Abstract
Sea cucumbers produce saponins as a chemical defense mechanism, however their cells can tolerate the cytotoxic nature of these chemicals. To elucidate the molecular mechanisms behind this tolerance a suite of complementary biophysical tools was used, firstly using liposomes for in vitro techniques then using in silico approaches for a molecular-level insight. The holothuroid saponin Frondoside A, caused significantly less permeabilization in liposomes containing a Δ7 holothuroid sterol than those containing cholesterol and resulted in endothermic interactions versus exothermic interactions with cholesterol containing liposomes. Lipid phases simulations revealed that Frondoside A has an agglomerating effect on cholesterol domains, however, induced small irregular Δ7 sterol clusters. Our results suggest that the structural peculiarities of holothuroid sterols provide sea cucumbers with a mechanism to mitigate the sterol-agglomerating effect of saponins, and therefore to protect their cells from the cytotoxicity of the saponins they produce.
Highlights
Saponins form a large and diverse group of secondary metabolites produced by several terrestrial and marine organisms and are thought to be involved in chemical defense mechanisms
Saponins have been detected in most sea cucumber tissue, they seem to be concentrated in the Cuverian tubules, a specialized defense system developed by some sea cucumber species belonging to the Holothuriidae family[23]
Isothermal Titration Calorimetry (ITC) experiments were conducted on three liposome compositions, fish-like, holothuroid-like and sterol-free lipids, to thermodynamically quantify their interaction with the holothuroid saponin, Frondoside A
Summary
Saponins form a large and diverse group of secondary metabolites produced by several terrestrial and marine organisms and are thought to be involved in chemical defense mechanisms These natural products are well documented in plants[1], and occur in marine sponges[2,3] and in two classes of echinoderms: Asteroidea or seastars[4,5] and Holothuroidea or sea-cucumbers[6,7,8,9]. The ability of the glycosides to form complexes with 5,6-unsaturated sterols of target cell membranes is thought to determine their biological activity including ichthyotoxic action that may protect sea cucumbers against fish predation[21,25,26,27] This complexing reaction leads to the formation of pores, permeabilization of cells and in the case of red blood cells the subsequent loss of haemoglobin in the extracellular medium[21,28]. The permeabilizing activity of the saponin decreased in the following order, in function of www.nature.com/scientificreports/
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