The involvement of thyroid hormones and cortisol in the osmotic acclimation of Solea senegalensis

Abstract

The peripheral conversion of the prohormone 3,5,3',5'-tetraiodothyronine (T4) to the biologically active 3,5,3'-triiodothyronine (T3), via enzymatic deiodination by deiodinases, is an important pathway in thyroid hormone metabolism. The aim of this study was to test if thyroid hormones and cortisol, as well as the outer ring deiodination (ORD) metabolic pathway, are involved in the osmoregulatory response of Senegalese sole (Solea senegalensis, Kaup 1858). We measured osmoregulatory and endocrine parameters in immature juveniles S. senegalensis acclimated to seawater (SW, 38 per thousand) and that were transferred and allowed to acclimate to different salinities (5 per thousand, 15 per thousand, 38 per thousand and 55 per thousand) for 17 days. An adjustment and a chronic regulatory period were identified following acclimation. The adjustment period immediately follows the transfer, and is characterized by altered plasma osmolalities. During this period, plasma cortisol levels increased while plasma free T4 (fT4) levels decreased. Both hormones levels returned to normal values on day 3 post-transfer. In the adjustment period, renal and hepatic ORD activities had increased concomitantly with the decrease in plasma fT4 levels in fishes transferred to extreme salinities (5 per thousand and 55 per thousand). In the chronic regulatory period, where plasma osmolality returned to normal values, plasma cortisol had increased, whereas plasma fT4 levels decreased in animals that were transferred to salinities other than SW. No major changes were observed in branchial ORD activity throughout the experiment. The inverse relationship between plasma cortisol and fT4 suggests an interaction between these hormones during both osmoregulatory periods while ORD pathway can be important in the short-term adjustment period.

Effects of cortisol and thyroid hormone on peripheral outer ring deiodination and osmoregulatory parameters in the Senegalese sole (Solea senegalensis)

“…This work confirms and extends previous results (Arjona et al 2008), and provides evidence for the involvement of cortisol in the regulation of the ORD pathway in S. senegalensis in an organ-specific manner as well as in physiological processes related to the hydromineral balance.…”

“…The approximately eightfold increase in plasma cortisol levels following treatment with implants is within the physiological range, as it compares very well to the stressor-induced 4-to 40-fold increases observed in S. senegalensis and other teleost species (Woodward & Strange 1987, Goss & Wood 1988, van den Burg et al 2005, Arjona et al 2008. There are very few reports on the use of slow-release thyroid hormone implants in fishes.…”

“…The notion of intracellular actions of locally produced T 3 also helps explain why plasma fT 3 concentrations were unaltered by cortisol injection. Indeed, osmotic challenges changed peripheral ORD activities in S. senegalensis and Sparus auratus but did not result in altered plasma fT 3 levels (Klaren et al 2007b, Arjona et al 2008. In S. fontinalis, circulating T 4 and T 3 remained unaltered after a cortisol treatment that had increased hepatic T 4 -ORD activities (Vijayan et al 1988).…”

“…We used reverse T 3 (rT 3 , 3,3 0 ,5 0 -triiodothyronine) and T 4 as the preferred substrates for 5 0 -deiodinases (Mol et al 1998). The requirements of the rT 3 -ORD and T 4 -ORD reactions for dithiothreitol (DTT) in S. senegalensis have been determined previously (Arjona et al 2008(Arjona et al , 2010. As DTT inhibited ORD, it was excluded from the assay media.…”

“…Experimental results show that, following acclimation of S. senegalensis to different osmotic conditions, plasma cortisol and free T 4 (fT 4 ) concentrations change in a concerted manner, hinting at an interaction between the hypothalamus-pituitary-inter-renal (HPI) and the thyroidal axes (Arjona et al 2008). Moreover, during the adjustment period that follows the transfer to a different ambient osmolarity, renal and hepatic ORD activities are elevated, and plasma cortisol concentrations are increased (Arjona et al 2008).…”