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

Taro Ikegami; Yusuke Maruyama; Hiroyuki Doi; Atsuhiko Hattori; Hironori Ando

doi:10.3389/fnins.2015.00009

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

Front Neurosci. 2015 Jan 30:9:9. doi: 10.3389/fnins.2015.00009. eCollection 2015.

Authors

Taro Ikegami¹, Yusuke Maruyama², Hiroyuki Doi³, Atsuhiko Hattori², Hironori Ando⁴

Affiliations

¹ Department of Chemistry, Biology, and Marine Science, Faculty of Science, University of the Ryukyus Okinawa, Japan.
² Department of Biology, College of Liberal Arts and Sciences, Tokyo Medical and Dental University Ichikawa, Japan.
³ Shimonoseki Marine Science Museum "Kaikyokan," Shimonoseki Academy of Marine Science Yamaguchi, Japan.
⁴ Sado Marine Biological Station, Faculty of Science, Niigata University Sado, Japan.

Abstract

Melatonin receptor gene expression as well as melatonin synthesis and secretion activities were examined in the pineal gland of the grass puffer, which exhibits unique lunar/tidal cycle-synchronized mass spawing: spawning occurs before high tide on the day of spring tide during spawing season. Melatonin synthesizing activity was assessed by the abundance of arylalkylamine N-acetyltransferase 2 (AANAT2) mRNA. The amount of aanat2 mRNA was low during light phase and initiated to increase after the light was turned off. The secretion of melatonin from primary pineal organ culture was stimulated after the light was turned off and ceased immediately after the light was turned on. The expression levels of four melatonin receptor subtype genes (mel 1a 1.4, mel 1a 1.7, mel1b, and mel1c) showed synchronous variations, and the levels tended to be high during the dark phase under light/dark conditions. These results suggest that the action of melatonin on the pineal gland is highly dependent on light and photoperiod, possibly with stronger action during night time. Under constant darkness, the expression of four melatonin receptor subtype genes showed unique ultradian oscillations with the period of 14.0-15.4 h, suggesting the presence of a circatidal oscillator in the pineal gland. The present results indicate that melatonin may serve local chronobiological functions in the pineal gland. These cyclic expressions of melatonin receptor genes in the pineal gland may be important in the control of the lunar/tidal cycle-synchronized mass spawning in the grass puffer.

Keywords: arylalkylamine N-acetyltransferase; circadian rhythm; circatidal rhythm; melatonin receptor; pineal gland; puffer; reproduction; ultradian rhythm.