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Molecular endocrinology of oocyte growth and maturation in fish

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Résumé

Les gonadotropines hypophysaires (GtHs) sont de première importance dans la stimulation de la croissance et de la maturation ovocytaires. Toutefois, les actions des GtHs ne sont pas directes, mais elles passent par l'intermédiaire d'une production ovarienne de médiateurs stéroïdiens, aussi bien pour la croissance (oestradiol-17β) que pour la maturation ovocytaire (hormone inductrice de la maturation, MIH; 17α,20β-dihydroxy-4-pregnen-3-one, 17α,20β-DP chez les salmonidés 17α,20β,21-trihydroxy-4-pregnen-3-one, 20βS chez les sciénidés). Il est acquis que les productions d'oestradiol-17β et de 17α,20β-DP par les follicules ovariens de salmonidés se font via l'interaction de deux couches cellulaires, la thèque et la granulosa (modèle de coopération cellulaire). Chez les salmonidés, un changement net de la stéroïdogenèse, passant de la production d'oestradiol-17β à celle de 17α,20β-DP, intervient dans les enveloppes folliculaires juste avant la maturation. Il est possible que ce changement soit une conséquence de modifications profondes dans l'expression des gènes codant pour diverses enzymes de la stéroïdogenèse. Comme étape initiale de l'étude de cette question, nous avons isolé et caractérisé les ADNc codant pour différentes enzymes de la stéroïdogenèse ovarienne, à savoir les ADNc, de truite arc-en-ciel, du cytochrome P-450 coupant la chaîne latérale du cholestérol, de la 3β-hydrostéroïde déhydrogénase (HSD), du cytochrome P-450 17α-hydroxylase/17,20 lyase, et du cytochrome P-450 aromatase, ainsi que l'ADNc de la 20β-HSD de porc.

L'oestradiol-17β stimule la synthèse et la sécrétion hépatique du précurseur du vitellus: la vitellogénine. Celle-ci est ensuite transportée vers l'ovaire où elle est sélectivement incorporée dans l'ovocyte par un processus impliquant des récepteurs spécifiques situés à la surface de la cellule. L'oestradiol-17β induit également la synthèse, par le foie, de protéines membranaires de l'oeuf. L'induction de la maturation, par la 17α,20β-DP ou la 20βS, se fait par l'intermédiaire de leur liaison à la membrane plasmique ovocytaire. Cette interaction, initiale, surface cellulaire-MIH est suivie par la formation du médiateur majeur du MIH, le facteur promoteur de la maturation (MPF). Nous avons purifié le MPF à partir d'ovocytes maturés de carpe. Le MPF de carpe est constitué de deux composants: l'homologue du produit du gène cdc2+ de levure (p34cdc2, et la cycline B. La protéine kinase cdc2+ est présenté dans les ovocytes immatures aussi bien que dans les ovocytes dont la maturation a été induite par un traitement à la 17α,20β-DP, tandis que les protéines de type cycline B ne peuvent être détectées que dans les ovocytes maturés. L'addition de cycline B de poisson rouge, exprimée dans des bactéries, à des extraits d'ovocytes immatures de poisson rouge induit l'activation du MPF. Ces résultats suggèrent que l'apparition des protéines de type cycline B est une étape cruciale dans l'induction de la maturation des ovocytes de poisson par la 17α,20β-DP.

Abstract

Pituitary gonadotropins (GTHs) are of primary importance in triggering oocyte growth and maturation. However, the actions of GTHs are not direct, but are mediated by the ovarian production of steroidal mediators of oocyte growth (estradiol-17β) and maturation (maturation-inducing hormone, MIH; 17α,20β-dihydroxy-4-pregnen-3-one, 17α,20β-DP in salmonid fishes; 17α,20β,21-trihydroxy-4-pregnen-3-one, 20β-S in sciaenid fishes). It is established that production of estradiol-17β and 17α,20β-DP by salmonid ovarian follicles occurs via the interaction of two cell layers, the thecal and granulosa cell layers (two-cell type model). A distinct shift in the salmonid steroidogenesis from estradiol-17β to 17α,20β-DP occurs in the ovarian follicle layer immediately prior to oocyte maturation. It is possible that this shift is a consequence of dramatic changes in the expression of the genes encoding various steroidogenic enzymes. As an initial step to address this question, we have isolated and characterized the cDNAs encoding a number of ovarian steroidogenic enzymes including the rainbow trout cholesterol side-chain cleavage cytochrome P-450, 3β-hydroxysteroid dehydrogenase (HSD), 17α-hydroxylase/17,20 lyase cytochrome P-450, aromatase cytochrome P-450 cDNAS as well as the pig 20β-HSD cDNA.

Estradiol-17β stimulates the hepatic synthesis and secretion of a yolk precursor, vitellogenin. Vitellogenin is then transported to the ovary where it is selectively taken up into the oocyte by a receptor-mediated process involving specific cell-surface receptors. Estradiol-17β was also shown to induce the synthesis of egg membrane proteins in the liver. The maturation-inducing action of 17α,20β-DP and 20β-S is through the binding to the oocyte plasma membrane. This initial MIH-surface interaction is followed by the formation of the major mediator of MIH, maturation-promoting factor (MPF). We have purified MPF from mature oocytes of carp. Carp MPF consists of two components: the homolog of the cdc2+ gene product of fission yeast (p34cdc2) and cyclin B. The cdc2 kinase protein is present in immature oocytes as well as in oocytes induced to mature by 17α,20β-DP treatment, while cyclin B proteins can be detected only in mature oocytes. Addition of bacterially expressed goldfish cyclin B to the extracts of immature goldfish oocytes induced MPF activation. These results suggest that the appearance of cyclin B protein is a crucial step for 17α,20β-DP-induced oocyte maturation in fish.

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Authors and Affiliations

  1. Laboratory of Reproductive Biology, National Institute for Basic Biology, Okazaki, 444, Japan

    Yoshitaka Nagahama, Michiyasu Yoshikuni, Masakane Yamashita, Noriyoshi Sakai & Minoru Tanaka

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  1. Yoshitaka Nagahama
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  2. Michiyasu Yoshikuni
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  3. Masakane Yamashita
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  4. Noriyoshi Sakai
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  5. Minoru Tanaka
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Nagahama, Y., Yoshikuni, M., Yamashita, M. et al. Molecular endocrinology of oocyte growth and maturation in fish. Fish Physiol Biochem 11, 3–14 (1993). https://doi.org/10.1007/BF00004545

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  • DOI: https://doi.org/10.1007/BF00004545

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