Melatonin Modulates Secretion of Growth Hormone and Prolactin by Trout Pituitary Glands and Cells in Culture

Abstract

In Teleost fish, development, growth, and reproduction are influenced by the daily and seasonal variations of photoperiod and temperature. Early in vivo studies indicated the pineal gland mediates the effects of these external factors, most probably through the rhythmic production of melatonin. The present investigation was aimed at determining whether melatonin acts directly on the pituitary to control GH and prolactin (PRL) secretion in rainbow trout. We show that 2-[125I]-iodomelatonin, a melatonin analog, binds selectively to membrane preparations and tissue sections from trout pituitaries. The affinity was within the range of that found for the binding to brain microsomal preparations, but the number of binding sites was 20-fold less than in the brain. In culture, melatonin inhibited pituitary cAMP accumulation induced by forskolin, the adenyl cyclase stimulator. Forskolin also induced an increase in GH release, which was reduced in the presence of picomolar concentrations of melatonin. At higher concentrations, the effects of melatonin became stimulatory. In the absence of forskolin, melatonin induced a dose-dependent increase in GH release, and a dose-dependent decrease in PRL release. Melatonin effects were abolished upon addition of luzindole, a melatonin antagonist. Our results provide the first evidence that melatonin modulates GH and PRL secretion in Teleost fish pituitary. Melatonin effects on GH have never been reported in any vertebrate before. The effects result from a direct action of melatonin on pituitary cells. The complexity of the observed responses suggests several types of melatonin receptors might be involved.

Photoperiodic modulation of reproductive physiology and behaviour in the cichlid fish Cichlasoma dimerus

“…It was also shown that in C. dimerus LP males had significant higher pituitary levels of PRL (about 2-fold) than SP males. This is consistent with studies in Oncorhynchus mykiss where it was demonstrated that melatonin, strongly related to photoperiod, inhibits pituitary PRL secretion [34]. C. dimerus SP males had been in the dark for 16 hs/day, and this probably result in a higher release of melatonin that may be reducing pituitary prolactin content when compared to LP males that were just 10 hs/day in the dark.…”

Photoperiodic modulation of reproductive physiology and behaviour in the cichlid fish Cichlasoma dimerus

“…It was also shown that in C. dimerus LP males had significant higher pituitary levels of PRL (about 2-fold) than SP males. This is consistent with studies in Oncorhynchus mykiss where it was demonstrated that melatonin, strongly related to photoperiod, inhibits pituitary PRL secretion [34]. C. dimerus SP males had been in the dark for 16 hs/day, and this probably result in a higher release of melatonin that may be reducing pituitary prolactin content when compared to LP males that were just 10 hs/day in the dark.…”

Melatonin synthesis under calcium constraint in gilthead sea bream (Sparus auratus L.)

“…Clearly, our results indicate a positive correlation between a (presumedly) enhanced PRL activity in DSW and observed enhanced melatonin production. This in vivo result does not corroborate the observation by Falcon et al (2003) and suggests multivariable control; the increase in PRL in response to DSW exposure might over rule the inhibition of a PRL cell response to melatonin as observed in vitro.…”

Pituitary Hormones mRNA Abundance in the Mediterranean Sea Bass Dicentrarchus labrax: Seasonal Rhythms, Effects of Melatonin and Water Salinity

“…Also, more investigations are needed in order to determine whether the effects on mRNA are followed or not by effects at the level of the corresponding proteins for each of the hormones investigated. ( 5 ) The in vitro effects of melatonin depended on the month investigated as described before in trout ( Falcón et al, 2003 ); this is in line with previous in vivo studies investigating the effects of pinealectomy on fish reproduction ( Falcón et al, 2010 ; ViviD and Bentley, 2018 ). This highlights the necessity to run seasonal investigations when studying the effects of melatonin on neuroendocrine regulations, whether in vivo or in vitro .…”

“…The current study supports previous investigations indicating melatonin treatment impacts LH, GH, and PRL productions in fish (Khan and Thomas, 1996;Falcón et al, 2003), and extends to POMC, SL, FSH, and TSH the range of hormones affected. In most cases, the conclusions were supported by the observed effects of the melatonin receptor agonist S20304 and antagonist luzindole.…”

Photoperiodic modulation of reproductive physiology and behaviour in the cichlid fish Cichlasoma dimerus

“…It was also shown that in C. dimerus LP males had significant higher pituitary levels of PRL (about 2-fold) than SP males. This is consistent with studies in Oncorhynchus mykiss where it was demonstrated that melatonin, strongly related to photoperiod, inhibits pituitary PRL secretion [34]. C. dimerus SP males had been in the dark for 16 hs/day, and this probably result in a higher release of melatonin that may be reducing pituitary prolactin content when compared to LP males that were just 10 hs/day in the dark.…”

Melatonin synthesis under calcium constraint in gilthead sea bream (Sparus auratus L.)

“…Clearly, our results indicate a positive correlation between a (presumedly) enhanced PRL activity in DSW and observed enhanced melatonin production. This in vivo result does not corroborate the observation by Falcon et al (2003) and suggests multivariable control; the increase in PRL in response to DSW exposure might over rule the inhibition of a PRL cell response to melatonin as observed in vitro.…”

Pituitary Hormones mRNA Abundance in the Mediterranean Sea Bass Dicentrarchus labrax: Seasonal Rhythms, Effects of Melatonin and Water Salinity

“…Also, more investigations are needed in order to determine whether the effects on mRNA are followed or not by effects at the level of the corresponding proteins for each of the hormones investigated. ( 5 ) The in vitro effects of melatonin depended on the month investigated as described before in trout ( Falcón et al, 2003 ); this is in line with previous in vivo studies investigating the effects of pinealectomy on fish reproduction ( Falcón et al, 2010 ; ViviD and Bentley, 2018 ). This highlights the necessity to run seasonal investigations when studying the effects of melatonin on neuroendocrine regulations, whether in vivo or in vitro .…”

“…The current study supports previous investigations indicating melatonin treatment impacts LH, GH, and PRL productions in fish (Khan and Thomas, 1996;Falcón et al, 2003), and extends to POMC, SL, FSH, and TSH the range of hormones affected. In most cases, the conclusions were supported by the observed effects of the melatonin receptor agonist S20304 and antagonist luzindole.…”

Photoperiodic modulation of reproductive physiology and behaviour in the cichlid fish Cichlasoma dimerus

“…It was also shown that in C. dimerus LP males had significant higher pituitary levels of PRL (about 2-fold) than SP males. This is consistent with studies in Oncorhynchus mykiss where it was demonstrated that melatonin, strongly related to photoperiod, inhibits pituitary PRL secretion [34]. C. dimerus SP males had been in the dark for 16 hs/day, and this probably result in a higher release of melatonin that may be reducing pituitary prolactin content when compared to LP males that were just 10 hs/day in the dark.…”

Melatonin synthesis under calcium constraint in gilthead sea bream (Sparus auratus L.)

“…Clearly, our results indicate a positive correlation between a (presumedly) enhanced PRL activity in DSW and observed enhanced melatonin production. This in vivo result does not corroborate the observation by Falcon et al (2003) and suggests multivariable control; the increase in PRL in response to DSW exposure might over rule the inhibition of a PRL cell response to melatonin as observed in vitro.…”

Pituitary Hormones mRNA Abundance in the Mediterranean Sea Bass Dicentrarchus labrax: Seasonal Rhythms, Effects of Melatonin and Water Salinity

“…Also, more investigations are needed in order to determine whether the effects on mRNA are followed or not by effects at the level of the corresponding proteins for each of the hormones investigated. ( 5 ) The in vitro effects of melatonin depended on the month investigated as described before in trout ( Falcón et al, 2003 ); this is in line with previous in vivo studies investigating the effects of pinealectomy on fish reproduction ( Falcón et al, 2010 ; ViviD and Bentley, 2018 ). This highlights the necessity to run seasonal investigations when studying the effects of melatonin on neuroendocrine regulations, whether in vivo or in vitro .…”

“…The current study supports previous investigations indicating melatonin treatment impacts LH, GH, and PRL productions in fish (Khan and Thomas, 1996;Falcón et al, 2003), and extends to POMC, SL, FSH, and TSH the range of hormones affected. In most cases, the conclusions were supported by the observed effects of the melatonin receptor agonist S20304 and antagonist luzindole.…”