Production of steroid hormones by male and female gonads of Sparus aurata (Teleostei, Sparidae)

doi:10.1016/0305-0491(78)90034-2

Comparative Biochemistry and Physiology Part B: Comparative Biochemistry

Volume 60, Issue 1, 1978, Pages 93-97

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Abstract

1.
1. The metabolism of steroids in male and female gonads of Sparus aurata, a protandrous hermaphroditic teleost, was studied in vitro at the end of the second year of life.
2.
2. Steroids were identified by thin-layer and gas-liquid chromatographies, as well as by formation of derivatives, and their yield-time correlation was plotted graphically.
3.
3. The identified metabolites of androstenedione are testosterone, 11-ketotestosterone (11-KT) and 11β-hydroxytestosterone (11β-OHT). Gonadotropin (HCG) treatment induced an enhanced production of 11-KT in gonadal components of both sexes, while 11β-OHT was stimulated by HCG only in the female.
4.
4. Testosterone production was stimulated in the ovary and was strongly inhibited in the testis.
5.
5. The significance of the inhibition of testosterone production by gonadotropin treatment in the testis prior to its transformation to an ovary for the mechanism of sex reversal is discussed.

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Steroids in the plasma of the winter flounder (Pseudopleuronectes americanus Walbaum)
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Steroid biosynthesis in vitro by the gonads of Sparus auratus L. (Teleostei) at different stages during natural sex reversal
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Metabolic pathways of steroid biosynthesis in ovarian tissue of a teleost, Tilapia aurea
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Cited by (16)

Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences
2002, Aquaculture
Citation Excerpt :
Similarly, although no effect of LHRH treatment on steroid hormone levels was observed in S. aurata, treatments did result in a reduced percentage of testicular tissue in the gonad (Vilia and Canario, 1995), suggesting that gonadotropins are involved in sex transformation in this protandrous species. In vitro treatment of S. aurata gonadal tissues with human chorionic gonadotropin (hCG) strongly suppressed radioactive androstenedione to testosterone conversion in testis but not in ovary (Eckstein et al., 1978), indicating a possible mechanism by which sex reversal may be mediated. Gonadotropins and their releasing hormones seem to be differentially regulated between the sexes in S. aurata (Elizur et al., 1995), and higher numbers of GnRH-producing cells are observed in the preoptic area of the brain in males than females in A. melanopus (Elofsson et al., 1997).
A great deal of information is known regarding the process of sex differentiation in fish, and the mechanisms involved in primary sex determination are now beginning to be defined. A range of gonadal differentiation types have been described for fish, including gonochoristic species possessing purely ovarian or testicular tissues, as well as hermaphroditic species that can initially mature either as males (protandrous) or females (protogynous). Sex determination in fish is a very flexible process with respect to evolutionary patterns observed among genera and families, and within individuals is subject to modification by external factors. These influences can affect the fate of both somatic and germ cells within the primordial gonad, and include the action of genetic, environmental (e.g. temperature), behavioural, and physiological factors. Exogenous sex steroids administered at the time of sex determination can strongly influence the course of sex differentiation in fish, suggesting that they play a critical role in assignment of gonad determination as well as subsequent differentiation. Detailed information is available from fish systems describing the production of sex steroids, as well as the enzymes involved in steroid production. Both estradiol and the maturation hormone 17α, 20β-dihydroxy-4-pregnen-3-one (17α, 20β-DP) are produced by a two-step process involving different cell layers in the gonad, and have effects on the differentiation of gonadal and nongonadal tissues. Gonadal development and differentiation in some fish is also controlled by hormones from the pituitary gland (gonadotropins) that are regulated by release hormones (GnRH) and other neuroendocrine and gonadal factors. Genetic determination of sex in fish can involve monogenic or polygenic systems, with factors located on the autosomes or on sex chromosomes. In the latter case, both male (XY) and female (ZW) heterogametic systems have been described, as well as many subtle variations on these themes. Sex chromosomes are found in approximately 10% of fish species examined, and sex-linked phenotypic traits, and protein and molecular genetic markers have been identified in several fish systems. Some species of fish reproduce gynogenetically, producing all-female populations. Several gene families known to be involved in sex determination in other vertebrates have recently been shown to be similarly involved in fish, suggesting conservation of sex determination pathways. The lability of sex-determination systems in fish makes some species sensitive to environmental pollutants capable of mimicking or disrupting sex hormone actions. Such observations provide important insight into potential impacts from endocrine disruptors, and can provide useful monitoring tools for impacts on aquatic environments.
Gonadal steroidogenesis in response to estradiol-17β administration in the sea bream (Sparus aurata L.)
2001, General and Comparative Endocrinology
The sea bream (Sparus aurata) is a protandrous hermaphrodite teleost fish in which estrogen administration induces testicular regression without influencing ovarian development. To analyze the changes in steroidogenesis of fish treated with two levels of estrogen (2 and 10 mg · kg⁻¹) and untreated control fish, fragments of gonads were incubated with tritiated 17-hydroxyprogesterone and the metabolites identified. The ability to extract radioactivity decreased with incubation time and was lower in gonads containing a larger proportion of ovarian tissue. The difference in steroidogenic capacity between control and estrogen-treated groups was generally quantitative rather than qualitative and paralleled the observed histological changes. The same metabolites were identified in all three groups, but estrogen treatment caused a marked inhibition of 5β-reduction, 3α-reduction, side-chain cleavage, and 11β-hydroxylation. The main androgens identified were 11β-hydroxy-4-androstene-3,17-dione and 3α-hydroxy-5β-androstane-3,17-dione, and the synthesis of both steroids was inhibited by estrogen treatment. Of the more polar pregnanes, 5β-pregnane-3α,17,20α-triol and 5β-pregnane-3α,17,20β-triol were detected in significant amounts, but only the latter appeared to be associated with development of the testis (in the untreated fish). A feature of sea bream gonadal steroidogenesis less common in other teleosts was the presence of 6α- and 6β-hydroxylation.
11-Ketotestosterone induces silvering-related changes in immature female short-finned eels, Anguilla australis
2001, Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology
The developmental transition from a residential, immature ‘yellow’ eel to a migratory, maturing adult ‘silver’ eel is accompanied by many morphological changes that appear to be under endocrine control. High circulating levels of the teleost, and usually male-specific, androgen 11-ketotestosterone (11-KT) are found in migrating female short-finned eels, Anguilla australis. We examined the role of this steroid in silvering by implanting immature, female short-finned eels either with blank vehicles or with vehicles containing 11-KT. Six weeks after they had received the implants, eels treated with 11-KT had developed ‘chisel-shaped’ snouts and black pectoral fins with tapered ends, and the size of their eyes had increased significantly. 11-KT treated eels had a thicker dermis than control eels and an epidermis with fewer or no mucous cells. Ventricular mass at the end of the experiment was two-fold larger than in control eels. 11-KT treated eels also had larger livers and gonads. Ovaries contained predominantly cortical alveolus stage III oocytes, as opposed to the smaller gonads of control eels containing previtellogenic stage II oocytes. All of these changes correspond to changes during the developmental transition from yellow to silver eels in the wild. This demonstrates that silvering in eels is under endocrine control and that the presumed male-specific steroid 11-KT is capable of inducing silvering-related changes in a female teleost. We discuss how species-specific responses to 11-KT may differ depending on tissue-specific androgen receptor abundance and how a dual demand on liver function can explain the apparently positive effects of 11-KT on liver growth.
The effect of estrogen on the gonads and on in vitro conversion of androstenedione to testosterone, 11-ketotestosterone, and estradiol-17β in Sparus aurata (Teleostei, Sparidae)
1999, General and Comparative Endocrinology
The effects of estrogen on gonad morphology and steroidogenesis of sea bream, Sparus aurata, a protandrous hermaphrodite teleost, were investigated. Fish were treated in winter/spring for different periods with 17α-ethynylestradiol (ethE₂; experiment 1) and in summer with two doses of estradiol-17β (E₂; experiment 2). Estrogen was more effective in summer. Its main effect on the gonad was inhibition of testicular growth and of male germ cell development beyond the spermatogonia stage, including mitosis. The effect of estrogen on ovarian development was slight and only apparent at the end of experiment 2 in the higher dose group. Gonadal fragments were incubated at different times during treatment with androstenedione and the output of testosterone (T), estradiol (E₂), and 11-ketotestosterone (11KT) was measured by radioimmunoassay. T and E₂ production was inversely correlated with the proportion of testicular tissue (and positively with ovarian tissue) in the gonad in experiment 2. However, the production of 11KT was not correlated with any type of tissue, possibly because of further metabolism. Inhibition of testicular development by estrogen was also associated with higher output of steroid conjugates.
Enzyme immunoassay for 11-ketotestosterone using acetylcholinesterase as laberl: application to the measurement of 11-ketotestosterone in plasma of Siberian sturgeon
1994, Comparative Biochemistry and Physiology. Part C: Pharmacology
A competitive enzyme immunoassay using 11-ketotestosterone (11-KT) covalently coupled to acetylcholinesterase (AChE) from electric eel is developed. Ninety-six well microtiter plates are coated with pure mouse-anti-rabbit-IgG monoclonal antibody and competition is performed in one-step reaction by adding successively 11-KT standard or samples, enzymatic tracer and 11-KT-specific antiserum. This assay is more sensitive (detection limit is 7 pg/ml) than radioimmunoassays previously described, and specificity was not modified by the use of enzymatic tracer. This assay can be performed in less than 5 hr. Validation of the EIA was achieved in a fish model, Siberian sturgeon (Acipenser baeri), by comparative determinations of 11-KT levels in plasma extracts using EIA and RIA. Application to the measurement of 11-KT in plasma of farmed Siberian sturgeon during the first reproductive cycle is reported.
Oocyte maturation and changes in plasma steroid levels in snapper Pagrus (=Chrysophrys) auratus (Sparidae) following treatment with human chorionic gonadotropin
1992, Aquaculture
Snapper Pagrus (= Chrysophrys) auratus were captured by long-lining from the Hauraki Gulf, NE New Zealand, and returned to the laboratory. Eighteen female fish were injected with either saline or 1000 U kg⁻¹ human chorionic gonadotropin (hCG). Blood samples were taken at the time of injection and subsequently at 1, 6 and 24 h post-injection (pi). Plasma levels of 17β-estradiol (E₂), 17,20β-dihydroxy-4-pregnen-3-one (17, 20βP), and testosterone (T) were measured by RIA. Seven out of the eleven hCG-injected fish ovulated within 24 h, whereas no control fish ovulated. In fish injected with hCG, plasma E₂ levels were elevated at 24 h pi, 17,20βP levels at 6 h pi, and T at 6 and 24 h pi, relative to controls.
In a second experiment, twelve fish were injected with 1000 U kg⁻¹ hCG as before and bled at 0, 4, 7, 13, 17 and 26 h pi. At each sample time a small piece of ovarian tissue was taken from each fish using a 12 G syringe needle introduced through the body wall. Aspirated follicles were measured and then cleared to determine the position of the germinal vesicle. Follicles from six of the fish underwent a significant increase in diameter, accompanied by germinal vesicle breakdown (GVBD) and oocyte hydration. Plasma E₂ and T levels were elevated in fish with maturing oocytes from 13 h pi. 17,20βP showed a peak at 4 h pi, but only in the group of fish in which oocyte maturation did not occur. There was no difference in plasma cortisol levels between fish that showed oocyte maturation and those that did not, suggesting that proximate stress factors were not responsible for the differential response to hCG treatment observed in this experiment.

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Comparative Biochemistry and Physiology Part B: Comparative Biochemistry

Abstract

References (17)

Steroids in the plasma of the winter flounder (Pseudopleuronectes americanus Walbaum)

The biosynthesis of steroids by the gonads of the ricefield eel, Monopterus albus at various phases during sex reversal

Gen. comp. Endocr.

Steroid biosynthesis in vitro by the gonads of Sparus auratus L. (Teleostei) at different stages during natural sex reversal

Gen. comp. Endocr.

Metabolic pathways of steroid biosynthesis in ovarian tissue of a teleost, Tilapia aurea

Gen. comp. Endocr.

The occurrence and biosynthesis in vitro of 11-ketotestosterone in ovarian tissue of a mullet, Mugil capito, derived from two biotopes

Gen. comp. Endocr.

Steroidogenesis in post- and pre-spawned ovaries of a cichlid fish, Tilapia aurea

Comp. Biochem. Physiol.

Isolation of 11-ketotestosterone and dehydroepiandrosterone from ovaries of the common mullet, Mugil capito

Gen. comp. Endocr.

In vitro steroid synthesis by the ovaries of the teleost fish, Centropristes striatus (L)

Gen. comp. Endocr.

Cited by (16)

Sex determination and sex differentiation in fish: An overview of genetic, physiological, and environmental influences

Gonadal steroidogenesis in response to estradiol-17β administration in the sea bream (Sparus aurata L.)

11-Ketotestosterone induces silvering-related changes in immature female short-finned eels, Anguilla australis

The effect of estrogen on the gonads and on in vitro conversion of androstenedione to testosterone, 11-ketotestosterone, and estradiol-17β in Sparus aurata (Teleostei, Sparidae)

Enzyme immunoassay for 11-ketotestosterone using acetylcholinesterase as laberl: application to the measurement of 11-ketotestosterone in plasma of Siberian sturgeon

Oocyte maturation and changes in plasma steroid levels in snapper Pagrus (=Chrysophrys) auratus (Sparidae) following treatment with human chorionic gonadotropin