Elsevier

General and Comparative Endocrinology

Volume 181, 15 January 2013, Pages 215-222
General and Comparative Endocrinology

Review
Melatonin: A potent candidate in the regulation of fish oocyte growth and maturation

https://doi.org/10.1016/j.ygcen.2012.09.015Get rights and content

Abstract

Recent studies on several fish species, especially carp, implicated pineal hormone melatonin (N-acetyl-5-methoxytryptamine) as a potent candidate in the regulatory mechanism of seasonal reproduction. Under natural conditions, the temporal pattern of serum melatonin varied with daily light–dark cycle and the reproductive status of the fish as well. Carefully controlled study revealed that exogenous administration of melatonin may result in stimulation or inhibition or no influences at all on the gonadal functions depending on the reproductive status of fish. Cross-talk between the melatonin and ovarian steroid has been evident from in vitro study, in which melatonin accelerated the action of 17α,20β-dihydroxy-4-pregnen-3-one or maturation inducing hormone (MIH) on meiotic cell cycle resumption in carp oocytes by formation of maturation promoting factor (MPF) – a complex of two proteins, cyclin B and cyclin dependant kinase Cdk1. While several lines of evidence suggest melatonin effects on hypothalamo-hypophyseal–gonadal axis, localization and dynamics of a 37-kDa melatonin receptor protein in carp oocytes argued in favor of extra-hypothalamic direct action of melatonin on fish reproduction. A recent study in carp indicated that influences of an identical regimen of photoperiods in different parts of annual cycle on ovarian functions vary in relation to the profiles of serum melatonin, but not to any rhythm parameters of MT1 or MT2 receptors on the gonad or brain. The purpose of this short review is to bring together the current knowledge on the biological effects of melatonin on fish reproduction mainly focusing the recent findings on carp.

Highlights

► Daily rhythms of serum melatonin vary with reproductive status of free-living fish. ► Exogenous melatonin depending on reproductive season may be pro-, or anti-gonadal. ► Melatonin accelerates the action of MIH on fish oocyte maturation by MPF formation. ► Presence of melatonin receptor in carp oocytes argues for extra-hypothalamic action. ► We used current data to explain mechanism of melatonin actions on fish reproduction.

Introduction

Reproduction in most fish, like many other vertebrates, is discontinuous. Seasonally breeding fish species exhibit peak reproductive activity or spawning for a short period, which is preceded by a long and complicated process of preparation. The seasonal events in an annual reproductive cycle are often synchronized with periodic changes in one or more environmental components in such a way that breeding occurs in the most favorable part of the year [23]. Temporal organization of seasonal breeding is a species specific phenomenon, which may be a self-sustained circannual rhythmic function [5], or influenced by the environment [6]. Annual changes in the duration of the solar day or photoperiod has been proved to be the primary and regular variable that individually, or in combination with water temperature or other component(s) of environment, impel the ‘driving function’ in determining the sexual periodicity in most fish species that breed at mid- and high latitudes [1], [6], [22], [48], [69], and even at low latitudes [2], [3], [18], [19].

The synchronization of reproductive events with the environment is mediated through a system, which is composed of sensors and circadian oscillators like the pineal organ, the lateral eyes and the suprachiasmatic nuclei (SCN) of the hypothalamus [50]. This circadian oscillator system among the fish species is located in the pineal organ and the eyes [24], [27], among which the pineal organ for its ability of cyclic synthesis and release of melatonin (N-acetyl-5-methoxytryptamine) is considered as the most important component of its responsive mechanism to the changes in environmental light and darkness [22]. The daily pattern of melatonin secretion is conserved among vertebrates, as it is low during the daytime and high during the night, and thereby serves as the internal neuro-hormonal signal of darkness [50]. A recent study revealed that dark-induced melatonin synthesis in the carp pineal is a multi-neuronal function, in which both adrenergic (α1 and β1, but not α2) and dopaminergic signals are stimulatory, whereas cholinergic signals are inhibitory [55]. Melatonin is recognized as the biological timekeeping hormone mainly due to the fact that it reflects the seasonal variations in day-length across the whole animal kingdom, rather than the existence of direct evidences of its role in the entrainment of reproduction in fishes [39]. However, over the past few decades, the role of melatonin in the regulation of fish reproduction remained far from being clear mainly due to insufficient data collected from well designed carefully controlled studies in the same species. Few recent studies provided evidence that melatonin interacts with the reproductive cascade at a number of key steps such as through the central hypothalamo-hypophyseal system as well as modulates actions of sex steroids in the final oocyte maturation. Moreover, reports on receptor independent free-radical scavenging actions of melatonin added further interest in the physiology and pathophysiology of gonadal functions in vertebrates [58]. This short review thus aims to bring together the current knowledge on the role of melatonin in the regulation of fish reproduction mainly focusing on temporal relationship between the circulating profiles of melatonin and its receptors on target tissues, gonadal responsiveness to exogenous melatonin, interplay between melatonin and other hormones during oocyte maturation, dynamics of melatonin receptors and role of several recently discovered novel hypothalamic peptides as well, and shape the current working hypotheses supported by recent findings on teleosts.

Section snippets

Implication of daily circulating profiles of melatonin in seasonal reproduction

Circadian profiles of melatonin in the blood are determined by the prevailing light–dark cycle [21], [39]. As a consequence, circulating melatonin levels are higher at night than during the day irrespective of the habit and habitat of the species so far examined [51]. This pattern of melatonin rhythms is conserved across all vertebrates. However, three variants of nocturnal melatonin profiles, namely type-A, -B and -C profiles have been identified in different vertebrates, including fish [22],

Influences of melatonin in the regulation of seasonal reproductive events

Growth and development of gonads in fish comprise of sequential events in an annual cycle. Primarily, on the basis of gametogenic status of gonads, the annual breeding cycle in fish is divided into four different phases, like (a) the preparatory phase, (b) the pre-spawning phase, (c) the spawning phase, and (d) the post-spawning phase. Each phase has a specific duration and is characterized by distinct germ cell profiles in the ovary [18] and the testis [3]. The ovaries exhibit mostly oogonia

Implication of melatonin in the regulation of oocyte maturation

Maturation of the fish oocyte is accomplished by means of two successive meiotic divisions, during the course of which the oocyte gives out two polar bodies. During this process, the enlarged nucleus of the primary oocyte, which is arrested at the diplotene stage, moves towards a more peripheral position, its membrane breaks down and with the extrusion of a polar body the first meiotic division is completed. Breakdown of the oocyte nuclear envelope or germinal vesicle breakdown (GVBD) occurring

Pathway of action of melatonin in reproduction

The data already gathered from a variety of fish species across the taxa have forwarded a general hypothesis that melatonin plays a pivotal role in the regulation of reproduction at different stages of growth and development of gonad in an annual cycle. However, the physiological mechanism by which this indole hormone regulates fish reproduction still remains speculative. While it is suggested that melatonin regulates gonadal functions through hypothalamo-hypophyseal axis, recent studies opened

Conclusions

The vast amount of research conducted on several fish species has led to a great progress in understanding the physiological importance of melatonin in the regulation of periodic events associated with the growth and maturation of gonad. The evidence that melatonin functions at multiple sites, brain–pituitary–gonad axis as well as gonad (through receptors and/or as receptor-independent free radical scavenger), made a major contribution to the current knowledge on the mechanism of action of this

Acknowledgments

Financial assistance from the Department of Biotechnology, Government of India, (BT/PR11423/AAQ/03/421/2008) and Council of Scientific and Industrial Research, New Delhi (37(1220)/05/EMR-II) is thankfully acknowledged. The authors are grateful to Professor K. Tsutsui, University of Waseda, Japan for his generous academic support and encouragements.

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