Diurnal and Circadian Oscillations in Expression of Kisspeptin, Kisspeptin Receptor and Gonadotrophin‐Releasing Hormone 2 Genes in the Grass Puffer, A Semilunar‐Synchronised Spawner

Abstract

In seasonally breeding animals, the circadian and photoperiodic regulation of neuroendocrine system is important for precisely-timed reproduction. Kisspeptin, encoded by the Kiss1 gene, acts as a principal positive regulator of the reproductive axis by stimulating gonadotrophin-releasing hormone (GnRH) neurone activity in vertebrates. However, the precise mechanisms underlying the cyclic regulation of the kisspeptin neuroendocrine system remain largely unknown. The grass puffer, Takifugu niphobles, exhibits a unique spawning rhythm: spawning occurs 1.5-2 h before high tide on the day of spring tide every 2 weeks, and the spawning rhythm is connected to circadian and lunar-/tide-related clock mechanisms. The grass puffer has only one kisspeptin gene (kiss2), which is expressed in a single neural population in the preoptic area (POA), and has one kisspeptin receptor gene (kiss2r), which is expressed in the POA and the nucleus dorsomedialis thalami. Both kiss2 and kiss2r show diurnal variations in expression levels, with a peak at Zeitgeber time (ZT) 6 (middle of day time) under the light/dark conditions. They also show circadian expression with a peak at circadian time 15 (beginning of subjective night-time) under constant darkness. The synchronous and diurnal oscillations of kiss2 and kiss2r expression suggest that the action of Kiss2 in the diencephalon is highly dependent on time. Moreover, midbrain GnRH2 gene (gnrh2) but not GnRH1 or GnRH3 genes show a unique semidiurnal oscillation with two peaks at ZT6 and ZT18 within a day. The cyclic expression of kiss2, kiss2r and gnrh2 may be important in the control of the precisely-timed diurnal and semilunar spawning rhythm of the grass puffer, possibly through the circadian clock and melatonin, which may transmit the photoperiodic information of daylight and moonlight to the reproductive neuroendocrine centre in the hypothalamus.

Seasonal Changes of Serum Gonadotropins and Testosterone in Men Revealed by a Large Data Set of Real-World Observations Over Nine Years

“…On the contrary, LH seasonality seems to be independent from environment, and a central mechanism, possibly regulating seasonal fluctuations of the hypothalamic gonadotropin-releasing hormone (GnRH), might be involved. It is well-known that LH secretion is the result of GnRH pulsatility, regulated by hypothalamic clock genes from one side (22) and pulsatile secretion of Kisspeptin on the other side (23), which is the main regulatory mechanism of GnRH secretion in vertebrates (24,25). In seasonally breeding animals, the circadian and photoperiodic regulation of the neuroendocrine system is largely demonstrated to modulate diurnal and semilunar spawning rhythm (23).…”

“…It is well-known that LH secretion is the result of GnRH pulsatility, regulated by hypothalamic clock genes from one side (22) and pulsatile secretion of Kisspeptin on the other side (23), which is the main regulatory mechanism of GnRH secretion in vertebrates (24,25). In seasonally breeding animals, the circadian and photoperiodic regulation of the neuroendocrine system is largely demonstrated to modulate diurnal and semilunar spawning rhythm (23). Similarly, a complex regulation of hormonal seasonality, involving the pineal pulse generator, is suggested in humans (26).…”

Corazonin signaling integrates energy homeostasis and lunar phase to regulate aspects of growth and sexual maturation in Platynereis

“…timing of semilunar/lunar synchronized spawners (19)(20)(21)(22)(23). However, this evidence is at present correlational.…”

Ultradian oscillation in expression of four melatonin receptor subtype genes in the pineal gland of the grass puffer, a semilunar-synchronized spawner, under constant darkness

“…This might be due to effects on melatonin receptor gene expression of some other environmental and internal conditions, such as water temperature, nutrition, sexual maturation, and infection (immune response) (Pandi-Perumal et al, 2006 ; Falcón et al, 2010 ). Nevertheless, it is of considerable interest to note that in the grass puffer diencephalon, kiss2 / kiss2r and lpxrfa / lpxrfa-r also showed daily and mostly synchronized oscillations (Shahjahan et al, 2011 ; Ando et al, 2014 ). These results suggest that the reproductive neuroendocrine activity may be cyclic within a day under the control of melatonin signals directly or indirectly via circadian clock in the pineal gland (Ando et al, 2013 , 2014 ).…”

“…In the diencephalon, all four melatonin receptor subtype genes are synchronously expressed with daily and circadian variations under light/dark (LD) and constant darkness (DD) conditions, respectively (Ikegami et al, 2009b ). In addition, not only kisspeptin ( kiss2 ) and its receptor ( kiss2r ) genes but also LPXRFamide peptide gene ( lpxrfa ), fish ortholog of GnIH gene, and its receptor ( lpxrfa-r ) gene clearly showed daily and circadian oscillations in expression, and their expression patterns are almost synchronized with each other (Shahjahan et al, 2011 ; Ando et al, 2014 ). These results indicate that melatonin signals are highly dependent on light/dark cycle in the diencephalon, and melatonin may have an important role in the cyclic expressions of kiss2 / kiss2r and lpxrfa / lpxrfa-r in the grass puffer.…”