Retinol metabolism in the mollusk Osilinus lineatus indicates an ancient origin for retinyl ester storage capacity.

Manuel Gesto,L Filipe C Castro,Miguel Machado Santos,Maria Armanda Reis-Henriques

doi:10.1371/journal.pone.0035138

Abstract

Although retinoids have been reported to be present and active in vertebrates and invertebrates, the presence of mechanisms for retinoid storage in the form of retinyl esters, a key feature to maintain whole-organism retinoid homeostasis, have been considered to date a vertebrate innovation. Here we demonstrate for the first time the presence of retinol and retinyl esters in an invertebrate lophotrochozoan species, the gastropod mollusk Osilinus lineatus. Furthermore, through a pharmacological approach consisting of intramuscular injections of different retinoid precursors, we also demonstrate that the retinol esterification pathway is active in vivo in this species. Interestingly, retinol and retinyl esters were only detected in males, suggesting a gender-specific role for these compounds in the testis. Females, although lacking detectable levels of retinol or retinyl esters, also have the biochemical capacity to esterify retinol, but at a lower rate than males. The occurrence of retinyl ester storage capacity, together with the presence in males and females of active retinoids, i.e., retinoic acid isomers, indicates that O. lineatus has a well developed retinoid system. Hence, the present data strongly suggest that the capacity to maintain retinoid homeostasis has arisen earlier in Bilateria evolution than previously thought.

Highlights

In vertebrates, retinoids play various key roles in cell differentiation and embryo development, as well as in many other processes such as growth, reproduction, vision, immune function and regeneration of tissues and organs [1,2,3]
Other retinyl esters distinct of retinyl palmitate (RP) were present in the complex, since the RP levels do not account for all the ROL increase after saponification
30% of the ROL in form of retinyl esters corresponds to RP

Summary

Introduction

Retinoids play various key roles in cell differentiation and embryo development, as well as in many other processes such as growth, reproduction, vision, immune function and regeneration of tissues and organs [1,2,3]. The biosynthesis of active retinoids such as retinoic acid (RA) relies on a complex system that depends on retinoids or carotenoids taken from the diet In this system, several retinoid precursors participate with specific functions (Figure 1): retinol (ROL), the main transport form, different retinyl esters (REs), the main storage form, and retinaldehyde (RAL), the immediate metabolic precursor of RA, which is the active retinoid form in the visual cycle. Several retinoid precursors participate with specific functions (Figure 1): retinol (ROL), the main transport form, different retinyl esters (REs), the main storage form, and retinaldehyde (RAL), the immediate metabolic precursor of RA, which is the active retinoid form in the visual cycle All these compounds are referred to as a group with the term vitamin A. In spite of the presence in invertebrate species of genes coding for enzymes and receptors that are involved in the metabolic and signaling modules of retinoids, the actual existence of active metabolic routes involving retinoid uptake, transport, storage, mobilization, activation and catabolism in invertebrates is as yet unknown

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Conclusion