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      The Role of Melatonin as a Hormone and an Antioxidant in the Control of Fish Reproduction

      review-article
      1 , * , 1
      Frontiers in Endocrinology
      Frontiers Media S.A.
      antioxidant, fish, hormone, melatonin, reproduction

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          Abstract

          Reproduction in most fish is seasonal or periodic, and the spawning occurs in an appropriate season to ensure maximum survival of the offspring. The sequence of reproductive events in an annual cycle is largely under the control of a species-specific endogenous timing system, which essentially relies on a well-equipped physiological response mechanism to changing environmental cues. The duration of solar light or photoperiod is one of the most predictable environmental signals used by a large number of animals including fish to coordinate their seasonal breeding. In vertebrates, the pineal gland is the major photoneuroendocrine part of the brain that rhythmically synthesizes and releases melatonin ( N-acetyl-5-methoxytryptamine) into the circulation in synchronization with the environmental light–dark cycle. Past few decades witnessed an enormous progress in understanding the mechanisms by which melatonin regulates seasonal reproduction in fish and in other vertebrates. Most studies emphasized hormonal actions of melatonin through its high-affinity, pertussis toxin-sensitive G-protein (guanine nucleotide-binding protein)-coupled receptors on the hypothalamus–pituitary–gonad (HPG) axis of fish. However, the discovery that melatonin due to its lipophilic nature can easily cross the plasma membrane of all cells and may act as a potent scavenger of free radicals and stimulant of different antioxidants added a new dimension to the idea explaining mechanisms of melatonin actions in the regulation of ovarian functions. The basic concept on the actions of melatonin as an antioxidant emerged from mammalian studies. Recently, however, some new studies clearly suggested that melatonin, apart from playing the role of a hormone, may also be associated with the reduction in oxidative stress to augment ovarian functions during spawning. This review thus aims to bring together the current knowledge on the role of melatonin as a hormone as well as an antioxidant in the control of fish reproduction and shape the current working hypotheses supported by recent findings obtained in carp or based on knowledge gathered in mammalian and avian species. In essence, this review highlights potential actions of melatonin as a hormone in determining temporal pattern of spawning and as an antioxidant in regulating oocyte maturation at the downstream of HPG axis in fish.

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          Most cited references78

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          Extrapineal melatonin: sources, regulation, and potential functions.

          Endogenous melatonin is synthesized from tryptophan via 5-hydroxytryptamine. It is considered an indoleamine from a biochemical point of view because the melatonin molecule contains a substituted indolic ring with an amino group. The circadian production of melatonin by the pineal gland explains its chronobiotic influence on organismal activity, including the endocrine and non-endocrine rhythms. Other functions of melatonin, including its antioxidant and anti-inflammatory properties, its genomic effects, and its capacity to modulate mitochondrial homeostasis, are linked to the redox status of cells and tissues. With the aid of specific melatonin antibodies, the presence of melatonin has been detected in multiple extrapineal tissues including the brain, retina, lens, cochlea, Harderian gland, airway epithelium, skin, gastrointestinal tract, liver, kidney, thyroid, pancreas, thymus, spleen, immune system cells, carotid body, reproductive tract, and endothelial cells. In most of these tissues, the melatonin-synthesizing enzymes have been identified. Melatonin is present in essentially all biological fluids including cerebrospinal fluid, saliva, bile, synovial fluid, amniotic fluid, and breast milk. In several of these fluids, melatonin concentrations exceed those in the blood. The importance of the continual availability of melatonin at the cellular level is important for its physiological regulation of cell homeostasis, and may be relevant to its therapeutic applications. Because of this, it is essential to compile information related to its peripheral production and regulation of this ubiquitously acting indoleamine. Thus, this review emphasizes the presence of melatonin in extrapineal organs, tissues, and fluids of mammals including humans.
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            Regulation of antioxidant enzymes: a significant role for melatonin.

            Antioxidant enzymes form the first line of defense against free radicals in organisms. Their regulation depends mainly on the oxidant status of the cell, given that oxidants are their principal modulators. However, other factors have been reported to increase antioxidant enzyme activity and/or gene expression. During the last decade, the antioxidant melatonin has been shown to possess genomic actions, regulating the expression of several genes. Melatonin also influences both antioxidant enzyme activity and cellular mRNA levels for these enzymes. In the present report, we review the studies which document the influence of melatonin on the activity and expression of the antioxidative enzymes glutathione peroxidase, superoxide dismutases and catalase both under physiological and under conditions of elevated oxidative stress. We also analyze the possible mechanisms by which melatonin regulates these enzymes.
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              Melatonin and reproduction revisited.

              This brief review summarizes new findings related to the reported beneficial effects of melatonin on reproductive physiology beyond its now well-known role in determining the sexual status in both long-day and short-day seasonally breeding mammals. Of particular note are those reproductive processes that have been shown to benefit from the ability of melatonin to function in the reduction of oxidative stress. In the few species that have been tested, brightly colored secondary sexual characteristics that serve as a sexual attractant reportedly are enhanced by melatonin administration. This is of potential importance inasmuch as the brightness of ornamental pigmentation is also associated with animals that are of the highest genetic quality. Free radical damage is commonplace during pregnancy and has negative effects on the mother, placenta, and fetus. Because of its ability to readily pass through the placenta, melatonin easily protects the fetus from oxidative damage, as well as the maternal tissues and placenta. Examples of conditions in which oxidative and nitrosative stress can be extensive during pregnancy include preeclampsia and damage resulting from anoxia or hypoxia that is followed by reflow of oxygenated blood into the tissue. Given the uncommonly low toxicity of melatonin, clinical trials are warranted to document the protection by melatonin against pathophysiological states of the reproductive system in which free radical damage is known to occur. Finally, the beneficial effects of melatonin in improving the outcomes of in vitro fertilization and embryo transfer should be further tested and exploited. The information in this article has applicability to human and veterinary medicine.
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                Author and article information

                Contributors
                URI : http://frontiersin.org/people/u/89397
                URI : http://frontiersin.org/people/u/344840
                Journal
                Front Endocrinol (Lausanne)
                Front Endocrinol (Lausanne)
                Front. Endocrinol.
                Frontiers in Endocrinology
                Frontiers Media S.A.
                1664-2392
                04 May 2016
                2016
                : 7
                : 38
                Affiliations
                [1] 1Department of Zoology, Visva-Bharati University , Santiniketan, India
                Author notes

                Edited by: Ishwar Parhar, Monash University, Malaysia

                Reviewed by: Lance Kriegsfeld, University of California, USA; Gustavo M. Somoza, Instituto de Investigaciones Biotecnológicas – Instituto Tecnológico Chascomús (IIB-INTECH), Argentina

                *Correspondence: Saumen Kumar Maitra, dgp_skmaitra@ 123456yahoo.co.in

                Specialty section: This article was submitted to Experimental Endocrinology, a section of the journal Frontiers in Endocrinology

                Article
                10.3389/fendo.2016.00038
                4854901
                27199895
                eb737055-a48e-4d59-9bb3-63a7b06c2161
                Copyright © 2016 Maitra and Hasan.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 02 January 2016
                : 21 April 2016
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 89, Pages: 11, Words: 9619
                Funding
                Funded by: Council of Scientific and Industrial Research 10.13039/501100001412
                Award ID: 37(1220)/05/EMR-II and 37(1390)/09/EMR-II
                Funded by: Department of Biotechnology, Ministry of Science and Technology 10.13039/501100001407
                Award ID: BT/PR11423/AAQ/03/421/2008
                Funded by: Department of Science and Technology, Ministry of Science and Technology 10.13039/501100001409
                Award ID: SR/SO/AS/72/2006
                Categories
                Endocrinology
                Review

                Endocrinology & Diabetes
                antioxidant,fish,hormone,melatonin,reproduction
                Endocrinology & Diabetes
                antioxidant, fish, hormone, melatonin, reproduction

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