Abstract
Fish are ectotherm, which rely on the external temperature to regulate their internal body temperature, although some may perform partial endothermy. Together with photoperiod, temperature oscillations, contribute to synchronizing the daily and seasonal variations of fish metabolism, physiology and behavior. Recent studies are shedding light on the mechanisms of temperature sensing and behavioral thermoregulation in fish. In particular, the role of some members of the transient receptor potential channels (TRP) is being gradually unraveled. The present study in the migratory Atlantic salmon, Salmo salar, aims at identifying the tissue distribution and abundance in mRNA corresponding to the TRP of the vanilloid subfamilies, TRPV1 and TRPV4, and at characterizing their putative role in the control of the temperature-dependent modulation of melatonin production—the time-keeping hormone—by the pineal gland. In Salmo salar, TRPV1 and TRPV4 mRNA tissue distribution appeared ubiquitous; mRNA abundance varied as a function of the month investigated. In situ hybridization and immunohistochemistry indicated specific labeling located in the photoreceptor cells of the pineal gland and the retina. Additionally, TRPV analogs modulated the production of melatonin by isolated pineal glands in culture. The TRPV1 agonist induced an inhibitory response at high concentrations, while evoking a bell-shaped response (stimulatory at low, and inhibitory at high, concentrations) when added with an antagonist. The TRPV4 agonist was stimulatory at the highest concentration used. Altogether, the present results agree with the known widespread distribution and role of TRPV1 and TRPV4 channels, and with published data on trout (Oncorhynchus mykiss), leading to suggest these channels mediate the effects of temperature on S. salar pineal melatonin production. We discuss their involvement in controlling the timing of daily and seasonal events in this migratory species, in the context of an increasing warming of water temperatures.
Highlights
In ectotherms, metabolism, physiology and behavior rely on the external temperature (Angilletta et al, 2002; Storey and Tanino, 2012; Salin et al, 2016)
TRPV1 mRNA abundance was high in the kidney, spleen and blood cells at both months investigated, while TRPV4 mRNA was abundant in the gills (February and July), adipose fin and heart (February only)
The present study in the Atlantic salmon brings novel information concerning the distribution of the thermo-sensitive TRPV1 and TRPV4 channels, in the photosensitive pineal gland and retina
Summary
Metabolism, physiology and behavior rely on the external temperature (Angilletta et al, 2002; Storey and Tanino, 2012; Salin et al, 2016). In response to the alternation of light (L) and darkness (D) of the 24 h LD cycle, the pineal photoreceptor cells produce two messengers: (i) an excitatory neurotransmitter (glutamate) released at the synaptic junctions established with neurons that project in different brain centers (Meissl et al, 1986); (ii) a neurohormone—melatonin—released into the blood stream and cerebrospinal fluid (CSF) (Falcón, 1999; Falcón et al, 2007) Both messengers are produced in higher amounts at night than during day, and both are modulated by the external temperature (Zachmann et al, 1992; Tabata and Meissl, 1993; Tabata et al, 1993; Thibault et al, 1993)
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