Are Cell Junctions Implicated in the Regulation of Vitellogenin Uptake? Insights from an RNAseq-Based Study in Eel, Anguilla australis.

Lucila Babio,Ludovic Dutoit,P Mark Lokman,Erin L Damsteegt

doi:10.3390/cells11030550

Abstract

At the onset of puberty, ovarian follicles become competent to incorporate large amounts of vitellogenin (Vtg). Using an RNAseq-based approach, transcriptomes from pre-vitellogenic (PV) and early vitellogenic (EV) ovaries from wild-caught eel, Anguilla australis, were compared to investigate the expression of specific genes encoding cell junction proteins that could be involved in regulating Vtg uptake. Partial support was found for the mechanical barrier hypothesis proposing that the access of Vtg to the oolemma is restricted by a tight junction (TJ) network within the granulosa cell layer, which changes between the PV and EV stage. Among 25 genes encoding TJ-constituting proteins, five were down-regulated and two were up-regulated. A chemical barrier hypothesis stating that gap junctions (GJs) are involved in modulating Vtg uptake was not supported, as only five GJs were found to be expressed in the ovary with no significant changes in expression between stages. Furthermore, the endocytic pathway was found to be up-regulated during the PV-EV transition. Finally, the study showed that gene expression patterns may help identify suitable candidates involved in the regulation of Vtg uptake, and provided novel sequence data for A. australis, including putative Vtg receptors corresponding to Lr8 and Lrp13 members of the low-density lipoprotein receptor family.

Highlights

Academic Editor: Daniel ŻarskiIn order to produce high quality eggs that have the ability to self-sustain the development of viable offspring, female oviparous animals need to actively deposit nutrients into the developing oocytes to form the egg yolk: a mass rich in lipids and proteins that will serve as a food source for the future embryo
The developmental period associated with yolk accrual into the oocyte is known as vitellogenesis—it is characterised by the incorporation of the bulk of the yolk proteins that are obtained through the uptake of very high-density lipoproteins, so-called vitellogenins (Vtg), from the circulation
When progressing from the PV to the early vitellogenic (EV) stage, significant increases were seen in gonadosomatic index (GSI), the hepatosomatic index (HSI)

Summary

Introduction

Academic Editor: Daniel ŻarskiIn order to produce high quality eggs that have the ability to self-sustain the development of viable offspring, female oviparous animals need to actively deposit nutrients into the developing oocytes to form the egg yolk: a mass rich in lipids and proteins that will serve as a food source for the future embryo. The developmental period associated with yolk accrual into the oocyte is known as vitellogenesis (vitellogenic growth)—it is characterised by the incorporation of the bulk of the yolk proteins that are obtained through the uptake of very high-density lipoproteins, so-called vitellogenins (Vtg), from the circulation. During this growth phase, different molecular events occurring within the ovarian follicle can affect Vtg uptake. Extensive evidence in many teleost species indicates that the vtgr gene is already expressed and translated at early stages of development [1,2,3], and its transcription either decreases [3,4] or remains constant during subsequent oocyte growth [5]. The fact that pre-vitellogenic (PV) follicles are not competent to internalise Vtg in vivo nor in vitro [6], even though the receptors are available [1], prompts the notion that other elements must be involved in activating and supporting the oocyte’s ability to accumulate great quantities of Vtg [6]

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