Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
Environmental salinity selectively modifies the outer-ring deiodinating activity of liver, kidney and gill in the rainbow trout
Introduction
Iodothyronine-specific genomic effects are mediated by T3, a hormone that is mainly derived from the extrathyroidal deiodination of T4 through the activating outer-ring deiodinating (ORD) pathway. This T4-activating route is catalyzed by two 5′-deiodinase enzymes, D1 and D2, which subserve the circulating and the local T3 pool, respectively. The inactivating inner-ring deiodinating (IRD) pathway is catalyzed by the enzyme 5′-deiodinase D3. These deiodination pathways and their corresponding regulation are organ-specific and depend mainly on three factors: the supply and availability of thyronines; the energy balance of the organism; and the interplay with certain neuroendocrine messengers (St. Germain and Galton, 1997, Köhrle, 1999).
We (Orozco et al., 1997) and others (Finnson et al., 1999) have shown that D1 and D2 are co-expressed in rainbow trout liver, which contrasts with the predominance of D1 in the liver of higher vertebrates. Fish liver is thus an excellent model in which to study ORD regulation. Studies aimed at analyzing the regulatory factors involved in the ORD pathway of fish are scarce and have assessed only total ORD hepatic activity (Cyr et al., 1988, Vijayan et al., 1988, De Luze et al., 1989, MacLatchy and Eales, 1990, Brown et al., 1991, Eales and Finnson, 1991, Sweeting and Eales, 1992a). However, we can use trout liver to study the possible differential regulation of the two hepatic ORD enzymes. One distinct aspect of fish physiology is the ability of euryhaline species to adapt to different environmental salinities. Equilibration of their internal milieu and the adaptation processes to the new environment involve a precise balance in which the coordinated interplay of a major portion of the neuroendocrine apparatus plays a pivotal role. Although scanty and confusing, the available data regarding the response of the thyroid gland to alterations in ambient salinity suggests a close interaction between iodothyronine bioactivity and osmotic balance in teleosts (Grau, 1987). Most of this information stems from studies in migratory salmon or in euryhaline fish exposed to acute changes in environmental salinity, and the effects of mild salinity changes which could naturally occur within a body of water have not been analyzed. Here we report the effect of a mild change in environmental salinity (5‰) on rainbow trout thyroidal status, analyzing circulating levels of T4, T3 and cortisol and the possible differential response of hepatic D1 and D2 activities, as well as branchial and renal D1.
Section snippets
Reagents
Non-radioactive iodothyronines were obtained from Henning Co. (Berlin, Germany). Outer ring [125I]-labeled T4, T3 and rT3 (sp. act. 1200, 1250 and 1174 μCi/μg, respectively) and [3H]Cortisol (sp.act. 70 Ci/mmol) were purchased from New England Nuclear (Boston, MA, USA). Non-radioactive corticosterone, propyl-2-thiouracil (PTU), 8-anilio-1-naphthalene sulfonic acid (ANS), 2,5-diphenyloxazole (PPO), diethylaminoethyl cellulose (DEAE Cellulose) and second antibody (anti-rabbit IgG) were obtained
Kidney
Protein-, time-, temperature- and pH dependencies were defined using [125I]rT3 as substrate. Enzyme activity was linear between 80 and 350 μg of protein per reaction mixture and optimal pH was 7. Optimal rates of deiodination were obtained at 23–25 °C and incubating for 1 h. This incubation time falls within the linear range of the curve (data not shown). Based on these results and using a wide range of rT3 concentrations (0.5–1000 nM), we examined substrate kinetics using high DTT
Discussion
A mild change in environmental salinity in rainbow trout, a freshwater-adapted osmoregulator, elicits significant and sustained changes in circulating levels of iodothyronines and cortisol, as well as in renal D1 and hepatic D2 activities. These findings are in accordance with the role played by TH in hydro-osmotic balance in vertebrates (Grau, 1987), and add further support to the notion of a close interaction between iodothyronine bioactivity and osmoregulation in teleosts.
Historically, the
Acknowledgements
We gratefully acknowledge Dr Jose Luis Arredondo for providing and maintaining the fish at the ‘Planta Dulceaquı́cola-UAM-I’. We also express our gratitude to Carlos Romero for measuring cortisol levels; Maria de Lourdes Lara Ayala for her technical assistance, and Dr Howard Bern and Dr Michael Jeziorski for critically reading the manuscript. This work was partially supported by grant UNAM-PAPIIT IN227599 and CONACYT 34311N.
References (36)
- et al.
Cortisol and osmotic adjustment in the euryhaline teleost Sarotherodon mossambicus
Gen. Comp. Endocrinol.
(1981) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding
Anal. Biochem.
(1976)- et al.
Effects of cortisol on aspects of 3,5,3′-triiodo-l-thyronine metabolism in rainbow trout Oncorhynchus mykiss
Gen. Comp. Endocrinol.
(1991) - et al.
The influence of short term 17-Estradiol treatment on plasma T3 levels and in vitro hepatic T4 5′-monodeiodinase activity in immature rainbow trout, Salmo gairdneri
Gen. Comp. Endocrinol.
(1988) - et al.
Effects of vertebrate prolactines and growth hormones on thyroxine 5′-monodeiodination in the eel (Anguilla anguilla): a potential bioassay for growth hormones
Gen. Comp. Endocrinol.
(1989) - et al.
Changes in plasma thyroxine during smoltification of coho salmon, Oncorhynchus kisutch
Gen. Comp. Endocrinol.
(1978) - et al.
Deiodination and conjugation of thyroid hormone conjugates and type I deiodination in liver of rainbow trout, Oncorhynchus mykiss
Gen. Comp. Endocrinol.
(1999) - et al.
Effect of T3 treatment and food ration on hepatic deiodination and conjugation of thyroid hormones in rainbow trout, Oncorhynchus mykiss
Gen. Comp. Endocrinol.
(1999) - et al.
The role of the thyroid gland in osmotic and ionic regulation in Fundulus heteroclitus acclimated to freshwater and seawater
Comp. Biochem. Physiol.
(1982) Local activation and inactivation of thyroid hormones: the deiodinase family
Mol. Cell. Endocrinol.
(1999)
The interrelationship of cortisol, gill (Na+K) ATPase, and homeostasis during the parr-smolt transformation of Atlantic salmon (Salmo salar L)
Gen. Comp. Endocrinol.
Growth hormone stimulates hepatic thyroxine 5′ monodeiodinase activity and 3,5,3′-triiodothyronine levels in rainbow trout (Salmo gairdneri)
Gen. Comp. Endocrinol.
Thyroid function in male killifish, Fundulus heteroclitus, adapted to high and low temperatures and to freshwater and seawater
Comp. Biochem. Physiol.
Thyroid hormone deiodination in brain, gill, heart and muscle of Atlantic salmon (Salmo salar) during photoperiodically-induced parr-smolt transformation. I. Outer-and inner-ring thyroxine deiodination
Gen. Comp. Endocrinol.
The effect of 3,5,3′-triiodo-l-thyronine on gill Na+K+ATPase of rainbow trout Salmo gairdneri, in fresh water
Comp. Biochem. Physiol.
Kinetic characterization of outer-ring deiodinase activity (ORD) in the liver, gill and retina of Fundulus heteroclitus
Comp. Biochem. Physiol.
Smoltification and seawater adaptation in Atlantic salmon (Salmo salar): plasma prolactin, growth hormone, and thyroid hormones
Gen. Comp. Endocrinol.
Cortisol and its effects on plasma thyroid hormone and electrolyte concentrations in fresh water and during seawater acclimatation in yealing coho salmon, Oncorhynchus kisutch
Gen. Comp. Endocrinol.
Cited by (44)
Maternal exposure to dietary uranium causes oxidative stress and thyroid disruption in zebrafish offspring
2023, Ecotoxicology and Environmental SafetyToxicity in Takifugu rubripes exposed to acute ammonia: Effects on immune responses, brain neurotransmitter levels, and thyroid endocrine hormones
2022, Ecotoxicology and Environmental SafetyRegulation of thyroid hormones and branchial iodothyronine deiodinases during freshwater acclimation in tilapia
2021, Molecular and Cellular EndocrinologyWaterborne uranium causes toxic effect and thyroid disruption in zebrafish larvae
2021, Ecotoxicology and Environmental SafetyToxicokinetics and persistent thyroid hormone disrupting effects of chronic developmental exposure to chlorinated polyfluorinated ether sulfonate in Chinese rare minnow
2020, Environmental PollutionCitation Excerpt :Downregulation of Dio1 and Dio2 genes in the juvenile fish also reflected a negative feedback in response to increased T3 and fT3 levels (Fig. 3) caused by Cl-PFESAs exposure. In fish, deiodinase enzymes, Dio1 and Dio2, convert T4 into biologically active T3 (Orozco et al., 2002). Dio1 plays a minimal role in the maintenance of THs homeostasis, while it is important in the iodine recovery and THs degradation (Geyten et al., 2001).