Plasma vitellogenin and 17β-estradiol levels during the annual reproductive cycle of Podarcis s. sicula Raf

doi:10.1016/0016-6480(91)90079-L

General and Comparative Endocrinology

Volume 84, Issue 3, December 1991, Pages 337-343

https://doi.org/10.1016/0016-6480(91)90079-L Get rights and content

Abstract

Plasma vitellogenin and 17β-estradiol concentration were determined during the annual reproductive cycle of the female lizard Podarcis s. sicula Raf. living around Naples. Plasma vitellogenin was purified from estrogenized males for characterization and to raise specific immune serum. Using ELISA, plasma vitellogenin titers were determined in relation to ovary weight; plasma 17β-estradiol was measured by RIA method. Native vitellogenin was present as two polypeptide bands: α and β. The electrophoretic patterns, studied in normal male and estrogenized male and female, showed vitellogenin to be a protein present in female and in estrogenized male plasma but not in normal males. Lizard monomeric VTG, determined by SDS-PAGE, was about 200 kDa. Correlations between seasonal ovarian weight variations and plasma vitellogenin and 17β-estradiol suggest that ovarian development in Podarcis depends on plasma vitellogenin synthesis, which in turn relies on plasma estradiol levels. The two ovulatory waves observed in this study coincided with the two peak values of plasma vitellogenin and 17β-estradiol.

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Cited by (50)

Temporal expression and gonadotropic regulation of aromatase and estrogen receptors in the ovary of wall lizard, Hemidactylus flaviviridis: Correlation with plasma estradiol and ovarian follicular development
2017, Steroids
The current study in Indian wall lizard Hemidactylus flaviviridis for the first time demonstrates the reproductive phase-dependent expression pattern of aromatase (cyp19) and estrogen receptor subtypes (er-α and er-β) as well as their gonadotropic regulation in the ovary of a squamate. The expression of cyp19 remained low during regressed phase, increased markedly in recrudescent and declined sharply in breeding phase. Further, temporal profile of plasma estradiol 17-β (E₂) was found to be relatively parallel to the expression pattern of ovarian cyp19. The expression pattern of estrogen receptors in the ovary showed subtype-specific variation along the reproductive cycle. Expression of ovarian er-α remained high from regressed to late recrudescence, while er-β expression that was low during regression dramatically increased with the initiation of follicular growth in early recrudescence and remained high until late recrudescence. Nonetheless, expression of both the receptors declined during breeding phase when ovary contained vitellogenic follicle. Regarding gonadotropic regulation, short-term treatment with Follicle stimulating hormone (3 injections of FSH) increased the ovarian expression of cyp19, er-α and er-β while prolongation of treatment (7 or 11 injections) resulted in a marked decrease in expression of these genes concomitant to formation of vitellogenic follicle. However, a marked increase in plasma E₂ was recorded after 7 injections of FSH. The direct role of gonadotropin in regulation of cyp19 and estrogen receptors was established by an in vitro study where FSH upregulated the expression of these genes in all stages of ovarian follicles (early growing, previtellogenic and early vitellogenic) of wall lizards.
Ectopic synthesis of vitellogenin in testis and epididymis of estrogen-treated lizard Podarcis sicula
2016, General and Comparative Endocrinology
Citation Excerpt :
Among these, our model is the oviparous lizard Podarcis sicula of which are known the reproductive cycle in females and males (Filosa, 1973). In this species we recorded VTG synthesis in wildlife females (Carnevali et al., 1991) and in liver and plasma of males experimentally treated with E2 (Verderame and Limatola, 2010) or exposed to estrogen-like contaminated food or soil (Verderame et al., 2011, 2016). The aim of the present research was to determine in this lizard if the male gonad may be a site of ectopic synthesis and/or accumulation of VTG.
In oviparous vertebrates, vitellogenin (VTG) is the major yolk precursor synthesized in the liver of sexually mature females during the reproductive period. In males, the VTG gene is silent, but it may be activated by estradiol-17β (E2) or estrogen-like substances. Until now, extra-hepatic expression and synthesis of VTG after estrogen exposure has been reported only for aquatic vertebrates. This study demonstrates the ability of testis and epididymis of the terrestrial oviparous lacertid Podarcis sicula to synthesize VTG following E2 exposure. The results of in situ hybridization and immunohistochemistry analysis show the presence of both VTG mRNA and protein in these districts besides the known induction in the liver. The possible contemporaneous uptake of the E2-induced hepatic VTG by means of the specific vitellogenin receptor has been also evaluated. Finally, histological analysis shows that the E2-treatment during the mating season impairs spermatogenesis.
Seasonal changes in plasma steroid levels in relation to ovarian steroidogenic ultrastructural features and progesterone receptors in the house gecko, Hemidactylus flaviviridis, in Oman
2012, General and Comparative Endocrinology
Citation Excerpt :
The data are based on freshly captured lizards to avoid stress and to ensure that the hormone concentrations were closely related to the natural conditions [43]. The pattern of plasma E2, P and T levels throughout the reproductive season are typical of those observed in other lizard species [24,41,16,10,13,47,34]. There was a significant increase in E2 levels during the active phase (January–May) which is essential to the vitellogenic process and follicular growth [6,25,45,40,20,42,24,4].
A comprehensive study of the annual ovarian cycle in the house gecko, Hemidactylus flaviviridis, was conducted in Oman. Circulating estradiol (E₂), progesterone (P), and testosterone (T) were measured during the active and inactive phases of the cycle. The steroid levels were related to the steroidogenic ultrastructural features such as the abundance of smooth endoplasmic reticulum (SER), the presence of cisternal whorls, and close association of lipid droplets with swollen vesiculated mitochondria and SER. The steroids were measured using a sensitive detection technique HPLC-MS/MS. E₂ levels began to rise in January at the onset of vitellogenesis and continued to rise between February and May relative to ovulation, postovulation, gravidity and oviposition. Afterwards, E₂ remained low during the inactive phase (June–December). P levels increased significantly in March and peaked in April, which coincided with luteinization. P levels began to decline relative to luteolysis (May–June). Afterwards, it remained low throughout the inactive phase. T levels rose significantly in March–April coinciding with vitellogenesis, but decreased rapidly and significantly in May and remained low during the inactive phase. Progesterone receptors (PR), identified using immunohistochemistry, were strongly expressed during the breeding period, but were absent during the non-breeding period. The appearance of the steroidogenic ultrastructural features in the preovulatory and lutein granulosa cells was correlated with the significant rise in the three steroid levels and the PR. As the steroid levels declined, the granulosa cells underwent a general degeneration and disruption of the associated steroidogenic features.
Expression of vitellogenin in the testis and kidney of the spotted ray Torpedo marmorata exposed to 17β-estradiol
2011, General and Comparative Endocrinology
In vertebrates, the liver was long thought to be the only site of vitellogenin (Vtg) production, but recent studies demonstrated that Vtg is also expressed in extrahepatic districts. The aim of this paper is to assess, by in situ hybridization and immunohistochemistry, the expression of Vtg in the testis and kidney of Torpedo marmorata exposed to 17β-estradiol (E₂). In treated samples vtg mRNA and Vtg were detected contemporaneously only in the testis; differently the kidney cells were positive to Vtg antibody, but negative to vtg mRNA. This is the first study to assess that male germ cells, after an exposure to E₂, synthesize Vtg in a stage-dependent manner. The presence of Vtg and the modifications observed in the kidney after E₂ treatment are discussed.
Experimentally nonylphenol-polluted diet induces the expression of silent genes VTG and ERα in the liver of male lizard Podarcis sicula
2011, Environmental Pollution
Endocrine Disruptor Chemicals (EDCs) with estrogen-like properties i.e nonylphenol (NP) induce vitellogenin (VTG) synthesis in males of aquatic and semi-aquatic specie. In the oviparous species VTG is a female-specific oestrogen dependent protein. Males are unable to synthesize VTG except after E₂ treatment.
This study aimed to verify if NP, administered via food and water, is able to induce the expression of VTG even in males of vertebrates with a terrestrial habitat such as the lizard Podarcis. By means of ICC, ISH, W/B and ELISA we demonstrated that NP induces the presence of VTG in the plasma and its expression in the liver. VTG, undetectable in untreated males, reaches the value of 4.34 μg/μl in the experimental ones. Expression analysis and ISH in the liver showed that an NP-polluted diet also elicits the expression of ERα in the liver which is known to be related to VTG synthesis in Podarcis.
Hormones and Reproductive Cycles in Lizards
2011, Hormones and Reproduction of Vertebrates - Volume 3
Overall, less attention has been paid to the biology of lizards and reptiles compared to other vertebrate groups. Lizard species occupy all continents except Antarctica, in habitats ranging from desert to rainforest, and exhibit arboreal, terrestrial, fossorial, and even semi-aquatic life histories. However, hormones and their relationship to reproductive cycles have been well described for relatively few lizard species, representing only 8 of 32 families—Lacertidae, Teiidae, Varanidae, Iguanidae, Agamidae, Scincidae, Cordylidae, and Eublepharidae. From a review of available data, it is clear that gonadal steroid profiles across the reproductive cycle and their hypothalamic–pituitary regulation have remained generally consistent across lizard species regardless of reproductive mode (e.g., oviparity vs. viviparity, genotypic vs. temperature-dependent sex determination (TSD)). Thus, evolutionary conservation is demonstrated in that gonadal steroids play critical roles in the physiology and behavior necessary for reproduction. Evolutionary innovation is demonstrated in the variety of organismal responses to these gonadal steroids. Targeted research with established model species along with underrepresented taxa, including work on the role of endogenous rhythms and seasonal control of reproduction, will greatly advance the understanding of lizard, and likely vertebrate, reproduction.

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General and Comparative Endocrinology

Abstract

References (32)

Annual cycles in levels of pituitary and plasma gonadotropin, gonadal steroids, and thyroidal activity in the Chinese cobra (Naja naia)

Gen. Comp. Endocrinol

Vitellogenesis in lizard Lacerta vivipara jacquin. II. Vitellogenin synthesis during the reproductive cycle and its control by ovarian steroids

Gen. Comp. Endocrinol

Evolution of viviparity in Scincidae (Reptilia, Lacertilia)

Acta Embryol. Morphol. Exper

Effect of hypophysectomy and ovariectomy on hepatic ER content in turtle, Chrysemys picta

Gen. Comp. Endocrinol

The relationship among ovarian condition, steroid hormones, and estrus behaviour in Anolis carolinensis

J. Exp. Zool

In vivo responses of female snakes (Natrix fasciata) and female turtles (Chrysemys picta) to ovine gonadotropins (FSH and LH) as measured by plasma progesterone, testosterone and estradiol levels

Gen. Comp. Endocrinol

Protein measurement with Follin phenol reagent

J. Biol. Chem

Effects of progesterone and estrogen on the histology of the oviduct of the garter snake Thamnophis elegans

Gen. Comp. Endocrinol

Estradiol receptor in the lizard liver (Podarcis s. sicula). Seasonal changes and estradiol and growth hormone dependence

Mol. Cell. Endocrinol

Plasma sex hormones and post-reproductive period in green frog Rana esculenta complex

Gen. Comp. Endocrinol

Ovarian development and sex steroid hormones during the reproductive cycle of Rana esculenta complex

Zool. Sci

Vitellogenesis and oocyte growth in nonmammalian vertebrates

Estrogen-induced synthesis of yolk proteins in roosters

Am. Zool

Vitellogenin synthesis in fish, amphibians and reptiles

“In vitro” induction of vitellogenin synthesis in Rana esculenta liver and fat bodies

Gen. Comp. Endocrinol

Hormones and reproduction in the lizard Podarcis s. sicula Raf

Cited by (50)

Temporal expression and gonadotropic regulation of aromatase and estrogen receptors in the ovary of wall lizard, Hemidactylus flaviviridis: Correlation with plasma estradiol and ovarian follicular development

Ectopic synthesis of vitellogenin in testis and epididymis of estrogen-treated lizard Podarcis sicula

Seasonal changes in plasma steroid levels in relation to ovarian steroidogenic ultrastructural features and progesterone receptors in the house gecko, Hemidactylus flaviviridis, in Oman

Expression of vitellogenin in the testis and kidney of the spotted ray Torpedo marmorata exposed to 17β-estradiol

Experimentally nonylphenol-polluted diet induces the expression of silent genes VTG and ERα in the liver of male lizard Podarcis sicula

Hormones and Reproductive Cycles in Lizards