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Molecular basis of egg formation in marine fish: the role of the oocyte aquaporin

AuthorsCerdà, Joan
Issue Date12-Jul-2012
PublisherSocietat Catalana de Biologia
CitationI CIBICAT: 177 (2012)
AbstractThe pre-ovulatory hydration of the oocyte of marine teleosts that produce pelagic (buoyant) eggs occurs concomitantly with meiosis resumption (oocyte maturation), and results in a massive expansion and dilution of the egg cytoplasm. This mechanism is critical for the development of viable gametes as it assures a water reservoir when eggs are released into the hyperosmotic seawater, and facilitates egg buoyancy and dispersal. Therefore, egg hydration and buoyancy are the first markers of egg quality in the aquaculture of marine fish. While a number of studies have identified the major inorganic and organic osmolytes that create the intracellular osmotic driving force for oocyte hydration, water influx was thought to occur passively. However, the discovery of molecular water channels (aquaporins) in all kingdoms of life recently led to the investigation of the role of these membrane proteins during teleost oocyte hydration. Initial studies in the gilthead seabream uncovered a novel water channel, now termed aquaporin-1ab (Aqp1ab), that mediates water permeation and resultant swelling of the oocytes. Further functional, genomic and phylogenetic analyses revealed that Aqp1ab belongs to a teleost-specific subfamily of water-selective aquaporins, which likely evolved by tandem duplication of a common ancestor. This gene is highly expressed in the ovary of marine and catadromous teleosts that produce hydrated eggs, including the Atlantic halibut, which spawns one of the largest pelagic eggs known. In this species, we recently obtained the first unequivocal functional evidence for the essential role of Aqp1ab during oocyte hydration. Interestingly, however, aqp1ab transcripts are also highly accumulated in the ovary of some freshwater species, such as the stinging catfish, in which oocytes partially hydrate during meiotic maturation, suggesting that Aqp1ab may also play a role in the oocyte of teleosts producing non-buoyant (benthic) eggs. Using the seabream as the experimental model, we recently demonstrated that the oocyte Aqp1ab is tightly regulated at the transcriptional and post-translational levels. Thus, transcriptional activation of the aqp1ab promoter in oogonia and primary growth oocytes is dependent on the nuclear progestin receptor (nPgr) and regulated by Sry-related high mobility group [HMG]-box (sox) genes, with Sox3 and Sox8b acting synergistically with the nPgr and Sox9b acting as a repressor. Translation of aqp1ab mRNAs occurs in primary oocytes, and subsequently, throughout the period of oocyte growth, Aqp1ab-containing vesicles are transported towards the oocyte cortex. Structural analyses have revealed that the cytoplasmic tail of Aqp1ab is highly divergent in teleosts, but retains specific motifs that regulate vesicular trafficking and temporal insertion in the oocyte plasma membrane during hydration. These processes appear to involve alternative mechanisms of phosphorylation and/or dephosphorylation of specific C-terminal residues. Evidence for the rapid neofunctionalization of the C-terminus is found in the Atlantic halibut, which causes ex vivo loss of function of Aqp1ab when expressed in amphibian oocytes, but not in zebrafish or native oocytes. These findings are revealing that the Aqp1ab-mediated mechanism of oocyte hydration in marine teleosts is a conserved, but divergently regulated process based on the interplay between osmolyte generation and the controlled synthesis and insertion of Aqp1ab at the oocyte surface. The discovery of Aqp1ab thus provides important new insight into the molecular basis of egg formation and quality in marine fish
DescriptionI Congrés Internacional de Biologia de Catalunya (CIBICAT): Global Questions on Advanced Biology. An international conference on interdisciplinary frontiers in biology. As part of the first Centenary of the Societat Catalana de Biologia. 9-12 July 2012, Barcelona
Publisher version (URL)http://scb-congres.espais.iec.cat/en/
Appears in Collections:(ICM) Comunicaciones congresos
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