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doi: 10.1242/jcs.01083

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Matrix-mediated canal formation in primmorphs from the sponge Suberites domuncula involves the expression of a CD36 receptor-ligand system

Werner E. G. Müller^1,*, Narsinh L. Thakur¹, Hiroshi Ushijima², Archana N. Thakur¹, Anatoli Krasko¹, Gaël Le Pennec¹, Madhavi M. Indap³, Sanja Perovi-Ottstadt¹, Heinz C. Schröder¹, Gerhard Lang⁴ and Gerhard Bringmann⁴

¹ Institut für Physiologische Chemie und Pathobiochemie, Abteilung Angewandte Molekularbiologie, Johannes Gutenberg-Universität M ainz, Duesbergweg 6, 55099 Mainz, Germany
² Institute of International Health, Graduate School of Medicine, The University of Tokyo, 7-3-1 Hongo, Bunkyo-Ku, Tokyo 113-0033, Japan
³ Department of Zoology, D. G. Ruparel College, Mahim, Mumbai 400016, India
⁴ Institut für Organische Chemie, Universität Würzburg, Am Hubland, 97074 Würzburg, Germany

^* Author for correspondence (e-mail: wmueller{at}mail.uni-mainz.de)

Accepted 6 January 2004

Sponges (Porifera), represent the phylogenetically oldest metazoan phylum still extant today. Recently, molecular biological studies provided compelling evidence that these animals share basic receptor/ligand systems, especially those involved in bodyplan formation and in immune recognition, with the higher metazoan phyla. An in vitro cell/organ-like culture system, the primmorphs, has been established that consists of proliferating and differentiating cells, but no canals of the aquiferous system. We show that after the transfer of primmorphs from the demosponge Suberites domuncula to a homologous matrix (galectin), canal-like structures are formed in these 3D-cell aggregates. In parallel with the formation of these structures a gene is expressed whose deduced protein falls into the CD36/LIMPII receptor family. The receptor was cloned and found to be strongly expressed after adhesion to the galectin matrix. This process was suppressed if primmorphs were co-incubated with a homologous polypeptide containing the CSVTCG domain, as found in thrombospondin-1 (and related) molecules of vertebrates. In situ hybridization studies revealed that the S. domuncula CD36/LIMPII receptor is localized in the pinacocytes that surround the canals of the sponge. Furthermore, a secondary metabolite from a sponge-associated bacterium was isolated and characterized, the 2-methylthio-1,4-naphthoquinone (MTN). MTN causes inhibition of cell proliferation of vertebrate tumor cells at concentrations of >80 ng/ml. However, doses of only 2 ng are required to potently inhibit angiogenesis in the chick chorio-allantoic membrane assay. At concentrations of 10 ng/ml this compound was also found to suppress the expression of the S. domuncula CD36/LIMPII; this result is a first indication that this secondary metabolite has a conserved functional activity: the suppression of the formation of the circulation system, from sponges to vertebrates.

Key words: Sponges, Porifera, Suberites domuncula, CD36, Lysosomal integral membrane protein II, Thrombospondin, 2-methylthio-1, 4-naphthoquinone, Canal formation, Angiogenesis

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