Effect of cortisol on the in vitro hepatic conversion of thyroxine to triiodothyronine in brook charr (Salvelinus fontinalis Mitchill)

doi:10.1016/0016-6480(88)90151-7

General and Comparative Endocrinology

Volume 70, Issue 2, May 1988, Pages 312-318

https://doi.org/10.1016/0016-6480(88)90151-7 Get rights and content

Abstract

In vitro studies with liver homogenates of brook charr (Salvelinus fontinalis) demonstrate that the conversion of thyroxine (T₄) to triiodothyronine (T₃) is dependent upon temperature, pH, substrate, and homogenate concentration, supporting the hypothesis of an enzymatic hepatic T₄ to T₃ conversion. Dithiothreitol has a marked stimulatory effect on the rate of conversion. The kinetics of the conversion, determined by Lineweaver-Burke analysis suggest a Michaelis-Menten (K_m) constant of 1.3 × 10⁻⁸ M, and a maximum velocity (V_max) of 0.42 pmol/mg protein/h. In brook charr given intraperitoneal implants of hydrogenated coconut oil containing cortisol at levels of 0, 5, and 50 mg/kg body weight, and sampled after 56 days, T₄ to T₃ conversion by homogenates of hepatic tissue in vitro was significantly (P < 0.01) higher in the fish implanted with 50 mg/kg of cortisol than in either of the other two groups. However, plasma cortisol, l-thyroxine (T₄) and triiodo-l-thyronine (T₃) concentrations, plasma T₃:T₄ ratios and hepatosomatic index were not significantly different in the three treatment groups.

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The elevated T3 and T4 levels in the fish treated with C50 pointed to an enhanced T4 secretion from thyroid tissue and an alteration in activity of deiodinase enzymes. Cortisol has been demonstrated to affect thyroid hormone production and peripheral deiodination in fish (Vijayan et al., 1988; Brown et al., 1991; Walpita et al., 2007; Arjona et al., 2011). The relationship between cortisol and thyroid hormones could account for their key and vital roles as metabolic hormones in the maintenance of homeostatic equilibrium and in acclimation with adverse condition, as reported previously by Peter and Peter (2011).
This study examined the effects of implanted cortisol on various aspects of intermediary metabolism of great sturgeon, Huso huso. Prior to experimentation all fish were examined using an endoscope to observe the stage of ovarian development. Subsequently, the 3-year-old female fish in the previtellogenic stage (mean body weight of 6759 ± 53.2 g) were intraperitoneally implanted with cocoa butter pellets containing cortisol to mimic the effects of chronic stress. The implant doses were 0 (C₀; as control), 5 (C₅) and 50 (C₅₀) mg cortisol/kg body weight. Blood samples were taken every seven days during the four weeks of the experiment and analyzed for cortisol, glucose, adrenocorticotropic hormone (ACTH), total protein, total lipid, triiodothyronine (T₃), thyroxine (T₄), cholesterol and triglyceride content. Growth was reduced in all experimental groups and was not affected by cortisol treatment. Surprisingly, serum cortisol levels were higher in the C₅ group than in the C₅₀ throughout the experiment. A significant increase in glucose levels was observed in the cortisol-implanted fish from day 14 onwards. The high dose of cortisol elicited a significant increase in serum T₃ and T₄ levels. Fish implanted with the high cortisol dose also showed increases in serum ACTH, total lipid and cholesterol levels throughout a 28-day experimental period. The present study reveals that the negative effects of endoscopic surgery remain for at least four weeks and that a sustained-release implant of cortisol to mimic the effects of chronic stress affects metabolic responses. Since the adverse effects of endoscopic surgery on sturgeon welfare can be amplified by cortisol, special attention should be paid to the potential effects of chronic stress on sturgeon in culture.
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Feeding and swimming can influence ion balance in fish. Therefore we investigated their impact on ionoregulation and its hormonal control in goldfish and common carp. As expected due to the osmorespiratory compromise, exhaustive swimming induced increases in gill Na⁺/K⁺ ATPase (NKA) activity in both species, resulting in stable levels of plasma ions. In contrast to our expectations, this only occurred in fed fish and feeding itself increased NKA activity, especially in carp. Fasting fish were able to maintain ion balance without increasing NKA activity, we propose that the increase in NKA activity is related to ammonia excretion rather than ion uptake per se. In goldfish, this increase in NKA activity coincided with a cortisol elevation whilst no significant change was found in carp. In goldfish, high conversion of plasma T₄ to T₃ was found in both fed and fasted fish resulting in low T₄/T₃ ratios, which increased slightly due to exhaustive swimming. In starved carp the conversion seemed much less efficient, and high T₄/T₃ ratios were observed. We propose that thyroid hormone regulation in carp was more related to its role in energy metabolism rather than ionoregulation. The present research showed that both species, whether fed or fasted, are able to sufficiently adapt their osmorepiratory strategy to minimise ions losses whilst maintaining gas exchange under exhaustive swimming.
Effects of long-term cortisol treatments on gonadal development, sex steroids levels and ovarian cortisol content in cultured great sturgeon Huso huso
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The objective of this study was to examine the effect of cortisol implantations on gonadal development, sex steroid levels, and ovarian cortisol content in cultured great sturgeon Huso huso. Three groups of 5 fish for each treatment were considered. The experimental groups included: control (capsules containing cocoa butter alone), low cortisol (C₅; 5 mg cortisol/kg body mass + cocoa butter) and, high cortisol (C₅₀; 50 mg cortisol/kg body mass + cocoa butter). The capsules containing hormones and cocoa butter were intraperitoneally implanted into 3-year-old female fish at pre-vitellogenic stage (mean initial body mass 6809.7 ± 73 g) every 6 weeks over a 6-month period from January to June. The serum levels of cortisol, glucose, cholesterol and sex steroids (testosterone and 17β-estradiol) were determined at the initial time and three weeks after each implantation. Oocyte histological characteristics (the diameter and area of the oocyte, the diameter and area of the nucleus and the ratio of the nucleus area to the oocyte area) were measured at the end of the experiment and compared to those at the initial time. Ovarian cortisol content was measured at the end of the experiment. The results showed that serum cortisol levels varied in a dose-independent manner, so that the highest cortisol concentrations were observed in C₅-treated fish throughout the experiment. Serum glucose levels were significantly higher in cortisol-treated groups than those in the control group. The high dose of cortisol elicited a significant constant increase in serum cholesterol concentrations. Fish implanted with the high cortisol dose showed significant declines in serum testosterone and 17β-estradiol concentrations throughout the experiment. No significant differences were found in oocyte histological characteristics among experimental groups. The cortisol implants elicited a dose-dependent increase in ovarian cortisol content. At the end of trial, body-growth indices were the lowest in C₅₀-implanted fish, while the low cortisol dose had no effect on growth relative to the controls. These results indicated that chronic stress induced by cortisol implantation in great sturgeon suppressed gonadal steroidogenesis and somatic growth but had no effect on ovarian growth and development.
Food deprivation induces chronic stress and affects thyroid hormone metabolism in Senegalese sole (Solea senegalensis) post-larvae
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In vertebrates, stress and thyroid systems interact closely, most likely because of the involvement of both systems in energy metabolism. However, studies on these interactions, especially during larval development, are scarce. Recently, cDNAs coding for corticotropin-releasing hormone (CRH) and CRH-binding protein (CRH-BP), two key players in the regulation of the neuroendocrine stress response, were characterized for the flatfish Senegalese sole (Solea senegalensis). To investigate the involvement of stress and thyroid systems in this species, the effects of food deprivation during early development of S. senegalensis were assessed. Growth was arrested in food-deprived post-larvae, which was also reflected by decreased carbon and nitrogen contents, indicating increased catabolism. Food deprivation induces chronic stress, as illustrated by enhanced whole-body cortisol levels, as well as an up regulation of crh and a decrease of crh-bp expression levels. Furthermore, whole-body total T3 concentrations of food-deprived post-larvae were reduced, although tshβ subunit expression levels remained unaffected. Our results show that food deprivation is a chronic stressor that induces energy-releasing catabolic processes that compensate for the reduced energy intake, and inhibits anabolic processes via the peripheral thyroid system.
The interruption of thyroid and interrenal and the inter-hormonal interference in fish: Does it promote physiologic adaptation or maladaptation?
2011, General and Comparative Endocrinology
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Similar negative interaction of thyroid with interrenal axes has been reported earlier for salmonids [104,96], though no correlation between thyroid activity and cortisol has been observed in rainbow trout [44,30] and mummichog [45]. In some studies the possibility of a rapid clearance of THs after cortisol treatment has been proposed [95,13]. For example, in brook trout, cortisol increased the hepatic conversion of T4 to T3 [95].
Endocrines, the chief components of chemical centers which produce hormones in tune with intrinsic and extrinsic clues, create a chemical bridge between the organism and the environment. In fishes also hormones integrate and modulate many physiologic functions and its synthesis, release, biological actions and metabolic clearance are well regulated. Consequently, thyroid hormones (THs) and cortisol, the products of thyroid and interrenal axes, have been identified for their common integrative actions on metabolic and osmotic functions in fish. On the other hand, many anthropogenic chemical substances, popularly known as endocrine disrupting chemicals, have been shown to disrupt the hormone–receptor signaling pathways in a number fish species. These chemicals which are known for their ability to induce endocrine disruption particularly on thyroid and interrenals can cause malfunction or maladaptation of many vital processes which are involved in the development, growth and reproduction in fish. On the contrary, evidence is presented that the endocrine interrupting agents (EIAs) can cause interruption of thyroid and interrenals, resulting in physiologic compensatory mechanisms which can be adaptive, though such hormonal interactions are less recognized in fishes. The EIAs of physical, chemical and biological origins can specifically interrupt and modify the hormonal interactions between THs and cortisol, resulting in specific patterns of inter-hormonal interference. The physiologic analysis of these inter-hormonal interruptions during acclimation and post-acclimation to intrinsic or extrinsic EIAs reveals that combinations of anti-hormonal, pro-hormonal or stati-hormonal interference may help the fish to fine-tune their metabolic and osmotic performances as part of physiologic adaptation. This novel hypothesis on the phenomenon of inter-hormonal interference and its consequent physiologic interference during thyroid and interrenal interruption thus forms the basis of physiologic acclimation. This interfering action of TH and cortisol during hormonal interruption may subsequently promote ecological adaptation in fish as these physiologic processes ultimately favor them to survive in their hostile environment.
The role of thyroid hormones in stress response of fish
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On the other hand, excess T3 has been shown to stimulate the interrenal tissue to produce more cortisol in freshwater tilapia [111] and perch (V.S. Peter, M.C.S. Peter, unpublished). This may lead to an increased clearance of T3 since there is evidence for cortisol-stimulated T3 clearance in European eels [136] and salmonids [135,168]. Brown and coworkers [19] report a similar interaction of cortisol with THs in rainbow trout.
Thyroxine (T₄) and triiodothyronine (T₃), the principal thyroid hormones (THs) secreted from the hypothalamic–pituitary–thyroid (HPT) axis, produce a plethora of physiologic actions in fish. The diverse actions of THs in fishes are primarily due to the sensitivity of thyroid axis to many physical, chemical and biological factors of both intrinsic and extrinsic origins. The regulation of THs homeostasis becomes more complex due to extrathyroidal deiodination pathways by which the delivery of biologically active T₃ to target cells has been controlled. As primary stress hormones and the end products of hypothalamic–pituitary–interrenal (HPI) and brain–sympathetic–chromaffin (BSC) axes, cortisol and adrenaline exert its actions on its target tissues where it promote and integrate osmotic and metabolic competence. Despite possessing specific osmoregulatory and metabolic actions at cellular and whole-body levels, THs may fine-tune these processes in accordance with the actions of hormones like cortisol and adrenaline. Evidences are presented that THs can modify the pattern and magnitude of stress response in fishes as it modifies either its own actions or the actions of stress hormones. In addition, multiple lines of evidence indicate that hypothalamic and pituitary hormones of thyroid and interrenal axes can interact with each other which in turn may regulate THs/cortisol-mediated actions. Even though it is hard to define these interactions, the magnitude of stress response in fish has been shown to be modified by the changes in the status of THs, pointing to its functional relationship with endocrine stress axes particularly with the interrenal axis. The fine-tuned mechanism that operates in fish during stressor-challenge drives the THs to play both fundamental and modulator roles in stress response by controlling osmoregulation and metabolic regulation. A major role of THs in stress response is thus evident in fish.

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Effect of cortisol on the in vitro hepatic conversion of thyroxine to triiodothyronine in brook charr (Salvelinus fontinalis Mitchill)

Abstract

Recent Progr. Horm. Res

Domest. Anim. Endocrinol

Gen. Comp. Endocrinol

Comp. Biochem. Physiol

Comp. Biochem. Physiol

Comp. Biochem. Physiol

Comp. Biochem. Physiol

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Gen. Comp. Endocrinol

Multiple effects of glucocorticoids on TSH secretion in unanesthetized rats

Endocrinology

Physical injury due to injections or blood removal causes transitory elevations of plasma thyroxine in rainbow trout Salmo gairdneri

Canad. J. Zool

Effects of dexamethasone on kinetics and distribution of triiodothyronine in the rat

Endocrinology

Pituitary-adrenal control of melanization in xanthic goldfish, Carassius auratus L

J. Exp. Zool

Effects of glucocorticoids on circulating concentrations of thyroxine (T4) and triiodothyronine (T3) and on peripheral monodeiodination in pre- and post-hatching chickens

Horm. Metabol. Res