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J. Biol. Chem., Vol. 281, Issue 17, 12001-12009, April 28, 2006

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Co-expression and Functional Interaction of Silicatein with Galectin

MATRIX-GUIDED FORMATION OF SILICEOUS SPICULES IN THE MARINE DEMOSPONGE SUBERITES DOMUNCULA^*

Heinz C. Schröder, Alexandra Boreiko, Michael Korzhev, Muhammad N. Tahir, Wolfgang Tremel, Carsten Eckert^¶, Hiroshi Ushijima^||, Isabel M. Müller, and Werner E. G. Müller¹

From the Institut für Physiologische Chemie, Abteilung Angewandte Molekularbiologie, Universität Mainz, Duesbergweg 6, D-55099 Mainz, Germany, Institut für Anorganische Chemie und Analytische Chemie, Universität Mainz, Duesbergweg 10-14, D-55099 Mainz, Germany, ^¶Museum für Naturkunde, Universität Berlin, Institut für Systematische Zoologie, Invalidenstrasse 43, D-10115 Berlin, Germany, and ^||Department of Developmental Medical Sciences, Institute of International Health, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan

Sponges (phylum Porifera) of the class of Demospongiae are stabilized by a siliceous skeleton. It is composed of silica needles (spicules), which provide the morphogenetic scaffold of these metazoans. In the center of the spicules there is an axial filament that consists predominantly of silicatein, an enzyme that catalyzes the synthesis of biosilica. By differential display of transcripts we identified additional proteins involved in silica formation. Two genes were isolated from the marine demosponge Suberites domuncula; one codes for a galectin and the other for a fibrillar collagen. The galectin forms aggregates to which silicatein molecules bind. The extent of the silicatein-mediated silica formation strongly increased if associated with the galectin. By applying a new and mild extraction procedure that avoids hydrogen fluoride treatment, native axial filaments were extracted from spicules of S. domuncula. These filaments contained, in addition to silicatein, the galectin and a few other proteins. Immunogold electron microscopic studies underscored the role of these additional proteins, in particular that of galectin, in spiculogenesis. Galectin, in addition to silicatein, presumably forms in the axial canal as well as on the surface of the spicules an organized net-like matrix. In the extraspicular space most of these complexes are arranged concentrically around the spicules. Taken together, these additional proteins, working together with silicatein, may also be relevant for potential (nano)-biotechnological applications of silicatein in the formation of surface coatings. Finally, we propose a scheme that outlines the matrix (galectin/silicatein)-guided appositional growth of spicules through centripetal and centrifugal synthesis and deposition of biosilica.

Received for publication, November 28, 2005 , and in revised form, February 16, 2006.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AM157178 [GenBank] and AM157177 [GenBank] .

^* This work was supported by grants from the European Commission (SILIBIOTEC), theDeutsche Forschungsgemeinschaft, the Bundesministerium für Bildung und Forschung Germany, and the International Human Frontier Science Program. 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 To whom correspondence should be addressed: Institut für Physiologische Chemie, Abteilung Angewandte Molekularbiologie, Universität, Duesbergweg 6, 55099 Mainz, Germany. Tel.: 49-6131-39-25910; Fax: 49-6131-39-25243. E-mail: wmueller{at}uni-mainz.de.

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