Stress inhibition of melatonin synthesis in the pineal organ of rainbow trout (Oncorhynchus mykiss) is mediated by cortisol.

Abstract

Summary Cortisol has been suggested to mediate the effect of stress on pineal melatonin synthesis in fish. Therefore, we aimed to determine how pineal melatonin synthesis is affected by exposing rainbow trout to different stressors, such as hypoxia, chasing and high stocking density. In addition, to test the hypothesis of cortisol as mediator of such stress-induced effects, a set of animals were IP implanted with coconut oil alone or containing cortisol (50 mg.kg-1 bw) and sampled 5 h or 48 h post injection at mid-day and mid-night. The specificity of such effect was also assessed in cultured pineal organs exposed to cortisol alone or with the general glucocorticoid receptor antagonist, mifepristone (RU486). The patterns of plasma and pineal organ melatonin content displaying highest values at night were affected by stressors (in particular chasing and high stocking density), resulting in decreased plasma and pineal organ melatonin content in both time periods, but with the most robust effect being found at night. The decrease in nocturnal melatonin levels in the pineal organ of stressed fish was accompanied by increased serotonin content and decreased AANAT2 enzymatic activity and mRNA abundance. Similar effects on pineal melatonin synthesis to those elicited by stress were observed in trout implanted with cortisol for either 5 h or 48 h. These data indicate that stress influences negatively the synthesis of melatonin in the pineal organ, thus attenuating the day-night variations of circulating melatonin. The effect might be be mediated by increased cortisol levels which bind to trout pineal organ specific glucocorticoid receptors to modulate melatonin rhythms. Our results in cultured pineal organs are on its support. Considering the relevant role of melatonin conveying photoperiodical information to the synchronization of daily and annual rhythms, the results suggest that stress-induced alterations in melatonin synthesis could affect the availability of fish to integrate rhythmic environmental information.