Ovothiol ensures the correct developmental programme of the sea urchin Paracentrotus lividus embryo

Abstract

Ovothiols are π-methyl-5-thiohistidines produced in great amounts in sea urchin eggs, where they can act as protective agents against the oxidative burst at fertilization and environmental stressors during development. Here we examined the biological relevance of ovothiol during the embryogenesis of the sea urchin Paracentrotus lividus by assessing the localization of the key biosynthetic enzyme OvoA, both at transcript and protein level, and perturbing its protein translation by morpholino antisense oligonucleotide-mediated knockdown experiments. In addition, we explored the possible involvement of ovothiol in the inflammatory response by assessing ovoA gene expression and protein localization following exposure to bacterial lipopolysaccharide. The results of the present study suggest that ovothiol may be a key regulator of cell proliferation in early developing embryos. Moreover, the localization of OvoA in key larval cells and tissues, in control and inflammatory conditions, suggests that ovothiol may ensure larval skeleton formation and mediate inflammatory processes triggered by bacterial infection. This work significantly contributes to the understanding of the biological function of ovothiols in marine organisms, and may provide new inspiration for the identification of the biological activities of ovothiols in humans, considering the pharmacological potential of these molecules.

The first genetic engineered system for ovothiol biosynthesis in diatoms reveals a mitochondrial localization for the sulfoxide synthase OvoA

“…Indeed, protein localization in the subcellular compartment may offer insightful suggestions on the OvoA biological function, which is far from being completely understood, particularly in diatoms, where the metabolite was only recently identified [16]. Thanks to their ability to scavenge peroxides and participate to redox exchange with GSH, ovothiols have been proposed to protect eggs and early embryos against the oxidative burst occurring at fertilization and during development in sea urchins [38,51], to be involved in the maturation and differentiation of sea urchins female gonads [52], to protect against the oxidative stress produced by the immune response of the host in Trypanosoma species [53], and against environmental pollutants in sea urchins and Mytilus galloprovincialis [26,54]. Therefore, the mitochondrial localization of the OvoA enzyme in diatoms represents a very interesting finding in light of the unique redox properties of ovothiol.…”

“…The first reaction is catalysed by the 5-histidylcysteine sulfoxide synthase OvoA, a bifunctional enzyme, which, starting from cysteine and histidine, catalyses first the formation of the 5-histidyl-cysteine sulfoxide conjugate [36] and then the methylation of the imidazole ring of 5-thiohistidine, obtained after the cleavage of the sulfoxide intermediate by a pyridoxal phosphate-dependent lyase, OvoB [37] (figure 1 b ). The recent identification of the genes responsible for ovothiol biosynthesis in bacteria [36] has prompted pioneering functional studies on their role in other organisms [38]. Indeed, very little is known about the functional characterization of OvoA.…”

Marine natural products

“…619 In addition to antioxidant properties, ovothiol appears to play a central role in the control of cell proliferation in the early stages of embryo development in the sea urchin Paracentrotus lividus . 620…”

Toxicological Impacts of Microplastics: Effects on Levels of Cellular Thiols in Mytilus galloprovincialis

“…Biochemically, OSH acts as a nonenzymatic glutathione peroxidase system, consuming H 2 O 2 and being reduced by GSH, thus protecting sea urchin eggs against the oxidative burst occurring at fertilization (Shapiro, 1991; Turner et al, 1986). From a biological point of view, OSH has many functions: it has been implicated in early embryo development in P. lividus and, in general, it appears to protect marine organisms from various environmental stressors (Castellano et al, 2016; Milito et al, 2022). We aimed to assess the effects of short‐term exposure to different concentrations of microplastics on the pools of OSH and GSH in different tissues of M. galloprovincialis .…”