institutes of Health Fogarty International Center Grant R03 TW05775 (to M. S. G. P.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

The on-line version of this article (available at http://www.jbc.org) contains supplemental Fig. 3C.

¹ Research fellows of CNPq.

² To whom correspondence should be addressed: Instituto de Bioquímica Médica, Centro de Ciências da Saúde, Cidade Universitária, Universidade Federal do Rio de Janeiro, Caixa Postal 68041, Rio de Janeiro, RJ, 21941-590, Brasil. Tel.: 55-21-2562-2093; Fax: 55-21-2562-2090; E-mail: mpavao{at}hucff.ufrj.br.

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