Central Pathways Integrating Metabolism and Reproduction in Teleosts
Identifieur interne : 000311 ( Pmc/Corpus ); précédent : 000310; suivant : 000312Central Pathways Integrating Metabolism and Reproduction in Teleosts
Auteurs : Md. Shahjahan ; Takashi Kitahashi ; Ishwar S. ParharSource :
- Frontiers in Endocrinology [ 1664-2392 ] ; 2014.
Abstract
Energy balance plays an important role in the control of reproduction. However, the cellular and molecular mechanisms connecting the two systems are not well understood especially in teleosts. The hypothalamus plays a crucial role in the regulation of both energy balance and reproduction, and contains a number of neuropeptides, including gonadotropin-releasing hormone (GnRH), orexin, neuropeptide-Y, ghrelin, pituitary adenylate cyclase-activating polypeptide, α-melanocyte stimulating hormone, melanin-concentrating hormone, cholecystokinin, 26RFamide, nesfatin, kisspeptin, and gonadotropin-inhibitory hormone. These neuropeptides are involved in the control of energy balance and reproduction either directly or indirectly. On the other hand, synthesis and release of these hypothalamic neuropeptides are regulated by metabolic signals from the gut and the adipose tissue. Furthermore, neurons producing these neuropeptides interact with each other, providing neuronal basis of the link between energy balance and reproduction. This review summarizes the advances made in our understanding of the physiological roles of the hypothalamic neuropeptides in energy balance and reproduction in teleosts, and discusses how they interact with GnRH, kisspeptin, and pituitary gonadotropins to control reproduction in teleosts.
Url:
DOI: 10.3389/fendo.2014.00036
PubMed: 24723910
PubMed Central: 3971181
Links to Exploration step
PMC:3971181Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Central Pathways Integrating Metabolism and Reproduction in Teleosts</title><author><name sortKey="Shahjahan, Md" sort="Shahjahan, Md" uniqKey="Shahjahan M" first="Md." last="Shahjahan">Md. Shahjahan</name><affiliation><nlm:aff id="aff1"><institution>Brain Research Institute, School of Medicine and Health Sciences, Monash University Malaysia</institution>,<addr-line>Petaling Jaya</addr-line>,<country>Malaysia</country></nlm:aff></affiliation></author><author><name sortKey="Kitahashi, Takashi" sort="Kitahashi, Takashi" uniqKey="Kitahashi T" first="Takashi" last="Kitahashi">Takashi Kitahashi</name><affiliation><nlm:aff id="aff1"><institution>Brain Research Institute, School of Medicine and Health Sciences, Monash University Malaysia</institution>,<addr-line>Petaling Jaya</addr-line>,<country>Malaysia</country></nlm:aff></affiliation></author><author><name sortKey="Parhar, Ishwar S" sort="Parhar, Ishwar S" uniqKey="Parhar I" first="Ishwar S." last="Parhar">Ishwar S. Parhar</name><affiliation><nlm:aff id="aff1"><institution>Brain Research Institute, School of Medicine and Health Sciences, Monash University Malaysia</institution>,<addr-line>Petaling Jaya</addr-line>,<country>Malaysia</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">24723910</idno><idno type="pmc">3971181</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3971181</idno><idno type="RBID">PMC:3971181</idno><idno type="doi">10.3389/fendo.2014.00036</idno><date when="2014">2014</date><idno type="wicri:Area/Pmc/Corpus">000311</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000311</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Central Pathways Integrating Metabolism and Reproduction in Teleosts</title><author><name sortKey="Shahjahan, Md" sort="Shahjahan, Md" uniqKey="Shahjahan M" first="Md." last="Shahjahan">Md. Shahjahan</name><affiliation><nlm:aff id="aff1"><institution>Brain Research Institute, School of Medicine and Health Sciences, Monash University Malaysia</institution>,<addr-line>Petaling Jaya</addr-line>,<country>Malaysia</country></nlm:aff></affiliation></author><author><name sortKey="Kitahashi, Takashi" sort="Kitahashi, Takashi" uniqKey="Kitahashi T" first="Takashi" last="Kitahashi">Takashi Kitahashi</name><affiliation><nlm:aff id="aff1"><institution>Brain Research Institute, School of Medicine and Health Sciences, Monash University Malaysia</institution>,<addr-line>Petaling Jaya</addr-line>,<country>Malaysia</country></nlm:aff></affiliation></author><author><name sortKey="Parhar, Ishwar S" sort="Parhar, Ishwar S" uniqKey="Parhar I" first="Ishwar S." last="Parhar">Ishwar S. Parhar</name><affiliation><nlm:aff id="aff1"><institution>Brain Research Institute, School of Medicine and Health Sciences, Monash University Malaysia</institution>,<addr-line>Petaling Jaya</addr-line>,<country>Malaysia</country></nlm:aff></affiliation></author></analytic><series><title level="j">Frontiers in Endocrinology</title><idno type="eISSN">1664-2392</idno><imprint><date when="2014">2014</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Energy balance plays an important role in the control of reproduction. However, the cellular and molecular mechanisms connecting the two systems are not well understood especially in teleosts. The hypothalamus plays a crucial role in the regulation of both energy balance and reproduction, and contains a number of neuropeptides, including gonadotropin-releasing hormone (GnRH), orexin, neuropeptide-Y, ghrelin, pituitary adenylate cyclase-activating polypeptide, α-melanocyte stimulating hormone, melanin-concentrating hormone, cholecystokinin, 26RFamide, nesfatin, kisspeptin, and gonadotropin-inhibitory hormone. These neuropeptides are involved in the control of energy balance and reproduction either directly or indirectly. On the other hand, synthesis and release of these hypothalamic neuropeptides are regulated by metabolic signals from the gut and the adipose tissue. Furthermore, neurons producing these neuropeptides interact with each other, providing neuronal basis of the link between energy balance and reproduction. This review summarizes the advances made in our understanding of the physiological roles of the hypothalamic neuropeptides in energy balance and reproduction in teleosts, and discusses how they interact with GnRH, kisspeptin, and pituitary gonadotropins to control reproduction in teleosts.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Schneider, Je" uniqKey="Schneider J">JE Schneider</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Fernandez Fernandez, R" uniqKey="Fernandez Fernandez R">R Fernandez-Fernandez</name></author><author><name sortKey="Martini, Ac" uniqKey="Martini A">AC Martini</name></author><author><name sortKey="Navarro, Vm" uniqKey="Navarro V">VM Navarro</name></author><author><name sortKey="Castellano, Jm" uniqKey="Castellano J">JM Castellano</name></author><author><name sortKey="Dieguez, C" uniqKey="Dieguez C">C Dieguez</name></author><author><name sortKey="Aguilar, E" 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Endocrinol (Lausanne)</journal-id><journal-id journal-id-type="iso-abbrev">Front Endocrinol (Lausanne)</journal-id><journal-id journal-id-type="publisher-id">Front. Endocrinol.</journal-id><journal-title-group><journal-title>Frontiers in Endocrinology</journal-title></journal-title-group><issn pub-type="epub">1664-2392</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">24723910</article-id><article-id pub-id-type="pmc">3971181</article-id><article-id pub-id-type="doi">10.3389/fendo.2014.00036</article-id><article-categories><subj-group subj-group-type="heading"><subject>Endocrinology</subject><subj-group><subject>Review Article</subject></subj-group></subj-group></article-categories><title-group><article-title>Central Pathways Integrating Metabolism and Reproduction in Teleosts</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Shahjahan</surname><given-names>Md.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>†</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/137608"></uri></contrib><contrib contrib-type="author"><name><surname>Kitahashi</surname><given-names>Takashi</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn001"><sup>†</sup></xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/122101"></uri></contrib><contrib contrib-type="author"><name><surname>Parhar</surname><given-names>Ishwar S.</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1">*</xref><uri xlink:type="simple" xlink:href="http://frontiersin.org/people/u/68196"></uri></contrib></contrib-group><aff id="aff1"><sup>1</sup><institution>Brain Research Institute, School of Medicine and Health Sciences, Monash University Malaysia</institution>,<addr-line>Petaling Jaya</addr-line>,<country>Malaysia</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Rosaria Meccariello, University of Naples Parthenope, Italy</p></fn><fn fn-type="edited-by"><p>Reviewed by: Teresa Chioccarelli, Second University of Naples, Italy; Erika Cottone, University of Turin, Italy</p></fn><corresp content-type="corresp" id="cor1">*Correspondence: Ishwar S. Parhar, Brain Research Institute, School of Medicine and Health Sciences, Monash University Malaysia, Petaling Jaya 46150, Malaysia e-mail: <email>ishwar@monash.edu</email></corresp><fn fn-type="other" id="fn001"><p><sup>†</sup>Md. Shahjahan and Takashi Kitahashi have contributed equally to this work.</p></fn><fn fn-type="other" id="fn002"><p>This article was submitted to Experimental Endocrinology, a section of the journal Frontiers in Endocrinology.</p></fn></author-notes><pub-date pub-type="epreprint"><day>21</day><month>2</month><year>2014</year></pub-date><pub-date pub-type="epub"><day>25</day><month>3</month><year>2014</year></pub-date><pub-date pub-type="collection"><year>2014</year></pub-date><volume>5</volume><elocation-id>36</elocation-id><history><date date-type="received"><day>10</day><month>2</month><year>2014</year></date><date date-type="accepted"><day>11</day><month>3</month><year>2014</year></date></history><permissions><copyright-statement>Copyright © 2014 Shahjahan, Kitahashi and Parhar.</copyright-statement><copyright-year>2014</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p>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.</license-p></license></permissions><abstract><p>Energy balance plays an important role in the control of reproduction. However, the cellular and molecular mechanisms connecting the two systems are not well understood especially in teleosts. The hypothalamus plays a crucial role in the regulation of both energy balance and reproduction, and contains a number of neuropeptides, including gonadotropin-releasing hormone (GnRH), orexin, neuropeptide-Y, ghrelin, pituitary adenylate cyclase-activating polypeptide, α-melanocyte stimulating hormone, melanin-concentrating hormone, cholecystokinin, 26RFamide, nesfatin, kisspeptin, and gonadotropin-inhibitory hormone. These neuropeptides are involved in the control of energy balance and reproduction either directly or indirectly. On the other hand, synthesis and release of these hypothalamic neuropeptides are regulated by metabolic signals from the gut and the adipose tissue. Furthermore, neurons producing these neuropeptides interact with each other, providing neuronal basis of the link between energy balance and reproduction. This review summarizes the advances made in our understanding of the physiological roles of the hypothalamic neuropeptides in energy balance and reproduction in teleosts, and discusses how they interact with GnRH, kisspeptin, and pituitary gonadotropins to control reproduction in teleosts.</p></abstract><kwd-group><kwd>neuropeptide</kwd><kwd>metabolism</kwd><kwd>energy balance</kwd><kwd>fish</kwd><kwd>reproduction</kwd></kwd-group><counts><fig-count count="2"></fig-count><table-count count="1"></table-count><equation-count count="0"></equation-count><ref-count count="283"></ref-count><page-count count="17"></page-count><word-count count="16763"></word-count></counts></article-meta></front><body><sec id="S1"><title>Introduction</title><p>A close connection between energy balance and reproduction has been well documented in mammals (<xref rid="B1" ref-type="bibr">1</xref>). Energy balance is maintained by a process that controls food consumption, energy expenditure, and energy storage. A number of hypothalamic neuropeptides including orexin, ghrelin, neuropeptide-Y (NPY), melanin-concentrating hormone (MCH), pituitary adenylate cyclase-activating polypeptide (PACAP), proopiomelanocortin (POMC)-derived peptides, cholecystokinin (CCK), chicken gonadotropin-releasing hormone-II (cGnRH-II), 26RFamide (26RFa), galanin (GAL), and cocaine- and amphetamine-regulated transcript (CART) have been implicated in the regulation of feeding behavior and energy balance. On the other hand, peripheral hormones such as leptin and ghrelin provide information about the availability of stored metabolic foods.</p><p>Initiation of reproduction is affected by the amount of body energy reserves and is responsive to diverse metabolic factors. The neuroendocrine mechanisms responsible for the association between energy balance and fertility are represented by metabolic hormones and neuropeptides that affect the hypothalamic center controlling the expression and release of gonadotropin-releasing hormone (GnRH) (<xref rid="B2" ref-type="bibr">2</xref>, <xref rid="B3" ref-type="bibr">3</xref>). Therefore, adequate body energy stores are crucial for full activation of the hypothalamus–pituitary–gonadal (HPG) axis at puberty and its proper functioning in adulthood (<xref rid="B4" ref-type="bibr">4</xref>). Generally high amount of food supply favor reproduction, while low food supply inhibits the reproductive system (<xref rid="B1" ref-type="bibr">1</xref>). During energetic challenges, the physiological mechanisms that partition energy into various activities tend to favor the processes for the survival of the individual over the processes for growth, longevity, and reproduction (<xref rid="B5" ref-type="bibr">5</xref>). Therefore, the reproductive system is suppressed by energetic challenges. At the same time it is also true that when the reproductive system is highly activated, animal primates reproduction rather than feeding. Many factors such as starvation, eating disorders, excessive exercise, cold exposure, and lactation act on both food intake and reproduction by increasing hunger and/or food ingestion and by suppressing reproductive processes (<xref rid="B5" ref-type="bibr">5</xref>, <xref rid="B6" ref-type="bibr">6</xref>).</p><p>Most feeding-related neuropeptides in mammals have also been identified in fish species (<xref rid="B7" ref-type="bibr">7</xref>), suggesting that the regulatory system of feeding has been well conserved from fish to mammals. On the other hand, as the links between energy balance and reproduction have been demonstrated in several vertebrates (<xref rid="B8" ref-type="bibr">8</xref>), this might also exist in teleosts. Indeed, seasonal changes in feeding often coincide with spawning migration and reproduction in fish, suggesting association between nutrition and reproduction (<xref rid="B9" ref-type="bibr">9</xref>).</p><p>This review focuses on the role of the neuropeptides that regulate feeding and energy balance on reproduction in teleosts, and discusses if the metabolic control of reproduction is conserved from fish to mammals.</p></sec><sec id="S2"><title>Regulation of Reproduction in Teleosts</title><p>In teleosts, as in other vertebrates, reproduction is coordinated by the HPG axis. The hypothalamus produces GnRH, which regulates the synthesis and release of gonadotropins (GTHs), follicle-stimulating hormone (FSH), and luteinizing hormone (LH), from the pituitary. The GTHs act on the gonads to stimulate gonadal development through the secretion of sex steroid hormones. These steroids, in turn, feedback to the brain and the pituitary to complete the HPG axis and to regulate the reproductive cycle (<xref rid="B10" ref-type="bibr">10</xref>, <xref rid="B11" ref-type="bibr">11</xref>). Thus, hypothalamic GnRH is considered as the key player in the regulation of reproduction in teleosts. Furthermore, recent findings of kisspeptin and gonadotropin-inhibitory hormone (GnIH) added new players in the reproductive system, which stimulate and inhibit mostly GnRH neurons, respectively.</p><sec id="S2-1"><title>Gonadotropin-releasing hormone (GnRH)</title><p>In the early 1970s, two research groups simultaneously reported the isolation of a LH-releasing factor from the hypothalamus of pigs and sheep (<xref rid="B12" ref-type="bibr">12</xref>, <xref rid="B13" ref-type="bibr">13</xref>), and named it LH-releasing hormone (LHRH). Later, this decapeptide was also found to stimulate FSH release, and accordingly re-named GnRH. The GnRH isolated from mammals is also functional in fish, and stimulates the release of GTH in the carp (<xref rid="B14" ref-type="bibr">14</xref>). The first fish GnRH was identified in salmon, and named as salmon GnRH (sGnRH) (<xref rid="B15" ref-type="bibr">15</xref>). To date, 15 different forms of GnRH have been identified in vertebrates (<xref rid="B13" ref-type="bibr">13</xref>, <xref rid="B15" ref-type="bibr">15</xref>–<xref rid="B25" ref-type="bibr">25</xref>), among them 10 original forms in fish species: salmon, sea bream, whitefish, medaka, catfish, herring, dogfish, and lamprey (lamprey I, II, and III). Most vertebrates possess two, and some teleosts have three, forms of GnRH in the brain (<xref rid="B23" ref-type="bibr">23</xref>, <xref rid="B25" ref-type="bibr">25</xref>–<xref rid="B31" ref-type="bibr">31</xref>). Based on phylogenetic analysis, recent classification defines the species-specific (hypophysiotropic) form as GnRH1, while the most evolutionarily conserved chicken GnRH-II as GnRH2 (<xref rid="B32" ref-type="bibr">32</xref>). The third form is GnRH3 (<xref rid="B33" ref-type="bibr">33</xref>), which is present only in the brain of certain teleost species (<xref rid="B31" ref-type="bibr">31</xref>, <xref rid="B34" ref-type="bibr">34</xref>).</p><p>Distribution of three different forms of GnRH in the brain was first reported in a perciform fish, the sea bream (<xref rid="B35" ref-type="bibr">35</xref>). GnRH1 neurons are generally present in the region from the ventral forebrain–preoptic area (POA) to basal hypothalamus, whereas GnRH2 neurons are restricted to the dorsal mesencephalon. GnRH3 neurons are located in the caudal-most olfactory bulb as a ganglion and along the terminal nerve in most fish species that possess three GnRH forms (<xref rid="B31" ref-type="bibr">31</xref>, <xref rid="B36" ref-type="bibr">36</xref>). On the other hand, in the sea bream and the European sea bass, the distribution of GnRH1 and GnRH3 cells overlap in the olfactory bulbs, ventral telencephalon, and POA (<xref rid="B37" ref-type="bibr">37</xref>–<xref rid="B40" ref-type="bibr">40</xref>). Similar results were reported in several other fish species (<xref rid="B41" ref-type="bibr">41</xref>–<xref rid="B45" ref-type="bibr">45</xref>). In the sea bass brain, GnRH1 neuronal fibers are observed in the ventral surface of the forebrain, associated with the ventral telencephalon, POA, and the hypothalamus, whereas GnRH2 and GnRH3 neuronal fibers show profuse distributions throughout the brain (<xref rid="B40" ref-type="bibr">40</xref>).</p><p>The function of GnRH in the central regulation of LH release has been recognized in all orders of teleosts. Although the assay for FSH peptide is lacking for most fish species, studies in the rainbow trout (<xref rid="B46" ref-type="bibr">46</xref>–<xref rid="B48" ref-type="bibr">48</xref>) and the Coho salmon (<xref rid="B49" ref-type="bibr">49</xref>) show that GnRH also stimulates FSH release in salmonids. However, the different patterns of fiber projections of each GnRH form suggest different physiological function of each GnRH form in the brain (<xref rid="B31" ref-type="bibr">31</xref>). GnRH1 neurons are generally present in the ventral forebrain–POA–hypothalamus and send neuronal fibers directly into the pituitary, which represents its primary role in the stimulation of GTH secretion. The physiological significance of GnRH1 as a regulator of GTH secretion and gametogenesis has been established in several teleosts (<xref rid="B28" ref-type="bibr">28</xref>, <xref rid="B50" ref-type="bibr">50</xref>–<xref rid="B54" ref-type="bibr">54</xref>).</p><p>GnRH2 neurons are exclusively present in the midbrain. The absence or low levels of GnRH2 peptide in the pituitary has been demonstrated in several <italic>perciformes</italic> (<xref rid="B50" ref-type="bibr">50</xref>, <xref rid="B51" ref-type="bibr">51</xref>, <xref rid="B55" ref-type="bibr">55</xref>–<xref rid="B57" ref-type="bibr">57</xref>) and pleuronectiformes species (<xref rid="B28" ref-type="bibr">28</xref>, <xref rid="B58" ref-type="bibr">58</xref>), suggesting that GnRH2 is not directly involved in GTH secretion. Rather, its wide fiber projection throughout the brain suggests that GnRH2 has neuromodulatory functions (<xref rid="B30" ref-type="bibr">30</xref>). However, in some fish species including the goldfish, GnRH2 seems to act as a hypophysiotropic GnRH together with GnRH3 (<xref rid="B59" ref-type="bibr">59</xref>).</p><p>GnRH3 has been shown to control reproductive behaviors in several fish species. GnRH3 stimulates nest-building behavior in the male dwarf gourami (<xref rid="B60" ref-type="bibr">60</xref>), homing migration in the sockeye salmon (<xref rid="B61" ref-type="bibr">61</xref>), and aggressive and nest-building behaviors in the male Nile tilapia (<xref rid="B62" ref-type="bibr">62</xref>), which suggests probable neuromodulatory roles of GnRH3. The neuromodulatory role of GnRH3 was confirmed by electrophysiological studies in the retina of goldfish (<xref rid="B63" ref-type="bibr">63</xref>, <xref rid="B64" ref-type="bibr">64</xref>) and olfactory receptor cells of the mudpuppy (<xref rid="B65" ref-type="bibr">65</xref>). The neuromodulatory function of GnRH3 has also been demonstrated in the rainbow trout (<xref rid="B66" ref-type="bibr">66</xref>, <xref rid="B67" ref-type="bibr">67</xref>) and the dwarf gourami [reviewed by Oka (<xref rid="B68" ref-type="bibr">68</xref>)]. Fish species such as some salmonids and the zebrafish possess only two forms of GnRH (GnRH2 and GnRH3). In these species, GnRH3 expressed in the basal forebrain acts as a hypophysiotropic GnRH (<xref rid="B45" ref-type="bibr">45</xref>, <xref rid="B69" ref-type="bibr">69</xref>–<xref rid="B71" ref-type="bibr">71</xref>).</p></sec><sec id="S2-2"><title>Kisspeptin</title><p>Kisspeptin is a neuropeptide that plays an important role in reproduction through the stimulation of GnRH neurons by activating GPR54 in mammals (<xref rid="B72" ref-type="bibr">72</xref>, <xref rid="B73" ref-type="bibr">73</xref>). In teleosts, two kisspeptin genes, namely <italic>kiss1</italic> and <italic>kiss2</italic>, have been identified in several fish species (<xref rid="B74" ref-type="bibr">74</xref>–<xref rid="B77" ref-type="bibr">77</xref>), whereas placental mammals possess only the <italic>kiss1</italic> gene. Similarly, two kisspeptin receptor genes, named <italic>kiss1r</italic> and <italic>kiss2r</italic>, were also identified in several fish species (<xref rid="B76" ref-type="bibr">76</xref>, <xref rid="B78" ref-type="bibr">78</xref>), suggesting two Kiss/Kissr systems in teleosts. However, this situation is not common among all fish species. Only one kisspeptin gene, <italic>kiss2</italic>, and one receptor, <italic>kiss2r</italic>, are present in some fish species including the Senegalese sole (<xref rid="B79" ref-type="bibr">79</xref>), orange-spotted grouper (<xref rid="B80" ref-type="bibr">80</xref>), grass puffer (<xref rid="B81" ref-type="bibr">81</xref>), and the Atlantic halibut (<xref rid="B82" ref-type="bibr">82</xref>), indicating that the <italic>kiss1</italic> and <italic>kiss1r</italic> genes have been lost during evolution in these species (<xref rid="B82" ref-type="bibr">82</xref>). Both <italic>kiss1</italic> and <italic>kiss2</italic> mRNAs are expressed in the brain and the gonads in several fish species (<xref rid="B74" ref-type="bibr">74</xref>, <xref rid="B76" ref-type="bibr">76</xref>–<xref rid="B78" ref-type="bibr">78</xref>, <xref rid="B83" ref-type="bibr">83</xref>). On the other hand, kisspeptin and kisspeptin receptor are also expressed in the fish pituitary, suggesting local actions of kisspeptin in the pituitary (<xref rid="B76" ref-type="bibr">76</xref>, <xref rid="B78" ref-type="bibr">78</xref>, <xref rid="B81" ref-type="bibr">81</xref>). In the medaka brain, two populations of <italic>kiss1</italic> neurons are found in the hypothalamus, one in the nucleus ventral tuberis (nVT) and the nucleus posterioris periventricularis (NPPv) (<xref rid="B74" ref-type="bibr">74</xref>, <xref rid="B84" ref-type="bibr">84</xref>), while neurons in the dorsal zone of the periventricular hypothalamus (Hd) express <italic>kiss2</italic>. In the zebrafish all hypothalamic populations express <italic>kiss2</italic> mRNA (<xref rid="B74" ref-type="bibr">74</xref>). A recent study showed that zebrafish Kiss2 neuronal fibers are found widely in the subpallium, POA, ventral and caudal hypothalamus, and the mesencephalon (<xref rid="B85" ref-type="bibr">85</xref>). The fact that all three GnRH neuron types express kisspeptin receptors in the Nile tilapia (<xref rid="B86" ref-type="bibr">86</xref>) suggests that the role of Kiss2 neurons in the regulation of the HPG axis is via the activation of the GnRH systems. The <italic>kiss1</italic> neurons are exclusively localized in the habenula in the zebrafish (<xref rid="B74" ref-type="bibr">74</xref>), and send fibers only to the ventral part of the interpeduncular nucleus (<xref rid="B85" ref-type="bibr">85</xref>, <xref rid="B87" ref-type="bibr">87</xref>). The habenula Kiss1 system is thus implicated in the modulation of serotonergic system rather than the HPG axis in the zebrafish (<xref rid="B87" ref-type="bibr">87</xref>).</p><p>The role of kisspeptin in the onset of puberty and sexual maturation is conserved among vertebrates including fish. In the zebrafish, both <italic>kiss1</italic> and <italic>kiss2</italic> mRNA levels are increased significantly at the start of the pubertal phase together with GnRH2 and GnRH3 mRNAs (<xref rid="B74" ref-type="bibr">74</xref>). Significant positive correlation is observed between the levels of <italic>kiss2</italic> mRNA and those of <italic>gnrh1</italic> mRNA during the spawning period in the grass puffer (<xref rid="B81" ref-type="bibr">81</xref>). Kiss2 but not Kiss1 stimulates GTH synthesis and release in the sea bass and the zebrafish (<xref rid="B74" ref-type="bibr">74</xref>, <xref rid="B75" ref-type="bibr">75</xref>). Administration of Kiss2–10 peptide increases GnRH1 mRNA levels in the sexually mature female orange-spotted grouper (<xref rid="B80" ref-type="bibr">80</xref>), indicating that <italic>Kiss2</italic> most probably plays an important role in the regulation of reproductive functions through the stimulation of GnRH1 secretion.</p><p>The information of the interaction between kisspeptin neuronal fibers and GnRH cell bodies had been limited in teleosts due to the lack of specific antibody to kisspeptins. A recent study using an antibody to prepro-Kiss2 proved that Kiss2 neuronal fibers make close contacts with POA GnRH (GnRH3) neurons in the zebrafish (<xref rid="B85" ref-type="bibr">85</xref>), suggesting that Kiss2 directly act on GnRH neurons. Moreover, kisspeptin receptor expression in the three GnRH neuronal populations (<xref rid="B86" ref-type="bibr">86</xref>) in tilapia suggests that kisspeptin directly stimulates not only GnRH1 neurons to induce LH secretion, but also GnRH2 and GnRH3 neurons to activate other aspects of the reproduction such as sexual behavior.</p></sec><sec id="S2-3"><title>Gonadotropin-inhibitory hormone (GnIH)</title><p>GnIH or RFamide-related peptide (RFRP), which has a characteristic C-terminal LPXRFa motif (X = L or Q), is a hypothalamic neuropeptide that was originally identified from the quail as a neuropeptide that inhibits gonadotropin release from the pituitary (<xref rid="B88" ref-type="bibr">88</xref>). Extensive studies revealed that GnIH functions at the level of GnRH neurons and at the level of pituitary gonadotropes to suppress reproduction in avian and mammalian species [see reviews in Ref. (<xref rid="B89" ref-type="bibr">89</xref>, <xref rid="B90" ref-type="bibr">90</xref>)]. GnIH in the teleost species has been named LPXRFamide peptide based on the amino acid sequence of the C-terminal motif. All precursors of teleost GnIH identified so far encode three GnIH orthologs (LPXRFa-1, -2, and -3), while only goldfish LPXRFa-3 has been purified as a mature peptide.</p><p>As in birds and in mammals, teleost GnIH neurons are located in the hypothalamus, in particular in the NPPv, and send neuronal fibers throughout the brain and to the pituitary (<xref rid="B91" ref-type="bibr">91</xref>, <xref rid="B92" ref-type="bibr">92</xref>). The physiological function of teleost GnIH in the control of reproduction is complicated. <italic>In vivo</italic> studies using the goldfish show that GnIH decreases plasma LH levels as in avian and mammalian species (<xref rid="B93" ref-type="bibr">93</xref>, <xref rid="B94" ref-type="bibr">94</xref>). On the other hand, GnIH significantly increases pituitary levels of mRNAs for LHβ and FSHβ in a reproductive state-dependent manner <italic>in vivo</italic>, whereas general suppression of LHβ and FSHβ mRNA levels is observed <italic>in vitro</italic> in a study (<xref rid="B93" ref-type="bibr">93</xref>). This differential <italic>in vivo</italic> effect of GnIH in different seasons can be explained by the differential action of GnIH on the gonads (<xref rid="B95" ref-type="bibr">95</xref>). GnIH does not affect plasma estradiol levels in the female goldfish, but increases plasma testosterone levels in the male goldfish (<xref rid="B96" ref-type="bibr">96</xref>). GnIH injections into the female goldfish suppress pituitary LHβ and FSHβ and hypothalamic GnRH mRNA levels (<xref rid="B95" ref-type="bibr">95</xref>). In addition, GnIH suppresses GnRH-induced increase in LHβ mRNA levels <italic>in vitro</italic> (<xref rid="B95" ref-type="bibr">95</xref>). Therefore, in the goldfish, the inhibition of the HPG axis at the level of hypothalamic GnRH neurons and pituitary gonadotropes appears as an evolutionarily conserved function of GnIH. On the contrary, goldfish GnIH peptides stimulate the synthesis and release of LH and FSH in cultured pituitary cells of the grass puffer and the sockeye salmon, respectively (<xref rid="B92" ref-type="bibr">92</xref>, <xref rid="B97" ref-type="bibr">97</xref>). Therefore, as in mammals (<xref rid="B98" ref-type="bibr">98</xref>), the stimulatory or inhibitory action of GnIH in fish is probably species dependent or species-specific GnIH peptide might be necessary for an inhibitory action.</p><p>More recently, it has been shown that medaka LPXRFa-2 (GnIH-2) peptide decreases the firing frequency of non-hypophsiotropic terminal nerve GnRH3 neurons in the dwarf gourami (<xref rid="B99" ref-type="bibr">99</xref>). Since GnRH3 controls nest-building, aggression, and homing migration (<xref rid="B60" ref-type="bibr">60</xref>–<xref rid="B62" ref-type="bibr">62</xref>), GnIH-2 might negatively regulate reproductive behaviors.</p></sec></sec><sec id="S3"><title>Metabolic Neuropeptides Involved in Reproduction</title><p>A number of hypothalamic neuropeptides have been identified in fish species (<xref rid="B7" ref-type="bibr">7</xref>), and found to be involved in the control of food intake as well as reproduction (Table <xref ref-type="table" rid="T1">1</xref>). To understand the overall metabolic control of reproduction, the involvement of metabolic neuropeptides in the regulation of GnRH and GTHs must be taken into consideration. However, compared to mammals, the information related to the role of metabolic neuropeptides in the regulation of reproduction is still limited in fish.</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p><bold>Neuropeptides and their functions in representative fish species</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Neuropeptide</th><th align="left" rowspan="1" colspan="1">Species</th><th align="left" rowspan="1" colspan="1">Function</th><th align="left" rowspan="1" colspan="1">Reference</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Orexin</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B100" ref-type="bibr">100</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Ornate wrasse</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B101" ref-type="bibr">101</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Inhibit spawning behavior, decrease GnRH2 mRNA level</td><td align="left" rowspan="1" colspan="1">(<xref rid="B102" ref-type="bibr">102</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">NPY</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B103" ref-type="bibr">103</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Rainbow trout</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B104" ref-type="bibr">104</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Puffer fish</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B105" ref-type="bibr">105</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Zebrafish</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B106" ref-type="bibr">106</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Stimulate GnRH and LH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B107" ref-type="bibr">107</xref>, <xref rid="B108" ref-type="bibr">108</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Common carp</td><td align="left" rowspan="1" colspan="1">Increase plasma LH level</td><td align="left" rowspan="1" colspan="1">(<xref rid="B109" ref-type="bibr">109</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Sea bream</td><td align="left" rowspan="1" colspan="1">Stimulate GnRH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B110" ref-type="bibr">110</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Sea bass</td><td align="left" rowspan="1" colspan="1">Increase plasma LH level</td><td align="left" rowspan="1" colspan="1">(<xref rid="B111" ref-type="bibr">111</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">PACAP</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B112" ref-type="bibr">112</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Stimulate LH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B113" ref-type="bibr">113</xref>, <xref rid="B114" ref-type="bibr">114</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Tilapia</td><td align="left" rowspan="1" colspan="1">Stimulate GTH subunit mRNA expression</td><td align="left" rowspan="1" colspan="1">(<xref rid="B115" ref-type="bibr">115</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Blue gourami</td><td align="left" rowspan="1" colspan="1">Stimulate FSHβ mRNA expression</td><td align="left" rowspan="1" colspan="1">(<xref rid="B116" ref-type="bibr">116</xref>, <xref rid="B117" ref-type="bibr">117</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">GnRH2</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B118" ref-type="bibr">118</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Zebrafish</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B119" ref-type="bibr">119</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Stimulate LH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B120" ref-type="bibr">120</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">26RFa</td><td align="left" rowspan="1" colspan="1">Mouse</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B121" ref-type="bibr">121</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Increase plasma LH level</td><td align="left" rowspan="1" colspan="1">(<xref rid="B122" ref-type="bibr">122</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">Galanin</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B123" ref-type="bibr">123</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Tench</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B124" ref-type="bibr">124</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">(Rat)</td><td align="left" rowspan="1" colspan="1">Stimulate GnRH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B125" ref-type="bibr">125</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">MCH</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B126" ref-type="bibr">126</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Stimulate LH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B127" ref-type="bibr">127</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">α-MSH</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B128" ref-type="bibr">128</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Rainbow trout</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B129" ref-type="bibr">129</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">(Mouse)</td><td align="left" rowspan="1" colspan="1">Stimulate GnRH neurons</td><td align="left" rowspan="1" colspan="1">(<xref rid="B130" ref-type="bibr">130</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">CART</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B131" ref-type="bibr">131</xref>, <xref rid="B132" ref-type="bibr">132</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">(Rat)</td><td align="left" rowspan="1" colspan="1">Stimulate GnRH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B133" ref-type="bibr">133</xref>, <xref rid="B134" ref-type="bibr">134</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">CCK</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B135" ref-type="bibr">135</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Stimulate LH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B136" ref-type="bibr">136</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">Nesfatin-1</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B137" ref-type="bibr">137</xref>, <xref rid="B138" ref-type="bibr">138</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Decrease plasma LH level</td><td align="left" rowspan="1" colspan="1">(<xref rid="B139" ref-type="bibr">139</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">Leptin</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B140" ref-type="bibr">140</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Rainbow trout</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B141" ref-type="bibr">141</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Sea bass</td><td align="left" rowspan="1" colspan="1">Stimulate LH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B142" ref-type="bibr">142</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Rainbow trout</td><td align="left" rowspan="1" colspan="1">Stimulate LH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B143" ref-type="bibr">143</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1">Ghrelin</td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Increase food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B144" ref-type="bibr">144</xref>–<xref rid="B146" ref-type="bibr">146</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Rainbow trout</td><td align="left" rowspan="1" colspan="1">Decrease food intake</td><td align="left" rowspan="1" colspan="1">(<xref rid="B147" ref-type="bibr">147</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Goldfish</td><td align="left" rowspan="1" colspan="1">Stimulate LH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B148" ref-type="bibr">148</xref>)</td></tr><tr><td align="left" rowspan="1" colspan="1"></td><td align="left" rowspan="1" colspan="1">Common carp</td><td align="left" rowspan="1" colspan="1">Stimulate LH release</td><td align="left" rowspan="1" colspan="1">(<xref rid="B149" ref-type="bibr">149</xref>)</td></tr></tbody></table></table-wrap><sec id="S3-4"><title>Orexin</title><p>Orexin has two well conserved molecular forms, a 33-amino acid peptide known as orexin A (OXA) and a 28-amino acid peptide known as orexin B (OXB) derived from the same precursor [see review in Ref. (<xref rid="B150" ref-type="bibr">150</xref>)]. Orexin was first identified as a ligand of an orphan receptor, and consequently found to stimulate feeding in mammals (<xref rid="B151" ref-type="bibr">151</xref>). The orexin’s orexigenic action is also observed in teleosts, including the goldfish and the ornate wrasse (<xref rid="B101" ref-type="bibr">101</xref>, <xref rid="B152" ref-type="bibr">152</xref>).</p><p>In mammals, orexin is known to stimulate the HPG axis via GnRH secretion (<xref rid="B153" ref-type="bibr">153</xref>–<xref rid="B155" ref-type="bibr">155</xref>). In the goldfish, an interaction between orexin and hypophysiotropic GnRH (GnRH2) has also been proposed. Intracerebroventricular administrations of OXA inhibit spawning behavior and lower GnRH2 mRNA levels, while treatment with GnRH decreases OXA mRNA levels (<xref rid="B102" ref-type="bibr">102</xref>). These results suggest that, unlike in mammals, orexins might act as inhibitory agents in the control of GnRH at least in some fish species. In addition, OXA is detected in the pituitary of the medaka (<xref rid="B156" ref-type="bibr">156</xref>) and the Japanese sea perch (<xref rid="B157" ref-type="bibr">157</xref>), whilst OXB is detected in the pituitary of the Nile tilapia (<xref rid="B158" ref-type="bibr">158</xref>), suggesting orexin’s local action at the level of pituitary. Thus orexin, an orexigenic neuropeptide, inhibits the HPG axis at the hypothalamus GnRH level and possibly also at the pituitary level, in fish.</p></sec><sec id="S3-5"><title>Neuropeptide-Y (NPY)</title><p>NPY which is composed of 36 amino acid residues, was first identified in the porcine brain (<xref rid="B159" ref-type="bibr">159</xref>), and was found to function as a powerful appetite enhancer in mammals (<xref rid="B160" ref-type="bibr">160</xref>). In fish species, NPY also show powerful orexigenic activity in the goldfish (<xref rid="B103" ref-type="bibr">103</xref>, <xref rid="B123" ref-type="bibr">123</xref>, <xref rid="B161" ref-type="bibr">161</xref>–<xref rid="B164" ref-type="bibr">164</xref>), trout (<xref rid="B104" ref-type="bibr">104</xref>), puffer fish (<xref rid="B105" ref-type="bibr">105</xref>, <xref rid="B165" ref-type="bibr">165</xref>), and the zebrafish (<xref rid="B106" ref-type="bibr">106</xref>).</p><p>Centrally or peripherally injected NPY increases plasma LH levels in the goldfish, common carp, rainbow trout, and in the sea bass (<xref rid="B107" ref-type="bibr">107</xref>, <xref rid="B109" ref-type="bibr">109</xref>, <xref rid="B111" ref-type="bibr">111</xref>), indicating that NPY stimulates teleost reproduction as was shown in mammals (<xref rid="B166" ref-type="bibr">166</xref>).</p><p>In the brown trout (<xref rid="B167" ref-type="bibr">167</xref>) and the rainbow trout (<xref rid="B168" ref-type="bibr">168</xref>), NPY neuronal fibers project to the areas where hypophysiotropic GnRH neurons exist, particularly in the ventral telencephalon, POA, and in the basal hypothalamus. Furthermore, double immunolabeling reveals close appositions of NPY fibers with GnRH cells in the POA of the ayu (<italic>Plecoglossus altivelis</italic>) (<xref rid="B169" ref-type="bibr">169</xref>) and the Siberian sturgeon (<xref rid="B170" ref-type="bibr">170</xref>), suggesting the direct action of NPY in the regulation of GnRH neurons. Indeed, NPY stimulates GnRH release <italic>in vitro</italic> in the goldfish (<xref rid="B108" ref-type="bibr">108</xref>) and in the sea bream (<xref rid="B110" ref-type="bibr">110</xref>).</p><p>Neuropeptide-Y also regulates the HPG axis at the level of pituitary. <italic>In vitro</italic> treatment with NPY stimulates LH release from pituitary cells in the goldfish (<xref rid="B107" ref-type="bibr">107</xref>) and increases LHβ and GTHα, but not FSHβ mRNA levels in the tilapia pituitary (<xref rid="B115" ref-type="bibr">115</xref>). In addition, NPY fibers make close appositions on LH cells in the catfish pituitary (<xref rid="B171" ref-type="bibr">171</xref>).</p><p>These findings provide strong support for the stimulatory role of NPY in fish reproduction at the levels of hypothalamic GnRH and pituitary LH cells.</p></sec><sec id="S3-6"><title>26RFamide (QRFP)</title><p>26RFamide is a 26-amino acid peptide, and was first isolated from the frog brain (<xref rid="B121" ref-type="bibr">121</xref>). In teleosts, 26RFa has been identified only in the goldfish (<xref rid="B172" ref-type="bibr">172</xref>). The 26RFa gene is highly expressed in the hypothalamus, and relatively less in the optic tectum-thalamus and in the testis (<xref rid="B122" ref-type="bibr">122</xref>). 26RFa and its mammalian homolog QRFP act as an orexigenic hormone in birds, mice (<xref rid="B121" ref-type="bibr">121</xref>, <xref rid="B172" ref-type="bibr">172</xref>–<xref rid="B174" ref-type="bibr">174</xref>), and probably in fish (<xref rid="B122" ref-type="bibr">122</xref>).</p><p>The role of 26RFa has been implicated in the integration of metabolism and reproduction in vertebrates, including fish [see review in Ref. (<xref rid="B89" ref-type="bibr">89</xref>)]. In mammals, 26RFa stimulates LH and FSH release in rats <italic>in vivo</italic> and <italic>in vitro</italic> (pituitary culture) (<xref rid="B175" ref-type="bibr">175</xref>). In teleost, intraperitoneal injections of 26RFa significantly increase plasma LH levels in the goldfish (<xref rid="B122" ref-type="bibr">122</xref>). On the other hand, <italic>in vitro</italic> treatment with 26RFa shows no effects on LH release from pituitary cells. These facts indicate that 26RFa might act on the stimulation of the HPG axis through GnRH1 release in fish.</p></sec><sec id="S3-7"><title>Galanin (GAL)</title><p>GAL is a 29-amino acid peptide, expressed in the central nervous system and in the intestine. GAL stimulates feeding in the goldfish (<xref rid="B123" ref-type="bibr">123</xref>) and the doctor fish tench (<xref rid="B124" ref-type="bibr">124</xref>), indicating that GAL acts as an orexigenic hormone in fish as in mammals (<xref rid="B176" ref-type="bibr">176</xref>, <xref rid="B177" ref-type="bibr">177</xref>).</p><p>Involvement of GAL in the control of HPG axis is evidenced in mammals. In rodents and humans, GAL neuronal fibers make close appositions with GnRH1 neurons (<xref rid="B178" ref-type="bibr">178</xref>–<xref rid="B180" ref-type="bibr">180</xref>), and GnRH neurons express a GAL receptor Gal-R1 in the rat (<xref rid="B181" ref-type="bibr">181</xref>). In fact, GAL stimulates <italic>in vitro</italic> GnRH release in rats (<xref rid="B125" ref-type="bibr">125</xref>). These data indicate that GAL is involved in the control of reproduction at the level of GnRH neurons.</p><p>In fish, there are no studies that demonstrated the role of GAL in the control of reproduction. However, close appositions of GAL fibers with gonadotropes in the proximal pars distalis (PPD) are seen in the sea bass (<xref rid="B182" ref-type="bibr">182</xref>). Similarly, fiber projections of GAL neurons in the PPD are observed in the rainbow trout (<xref rid="B183" ref-type="bibr">183</xref>), sea bream (<xref rid="B184" ref-type="bibr">184</xref>), and Senegalese sole (<xref rid="B185" ref-type="bibr">185</xref>), while no GAL fibers are observed in the pituitary of the Siberian sturgeon (<xref rid="B170" ref-type="bibr">170</xref>). Therefore, GAL might modulate the HPG axis at the pituitary level at least in some fish species.</p></sec><sec id="S3-8"><title>GnRH2</title><p>As mentioned before, among the different forms of GnRH, neuronal fibers of GnRH2 (also known as chicken GnRH-II) are widely distributed in the vertebrate brain. In an insectivore, the musk shrew, GnRH2 stimulates sexual behavior and seduces food intake (<xref rid="B186" ref-type="bibr">186</xref>, <xref rid="B187" ref-type="bibr">187</xref>), indicating that GnRH2 plays a role in connecting reproductive function and feeding regulation.</p><p>In fish species, the suppressive effect of GnRH2 on feeding has also been confirmed. Food consumption is significantly decreased by intracerebroventricular injections of GnRH2 but not GnRH3 in a dose dependent manner in the goldfish (<xref rid="B102" ref-type="bibr">102</xref>, <xref rid="B118" ref-type="bibr">118</xref>) and the zebrafish (<xref rid="B119" ref-type="bibr">119</xref>).</p><p>GnRH2 also has effects on sexual behavior of fish. In the goldfish, GnRH2 stimulates reproductive behavior (<xref rid="B188" ref-type="bibr">188</xref>). Furthermore, there is a strong positive correlation between spawning behavior and GnRH2 gene expression (<xref rid="B189" ref-type="bibr">189</xref>), suggesting stimulatory role of GnRH2 in reproductive behavior. GnRH2 is also detected in the goldfish pituitary (<xref rid="B190" ref-type="bibr">190</xref>) and induces LH release <italic>in vitro</italic> (<xref rid="B120" ref-type="bibr">120</xref>). Positive correlation between the pituitary GnRH2 levels and gonadal development is also observed in the striped bass (<xref rid="B51" ref-type="bibr">51</xref>), suggesting that it also have a hypophysiotropic role in some fish species. In the grass puffer, the amount of GnRH2 mRNA is slightly higher in the post-spawning females compared to spawning female (<xref rid="B191" ref-type="bibr">191</xref>). Therefore, GnRH2 may have different physiological roles depending on the physiological conditions of the fish.</p></sec><sec id="S3-9"><title>Pituitary adenylate cyclase-activating polypeptide (PACAP)</title><p>PACAP was first isolated from the rat hypothalamus (<xref rid="B192" ref-type="bibr">192</xref>). PACAP is an anorexigenic factor in various vertebrates, including rodents (<xref rid="B193" ref-type="bibr">193</xref>), chicks (<xref rid="B194" ref-type="bibr">194</xref>, <xref rid="B195" ref-type="bibr">195</xref>), and fish (<xref rid="B196" ref-type="bibr">196</xref>). To date, the role of PACAP in feeding has been studied only in one fish species, the goldfish.</p><p>PACAP increases plasma LH levels <italic>in vivo</italic> in the goldfish (<xref rid="B197" ref-type="bibr">197</xref>). <italic>In vitro</italic> studies showed that the stimulatory effect of PACAP on LH release is exerted at the level of the pituitary (<xref rid="B113" ref-type="bibr">113</xref>, <xref rid="B114" ref-type="bibr">114</xref>). PACAP also stimulates the levels of GTH subunit mRNAs and FSHβ mRNA in the pituitary of tilapia (<xref rid="B115" ref-type="bibr">115</xref>) and in the female blue gourami (<xref rid="B116" ref-type="bibr">116</xref>, <xref rid="B117" ref-type="bibr">117</xref>), respectively. Dense projection of PACAP nerve terminals is seen in the pars distalis of the pituitary, where gonadotropes are localized, in the goldfish (<xref rid="B198" ref-type="bibr">198</xref>) and in the European eel (<xref rid="B199" ref-type="bibr">199</xref>). The expression of PACAP receptor in the pituitary is also observed in the goldfish (<xref rid="B197" ref-type="bibr">197</xref>). Therefore, PACAP stimulates GTH secretion in fish pituitary.</p></sec><sec id="S3-10"><title>Melanin-concentrating hormone (MCH)</title><p>MCH is a cyclic peptide, originally isolated from the pituitary of the chum salmon as a hormone involved in body color change (<xref rid="B200" ref-type="bibr">200</xref>). In the winter and barfin flounders, fasting stimulates hypothalamic expression of MCH (<xref rid="B201" ref-type="bibr">201</xref>, <xref rid="B202" ref-type="bibr">202</xref>), suggesting that MCH acts as an orexigenic hormone as in mammals (<xref rid="B203" ref-type="bibr">203</xref>, <xref rid="B204" ref-type="bibr">204</xref>). However, MCH acts as an anorexigenic hormone in the goldfish (<xref rid="B105" ref-type="bibr">105</xref>, <xref rid="B126" ref-type="bibr">126</xref>, <xref rid="B205" ref-type="bibr">205</xref>, <xref rid="B206" ref-type="bibr">206</xref>). Therefore, like ghrelin, MCH acts as an orexigenic and anorexigenic neuropeptide depending on the fish species, although its orexigenic action in fish has to be confirmed.</p><p>In mammals, MCH modulates LH secretion in an estradiol-dependent manner [see a review in Ref. (<xref rid="B207" ref-type="bibr">207</xref>)]. The close appositions between MCH fibers and hypothalamic GnRH neurons (<xref rid="B208" ref-type="bibr">208</xref>, <xref rid="B209" ref-type="bibr">209</xref>) and the expression of MCH receptors in GnRH neurons (<xref rid="B209" ref-type="bibr">209</xref>) suggest the direct action of MCH on GnRH neurons in mammals. MCH also acts at the pituitary level to modulate the release of LH (<xref rid="B210" ref-type="bibr">210</xref>). In teleosts, an <italic>in vitro</italic> study showed that salmon MCH stimulates the release of LH in a dose response manner from dispersed pituitary cells in the goldfish, suggesting a direct action of MCH on LH cells (<xref rid="B127" ref-type="bibr">127</xref>). Whether MCH acts on GnRH neurons in fish as in mammals remains unknown.</p></sec><sec id="S3-11"><title>α-Melanocyte stimulating hormone (α-MSH)</title><p>α-MSH is one of melanocortins and derived from a precursor peptide encoded by the POMC gene (<xref rid="B211" ref-type="bibr">211</xref>). Among melanocortins and their receptors, α-MSH and melanocortin receptor 4 (MC4R) are involved in the control of food intake in vertebrates including fish. α-MSH or MC4R agonist inhibits food intake in the goldfish (<xref rid="B128" ref-type="bibr">128</xref>, <xref rid="B212" ref-type="bibr">212</xref>) and in the rainbow trout (<xref rid="B129" ref-type="bibr">129</xref>), suggesting that the α-MSH/MC4R system play a role in the anorexigenic regulation of feeding in fish as in mammals.</p><p>Although the α-MSH/MC4R system is known to play a stimulatory role in reproduction at the level of GnRH neurons in mammals [see a review in Ref. (<xref rid="B130" ref-type="bibr">130</xref>)], available information is limited in teleost. Projection of α-MSH fibers in the PPD of the pituitary and differential expression of POMC gene between sexually inactive and active fish in the zebrafish suggests that some of POMC-derived products are involved in the stimulation of fish reproduction (<xref rid="B213" ref-type="bibr">213</xref>).</p></sec><sec id="S3-12"><title>Cocaine- and amphetamine-regulated transcript (CART)</title><p>CART is an anorexigenic neuropeptide originally isolated from the rat brain (<xref rid="B160" ref-type="bibr">160</xref>, <xref rid="B214" ref-type="bibr">214</xref>). In fish, CART might also act as anorexigenic hormone in the goldfish (<xref rid="B131" ref-type="bibr">131</xref>), winter flounder (<xref rid="B215" ref-type="bibr">215</xref>), cod (<xref rid="B216" ref-type="bibr">216</xref>), channel catfish (<xref rid="B217" ref-type="bibr">217</xref>), zebrafish (<xref rid="B218" ref-type="bibr">218</xref>), and in the Atlantic salmon (<xref rid="B219" ref-type="bibr">219</xref>).</p><p>In mammals, CART is involved in the control of GnRH neurons. CART stimulates GnRH pulsatile release in rats (<xref rid="B133" ref-type="bibr">133</xref>, <xref rid="B134" ref-type="bibr">134</xref>). The existence of close appositions between CART fibers and hypothalamic GnRH neurons in the Siberian hamster suggests the effect of CART on GnRH neuronal activity is a direct action (<xref rid="B220" ref-type="bibr">220</xref>).</p><p>In the catfish, the projections of CART fibers are observed in the PPD of the pituitary (<xref rid="B221" ref-type="bibr">221</xref>). CART is also expressed in LH cells of the catfish pituitary but only during sexual maturation period (<xref rid="B222" ref-type="bibr">222</xref>), suggesting its local function in the sexual maturation process. However, it should be noted that while similar expression of CART in LH cells is observed in the rat pituitary, CART inhibits the release of prolactin but not GTHs (<xref rid="B223" ref-type="bibr">223</xref>). Thus, the role of CART in the fish pituitary has to be examined.</p></sec><sec id="S3-13"><title>Cholecystokinin (CCK)</title><p>CCK is found in the brain and in the gastrointestinal tract of various vertebrates. It has multiple biologically active forms, among which CCK-8 is the most abundant form in the brain (<xref rid="B224" ref-type="bibr">224</xref>). As in mammals, CCK has many physiological roles in fish, but functions primarily in the control of food intake as a satiety indicator (<xref rid="B135" ref-type="bibr">135</xref>).</p><p>In mammals, CCK decreases the pulse interval of GnRH release in goats (<xref rid="B225" ref-type="bibr">225</xref>). Furthermore, CCK implants into the POA, where GnRH neurons are located, increase the plasma levels of LH in rats (<xref rid="B226" ref-type="bibr">226</xref>). These data suggest that CCK acts at the levels of GnRH and stimulates reproduction. In fish, on the other hand, CCK seems to acts on the pituitary. An immunohistochemical study showed that CCK neurons innervate into the PPD of the pituitary and that CCK stimulates LH release <italic>in vitro</italic> in the goldfish (<xref rid="B136" ref-type="bibr">136</xref>).</p></sec><sec id="S3-14"><title>Nesfatin-1</title><p>Nesfatin-1, a nucleobindin-2 (NUCB2) encoded unmodified peptide, was first characterized in rats (<xref rid="B227" ref-type="bibr">227</xref>), and was shown to have anorexigenic actions in the goldfish (<xref rid="B137" ref-type="bibr">137</xref>, <xref rid="B138" ref-type="bibr">138</xref>).</p><p>The number of studies about the function of nesfatin-1 in the control of reproduction is still limited. However, recent studies showed that nesfatin-1 acts as an inhibitory signal in the control of fish reproduction. Although nesfatin-1 plays a stimulatory role in LH secretion in rats (<xref rid="B228" ref-type="bibr">228</xref>), an intraperitoneal injection of nesfatin-1 decreases plasma levels of LH in the goldfish (<xref rid="B139" ref-type="bibr">139</xref>). At the same time, nesfatin-1 down regulates expression of GnRH, LHβ, and FSHβ genes, suggesting that the inhibitory action of nesfatin-1 takes place at the levels of GnRH neurons. Whether nesfatin-1 also functions at the level of the pituitary remains unclear.</p></sec></sec><sec id="S4"><title>Peripheral Hormones Involved in Feeding, Metabolism, and Reproduction</title><sec id="S4-15"><title>Leptin</title><p>Leptin is primarily produced by adipocytes of the white adipose tissue (<xref rid="B229" ref-type="bibr">229</xref>), and secreted into the blood circulation in proportion to the mass of body fat. The change in plasma leptin levels is detected by the hypothalamus and thereby it acts as a peripheral factor that signals nutritional status to the CNS [see review by Crown et al. (<xref rid="B230" ref-type="bibr">230</xref>)]. In teleosts including the goldfish and the rainbow trout, leptin functions as a peripheral signal to inhibit food intake (<xref rid="B140" ref-type="bibr">140</xref>, <xref rid="B141" ref-type="bibr">141</xref>, <xref rid="B231" ref-type="bibr">231</xref>, <xref rid="B232" ref-type="bibr">232</xref>) as in mammals (<xref rid="B233" ref-type="bibr">233</xref>).</p><p>In mammals, leptin stimulates the HPG axis by promoting the synthesis and release of GnRH from the hypothalamus, and LH and FSH from the pituitary (<xref rid="B234" ref-type="bibr">234</xref>–<xref rid="B236" ref-type="bibr">236</xref>). In teleosts, leptin also stimulates the reproductive axis. Leptin increases <italic>in vitro</italic> LH release from the pituitary culture in the sea bass (<xref rid="B142" ref-type="bibr">142</xref>) and the rainbow trout (<xref rid="B143" ref-type="bibr">143</xref>). However, it should be noted that the stimulating effect of leptin on LH release is observed only on the pituitary samples from the fish in maturational stages. Furthermore, leptin expression levels increase with the onset of sexual maturation in the Arctic char (<xref rid="B237" ref-type="bibr">237</xref>) and the Atlantic salmon (<xref rid="B238" ref-type="bibr">238</xref>). Therefore, the role of leptin in sexual maturation seems to be conserved among vertebrate species.</p></sec><sec id="S4-16"><title>Ghrelin</title><p>As in mammals, ghrelin is highly expressed in the stomach and moderately in the brain (<xref rid="B144" ref-type="bibr">144</xref>, <xref rid="B239" ref-type="bibr">239</xref>, <xref rid="B240" ref-type="bibr">240</xref>), and is involved in appetite stimulation, energy balance, feeding, and metabolism [see reviews in Ref. (<xref rid="B241" ref-type="bibr">241</xref>, <xref rid="B242" ref-type="bibr">242</xref>)]. Interestingly, the role of ghrelin in fish differs in different fish species. It acts as an orexigenic hormone in the goldfish (<xref rid="B144" ref-type="bibr">144</xref>–<xref rid="B146" ref-type="bibr">146</xref>) and probably in the sea bass (<xref rid="B243" ref-type="bibr">243</xref>) and the zebrafish (<xref rid="B244" ref-type="bibr">244</xref>). On the other hand, ghrelin acts as an anorexigenic hormone in the rainbow trout (<xref rid="B147" ref-type="bibr">147</xref>) and probably in the burbot (<xref rid="B245" ref-type="bibr">245</xref>, <xref rid="B246" ref-type="bibr">246</xref>). The opposite effects of ghrelin on food intake can be explained by species-specific neural pathways mediating the effect of ghrelin (<xref rid="B247" ref-type="bibr">247</xref>). The variations in the role of ghrelin in feeding may reflect different regulatory mechanisms of feeding in different teleost species.</p><p>In fish species, ghrelin acts as a stimulatory factor in the reproduction, although ghrelin inhibits the HPG axis in mammals [reviewed by Tena-Sempere (<xref rid="B248" ref-type="bibr">248</xref>)]. Intracerebroventricular injection of ghrelin increases plasma LH levels in the goldfish (<xref rid="B148" ref-type="bibr">148</xref>), indicating its stimulatory action on the HPG axis. The increase of plasma LH levels is, however, small and slow compared to the increase of plasma GH levels. This suggests that the stimulatory effect of ghrelin on plasma LH levels is not through the action of ghrelin on hypothalamic GnRH. Actually, the highest levels of ghrelin receptor mRNA are observed in the sea bream and goldfish pituitary (<xref rid="B249" ref-type="bibr">249</xref>, <xref rid="B250" ref-type="bibr">250</xref>). <italic>In vitro</italic> treatment with ghrelin stimulates LH release in the goldfish (<xref rid="B148" ref-type="bibr">148</xref>, <xref rid="B250" ref-type="bibr">250</xref>) and in the common carp (<xref rid="B149" ref-type="bibr">149</xref>), while pituitary levels of mRNA for LHβ subunit is also increased. As no reports show fiber projections of hypothalamic ghrelin neurons into the pituitary in fish, ghrelin released from stomach/intestine might play a role in the LH secretion from the pituitary. Therefore, ghrelin might act as a stimulatory peripheral factor in reproduction at the level of pituitary, whereas its action on GnRH neurons is uncertain.</p></sec></sec><sec id="S5"><title>Interactions between Metabolic Neuropeptides and the Reproductive System in the Control of Reproduction</title><p>As shown in the above section, many metabolic neuropeptides are involved in the control of reproduction at the level of hypothalamic GnRH neurons and at the level of pituitary gonadotropes (Figure <xref ref-type="fig" rid="F1">1</xref>). Among these metabolic neuropeptides, NPY and nesfatin-1 function as inhibitory factors on GnRH neurons, while orexin stimulates GnRH neurons. It is interesting that NPY and orexin, which possess orexigenic activity, act on the reproductive system in an opposite manner in the goldfish. It suggests that different metabolic neuropeptides might play a role in the control of reproduction under different physiological conditions. It should be noted, however, that the inhibitory role of orexin on spawning behavior and GnRH gene expression might be the result of orexin action on non-hypophysiotropic GnRH system. In the goldfish brain, hypophysiotropic GnRH type is expressed not only in the hypothalamic population but also in the olfactory bulb and midbrain populations (<xref rid="B190" ref-type="bibr">190</xref>). Therefore, the inhibitory effect of orexin on the HPG axis need to be confirmed although it is clear that orexin has suppressive role in some aspects of reproduction.</p><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold>Effects of central and peripheral metabolic hormones on the reproductive system</bold>. The hypothalamus–pituitary axis receives many stimulatory and inhibitory inputs from central metabolic neuropeptide neurons and peripheral metabolic signals to control the reproductive system according to the energy status. The hormones indicated with blue circles are orexigenic hormones, while those with orange squares are anorexigenic ones. Red lines indicate stimulatory action and blue lines indicate inhibitory action. Most anorexigenic hormones stimulate gonadotropin secretion at the pituitary level. In the goldfish, NPY and ghrelin, which act as orexigenic hormones, also stimulate the reproductive system at the brain and pituitary levels. It should be noted that this figure is drew primarily based on the information obtained from the goldfish. Function of each metabolic hormone might differ in different species [e.g., Ghrelin functions as an anorexigenic factor in the rainbow trout (<xref rid="B147" ref-type="bibr">147</xref>) and GnIH stimulates GTH subunit mRNA expression in the puffer fish (<xref rid="B97" ref-type="bibr">97</xref>) and the sockeye salmon (<xref rid="B92" ref-type="bibr">92</xref>).]. CCK, cholecystokinin; GnIH, gonadotropin-inhibitory hormone; GnRH, gonadotropin-releasing hormone; MCH, melanin-concentrating hormone; NPY, neuropeptide-Y; PACAP, pituitary adenylate cyclase-activating polypeptide.</p></caption><graphic xlink:href="fendo-05-00036-g001"></graphic></fig><p>At the pituitary level, it is evident that many metabolic neuropeptides including NPY, MCH, GnRH2, PACAP, and CCK stimulate LH secretion. In addition, peripheral metabolic signals such as ghrelin and leptin also stimulate LH secretion at the pituitary. The fact that most central neuropeptides and peripheral metabolic signals regulate the reproductive system indicates fundamental interaction between energy balance and reproduction, which is evolutionarily conserved from fish to mammal. However, both orexigenic and anorexigenic metabolic signals act as stimulatory factors in the reproductive system in fish. In mammals, feeding and reproduction are two alternatives in general. Therefore, orexigenic factors inhibit reproduction and anorexigenic factors stimulate reproduction [see review in Ref. (<xref rid="B251" ref-type="bibr">251</xref>)]. In fish species, on the other hand, a central orexigenic neuropeptide NPY and a peripheral orexigenic peptide ghrelin inhibit LH secretion in the goldfish and other species (Table <xref ref-type="table" rid="T1">1</xref>). This indicates that metabolic regulation of the reproductive system in teleost is different from that in mammals, at least in some species.</p><p>Fish species have a variety of feeding and reproductive behaviors. For example, most salmonids and the winter flounder undergo a period of fasting just before the spawning season as a part of their normal physiology (<xref rid="B252" ref-type="bibr">252</xref>), whereas the goldfish do not have such fasting period. The halt of food intake during final maturation might require the differential usage of metabolic signals in these species.</p><p>Recently, kisspeptin has been proposed as a mediator of metabolic signals in the mammalian reproductive system, in particular on GnRH neurons [see reviews in Ref. (<xref rid="B89" ref-type="bibr">89</xref>, <xref rid="B253" ref-type="bibr">253</xref>)]. In mice (<xref rid="B254" ref-type="bibr">254</xref>) and in the sheep (<xref rid="B255" ref-type="bibr">255</xref>), kisspeptin neurons in the arcuate nucleus possess leptin receptors, suggesting direct action of leptin on kisspeptin neurons. Furthermore, kisspeptin neurons receive innervations from other neurons that express leptin receptor (<xref rid="B255" ref-type="bibr">255</xref>). These facts suggest that leptin controls GnRH neurons through kisspeptin neurons <italic>via</italic> direct and indirect actions. Furthermore, kisspeptin neurons receive fiber projections from NPY and POMC neurons in mammals (<xref rid="B255" ref-type="bibr">255</xref>, <xref rid="B256" ref-type="bibr">256</xref>). Therefore kisspeptin neurons might play an important role in the integration of metabolic signals to control the reproductive system. In teleost, fasting induces a significant increase in <italic>kiss2</italic> mRNA levels in the hypothalamus, as well as an increase in LHβ and FSHβ mRNA levels in the pituitary in the Senegalese sole (<italic>Solea senegalensis</italic>) (<xref rid="B257" ref-type="bibr">257</xref>), suggesting negative correlation between energy balance and reproduction. However, to our knowledge, there is no information available regarding direct evidence of metabolic regulation of kisspeptin neurons in fish.</p><p>In addition to its primary role in reproduction, GnIH stimulates food intake in chickens (<xref rid="B258" ref-type="bibr">258</xref>) and in rats (<xref rid="B259" ref-type="bibr">259</xref>, <xref rid="B260" ref-type="bibr">260</xref>), suggesting its potential role to switch from reproduction to feeding. Close appositions of GnIH fibers with NPY, orexin, MCH, and POMC neurons in the sheep (<xref rid="B261" ref-type="bibr">261</xref>) indicate the involvement of several feeding regulatory pathways. However, there are no studies reporting metabolic regulation of GnIH neurons in vertebrates. On the other hand, GnIH is known to be regulated by stress, photoperiod, and gonadal steroids to suppress the reproductive system (<xref rid="B89" ref-type="bibr">89</xref>). Therefore, GnIH neurons might have a role in the modulation of feeding according to the environmental factors in mammals. Whether GnIH plays a similar role in teleosts requires more studies.</p></sec><sec id="S6"><title>Interactions among Neuropeptides to Control Feeding</title><p>To monitor the amount of energy stock, central metabolic neuropeptide neurons receive peripheral signals including leptin and ghrelin. For example, in mammals leptin receptor is expressed in many metabolic neuropeptide neurons including orexin, NPY, GAL, MCH, POMC, CART, and CCK neurons [see reviews in Ref. (<xref rid="B262" ref-type="bibr">262</xref>, <xref rid="B263" ref-type="bibr">263</xref>)]. In fish species, leptin also affects several central neuropeptide neurons. Administration of leptin reduces NPY mRNA levels in the goldfish (<xref rid="B140" ref-type="bibr">140</xref>), grass carp (<xref rid="B264" ref-type="bibr">264</xref>), and in the rainbow trout (<xref rid="B141" ref-type="bibr">141</xref>, <xref rid="B265" ref-type="bibr">265</xref>). On the other hand, leptin increases the mRNA levels of CCK and POMC, which are anorexigenic neuropeptides, in the goldfish (<xref rid="B140" ref-type="bibr">140</xref>) and the rainbow trout (<xref rid="B141" ref-type="bibr">141</xref>, <xref rid="B265" ref-type="bibr">265</xref>), respectively. A recent study showed that leptin receptor knockout medaka exhibit higher levels of NPY mRNA before and after feeding and lower levels of POMC mRNA levels after feeding together with increased food intake (<xref rid="B266" ref-type="bibr">266</xref>). Therefore leptin’s anorexigenic effect might be mediated by these neuropeptides.</p><p>Double immunostaining revealed interactions among orexigenic/anorexigenic neuropeptide neurons in teleosts, in particular in the goldfish (Figure <xref ref-type="fig" rid="F2">2</xref>). Among anorexigenic neuropeptide neurons, MCH neuronal fibers project to α-MSH neurons (<xref rid="B206" ref-type="bibr">206</xref>) and α-MSH neuronal fibers project to CRH neurons (<xref rid="B267" ref-type="bibr">267</xref>). Furthermore, a study using antagonists against α-MSH receptor and CRH receptor showed that anorexigenic action of MCH is mediated by α-MSH and CRH (<xref rid="B268" ref-type="bibr">268</xref>). In addition, GnRH2 mediates anorexigenic effect of α-MSH and CRH (<xref rid="B269" ref-type="bibr">269</xref>). These results suggest that the MCH–α-MSH–CRH–GnRH2 pathway suppresses food intake in the goldfish, although it is not known whether CRH directly acts on GnRH2 neurons.</p><fig id="F2" position="float"><label>Figure 2</label><caption><p><bold>Interaction between the orexigenic circuit and anorexigenic circuit and among neurons in each circuit in the goldfish</bold>. Hormones in the orexigenic circuit are shown in blue and those in the anorexigenic circuit are shown in orange. The orexigenic and anorexigenic circuits are connected each other via inhibitory neuronal fiber projections to form an on-off switch. Reciprocal interaction is observed especially between neurons in the orexigenic circuit. Arrows with dotted lines indicate the interactions that have not been confirmed whether direct or indirect. The complex interaction among metabolic neuropeptides suggests that a change in one metabolic signal can affect the reproductive system through the action via other metabolic neuropeptides. Note that in the goldfish ghrelin secreted in the brain also function as an orexigenic signal. α-MSH, alpha-melanocyte stimulating hormone; CRH, corticotropin-releasing hormone; GAL, galanin; GnRH, gonadotropin-releasing hormone; MCH, melanin-concentrating hormone; NPY, neuropeptide-Y; OXA, orexin A; PACAP, pituitary adenylate cyclase-activating polypeptide.</p></caption><graphic xlink:href="fendo-05-00036-g002"></graphic></fig><p>Among orexigenic neuropeptide neurons, NPY and orexin neurons make reciprocal connections in fish as in mammals. NPY neuronal fibers make close appositions with orexin neurons, whereas orexin neuronal fibers make close appositions with NPY neurons in the NPPv in the goldfish (<xref rid="B270" ref-type="bibr">270</xref>). Furthermore, co-injections of OXA and NPY result in food intake higher than that observed in fish treated with NPY alone (<xref rid="B132" ref-type="bibr">132</xref>). These results indicate that orexins and NPY induce orexigenic actions by mutual signaling pathways in the CNS in teleost. Probably the reciprocal interaction between NPY and orexin functions as a positive-feedback system to maintain food intake.</p><p>Moreover, the orexigenic and the anorexigenic circuits are also connected with each other. α-MSH neuronal fibers make close appositions with NPY neurons, whereas NPY neuronal fibers project to α-MSH neurons in the goldfish (<xref rid="B271" ref-type="bibr">271</xref>). In addition, MCH neuronal fibers make close appositions with NPY neurons (<xref rid="B272" ref-type="bibr">272</xref>). These inhibitory inputs between the orexigenic and anorexigenic neurons might function as an on/off switch to decide whether eat or not eat by activating only one of the two circuits.</p><p>Studies using antagonists against of the receptors for metabolic neuropeptides further provided possible interaction among central metabolic neuropeptides in the goldfish. For example, GAL mediates the orexigenic action of orexin, and orexin mediates the orexigenic action of GAL (<xref rid="B123" ref-type="bibr">123</xref>). GAL also mediates NPY’s action on food intake and <italic>vice versa</italic> (<xref rid="B123" ref-type="bibr">123</xref>). Besides, orexin mediates central action of ghrelin in food intake and central ghrelin mediates the action of orexin (<xref rid="B273" ref-type="bibr">273</xref>). Furthermore, NPY mediates the orexigenic action of ghrelin (<xref rid="B274" ref-type="bibr">274</xref>). These results indicate complex neuronal interactions especially among central orexigenic neuropeptides. This complex neuronal network suggests that many central neuropeptide neurons function in a coordinated manner to regulate food intake. To fully understand the whole circuit that controls food intake, further information on the neuronal interaction among central metabolic neuropeptides have to be obtained.</p><p>In addition to the evident neuronal interactions in the goldfish, more combinations of neuronal interactions were reported in other fish species. In the masu salmon (<xref rid="B275" ref-type="bibr">275</xref>) and the Siberian sturgeon (<xref rid="B170" ref-type="bibr">170</xref>), NPY and GAL neurons make reciprocal connections. In the medaka, orexin and MCH neurons send neuronal fibers to each other (<xref rid="B156" ref-type="bibr">156</xref>). In the barfin flounder, reciprocal connection between orexin and MCH neurons and between α-MSH and MCH neurons was reported (<xref rid="B156" ref-type="bibr">156</xref>). In the rainbow trout, CRH mediates the anorexigenic action of ghrelin (<xref rid="B147" ref-type="bibr">147</xref>). These facts suggest that the interaction among central metabolic neuropeptides is really complicated. Therefore, more fiber projection studies together with the localization of the neuropeptide receptors are necessary to understand proper relationships among these neuropeptides that consist of the regulatory circuits of food intake.</p></sec><sec id="S7"><title>Perspectives</title><sec id="S7-17"><title>Direct interactions among central metabolic neuropeptides and reproductive system</title><p>Significant amount of information about the relationship among orexigenic and anorexigenic neuropeptides have been accumulated, particularly in the goldfish. However, the knowledge of direct interactions among these neurons is still not enough to draw a complete diagram of the neuronal circuit to control food intake and reproduction in fish. In particular, metabolic regulation of kisspeptin and GnRH neurons are still unknown, while it is suggested from mammalian studies. Further fiber projection studies using double immunostaining and localization of the neuropeptide receptors in certain neuronal cell bodies need to be performed.</p></sec><sec id="S7-18"><title>Species differences</title><p>There are many differences in the regulatory mechanism of food intake and reproduction not only between mammals and fish but also between fish species. The significant difference between fish species might be the result of the adaptation to a wide range of feeding habits and reproductive strategies. Therefore we have to be careful to combine data obtained from different species.</p></sec><sec id="S7-19"><title>Sex and maturational stages</title><p>Several studies reported that the responses of the reproductive system to metabolic signals differ depending on the sex and the stage of sexual maturation. In fact, gonadal steroids modulate the effect of NPY on GnRH and LH release in the goldfish (<xref rid="B276" ref-type="bibr">276</xref>). Each study should use a particular sex and maturational stage to make comparison easy.</p></sec><sec id="S7-20"><title>Nutritional conditions</title><p>Animals might change the metabolic control of reproduction according to the available energy stock. For example, short term food limitation attenuates sexual motivation, while remaining energy stock still maintains activity of the HPG axis. On the other hand, long term food limitation depletes the energy stock and stops the HPG axis to prioritize the energy supply to the survival. Thus, feeding conditions and the timing of experiment might be important to obtain comparable data.</p></sec><sec id="S7-21"><title>Endocannabinoid system</title><p>The endocannabinoid system is involved in a variety of physiology including pain-sensation, mood, and memory. Importantly, both energy balance and reproduction are modulated by the endocannabinoid system. Endocannabinoids modulate several hypothalamic metabolic neuropeptides in mammals [see reviews in Ref. (<xref rid="B277" ref-type="bibr">277</xref>, <xref rid="B278" ref-type="bibr">278</xref>)]. The endocannabinoid system also regulates food intake in fish (<xref rid="B279" ref-type="bibr">279</xref>, <xref rid="B280" ref-type="bibr">280</xref>). In mammalian and non-mammalian vertebrates, the endocannabinoid system regulates hypothalamic GnRH neurons and pituitary LH cells directly and indirectly [see reviews in Ref. (<xref rid="B281" ref-type="bibr">281</xref>, <xref rid="B282" ref-type="bibr">282</xref>)]. Interrelation among these systems might be an additional mechanism underlying the interaction between mood, stress, appetite, and reproduction.</p></sec></sec><sec id="S8"><title>Conclusion</title><p>In summary, the cellular and molecular basis for the integration of feeding and reproduction involves a complex interaction of the reproductive system with metabolic neuropeptides and peripheral fuels. The metabolic neuropeptides, particularly orexin, NPY, PACAP, MCH, nesfatin, GnRH2, and CCK play an important role in the reproduction by either regulating GnRH neurons in the hypothalamus or by stimulating gonadotropes in the pituitary. Peripheral metabolic signals such as ghrelin and leptin also act on the pituitary to stimulate LH secretion. It should be, however, noted that compared to mammals, fishes show a great variety of feeding and reproductive habits. The variations of metabolic control of reproduction in different teleost species may reflect different requirement of energy status for reproduction in different species. Compared to mammals, fish represent a vast phylogenetic group, which shows a significant level of diversity with regards to morphology, ecology, behavior, and genomes (<xref rid="B283" ref-type="bibr">283</xref>). Thus, species differences in the neuroendocrine control of reproduction have to be taken into consideration in teleosts. In addition, more detailed studies about the interconnections among metabolic neuropeptide neurons, effects of sexual maturation, and nutritional conditions will provide more precise figure of the metabolic control of reproduction. Furthermore, differential control of multiple GnRH neuronal population by the neuropeptides and metabolic signals should be examined to elucidate their roles in different aspects of metabolic control of reproduction.</p></sec><sec id="S9"><title>Conflict of Interest Statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></body><back><ack><p>This work was supported by grants from Monash University Malaysia, MM-2-5-06, MM-7-07, and MCG006 (to Ishwar S. 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