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

Abstract

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.

Identification and characterization of class B scavenger receptor CD36 from the hard tick, Haemaphysalis longicornis

“…The SRB has been identified in most orders of insects (Diptera, Hymenoptera, Coleoptera, and Lepidoptera) (Hart and Wilcox 1993) as well as nematodes, sponges, and slime mold (Muller et al 2004). Many insect species have an SRB ortholog, the sensory neuron membrane protein (SNMP), on dendrites of the specialized neural cells in antennae involved in pheromone detection (Acton et al 1996;Nichols and Vogt 2008).…”

Okadaic Acid, an Apoptogenic Toxin for Symbiotic/Parasitic Annelids in the Demosponge Suberites domuncula

“…The elucidation of the molecular and cellular mechanism(s) by which sponges protect themselves against parasitic metazoans has begun only recently. It could be demonstrated that sponge-associated bacteria produce 2-methylthio-1,4-napthoquinone, a compound that suppresses the CD36/LIMPII signal transduction pathway that modulates angiogenesis (in vertebrates) and canal formation (in S. domuncula) (37).…”

Significance of the zebrafish model in the discovery of bioactive molecules from nature

“…These NPs include shark cartilage, curcumin, the omega-3 and omega-6 fatty acids, green tea, licorice, quercetin, squalamine and vitamin D3 (Marwick 2001). Apart from shark cartilage (Cho and Kim 2002;Gingras et al 2003), some marine natural compounds from sponges (Zhou et al 2000;Shin et al 2001;Rodriguez-Nieto et al 2002) and sponge-associated bacteria (Müller et al 2004;Thakur et al 2005) have also been reported to possess anti-angiogenic potential, highlighting the importance of including NPs in the search for anti-angiogenic molecules.…”