Involvement of the lysosomal system in yolk protein deposit and degradation during vitellogenesis and embryonic development in trout

Abstract

In adult female rainbow trout (Oncorhynchus mykiss), an immunocytochemical study of the oocyte has shown that a proteolytic enzyme, cathepsin D, is localized in multivesicular bodies (MVB) which begin to differentiate before the phase of vitellogenesis. Estrogens cause the liver to synthesize the protein vitellogenin (VTG), which then enters the systemic circulation. During vitellogenesis, endocytosed VTG is co-localized with cathepsin D in the MVB.Assays of oocyte cathepsin activities have shown that the only proteolytic activity of note is that of cathepsin D. Along with the yolk proteins derived from VTG, this enzyme will be included in the central coalescent yolk mass.With the installation of the yolk syncytial layer and the surrounding yolk vascular system, embryonic development is characterized by high lysosomal activity, especially in the syncytial layer. At this level, proteolytic activity concerns a cathepsin L, secreted as a proenzyme. We propose the hypothesis that cathepsin D, along with the yolk proteins in the yolk globules that break away from the yolk mass in the vitellolysis zone, activates the proenzyme and leads to protein degradation, which then becomes very rapid. 0 1994 Wiley-Liss, Inc.Embryonic development in oviparous vertebrates is related to the size of egg reserves, namely vitellus or yolk. In fish as in amphibians, protein accumulation is the essential process involved in oocyte growth. The sequence of events contributing to protein "vitellogenesis" has been thoroughly described and illustrated in several reviews (Wallace, '85; Wallace and Selman, '90). In the rainbow trout, a salmonid teleost, large quantities of vitellogenin (VTG), a phosphoglycolipoprotein, are synthesized by the liver cells of mature females under estrogenic control. The VTG transported by the blood flow is incorporated in oocytes by receptor-mediated endocytosis (Tyler et al., '88, '90, '91). Cytoplasmic translocation in the oocyte is accompanied by the proteolytic processing of VTG, which undergoes specific cleavage into yolk proteins: lipovitellin (LV), phosvitin (PV), and possibly others.Multivesicular bodies (MVB) are differentiated during the initial phase of oocyte growth. Their role in the processing of endocytosed VTG in amphibians has been proposed by Wall and Patel ('87a).MVB are considered as potential contributors to hydrolase activity. Passage via MVB is required to cleave VTG to yolk proteins, as well as for their subsequent distribution to mature "heavy yolk platelets" (Wall and Patel, '87b).The first step of the present study was a n at-tempt to delineate specific yolk processing pathways in the trout oocyte by means of a n immunocytochemical study and by measuring lysosomal activities. It was found that cathepsin D is co-localized with VTG in the MVl3, which have become pre-yolk bodies. Cathepsin D is subsequently found in the yolk bodies and in the central yolk mass resulting from their coalescence, along with yolk proteins arising from VTG hydrolysis. Cathepsin D is the only protease act...

Particularities of reproduction and oogenesis in teleost fish compared to mammals

“…After leaving the blood vessels, vtg goes through the follicle wall and is selectively incorporated into the oocyte [105], by receptor-mediated endocytosis [106,107]. Vtg is then transferred into multivesicular bodies from the lysosomial compartment [108] where it is colocalised with a proteolytic enzyme, cathepsin D [109], which is probably responsible for its cleavage into yolk proteins.…”

Molecular cloning and expression characterization of ApoC-I in the orange-spotted grouper

“…In the past decade, many attempts have been undertaken on the biochemical composition of egg yolk components and their digestion, synthesis and transformation during embryonic development of teleosts (Henderson and Tocher 1987;Heming and Buddington 1988;Rønnestad and Fyhn 1993;Wiegand 1996;Poupard et al 2000). A large amount of data revealed that the formation of a YSL (yolk syncytial layer), a structure unique to teleosts, enables the resorption of the yolk reserves and development to the larval stage (Manfredi Romanini et al 1969;Walzer and Schönenberger 1979a;Shimizu and Yamada 1980;Cousin et al 1987;Sire et al 1994;Mani-Ponset et al 1996;Babin et al 1997;Poupard et al 2000). However, the developmental behavior of genes that control the utilization of yolk reserves is virtually unknown (Poupard et al 2000).…”

The Nature of Exocytosis in the Yolk Trophoblastic Layer of Silver Arowana (Osteoglossum bicirrhosum) Juvenile, the Representative of Ancient Teleost Fishes

“…The presence of cellular organelles in the cytoplasmic region in the silver arowana corresponds to those in the larvae of trout, Atlantic halibut (Hippoglossus hippoglossus), sea bass (Dicentrarchus labrax), and pike-perch (Sander lucioperca; Walzer and Schönenberger, 1979a,b;Kjørsvik and Reiersen, 1992;Sire et al, 1994;ManiFig. 3.…”

“…Then, the function of the ysl in initiating cell movement becomes less distinct after the completion of gastrulation, and its role in yolk utilization becomes more profound. Most studies thus far dealt with the histochemical aspect of the yolk utilization sequence in teleost development (Vernier and Sire, 1977a,b;Walzer and Schönenberger, 1979a,b;Sire et al, 1994). Poupard et al (2000) described the process of the utilization of yolk reserves during larval development of turbot (Scophthalmus maximus) and emphasized that the apoE gene expression in the yolk cell is parallel to very lowdensity lipoprotein particles exocytosis into a perisyncytial space.…”

“…Poupard et al (2000) described the process of the utilization of yolk reserves during larval development of turbot (Scophthalmus maximus) and emphasized that the apoE gene expression in the yolk cell is parallel to very lowdensity lipoprotein particles exocytosis into a perisyncytial space. However, a few investigators have addressed the cytological basis of endogenous feeding, particularly utilization of yolk reserves in teleost fish embryos (Shimizu and Yamada, 1980;Sire et al, 1994) and larvae (Vernier and Sire, 1977a,b;Sire and Vernier, 1979;Walzer and Schönenberger, 1979a,b;Kjørsvik and Reiersen, 1992;Mani-Ponset et al, 1994). As much as we know about the roles of the ysl in early development and organogenesis, the structure that correlates with its function in larval/yolksac juvenile of fish development remains unexplored, especially in the most ancient teleost fish, Osteoglossomorpha (Assheton, 1907).…”