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J. Biol. Chem., Vol. 281, Issue 9, 5992-5999, March 3, 2006

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Proteoglycan Mechanics Studied by Single-molecule Force Spectroscopy of Allotypic Cell Adhesion Glycans^*

Sergi Garcia-Manyes¹, Iwona Bucior^¶||, Robert Ros^**, Dario Anselmetti^**, Fausto Sanz, Max M. Burger^¶||, and Xavier Fernàndez-Busquets, Holder of Ramón y Cajal tenure track position from the Ministerio de Educación y Ciencia, Spain^||2

From the Research Center for Bioelectronics and Nanobioscience, Barcelona Science Park, University of Barcelona, Josep Samitier 1-5, Barcelona E-08028, Spain, the Departament de Química Física, University of Barcelona, Martíi Franquès 1, Barcelona E-08028, Spain, the ^¶Friedrich Miescher-Institut, Basel CH-4002, Switzerland, the ^||Marine Biological Laboratory, Woods Hole, Massachusetts 02543, and the ^**Department of Experimental Biophysics and Applied Nanoscience, University of Bielefeld, Physics Faculty, Universitätsstrasse 25, Bielefeld D-33615, Germany

Early Metazoans had to evolve the first cell adhesion system addressed to maintaining stable interactions between cells constituting different individuals. As the oldest extant multicellular animals, sponges are good candidates to have remnants of the molecules responsible for that crucial innovation. Sponge cells associate in a species-specific process through multivalent calcium-dependent interactions of carbohydrate structures on an extracellular membrane-bound proteoglycan termed aggregation factor. Single-molecule force spectroscopy studies of the mechanics of aggregation factor self-binding indicate the existence of intermolecular carbohydrate adhesion domains. A 200-kDa aggregation factor glycan (g200) involved in cell adhesion exhibits interindividual differences in size and epitope content which suggest the existence of allelic variants. We have purified two of these g200 distinct forms from two individuals of the same sponge species. Comparison of allotypic versus isotypic g200 binding forces reveals significant differences. Surface plasmon resonance measurements show that g200 self-adhesion is much stronger than its binding to other unrelated glycans such as chondroitin sulfate. This adhesive specificity through multiple carbohydrate binding domains is a type of cooperative interaction that can contribute to explain some functions of modular proteoglycans in general. From our results it can be deduced that the binding strength/surface area between two aggregation factor molecules is comparable with that of focal contacts in vertebrate cells, indicating that strong carbohydrate-based cell adhesions evolved at the very start of Metazoan history.

Received for publication, July 20, 2005 , and in revised form, December 13, 2005.

^* This work was supported in part by Grants BIO2002-00128 and BIO2005-01591 (both to X. F.-B.) from the Ministerio de Educación y Ciencia, Spain, which included Fondo Europeo de Desarrollo Regional funds. 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.

¹ Recipient of a fellowship from the Departament d'Universitats, Recerca i Societat de la Informació (Generalitat de Catalunya, Spain).

² To whom correspondence should be addressed: Research Center for Bioelectronics and Nanobioscience, Barcelona Science Park, Josep Samitier 1-5, Barcelona E-08028, Spain. Tel.: 34-93-403-7180; Fax: 34-93-403-7181; E-mail: xfernandez_busquets{at}ub.edu.

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