Abstract
The hormone melatonin connects environmental cues, such as photoperiod and temperature, with a number of physiological and behavioural processes, including seasonal reproduction, through binding to their cognate receptors. This study reports the structural, functional and physiological characterization of five high-affinity melatonin receptors (Mtnr1aaα, Mtnr1aaβ, Mtnr1ab, Mtnr1al, Mtnr1b) in Atlantic salmon. Phylogenetic analysis clustered salmon melatonin receptors into three monophyletic groups, Mtnr1A, Mtnr1Al and Mtnr1B, but no functional representative of the Mtnr1C group. Contrary to previous studies in vertebrates, pharmacological characterization of four receptors in COS-7, CHO and SH-SY5Y cell lines (Mtnr1Aaα, Mtnr1Aaβ, Mtnr1Ab, Mtnr1B) showed induction of intracellular cAMP levels following 2-iodomelatonin or melatonin exposure. No consistent response was measured after N-acetyl-serotonin or serotonin exposure. Melatonin receptor genes were expressed at all levels of the hypothalamo-pituitary-gonad axis, with three genes (mtnr1aaβ, mtnr1ab and mtnr1b) detected in the pituitary. Pituitary receptors displayed daily fluctuations in mRNA levels during spring, prior to the onset of gonadal maturation, but not in autumn, strongly implying a direct involvement of melatonin in seasonal processes regulated by the pituitary. To the best of our knowledge, this is the first report of cAMP induction mediated via melatonin receptors in a teleost species.
Highlights
Melatonin is a highly conserved neurohormone produced in vertebrates by the pineal gland and retina, as well as a number of peripheral tissues, notably the gastrointestinal tract.[1,2] In all organisms, circulating melatonin levels show a pronounced diurnal rhythm, being high during the night and low during the day; in teleost fishes, the nocturnal rise in plasma melatonin is clearly a function of pineal production.[3]
Comparison of deduced amino acid sequences with the human Mtnr1A and Mtnr1B reveals that the five putatively functional salmon Mtnr possesses the characteristic features of melatonin receptors, including seven transmembrane domains (TM) with the typical NRY and NAXXY motifs and conserved residues interacting with G‐protein in the TM3 (Figures S2‐S4)
The three mntr expressed in the pituitary of male Atlantic salmon parr showed no significant differences in transcript levels between maturing and nonmaturing salmon during the initial stages of sexual maturation (Figure 5A‐C; Figure S12)
Summary
Melatonin is a highly conserved neurohormone produced in vertebrates by the pineal gland and retina, as well as a number of peripheral tissues, notably the gastrointestinal tract.[1,2] In all organisms, circulating melatonin levels show a pronounced diurnal rhythm, being high during the night and low during the day; in teleost fishes, the nocturnal rise in plasma melatonin is clearly a function of pineal production.[3]. In the Senegalese sole (Solea senegalensis), mtnr1a and mtnr1b display circannual fluctuations in pituitary expression levels, with higher expression towards the end of the spawning season in June than in the rest of the season.[23] Other studies have reported circadian fluctuations in Mtnr gene expression, peaking either during the daytime or during the night depending on tissue, species and gene. To understand further the effect of melatonin on pituitary cells, the gonadotrope cells controlling gonadal maturation, we have characterized five functional Mtnr genes in Atlantic salmon; three paralogs of the Mtnr1A sub‐group and single genes of the Mtnr1Al and Mtnr1B sub‐groups. The three Mtnr genes expressed in the salmon pituitary (mtnr1aaβ, mtnr1ab and mtnr1b), all display daily fluctuations in expression levels in springtime, just prior to initiation of gonadal maturation, but not in the autumn
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