Influence of light and food on the circadian clock in liver of rainbow trout, Oncorhynchus mykiss

Abstract

Several reports support the existence of multiple peripheral oscillators in fish, which may be able to modulate the rhythmic functions developed by those tissues hosting them. Thus, a circadian oscillator has been proposed to be located within fish liver. In this vertebrate group, the role played by the circadian system in regulating metabolic processes in liver is mostly unknown. We, therefore investigated the liver of rainbow trout (Oncorhynchus mykiss) as a potential element participating in the regulation of circadian rhythms in fish by hosting a functional circadian oscillator. The presence and expression pattern of main components of the circadian molecular machinery (clock1a, bmal1, per1 and rev-erbβ-like) were assessed. Furthermore, the role of environmental cues such as light and food, and their interaction in order to modulate the circadian oscillator was also assessed by exposing animals to constant conditions (absence of light for 48 h, and/or a 4 days fasting period). Our results demonstrate the existence of a functional circadian oscillator within trout liver, as demonstrated by significant rhythms of all clock genes assessed, independently of the environmental conditions studied. In addition, the daily profile of mRNA abundance of clock genes is influenced by both light (mainly clock1a and per1) and food (rev-erbβ-like), which is indicative of an interaction between both synchronizers. Our results point to rev-erbβ-like as possible mediator between the influence of light and food on the circadian oscillator within trout liver, since its daily profile is influenced by both light and food, thus affecting that of bmal1.

Influence of Stress on Liver Circadian Physiology. A Study in Rainbow Trout, Oncorhynchus mykiss, as Fish Model

“…With respect to lipids metabolism within the liver of rainbow trout, daily variations of mRNA abundance are observed for fas and hoad , but the respective enzyme activities do not display such oscillation. This is in agreement with our previous data describing daily rhythms of lipid metabolism-related parameter in liver of the same species (Hernández-Pérez et al, 2015, 2017), thus with the control exerted by a circadian oscillator. Stress exposure results in altered enzyme activities, but also in a change of the rhythm of fas abundance.…”

“…Daily rhythms of enzyme activity and mRNA abundance are observed in most of the carbohydrate metabolism-related parameters within the liver of non-stressed trout. These rhythms are reported to be under circadian control in trout liver (Hernández-Pérez et al, 2015, 2017). Stress affects the daily oscillation of enzyme activities in a way that the amplitude of most of them decreases (GK, PK) and even disappears (PEPCK).…”

“…In addition to hypothalamus in fish, retina and pineal organ also host circadian oscillators, since both tissues are photosensitive, clock genes express rhythmically within them, and release an endocrine output, such as the melatonin (Falcón, 1999; Falcón et al, 2007). In the same way than that of mammals, clock genes rhythmically express in peripheral tissues of non-mammalian vertebrates, such as liver, heart, intestine, and muscle of birds (Chong et al, 2003), liver, heart, muscle, lung, and testis of reptiles (Della Ragione et al, 2005; Vallone et al, 2007), and liver, heart, spleen, and gall bladder of fish (Kaneko et al, 2006; Velarde et al, 2009; Betancor et al, 2014; Hernández-Pérez et al, 2017).…”

“…One of the peripheral locations described for the circadian system is the liver. In fish, some reports describe rhythmic expression of clock genes within this tissue in different species such as goldfish ( per and cry , Velarde et al, 2009), Atlantic salmon ( bmal1 , Betancor et al, 2014) and rainbow trout ( clock, bmal1, per and rev-erbβ , Hernández-Pérez et al, 2017). Interestingly, such rhythms perfectly fit with those of metabolism-related parameters within this peripheral location (Polakof et al, 2007; Betancor et al, 2014; Paredes et al, 2014; Hernández-Pérez et al, 2015).…”

“…In this way, goldfish receiving a cortisol administration display similar results than those observed in mammals, with inhibited expression of some clock genes within the liver (Sánchez-Bretaño et al, 2015). However, no evidence exists relative to how stress affects rhythmic physiology within this tissue in this vertebrate group, but recent results indicate altered metabolism-related parameters within rainbow trout liver following acute stress (López-Patiño et al, 2014b), where a circadian oscillator has been reported to exist in the same species (Hernández-Pérez et al, 2015, 2017).…”