The influence of stress on thyroid hormone production and peripheral deiodination in the Nile tilapia (Oreochromis niloticus)
Introduction
The primary thyroid hormone (TH) synthesized by the thyroid in teleost fish, as in other vertebrates, is l-thyroxine (T4). Ultimately, most T4 is converted enzymatically to active or inactive derivatives in extrathyroidal tissues. Outer ring deiodination (ORD) removes an iodine from the T4 phenolic ring, thereby creating the receptor-active 3,5,3′-triiodo-l-thyronine (T3). Alternatively, inner ring deiodination (IRD) removes an iodine from the tyrosyl ring to form the receptor-inactive 3,3′, 5′-triiodo-l-thyronine (rT3). T3 itself can be further degraded to inactive 3,3′-diiodo-l-thyronine (T2) through IRD. These ORD and IRD pathways contribute to the regulation of thyroidal status by adjusting T3 availability in plasma and tissues. As in mammals, thyroid hormone deiodination in fish is catalyzed by at least three iodothyronine deiodinases: D1, D2 and D3, that in general have similar biochemical properties as their mammalian counterparts (Byamungu et al., 1990, Leatherland et al., 1990, Mol et al., 1997, Mol et al., 1998, Orozco et al., 2002, Orozco et al., 2003, Sanders et al., 1997, Sanders et al., 1999, Van der Geyten et al., 1998).
Glucocorticoids, predominantly secreted as a response to stress (Harvey et al., 1984), have been demonstrated to affect thyroid function by interacting at both the central and peripheral level in mammals and birds (Decuypere et al., 1983, Kaplan, 1986, Kühn et al., 1998). Stress responses in fish have many similarities to those of other vertebrates (Barton and Iwama, 1991, Wendelaar Bonga, 1997), and thus are probably equally important in regulating thyroid economy in teleost fish. There is, however, surprisingly limited data available concerning the interaction of glucocorticoids with thyroid hormone production and peripheral deiodination in fish. A chronic pharmacological dose of cortisol (50 μg/kg) increased plasma T4 concentrations in rainbow trout (Oncorhynchus mykiss) whereas plasma T3 levels tended to decrease (Milne and Leatherland, 1980). In contrast, Redding and co-workers (1986) demonstrated that a single intravenous injection of cortisol hemisuccinate (15–150 μg/kg) in European eel (Anguilla anguilla) decreased plasma concentrations of T3 and T4 in a dose-dependent manner, without affecting plasma T4 clearance, but increasing plasma T3 clearance. These data suggest that cortisol under these conditions decreased thyroid hormone production and increased T3 degradation. However, in contrast to the above findings, long term (56 days) intraperitoneal implantation of cortisol (50 μg/kg) in a medium of hydrogenated coconut oil had no effect on plasma T4 and T3 concentrations in brook charr (Salvelinus fontinalis), although the T4 to T3 conversion had significantly increased (Vijayan et al., 1988). This discrepancy could only be explained by assuming that under these conditions the clearance of T3 from plasma had increased, which is in agreement with the data obtained in eel (Redding et al., 1986). Intraperitoneal implantation of cortisol (10–25 mg/kg) in hydrogenated corn oil caused a significant decrease in plasma T3 that was again accompanied by an increase in T3 clearance rate in rainbow trout (O. mykiss) without affecting the T4 levels and hepatic monodeiodinase activity, thereby suggesting that chronic physiological levels of cortisol enhance plasma T3 clearance while having no effect on T4 production and hepatic conversion into T3 (Brown et al., 1991).
In summary, all the available data on the effects of glucocorticoids on plasma thyroid hormone levels and peripheral deiodination in fish so far do not allow to formulate any clear cut conclusions. Although it appears that exposure to glucocorticoids tends to decrease plasma T3 levels, changes in plasma T4 levels are more variable. Furthermore, so far, insufficient data are available to allow any speculations about the role of the iodothyronine deiodinases in this scheme. The goal of the present study was therefore to investigate the effects of a single injection of a long acting synthetic glucocorticoid—dexamethasone—on circulating TH levels and on peripheral thyroid hormone metabolism in Nile tilapia (Oreochromis niloticus). To take into account the effect of handling stress, this treatment was compared both to a non-treated and to a saline injected group. The Nile tilapia was chosen as an experimental model, because in the last decade it has become one of the most extensively studied fish species in the field of thyroid physiology, especially when it comes to elucidating the function and regulation of iodothyronine deiodinases in fish (Orozco and Valverde, 2005).
Section snippets
Experimental design
Nile tilapia (O. niloticus) were obtained from a commercial fish farm (Maryn Donkers, Boerdonk, The Netherlands). One hundred and forty fishes with a mean weight of 290 ± 20 g were randomly distributed over seven tanks and were acclimatized for 2 weeks in the laboratory in 200-l white fiberglass tanks supplied with aerated running tap water of 25 ± 0.5 °C (flow rate: 1.1 l/min). Light–dark regime was 12/12 h. The fish were fed ad libitum with commercial tilapia pellets (Tilapia TI-3 feed, Skretting.
Results
Table 2 shows the F and p values of the two-way ANOVA analysis of all parameters for non-treated, saline and DEX injected fish.
Discussion
The present study clearly demonstrates that in Nile tilapia, the administration of 25 μg DEX per 100 g body weight can acutely reduce plasma T3 concentrations. These finding are in agreement with previous studies done in yearling coho salmon (Oncorhynchus kisutch) and European eel (A. anguilla) where cortisol injection decreased plasma T3 levels (Redding et al., 1984, Redding et al., 1986). Similar results were also obtained in rainbow trout (O. mykiss) using cortisol implants (Brown et al., 1991
Acknowledgments
We wish to thank L. Noterdaeme, W. Van Ham and F. Voets for their technical assistance during the experiment. This study was supported by the FWO Grant G.0272.04. C.N. Walpita was supported by an IRO scholarship from the KU Leuven and the Flemish Interuniversity Council (VLIR). Serge Van der Geyten was supported by the Fund for Scientific Research—Flanders. The authors declare that there is no conflict of interests that would prejudice the impartiality of this scientific work.
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