Changes in plasma thyroxine during smoltification of coho salmon, Oncorhynchus kisutch

doi:10.1016/0016-6480(78)90027-8

General and Comparative Endocrinology

Volume 36, Issue 2, October 1978, Pages 229-232

https://doi.org/10.1016/0016-6480(78)90027-8 Get rights and content

Abstract

Plasma thyroxine (T-4) levels of coho salmon at two different Columbia River hatcheries were measured by radioimmunoassay during the smoltification process. The T-4 concentration in plasma samples taken at 2-week intervals from late winter through spring showed a distinct peak. Basal levels (14 and 18 ng/ml) rose to as high as 65 and 91 ng/ml in mid-spring and subsequently returned to basal levels before summer solstice. The magnitude, duration and time of onset of the T-4 surge varied in the different stocks of coho salmon investigated. These results support the contention that the thyroid plays a role in regulation of salmon smoltification.

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Euryhaline fishes are capable of maintaining osmotic homeostasis in a wide range of environmental salinities. Several pleiotropic hormones, including prolactin, growth hormone, and thyroid hormones (THs) are mediators of salinity acclimation. It is unclear, however, the extent to which THs and the pituitary-thyroid axis promote the adaptive responses of key osmoregulatory organs to freshwater (FW) environments. In the current study, we characterized circulating thyroxine (T4) and 3-3’-5-triiodothyronine (T3) levels in parallel with the outer ring deiodination (ORD) activities of deiodinases (dios) and mRNA expression of dio1, dio2, and dio3 in gill during the acclimation of Mozambique tilapia (Oreochromis mossambicus) to FW. Tilapia transferred from seawater (SW) to FW exhibited reduced plasma T4 and T3 levels at 6 h. These reductions coincided with an increase in branchial dio2-like activity and decreased branchial dio1 gene expression. To assess whether dios respond to osmotic conditions and/or systemic signals, gill filaments were exposed to osmolalities ranging from 280 to 450 mOsm/kg in an in vitro incubation system. Gene expression of branchial dio1, dio2, and dio3 was not directly affected by extracellular osmotic conditions. Lastly, we observed that dio1 and dio2 expression was stimulated by thyroid-stimulating hormone in hypophysectomized tilapia, suggesting that branchial TH metabolism is regulated by systemic signals. Our collective findings suggest that THs are involved in the FW acclimation of Mozambique tilapia through their interactions with branchial deiodinases that modulate their activities in a key osmoregulatory organ.
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In plasma, thyroid hormone (TH) is bound to several TH distributor proteins (THDPs), constituting a TH delivery/distribution network. Extensive studies of THDPs from tetrapods has proposed an evolutionary scenario concerning structural and functional changes in THDPs, especially for transthyretin (TTR). When assessing, in an evolutionary context, the roles of THDPs as a component constituting part of the vertebrate thyroid system, the data from fish THDPs are critical. In this review the phylogenetic distributions, spatiotemporal expression patterns and binding properties of THDPs in fish are described, and the question of whether the evolutionary hypotheses proposed in tetrapod THDPs can be applied to fish THDPs is assessed. The phylogenetic distributions of THDPs are highly variable among fish groups. Analysis in this review reveals that the evolutionary hypotheses proposed in tetrapod THDPs cannot be applied to fish THDPs, and that the role of plasma lipoproteins as THDPs grows in importance in fish groups. In primitive fish, zinc is an import factor in TH binding to TTR, and high zinc content may facilitate the acquisition of high TH binding activity during the early evolution of TTR. Finally, the possible roles of THDPs in the vertebrate thyroid system are discussed.
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Temperature has unequivocal effects on several aspects of fish physiology, but the full extent of its interaction with key endocrine signaling systems to influence metabolic function remains unknown. The aim of the current study was to assess the individual and combined effects of elevated temperature and hyperthyroidism on hepatic metabolism in juvenile lake whitefish by quantifying mRNA abundance and activity of key metabolic enzymes. Fish were exposed to 13 (control), 17 or 21 °C for 0, 4, 8 or 24 days in the presence or absence of low-T₄ (1 µg × g body weight⁻¹) or high-T₄ (10 µg × g body weight⁻¹) treatment. Our results demonstrate moderate sensitivity to elevated temperature in this species, characterized by short-term changes in mRNA abundance of several metabolic enzymes and long-term declines in citrate synthase (CS) and cytochrome c oxidase (COX) activities. T₄-induced hyperthyroidism also had several short-term effects on mRNA abundance of metabolic transcripts, including depressions in acetyl-coA carboxylase β (accβ) and carnitine palmitoyltransferase 1β (cpt1β), and stabilization of cs mRNA levels; however, these effects were primarily limited to elevated temperature groups, indicating temperature-dependent effects of exogenous T₄ treatment in this species. In contrast, maximal CS and COX activities were not altered by hyperthyroidism at any temperature. Collectively, our data suggest that temperature has the potential to manipulate thyroid hormone physiology in juvenile lake whitefish and, under warm-conditions, hyperthyroidism may suppress certain elements of the β-oxidation pathway without substantial impacts on overall cellular oxidative capacity.
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Citation Excerpt :
Physiological functions of the lamprey TTR remain paradoxical. Post-embryonic transformations including salmonid smoltification (Dickhoff et al., 1978), amphibian metamorphosis (Leloup and Buscaglia, 1977) and hatching in reptiles (Shepherdley et al., 2002) take place in correlation with increases in plasma TH levels. The surge in THs correlated with increases in the transcript or protein levels of THDPs, such as TTR (Yamauchi et al., 1993; Richardson et al., 2005).
Transthyretin (TTR) is a plasma thyroid hormone (TH) binder that emerged from an ancient hydroxyisourate hydrolase by gene duplication. To know how an ancient TTR had high affinity for THs, molecular and TH binding properties of lamprey TTRs were investigated. In adult serum, the lipoprotein LAL was a major T3 binder with low affinity. Lamprey TTRs had an N-terminal histidine-rich segment, and had two classes of binding sites for 3,3′,5-triiodo-L-thyronine (T3): a high-affinity and a low-affinity site. Mutant TTRΔ_3-11, lacking the N-terminal histidine-rich segment, lost the high-affinity T3 binding site. [¹²⁵I]T3 binding to wild type TTR and mutant TTRΔ_3-11, was differentially modulated by Zn²⁺. Zn²⁺ contents of wild type TTR were 7–10/TTR (mol/mol). Our results demonstrate that lamprey TTR is a Zn²⁺-dependent T3 binder. The N-terminal histidine-rich segment may be essential for neo-functionalization (i.e., high-affinity T3 binding activity) of an ancient TTR after gene duplication.
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Thermal acclimation is known to elicit metabolic adjustments in ectotherms, but the cellular mechanisms and endocrine control of these shifts have not been fully elucidated. Here we examined the relationship between thermal acclimation, thyroid hormones and oxidative metabolism in juvenile lake whitefish. Impacts of thermal acclimation above (19 °C) or below (8 °C) the thermal optimum (13 °C) and exposure to exogenous thyroid hormone (60 µg T₄/g body weight) were assessed by quantifying citrate synthase and cytochrome c oxidase activities in liver, red muscle, white muscle and heart. Warm acclimation decreased citrate synthase activity in liver and elevated both citrate synthase and cytochrome c oxidase activities in red muscle. In contrast, induction of hyperthyroidism in warm-acclimated fish stimulated a significant increase in liver citrate synthase and heart cytochrome c oxidase activities, and a decrease in the activity of both enzymes in red muscle. No change in citrate synthase or cytochrome c oxidase activities was observed following cold acclimation in either the presence or absence of exogenous thyroid hormones. Collectively, our results indicate that thyroid hormones influence the activity of oxidative enzymes more strongly in warm-acclimated than in cold-acclimated lake whitefish, and they may play a role in mediating metabolic adjustments observed during thermal acclimation.
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The anadromous Atlantic salmon utilizes both fresh and salt water (FW and SW) habitats during its life cycle. The parr-smolt transformation (PST) is an important developmental transition from a FW adapted juvenile parr to a SW adapted smolt. Physiological changes in osmoregulatory tissues, particularly the gill, are key in maintaining effective ion regulation during PST. Changes are initiated prior to SW exposure (preparative phase), and are completed when smolts enter the sea (activational phase) where osmotic stress may directly stimulate changes in gene expression. In this paper we identify 4 nuclear factor of activated T cells (NFAT5, an osmotic stress transcription factor) paralogues in Atlantic salmon, which showed strong homology in characterized functional domains with those identified in other vertebrates. Two of the identified paralogues (NFAT5b1 and NFAT5b2) showed increased expression following transfer from FW to SW. This effect was largest in parr that were maintained under short day photoperiod, and showed the highest increases in chloride ion levels in response to SW exposure. The results of this study suggest that NFAT5 is involved in the osmotic stress response of Atlantic salmon.

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^☆: We acknowledge the assistance of W. S. Zaugg for collection of plasma samples and Ms. Jane Turnbull for T-4 RIA.

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General and Comparative Endocrinology

Abstract

References (13)

Measurement of l-thyroxine and 3, 5, 3′-triiodo-l-thyronine levels in fish plasma by radioimmunoassay

Canad. J. Zool

Effects of thyroxine and thiourea on the early development of Chum salmon (Oncorhynchus keta)

Canad. J. Zool

Physiological mechanisms in the migration of marine and amphihaline fish

Advan. Mar. Biol

Measurement of circulating thyroxine in several freshwater teleosts by competitive binding analysis

Canad. J. Zool

The thyroid gland of the Atlantic salmon

J. Morphol

Smolt transformation: Evolution, behavior and physiology

J. Fish. Res. Bd. Canad

Cited by (246)

Regulation of thyroid hormones and branchial iodothyronine deiodinases during freshwater acclimation in tilapia

Evolution of thyroid hormone distributor proteins in fish

Expression and activity of lipid and oxidative metabolism enzymes following elevated temperature exposure and thyroid hormone manipulation in juvenile lake whitefish (Coregonus clupeaformis)

Molecular and thyroid hormone binding properties of lamprey transthyretins: The role of an N-terminal histidine-rich segment in hormone binding with high affinity

Exogenous thyroid hormones regulate the activity of citrate synthase and cytochrome c oxidase in warm- but not cold-acclimated lake whitefish (Coregonus clupeaformis)

NFAT5 genes are part of the osmotic regulatory system in Atlantic salmon (Salmo salar)

Changes in plasma thyroxine during smoltification of coho salmon, Oncorhynchus kisutch☆

Abstract

Measurement of l-thyroxine and 3, 5, 3′-triiodo-l-thyronine levels in fish plasma by radioimmunoassay

Canad. J. Zool

Effects of thyroxine and thiourea on the early development of Chum salmon (Oncorhynchus keta)

Canad. J. Zool

Physiological mechanisms in the migration of marine and amphihaline fish

Advan. Mar. Biol

Measurement of circulating thyroxine in several freshwater teleosts by competitive binding analysis

Canad. J. Zool

The thyroid gland of the Atlantic salmon

J. Morphol

Smolt transformation: Evolution, behavior and physiology

J. Fish. Res. Bd. Canad