Review articlePeriodic regulation of expression of genes for kisspeptin, gonadotropin-inhibitory hormone and their receptors in the grass puffer: Implications in seasonal, daily and lunar rhythms of reproduction
Introduction
Synchronous reproduction is crucial to reproductive success in most vertebrate species. Many organisms use a combination of photic (e.g. daylight and moonlight) and non-photic (e.g. temperature, nutrition and tidal change for marine organisms) environmental cues to synchronize their sexual maturation and spawning to specific seasons, to particular moon phases and/or to particular times of the day. These cues are integrated to regulate the activity of hypothalamic neuropeptides that control reproduction, such as kisspeptin, gonadotropin-inhibitory hormone (GnIH) and gonadotropin-releasing hormone (GnRH). The periodic regulation of these neuropeptide neurons is thought to be brought through complex networks of the photic and non-photic signal-dependent control mechanisms, currently which are mostly unknown.
To address the molecular mechanisms of the periodic regulation of these neuropeptides, the grass puffer (Takifugu alboplumbeus) provides a unique and excellent animal model because its spawning is synchronized with seasonal, daily and lunar cycles. Grass puffer is a common intertidal puffer species found in the northwest Pacific Ocean form Japan to Vietnam. In early summer from May to July, they spawn exclusively during spring tide, that is, on the day of new and full moon every two weeks (Fig. 1, Motohashi et al., 2010, Ando et al., 2013). On the day of spawning, sexually mature fish aggregate at a certain seashore location for spawning 2.5–3 h before high tide. Then, spawning starts 1.5–2 h before high tide and continues for about 1 h during the rising tidal phase (Motohashi et al., 2010). Therefore, the timing of spawning is tightly connected with lunar and tidal rhythms as well as daily rhythm. Our previous studies on the grass puffer showed distinctive cyclic variations in expression of the genes encoding kisspeptin (kiss2), kisspeptin receptor (kiss2r), GnIH (gnih) and GnIH receptor (gnih-r) in the brain. In the present article, we reviewed current understanding of the changes in expression of these genes, and discussed implications of kisspeptin and GnIH in the regulation of the precisely-timed and semilunar-synchronized spawning of the grass puffer.
Section snippets
Roles of kisspeptin and GnIH in the control of reproduction
Kisspeptin is a member of the RFamide peptide family and is encoded by the KISS1/Kiss1 gene. The receptor for kisspeptin, KISS1r, was originally identified as an orphan G-protein coupled receptor, GPR54, and mutations in GPR54 was found to be responsible for idiopathic hypogonadotropic hypogonadism (de Roux et al., 2003, Seminara et al., 2003). Since then, it has been shown in mammals that kisspeptin has a key role in the neuroendocrine regulation of reproduction with its stimulatory action on
Seasonal regulation of kiss2/kiss2r and gnih/gnih-r expressions
Our previous studies on seasonal variations in the expression of kiss2/kiss2r and gnih/gnih-r have revealed that they show distinct changes during reproductive cycle both in the hypothalamus and pituitary in concordant with gonadal maturation and regression (Shahjahan et al., 2010b, Shahjahan et al., 2011, Ando et al., 2013). Interestingly, the expression patterns were highly similar between the ligand and receptor, i.e. kiss2 and kiss2r, and gnih and gnih-r. We have determined the changes in
Daily and circadian regulation of kiss2/kiss2r and gnih/gnih-r expressions
The mRNA levels of kiss2 and kiss2r in the diencephalon clearly showed daily variations with one peak at Zeitgeber time (ZT) 6 (early light phase) under natural light/dark (LD) conditions (Ando et al., 2014). Under constant dark (DD) conditions, the expression levels of kiss2/kiss2r were significantly increased, and clearly showed circadian variations with one peak at circadian time (CT) 15 (beginning of subjective nighttime). Similarly, gnih/gnih-r showed daily variations in expression with
Implications in semilunar-synchronized reproduction
In contrast to the molecular mechanisms of circadian rhythm that have been the focus of considerable attention, those of lunar or semilunar rhythm are little understood. For explanation of semilunar rhythm, different hypotheses have been proposed (Zantke et al., 2013, Numata et al., 2015). One model relies on beating reaction of circadian (ca. 24 h) and circatidal (ca. 12.4 h) clocks: two oscillators only coincide once per semilunar month (Fig. 3A). As a first step to studying the molecular
Conclusion
In the grass puffer, a semilunar spawner, genes for Kiss2, GnIH and their receptors showed distinct seasonal, daily and circadian variations in expression in the diencephalon. kiss2/kiss2r and gnih/gnih-r showed similar expression patterns with respect to seasonal, daily and circadian oscillations, suggesting that they are regulated by common regulatory mechanisms involving melatonin, circadian clock and water temperature (Fig. 4). For implications in semilunar-synchronized spawning rhythm,
Acknowledgments
We are grateful to Dr. Hiroyuki Doi, Dr. Eiji Motohashi, Dr. Satoshi Awata, Mr. Tomonobu Uryu, Mr. Yoichiro Kato for their help in sampling fish. The authors thank laboratory members of the Fishery Research Laboratory Station, Kyushu University for their help in keeping fish. The authors also thank Dr. Taro Ikegami for mel1b and per1b mRNA assays, Dr. Satoshi Ogawa and Dr. Ishwar Parhar for study of kiss2/kiss2r brain localization, Dr. Atsuhiko Hattori and Dr. Yusuke Maruyama for melatonin
References (43)
- et al.
Molecular neuroendocrine basis of lunar-related spawning in grass puffer
Gen. Comp. Endocrinol.
(2013) - et al.
Kisspeptin-1 directly stimulates LH and GH secretion from goldfish pituitary cells in a Ca2+-dependent manner
Gen. Comp. Endocrinol.
(2012) - et al.
Evidence for two distinct KiSS genes in non-placental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals
Mol. Cell. Endocrinol.
(2009) - et al.
Synchronized diurnal and circadian expressions of four subtypes of melatonin receptor genes in the diencephalon of a puffer fish with lunar-related spawning cycles
Neurosci. Lett.
(2009) - et al.
Kisspeptin regulates the hypothalamus-pituitarygonad axis gene expression during sexual maturation in the cinnamon clownfish, Amphiprion melanopus
Comp. Biochem. Physiol. B: Biochem. Mol. Biol.
(2014) - et al.
Seasonal effect of GnIH on gonadotrope functions in the pituitary of goldfish
Mol. Cell. Endocrinol.
(2012) - et al.
Anatomy of the kisspeptin systems in teleosts
Gen. Comp. Endocrinol.
(2013) - et al.
Functional analysis of kisspeptin peptides in adult immature chub mackerel (Scomber japonicus) using an intracerebroventricular administration method
Neurosci. Lett.
(2014) - et al.
Evidences for the regulation of GnRH and GTH expression by GnIH in the goldfish, Carassius auratus
Mol. Cell. Endocrinol.
(2013) - et al.
Differential expression of three types of gonadotropin-releasing hormone genes during the spawning season in grass puffer, Takifugu niphobles
Gen. Comp. Endocrinol.
(2010)
Elevation of Kiss2 and its receptor gene expression in the brain and pituitary of grass puffer during the spawning season
Gen. Comp. Endocrinol.
Differential expression patterns of PQRFamide peptide and its two receptor genes in the brain and pituitary of grass puffer during the reproductive cycle
Gen. Comp. Endocrinol.
LPXRFamide peptide stimulates growth hormone and prolactin gene expression during the spawning period in the grass puffer, a semi-lunar synchronized spawner
Gen. Comp. Endocrinol.
Temperature affects sexual maturation through the control of kisspeptin, kisspeptin receptor, GnRH and GTH subunit gene expression in the grass puffer during the spawning season
Gen. Comp. Endocrinol.
Kisspeptin and the seasonal control of reproduction in hamsters
Peptides
Molecular, cellular, morphological, physiological and behavioral aspects of gonadotropin-inhibitory hormone
Gen. Comp. Endocrinol.
Circadian and circalunar clock interactions in a marine annelid
Cell Rep.
Structural diversity of the gnih/gnih receptor system in teleost: its involvement in early development and the negative control of LH release
Peptides
Novel fish hypothalamic neuropeptides stimulate the release of gonadotrophins and growth hormone from the pituitary of sockeye salmon
J. Endocrinol.
Diurnal and circadian oscillations in expression of kisspeptin, kisspeptin receptor and gonadotrophin-releasing hormone 2 genes in the grass puffer, a semilunar-synchronised spawner
J. Neuroendocrinol.
LPXRFa, the piscine ortholog of GnIH, and LPXRF receptor positively regulate gonadotropin secretion in tilapia (Oreochromis niloticus)
Endocrinology
Cited by (26)
Influences of photoperiod on growth and reproduction of farmed fishes - prospects in aquaculture
2024, Aquaculture ReportsEffects of different photoperiod conditions on survival, growth, and gonadal development of Takifugu rubripes adults
2023, AquacultureCitation Excerpt :The regulatory effect of GnIH on the release of GTH has been confirmed in many fishes (Biran et al., 2014; Ubuka et al., 2016). In the grass puffer, the administration of gnih stimulated the expression of fshb and lhb genes (Shahjahan et al., 2016; Ando et al., 2018). In tiger puffer, the expression of gnih mRNAs of females at the later developing phase under the 12L:12D photoperiod was significantly higher than that in the other two photoperiod treatments, suggesting that gnih may also been affected by photoperiod.
Biological rhythms: Hormones under moon control
2022, Current BiologyImpacts of heavy metals on early development, growth and reproduction of fish – A review
2022, Toxicology Reports