Vitellogenin hormonal control in the green frog, Pana esculenta. interplay between estradiol and pituitary hormones

doi:10.1016/0300-9629(85)90495-5

Comparative Biochemistry and Physiology Part A: Physiology

Volume 82, Issue 4, 1985, Pages 855-858

Comparative Biochemi...

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Abstract

1.
1. The effect of estradiol and pituitary hormones on the titre of serum vitellogenin has been studied in Rana esculenta by rocket immunoelectrophoresis.
2.
2. Hepatic synthesis of vitellogenin depends on physiological doses of estradiol.
3.
3. Gonadotropins enhance the uptake, presumably by acting directly on the oocyte plasma membrane.
4.
4. In addition, our data support a direct pituitary intervention on liver synthesis and/or release of vitellogenin.
5.
5. Hormonal response, as evaluated by vitellogenin serum titres, tends to increase from November to July. This could be the expression of a modification, throughout the sexual cycle, of liver sensitivity to the hormones.

References (12)

F Giorgi et al.
Variations in the vitellogenin during the reproductive cycle of Rana esculenta L
Comp. Biochem. Physiol.
(1982)
S.M Ho et al.
Effect of hypophysectomy and growth hormone on estrogen induced vitellogenesis in the freshwater turtle, Chrysemys picta
Gen. comp. Endocrinol.
(1982)
C.B Laurell
Quantitative estimation of protein by electrophoresis in agarose containing antibodies
Analyt. Biochem.
(1966)
F.E.B.M May et al.
Patterns of protein synthesis in livers of Xenopus laevis during metamorphosis: effects of estrogen in normal and thyrostatic animals
Develop. Biol.
(1981)
G Signorini et al.
Vitellogenin synthesis induced by estradiol-17β in the newt Triturus cristatus carnifex (Laurenti)
Comp. Biochem. Physiol.
(1981)
B.I Sundararaj et al.
Role of testosterone, estradiol-17β and Cortisol during vitellogenin synthesis in the catfish, Heteropneustes fossilis (Block)
Gen. comp. Endocrinol.
(1982)

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Cited by (29)

Celebrating 50+ years of research on the reproductive biology and endocrinology of the green frog: An overview
2020, General and Comparative Endocrinology
Citation Excerpt :
Concomitant with the increase in E2, VTG levels are high in the liver, plasma, and ovary (Varriale et al., 1988; Polzonetti-Magni et al., 2004). The effects of gonadotropins enhance the VTG uptake, presumably by acting directly on the oocyte plasma membrane (Gobbetti et al., 1985; Carnevali and Mosconi, 1992). Further, in in vivo and in vitro systems, hepatic VTG synthesis can be induced by GH in both sexes (Carnevali et al., 1995) and involve tyrosine kinase and cAMP in GH-induced VTG synthesis (Carnevali et al., 2000).
This issue is dedicated to the late Professor Giovanni Chieffi, and this article is an overview of the research on Comparative Endocrinology of reproduction using Rana esculenta (alias Pelophylax esculentus) as a model system. Starting from the early 1970s till today, a large quantity of work have been conducted both in the fields of experimental endocrinology and in the definition of the diffuse neuroendocrine system, with a major focus on the increasing role of regulatory peptides. The various aspects investigated concerned the histological descriptions of principal endocrine glands of the hypothalamic–pituitary–gonadal (HPG) axis, the localization and distribution in the HPG of several different substances (i.e. neurosteroids, hypothalamic peptide hormones, pituitary gonadotropins, gonadal sex steroids, and other molecules), the determination of sex hormone concentrations in both serum and tissues, the hormone manipulations, as well as the gene and protein expression of steroidogenic enzymes and their respective receptors. All together these researches, often conducted considering different periods of the annual reproductive cycle of the green frog, allowed to understand the mechanism of cascade control/regulation of the HPG axis of R. esculenta, characterizing the role of different hormones in the two sexes, and testing the hypotheses about the function of single hormones in different target organs. It becomes evident from the review that, in their simplest form, several features of this species are specular as compared to those of other vertebrate species and that reproduction in this frog species is either under endogenous multi-hormonal control or by a wide array of different factors. Our excursus of this research, spanning almost five decades, shows that R. esculenta has been intensively and successfully used as an animal model in reproductive endocrinology as well as several field studies such as those involving environmental concerns that focus on the effects of endocrine disruptors and other environmental contaminants.
Vulnerability of marsh frog Pelophylax ridibundus to the typical wastewater effluents ibuprofen, triclosan and estrone, detected by multi-biomarker approach
2017, Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology
Citation Excerpt :
The induction of vitellogenesis by estrogen E1 in frog was expected. The dependence of the serum vitellogenin level on physiological doses of estradiol in Rana esculenta was described earlier (Gobbetti et al., 1985). The chronic exposure of wood frog Lithobates sylvaticus to 17α-ethynylestradiol, the synthetic estrogen used in oral contraceptives, during the larval period led to the elevated abundances of transcripts of vitellogenin A2 in the liver (1.8–280-fold greater compared to controls).
Pharmaceutical and personal care products (PPCPs) are the environmental pollutants of growing concern. The aim of this study was to indicate the effects of typical PPCPs on the marsh frog Pelophylax ridibundus. We treated male frogs with waterborne ibuprofen (IBU, 250 ng·L^− 1), triclosan (TCS, 500 ng·L^− 1), or estrone (E1, 100 ng·L^− 1) for 14 days. Common vulnerability of the frogs was detected from dramatic decrease of Zn, total and metalated metallothionein (MT) concentrations, Zn/Cu ratio, the elevation of activity of glutathione-S-transferase, cathepsin D and DNA instability in the liver, the depletion of cholinesterase in the brain and cortisol in the blood plasma in all exposures. Nevertheless, lipofuscin concentration in the liver was always decreased. The groups were best distinguished by cytochrome P450 (CYP450) activity determined by ELISA. The exposure to IBU caused lesser damage, but elevated the levels of oxyradicals and glutathione (GSH and GSSG) and lysosomal membrane instability. Exposures to TCS and E1 provoked the endocrine disturbance (increased levels of vitellogenin and thyrotropin in blood plasma), decreased lactate dehydrogenase activity and increased level of pyruvate in the liver. TCS caused the increase of GSSG by 7.3 times and lactate levels. Only E1 lead to decrease of deiodinase activity in the liver, activation of CYP450 and caspase-3 and efflux of cathepsin D from lysosomes. Spectrophotometric and ELISA assays of MTs and CYP450 gave distinct results in E1-group. Broad disruption of the hormonal pathways caused by E1 could be of concern for the health status of frogs in their habitats.
17β-Estradiol induces supernumerary primordial germ cells in embryos of the polychaete Platynereis dumerilii
2014, General and Comparative Endocrinology
Citation Excerpt :
Estrogens are steroid hormones involved in a multitude of processes related to reproduction, including sex determination, maturation of sexual organs, gametogenesis, induction of vitellogenesis, estrous cycles, and mating behaviors (Butcher et al., 1974; Gobbetti et al., 1985; Pfaff, 1970; Wallen, 2005).
In the polychaete Platynereis dumerilii exactly four primordial germ cells (PGCs) arise in early development and are subject to a transient mitotic arrest until the animals enter gametogenesis. In order to unravel the mechanisms controlling the number of PGCs in Platynereis, we tested whether the steroid 17β-estradiol (E2) is able to induce PGC proliferation, as it had been described in other species. Our data provide strong support for such a mechanism, showing that E2 significantly increases the occurrence of larvae with supernumerary PGCs in Platynereis in a dose dependent manner. E2 responsiveness is restricted to early developmental stages, when the PGCs are specified. During these stages, embryos exhibit high expression levels of the estradiol receptor (ER). The ER transcript localizes to the yolk-free cytoplasm of unfertilized eggs and segregates into the micromeres during cleavage stages. Nuclear ER protein is found asymmetrically distributed between daughter cells. Neither transcript nor protein is detectable in PGCs at larval stages. Addition of the specific estradiol receptor inhibitor ICI-182,780 (ICI) abolishes the proliferative effect of E2, suggesting that it is mediated by ER signaling. Our study reports for the first time an ER mediated proliferative effect of E2 on PGCs in an invertebrate organism.
Immunolocalization of hepatic estrogen and progesterone receptors in the female lizard Uromastyx acanthinura
2012, Comptes Rendus - Biologies
Citation Excerpt :
It consists in the synthesis of vitellogenin, its specific incorporation in primary oocytes in growth, and accumulation of yolk [1–3]. In the liver of all oviparous species, the synthesis of vitellogenin is under control of estrogen [4–14]. Growth hormone plays a direct role in potentiating the induction of hepatic 17β-estradiol [15–17], and its action could be associated with hepatic synthesis of estrogen receptors.
The hormonal regulation of hepatic synthesis of vitellogenin during the annual reproductive cycle was performed for the first time in the deserticole, oviparous, diurnal and herbivorous Uromastyx acanthinura, a lizard belonging to the Agamidae family. In order to elucidate what kind of estrogen receptor is involved in this process, an immunohistochemical study was performed. Changes were obtained in the labeling and cellular distribution of the estrogen and progesterone receptors according to the period of the reproductive cycle and the experimental administration of 17β-estradiol. Only the ERβ subtype was present; it was found in all phases of the cycle with a variable localization: nuclear and cytosolic during vitellogenesis, mainly cytosolic in the female with egg retention (luteal phase) and strictly cytosolic in females at sexual rest. The progesterone receptors were present only at the luteal phase and during sexual rest and disappeared completely from females after 17β-estradiol treatment in sexual rest. Our data suggested that mediation of action of the 17β-estradiol in the vitellogenin synthesis in the lizard U. acanthinura occured via ERβ. PRA and PRB could both be necessary for the negative effect of progesterone on the hepatic synthesis of vitellogenin.
La régulation hormonale de la synthèse hépatique de la vitellogénine au cours du cycle reproducteur annuel est réalisée pour la première fois chez Uromastyx acanthinura, lézard déserticole, ovipare, diurne et herbivore de la famille des Agamidae. Dans le but de préciser le type de récepteur des œstrogènes impliqué dans ce processus, une étude immunohistochimique a été réalisée. Des changements dans le marquage et la distribution cellulaire des récepteurs des œstrogènes et de la progestérone selon la période du cycle reproducteur et le traitement à l’œstradiol 17β sont mis en évidence. Seul le sous-type REβ est présent, il est retrouvé à toutes les phases du cycle avec une localisation variable : nucléaire et cytosolique lors de la vitellogenèse, essentiellement cytosolique pendant la rétention des œufs (phase lutéale) et strictement cytosolique chez les femelles au repos sexuel. Les récepteurs de la progestérone sont exprimés uniquement au cours de la phase lutéale et durant le repos sexuel et disparaissent totalement après le traitement œstrogénique chez les femelles au repos sexuel. Nos données suggèrent que la médiation de l’action de l’œstradiol 17β dans la synthèse de la vitellogénine chez le lézard U. acanthinura s’exerce via REβ. RPA et RPB pourraient être tous les deux nécessaires pour l’effet négatif de la progestérone sur la synthèse hépatique de la vitellogénine.
Multihormonal control of vitellogenesis in lower vertebrates
2004, International Review of Cytology
Citation Excerpt :
This protein is normally never detected in untreated males, although the hepatocytes are capable of synthesizing the yolk precursor when stimulated with unphysiologically high doses of estradiol-17β. This aspect has been pointed out in several oviparous species (Carnevali et al., 1992b, 1995; Gobbetti et al., 1985a; Mosconi et al., 1998, 2002b) including the Mixiniformes Lampetra fluviatilis (Mewes et al., 2002). Regarding chondrichthyan fishes, it has recently been shown that in Torpedo marmorata, oocyte growth is not only caused by the uptake of exogeneous molecules but also by the contributions of the oocytes themselves (Prisco et al., 2002); in oviparous dogfish, Scyliorhinus canicula (Craik, 1978a,b,c,d, 1979), and in the little skate, Raja erinacea (Perez and Callard, 1992), vitellogenesis does not differ fundamentally from that of other vertebrates in the mechanisms of synthesis and storage of vitellogenin.
The comparative approach on how and when vitellogenesis occurs in the diverse reproductive strategies displayed by aquatic and terrestrial lower vertebrates is presented in this chapter; moreover, attention has been paid to the multihormonal control of hepatic vitellogenin synthesis as it is related to seasonal changes and to vitellogenin use by growing oocytes. The hormonal mechanisms regulating vitellogenin synthesis are also considered, and the effects of environmental estrogens on the feminization process in wildlife and humans have been reported. It is then considered how fundamental nonmammalian models appear to be, for vitellogenesis research, addressed to clarifying the yolkless egg and the evolution of eutherian viviparity.
Production of a recombinant newt growth hormone and its application for the development of a radioimmunoassay
2000, General and Comparative Endocrinology
Complementary DNA (cDNA) encoding newt (Cynops pyrrhogaster) growth hormone (nGH) was cloned from a cDNA library constructed from mRNAs of newt pituitary glands and was expressed in Escherichia coli. Based on Northern blot analysis using the cDNA as a probe, the nGH mRNA was estimated to be 940 bases in length. The recombinant nGH (nGHr) had a molecular mass of 22 kDa as determined by SDS–PAGE and possessed considerable bioactivity as determined in a Xenopus cartilage assay. Using the nGHr, we produced a polyclonal antibody against nGHr. Western blot analysis of newt anterior pituitary gland homogenates revealed that this antiserum specifically detected a single 22-kDa band, and histological studies of newt pituitary gland sections showed that the cells that reacted immunologically by the anti-nGHr antiserum corresponded to those stained by an antiserum against rat GH. A radioimmunoassay (RIA) that is specific and sensitive for nGH was developed, employing the antiserum thus produced. The sensitivity of the RIA was 57 ± 7 pg/100 μl assay buffer. Interassay and intraassay coefficients of variation were 1.22 and 2.70%, respectively. Serial dilutions of plasma and pituitary homogenate of C. pyrrhogaster yielded dose-response curves that were parallel to the standard curve. Plasma from hypophysectomized newts showed no cross-reactivity. Moreover, displacement curves obtained using pituitary homogenates of the sword-tailed newt (C. ensicauda) and the crested newt (Triturus carnifex) were also parallel to the standard curve. Mammalian and frog GHs and prolactins (PRLs), as well as newt PRL, showed no inhibition of binding, even at relatively high doses, in this RIA. The RIA was used to measure GH released from newt pituitaries in vitro. Enhancement of GH release by 10⁻⁷ M thyrotropin-releasing hormone was observed in cultures of newt pituitaries.

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Comparative Biochemistry and Physiology Part A: Physiology

Abstract

References (12)

Variations in the vitellogenin during the reproductive cycle of Rana esculenta L

Comp. Biochem. Physiol.

Effect of hypophysectomy and growth hormone on estrogen induced vitellogenesis in the freshwater turtle, Chrysemys picta

Gen. comp. Endocrinol.

Quantitative estimation of protein by electrophoresis in agarose containing antibodies

Analyt. Biochem.

Patterns of protein synthesis in livers of Xenopus laevis during metamorphosis: effects of estrogen in normal and thyrostatic animals

Develop. Biol.

Vitellogenin synthesis induced by estradiol-17β in the newt Triturus cristatus carnifex (Laurenti)

Comp. Biochem. Physiol.

Role of testosterone, estradiol-17β and Cortisol during vitellogenin synthesis in the catfish, Heteropneustes fossilis (Block)

Gen. comp. Endocrinol.

Cited by (29)

Celebrating 50+ years of research on the reproductive biology and endocrinology of the green frog: An overview

Vulnerability of marsh frog Pelophylax ridibundus to the typical wastewater effluents ibuprofen, triclosan and estrone, detected by multi-biomarker approach

17β-Estradiol induces supernumerary primordial germ cells in embryos of the polychaete Platynereis dumerilii

Immunolocalization of hepatic estrogen and progesterone receptors in the female lizard Uromastyx acanthinura

Multihormonal control of vitellogenesis in lower vertebrates

Production of a recombinant newt growth hormone and its application for the development of a radioimmunoassay