Abstract
Ghrelin, a gut-brain peptide hormone, is implicated in a multiplicity of biological functions, including energy homeostasis and reproduction. Neuronal systems that are involved in energy homeostasis as well as reproduction traverse the hypothalamus; however, the mechanism by which they control energy homeostasis is not fully understood. The present study analyzes the anatomical relationship of neurons expressing gonadotropin-releasing hormone (GnRH), neuropeptide Y (NPY) and growth hormone-releasing hormone (GHRH) in a cichlid, tilapia (Oreochromis niloticus). Additionally, we examine in vivo effects of ghrelin on these hypothalamic neurons and plasma growth hormone (GH) and insulin-like growth factor-1 (IGF-1) levels. Double-immunofluorescence showed neuronal fiber associations between GnRH, NPY and GHRH in the brain and pituitary. Intracerebroventricular injection of ghrelin had no effect on numbers, soma size, or optical density of GnRH and NPY neurons, whereas the number of GHRH neurons was significantly decreased in the animals injected with ghrelin when compared to controls, which may indicate administered ghrelin promoted GHRH release. Plasma GH and pituitary GH mRNA levels were significantly increased in the animals injected with ghrelin. These results suggest that central administration of ghrelin primarily act on hypothalamic GHRH neurons to stimulate GH release from the pituitary in the tilapia.
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Abbreviations
- GnRH:
-
Gonadotropin-releasing hormone
- NPY:
-
Neuropeptide Y
- GHRH:
-
Growth hormone-releasing hormone
References
Abizaid A (2009) Ghrelin and dopamine: new insights on the peripheral regulation of appetite. J Neuroendocrinol 21:787–793
Arvat E, Maccario M, Di Vito L, Broglio F, Benso A, Gottero C, Papotti M, Muccioli G, Dieguez C, Casanueva FF (2001) Endocrine activities of ghrelin, a natural growth hormone secretagogue (GHS), in humans: comparison and interactions with hexarelin, a nonnatural peptidyl GHS, and GH-releasing hormone. J Clin Endocrinol Metab 86:1169–1174
Ayson FG, Kaneko T, Tagawa M, Hasegawa S, Grau EG, Nishioka RS, King DS, Bern HA, Hirano T (1993) Effects of acclimation to hypertonic environment on plasma and pituitary levels of two prolactins and growth hormone in two species of tilapia, Oreochromis mossambicus and Oreochromis niloticus. Gen Comp Endocrinol 89:138–148
Banks WA, Tschöp M, Robinson SM, Heiman ML (2002) Extent and direction of ghrelin transport across the blood-brain barrier is determined by its unique primary structure. J Pharmacol Exp Ther 302:822–827
Barreiro ML, Tena-Sempere M (2004) Ghrelin and reproduction: a novel signal linking energy status and fertility? Mol Cell Endocrinol 226:1–9
Barreiro-Iglesias A, Anadón R, Rodicio M (2010) New insights on the neuropeptide Y system in the larval lamprey brain: neuropeptide Y immunoreactive neurons, descending spinal projections and comparison with tyrosine hydroxylase and GABA immunoreactivities. Neuroscience 167:396–413
Batten TF, Cambre ML, Moons L, Vandesande F (1990) Comparative distribution of neuropeptide-immunoreactive systems in the brain of the green molly, Poecilia latipinna. J Comp Neurol 302:893–919
Bowers C, Reynolds G, Durham D, Barrera C, Pezzoli S, Thorner M, Forloni F, Pinchera A, Faglia G (1990) Growth hormone (GH)-releasing peptide stimulates GH release in normal men and acts synergistically with GH-releasing hormone. J Clin Endocrinol Metab 70:975–982
Breton B, Mikolajczyk T, Popek W, Bieniarz K, Epler P (1991) Neuropeptide Y stimulates in vivo gonadotropin secretion in teleost fish. Gen Comp Endocrinol 84:277–283
Brunetti L, Recinella L, Orlando G, Michelotto B, Di Nisio C, Vacca M (2002) Effects of ghrelin and amylin on dopamine, norepinephrine and serotonin release in the hypothalamus. Eur J Pharmacol 454:189–192
Burcelin R, Thorens B, Glauser M, Gaillard RC, Pralong FP (2003) Gonadotropin-releasing hormone secretion from hypothalamic neurons: stimulation by insulin and potentiation by leptin. Endocrinology 144:4484–4491
Cabral A, López Soto EJ, Epelbaum J, Perelló M (2017) Is ghrelin synthesized in the central nervous system? Int J Mol Sci 18:638
Carnevali O, Cardinali M, Maradonna F, Parisi M, Olivotto I, Polzonetti-Magni AM, Mosconi G, Funkenstein B (2005) Hormonal regulation of hepatic IGF-I and IGF-II gene expression in the marine teleost Sparus aurata. Mol Reprod Dev 71:12–18
Castro A, Becerra M, Manso MJ, Tello J, Sherwood NM, Anadon R (2009) Distribution of growth hormone-releasing hormone-like peptide: immunoreactivity in the central nervous system of the adult zebrafish (Danio rerio). J Comp Neurol 513:685–701
Chang JP, Wong AOL (2009) Chapter 4 growth hormone regulation in fish. Fish Physiol 28:151–195
Chiba A, Honma Y (1994) Neuropeptide Y-immunoreactive structures in the telencephalon and diencephalon of the white sturgeon, Acipenser transmontanus, with special regard to the hypothalamo-hypophyseal system. Arch Histol Cytol 57:77–86
Cummings DE, Shannon MH (2003) Roles for ghrelin in the regulation of appetite and body weight. Arch Surg 138:389–396
Farkas I, Vastagh C, Sárvári M, Liposits Z (2013) Ghrelin decreases firing activity of gonadotropin-releasing hormone (GnRH) neurons in an estrous cycle and endocannabinoid signaling dependent manner. PLoS One 8:e78178
Feng DD, Yang SK, Loudes C, Simon A, Al-Sarraf T, Culler M, Alvear-Perez R, Llorens-Cortes C, Chen C, Epelbaum J (2011) Ghrelin and obestatin modulate growth hormone-releasing hormone release and synaptic inputs onto growth hormone-releasing hormone neurons. Eur J Neurosci 34:732–744
Fernández-Fernández R, Tena-Sempere M, Navarro VM, Barreiro ML, Castellano JM, Aguilar E, Pinilla L (2005) Effects of ghrelin upon gonadotropin-releasing hormone and gonadotropin secretion in adult female rats: in vivo and in vitro studies. Neuroendocrinology 82:245–255
Fernandez-Fernandez R, Martini AC, Navarro VM, Castellano JM, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M (2006) Novel signals for the integration of energy balance and reproduction. Mol Cell Endocrinol 254-255:127–132
Fletcher T, Thomas G, Clarke I (1996) Growth hormone-releasing hormone and somatostatin concentrations in the hypophysial portal blood of conscious sheep during the infusion of growth hormone-releasing peptide-6. Domest Anim Endocrinol 13:251–258
Forbes S, Li XF, Kinsey-Jones J, O’Byrne K (2009) Effects of ghrelin on Kisspeptin mRNA expression in the hypothalamic medial preoptic area and pulsatile luteinising hormone secretion in the female rat. Neurosci Lett 460:143–147
Fox BK, Naka T, Inoue K, Takei Y, Hirano T, Grau EG (2007a) In vitro effects of homologous natriuretic peptides on growth hormone and prolactin release in the tilapia, Oreochromis mossambicus. Gen Comp Endocrinol 150:270–277
Fox BK, Riley LG, Dorough C, Kaiya H, Hirano T, Grau EG (2007b) Effects of homologous ghrelins on the growth hormone/insulin-like growth factor-I Axis in the Tilapia, Oreochromis mossambicus. Zool Sci 24:391–400
Furness JB, Hunne B, Matsuda N, Yin L, Russo D, Kato I, Fujimiya M, Patterson M, McLeod J, Andrews ZB, Bron R (2011) Investigation of the presence of ghrelin in the central nervous system of the rat and mouse. Neuroscience 193:1–9
Gao Y-J, Tian L-X, Yang H-J, Liang G-Y, Yue Y-R, Liu Y-J (2012) The influence of ghrelin and des-ghrelin on feed intake, growth performance and hypothalamic NPY mRNA expression of grouper Epinephelus coioides. Aquaculture 364:19–24
Garcia MC, Lopez M, Alvarez CV, Casanueva F, Tena-Sempere M, Dieguez C (2007) Role of ghrelin in reproduction. Reproduction 133:531–540
Grey CL, Chang JP (2013) Growth hormone-releasing hormone stimulates GH release while inhibiting ghrelin- and sGnRH-induced LH release from goldfish pituitary cells. Gen Comp Endocrinol 186:150–156
Hataya Y, Akamizu T, Takaya K, Kanamoto N, Ariyasu H, Saijo M, Moriyama K, Shimatsu A, Kojima M, Kangawa K, Nakao K (2001) A low dose of ghrelin stimulates growth hormone (GH) release synergistically with GH-releasing hormone in humans. J Clin Endocrinol Metab 86:4552
Jaffe CA, Ocampo-Lim B, Guo W, Krueger K, Sugahara I, DeMott-Friberg R, Bermann M, Barkan AL (1998) Regulatory mechanisms of growth hormone secretion are sexually dimorphic. J Clin Invest 102:153–164
Kaiya H, Kojima M, Hosoda H, Moriyama S, Takahashi A, Kawauchi H, Kangawa K (2003) Peptide purification, complementary deoxyribonucleic acid (DNA) and genomic DNA cloning, and functional characterization of ghrelin in rainbow trout. Endocrinology 144:5215–5226
Kaiya H, Miyazato M, Kangawa K, Peter RE, Unniappan S (2008) Ghrelin: a multifunctional hormone in non-mammalian vertebrates. Comp Biochem Physiol A Mol Integr Physiol 149:109–128
Kamegai J, Unterman TG, Frohman LA, Kineman RD (1998) Hypothalamic/pituitary-axis of the spontaneous dwarf rat: autofeedback regulation of growth hormone (GH) includes suppression of GH releasing-hormone receptor messenger ribonucleic acid. Endocrinology 139:3554–3560
Kamegai J, Tamura H, Shimizu T, Ishii S, Sugihara H, Wakabayashi I (2000) Central effect of ghrelin, an endogenous growth hormone secretagogue, on hypothalamic peptide gene expression. Endocrinology 141:4797–4800
Kamegai J, Tamura H, Shimizu T, Ishii S, Sugihara H, Wakabayashi I (2001) Chronic central infusion of ghrelin increases hypothalamic neuropeptide Y and agouti-related protein mRNA levels and body weight in rats. Diabetes 50:2438–2443
Keen-Rhinehart E, Bartness TJ (2005) Peripheral ghrelin injections stimulate food intake, foraging, and food hoarding in Siberian hamsters. Am J Phys Regul Integr Comp Phys 288:R716–R722
Kojima M, Hosoda H, Date Y, Nakazato M, Matsuo H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide from stomach. Nature 402:656–660
Krishna NSR, Subhedar N (1989) Hypothalamic innervation of the pituitary in the catfish, Clarias batrachus (L.): a retrograde horseradish peroxidase study. Neurosci Lett 107:39–44
Lebrethon MC, Aganina A, Fournier M, Gerard A, Parent AS, Bourguignon JP (2007) Effects of in vivo and in vitro administration of ghrelin, leptin and neuropeptide mediators on pulsatile gonadotrophin-releasing hormone secretion from male rat hypothalamus before and after puberty. J Neuroendocrinol 19:181–188
Lee A, Mathuru AS, Teh C, Kibat C, Korzh V, Penney TB, Jesuthasan S (2010) The habenula prevents helpless behavior in larval zebrafish. Curr Biol 20:2211–2216
Lin H, Lu M, Lin X, Zhang W, Sun Y, Chen L (1995) Effects of gonadotropin-releasing hormone (GnRH) analogs and sex steroids on growth hormone (GH) secretion and growth in common carp (Cyprinus carpio) and grass carp (Ctenopharyngodon idellus). Aquaculture 135:173–184
Ma X, Zheng L, Mao L, Zhou L, Wang A (2013) Neuropeptide Y in black seabream Acanthopagrus schlegelii: identification, distribution and mRNA expression responses to ghrelin. J Fish Biol 82:1441–1447
Marchant TA, Chang JP, Nahorniak CS, Peter RE (1989) Evidence that gonadotropin-releasing hormone also functions as a growth hormone-releasing factor in the goldfish. Endocrinology 124:2509–2518
Marivoet S, Moons L, Vandesande F (1988) Localization of growth hormone releasing factor-like immunoreactivity in the hypothalamo-hypophyseal system of the frog (Rana temporaria) and the sea bass (Dicentrarchus labrax). Gen Comp Endocrinol 72:72–79
Mazumdar M, Lal B, Sakharkar AJ, Deshmukh M, Singru PS, Subhedar N (2006) Involvement of neuropeptide Y Y1 receptors in the regulation of LH and GH cells in the pituitary of the catfish, Clarias batrachus: an immunocytochemical study. Gen Comp Endocrinol 149:190–196
McVey DC, Rittschof D, Mannon PJ, Vigna SR (1996) Localization and characterization of neuropeptide Y/peptide YY receptors in the brain of the smooth dogfish (Mustelis canis). Regul Pept 61:167–173
Melamed P, Eliahu N, Levavi-Sivan B, Ofir M, Farchi-Pisanty O, Rentier-Delrue F, Smal J, Yaron Z, Naor Z (1995) Hypothalamic and thyroidal regulation of growth hormone in tilapia. Gen Comp Endocrinol 97:13–30
Melamed P, Rosenfeld H, Elizur A, Yaron Z (1998) Endocrine regulation of gonadotropin and growth hormone gene transcription in fish. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 119:325–338
Miranda LA, Strobl-Mazzulla PH, Somoza GM (2002) Ontogenetic development and neuroanatomical localization of growth hormone-releasing hormone (GHRH) in the brain and pituitary gland of pejerrey fish Odontesthes bonariensis. Int J Dev Neurosci 20:503–510
Northcutt RG (1982) Localization of neurons afferent to the optic tectum in longnose gars. J Comp Neurol 204:325–335
Ogawa S, Akiyama G, Kato S, Soga T, Sakuma Y, Parhar IS (2006) Immunoneutralization of gonadotropin-releasing hormone type-III suppresses male reproductive behavior of cichlids. Neurosci Lett 403:201–205
Ogawa S, Sivalingam M, Biran J, Golan M, Anthonysamy RS, Levavi-Sivan B, Parhar IS (2016) Distribution of LPXRFa, a gonadotropin-inhibitory hormone ortholog peptide, and LPXRFa receptor in the brain and pituitary of the tilapia. J Comp Neurol 524:2753–2775
Olivereau M, Olivereau J, Vandesande F (1990) Localization of growth hormone-releasing factor-like immunoreactivity in the hypothalamo-hypophysial system of some teleost species. Cell Tissue Res 259:73–80
Osterstock G, Escobar P, Mitutsova V, Gouty-Colomer L-A, Fontanaud P, Molino F, Fehrentz J-A, Carmignac D, Martinez J, Guerineau NC (2010) Ghrelin stimulation of growth hormone-releasing hormone neurons is direct in the arcuate nucleus. PLoS One 5:e9159
Pan J, Lechan R, Lin H, Jackson I (1985) Immunoreactive neuronal pathways of growth hormone-releasing hormone (GRH) in the brain and pituitary of the teleost Gadus morhua. Cell Tissue Res 241:487–493
Parhar IS, Iwata M (1996) Intracerebral expression of gonadotropin-releasing hormone and growth hormone-releasing hormone is delayed until smoltification in the salmon. NeurosciRes 26:299–308
Parhar IS, Pfaff DW, Schwanzel-Fukuda M (1996) Gonadotropin-releasing hormone gene expression in teleosts. Mol Brain Res 41:216–227
Parhar IS, Sato H, Sakuma Y (2003) Ghrelin gene in cichlid fish is modulated by sex and development. Biochem Biophys Res Commun 305:169–175
Parhar IS, Ogawa S, Sakuma Y (2004) Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel G protein-coupled receptor (Gpr54) during maturation in cichlid fish. Endocrinology 145:3613–3618
Parhar IS, Ogawa S, Sakuma Y (2005) Three GnRH receptor types in laser-captured single cells of the cichlid pituitary display cellular and functional heterogeneity. Proc Natl Acad Sci U S A 102:2204–2209
Park MK, Wakabayashi K (1986) Preparation of a monoclonal antibody to common amino acid sequence of LHRH and its application. Endocrinol Jpn 33:257–272
Peddu SC, Breves JP, Kaiya H, Gordon Grau E, Riley LG Jr (2009) Pre- and postprandial effects on ghrelin signaling in the brain and on the GH/IGF-I axis in the Mozambique tilapia (Oreochromis mossambicus). Gen Comp Endocrinol 161:412–418
Peng C, Huang Y-P, Peter RE (1990) Neuropeptide Y stimulates growth hormone and gonadotropin release from the goldfish pituitary in vitro. Neuroendocrinology 52:28–34
Peng C, Chang J, Yu KL, Wong A, Van Goor F, Peter R, Rivier J (1993) Neuropeptide-Y stimulates growth hormone and gonadotropin-II secretion in the goldfish pituitary: involvement of both presynaptic and pituitary cell actions. Endocrinology 132:1820–1829
Peter RE, Yu KL, Marchant TA, Rosenblum PM (1990) Direct neural regulation of the teleost adenohypophysis. J Exp Zool 256:84–89
Peyon P, Vega-Rubin de Celis S, Gomez-Requeni P, Zanuy S, Perez-Sanchez J, Carrillo M (2003) In vitro effect of leptin on somatolactin release in the European sea bass (Dicentrarchus labrax): dependence on the reproductive status and interaction with NPY and GnRH. Gen Comp Endocrinol 132:284–292
Picha ME, Strom CN, Riley LG, Walker AA, Won ET, Johnstone WM, Borski RJ (2009) Plasma ghrelin and growth hormone regulation in response to metabolic state in hybrid striped bass: effects of feeding, ghrelin and insulin-like growth factor-I on in vivo and in vitro GH secretion. Gen Comp Endocrinol 161:365–372
Popovic V, Miljic D, Micic D, Damjanovic S, Arvat E, Ghigo E, Dieguez C, Casanueva FF (2003) Ghrelin main action on the regulation of growth hormone release is exerted at hypothalamic level. J Clin Endocrinol Metab 88:3450–3453
Rao SD, Rao PP, Peter RE (1996) Growth hormone-releasing hormone immunoreactivity in the brain, pituitary, and pineal of the goldfish, Carassius auratus. Gen Comp Endocrinol 102:210–220
Riley LG, Hirano T, Grau EG (2002) Rat ghrelin stimulates growth hormone and prolactin release in the tilapia, Oreochromis mossambicus. Zool Sci 19:797–800
Riley LG, Fox BK, Kaiya H, Hirano T, Grau EG (2005) Long-term treatment of ghrelin stimulates feeding, fat deposition, and alters the GH/IGF-I axis in the tilapia, Oreochromis mossambicus. Gen Comp Endocrinol 142:234–240
Saito H, Saito S, Yamazaki R, Hosoi E (1984) Clinical value of radioimmunoassay of plasma growth-hormone-releasing factor. Lancet 324:401–402
Sakharkar AJ, Singru PS, Sarkar K, Subhedar NK (2005) Neuropeptide Y in the forebrain of the adult male cichlid fish Oreochromis mossambicus: distribution, effects of castration and testosterone replacement. J Comp Neurol 489:148–165
Sánchez-Bretaño A, Blanco AM, Unniappan S, Kah O, Gueguen M-M, Bertucci JI, Alonso-Gómez ÁL, Valenciano AI, Isorna E, Delgado MJ (2015) In situ localization and rhythmic expression of ghrelin and ghs-r1 ghrelin receptor in the brain and gastrointestinal tract of goldfish (Carassius auratus). PLoS One 10:e0141043
Senthilkumaran B, Okuzawa K, Gen K, Ookura T, Kagawa H (1999) Distribution and seasonal variations in levels of three native GnRHs in the brain and pituitary of perciform fish. J Neuroendocrinol 11:181–186
Shepherd BS, Drennon K, Johnson J, Nichols JW, Playle RC, Singer TD, Vijayan MM (2005) Salinity acclimation affects the somatotropic axis in rainbow trout. Am J Phys Regul Integr Comp Phys 288:R1385–R1395
Shepherd BS, Johnson JK, Silverstein JT, Parhar IS, Vijayan MM, McGuire A, Weber GM (2007) Endocrine and orexigenic actions of growth hormone secretagogues in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol A Mol Integr Physiol 146:390–399
Sherwood NM, von Schalburg KR, Lescheid DW (1997) Origin and evolution of GnRH in vertebrates and invertebrates. In: Parhar IS, Sakuma Y (eds) GnRH neurons: from genes to behavior. Brain Shuppan, Tokyo, pp 3–25
Shimizu M, Swanson P, Fukada H, Hara A, Dickhoff WW (2000) Comparison of extraction methods and assay validation for salmon insulin-like growth factor-I using commercially available components. Gen Comp Endocrinol 119:26–36
Shintani M, Ogawa Y, Ebihara K, Aizawa-Abe M, Miyanaga F, Takaya K, Hayashi T, Inoue G, Hosoda K, Kojima M (2001) Ghrelin, an endogenous growth hormone secretagogue, is a novel orexigenic peptide that antagonizes leptin action through the activation of hypothalamic neuropeptide Y/Y1 receptor pathway. Diabetes 50:227–232
Stamatakis AM, Van Swieten M, Basiri ML, Blair GA, Kantak P, Stuber GD (2016) Lateral hypothalamic area glutamatergic neurons and their projections to the lateral habenula regulate feeding and reward. J Neurosci 36:302–311
Subhedar N, Cerdá J, Wallace RA (1996) Neuropeptide Y in the forebrain and retina of the killifish, Fundulus heteroclitus. Cell Tissue Res 283:313–323
Tang-Christensen M, Vrang N, Ortmann S, Bidlingmaier M, Horvath TL, Tschop M (2004) Central administration of ghrelin and agouti-related protein (83-132) increases food intake and decreases spontaneous locomotor activity in rats. Endocrinology 145:4645–4652
Tannenbaum GS, Bowers CY (2001) Interactions of growth hormone secretagogues and growth hormone-releasing hormone/somatostatin. Endocrine 14:21–27
Tena-Sempere M (2005) Ghrelin: novel regulator of gonadal function. J Endocrinol Investig 28:26–29
Tolle V, Zizzari P, Tomasetto C, Rio M-C, Epelbaum J, Bluet-Pajot M-T (2001) In vivo and in vitro effects of ghrelin/motilin-related peptide on growth hormone secretion in the rat. Neuroendocrinology 73:54–61
Tomas HK, Davor S, Staci DS, Jesse CG, Ida N, Gustavo P, Fernanda L, Serguei F, Charlotte L, Herbert H, Jeanette EJ, Ruud U, Karl HP (2008) NPY and its involvement in axon guidance, neurogenesis, and feeding. Nutrition 24:860–868
Tschop M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407:908–913
Uchida H, Ogawa S, Harada M, Matushita M, Iwata M, Sakuma Y, Parhar IS (2005) The olfactory organ modulates gonadotropin-releasing hormone types and nest-building behavior in the tilapia Oreochromis niloticus. J Neurobiol 65:1–11
Unniappan S (2010) Ghrelin: an emerging player in the regulation of reproduction in non-mammalian vertebrates. Gen Comp Endocrinol 167:340–343
Unniappan S, Peter RE (2004) In vitro and in vivo effects of ghrelin on luteinizing hormone and growth hormone release in goldfish. Am J Phys Regul Integr Comp Phys 286:R1093–R1101
Unniappan S, Peter RE (2005) Structure, distribution and physiological functions of ghrelin in fish. Comp Biochem Physiol A Mol Integr Physiol 140:396–408
Vallarino M, Danger J, Fasolo A, Pelletier G, Saint-Pierre S, Vaudry H (1988) Distribution and characterization of neuropeptide Y in the brain of an elasmobranch fish. Brain Res 448:67–76
Veldhuis JD, Bowers CY (2003) Sex-steroid modulation of growth hormone (GH) secretory control: three-peptide ensemble regulation under dual feedback restraint by GH and IGF-I. Endocrine 22:25–40
Villani L, Zironi I, Guarnieri T (1996) Telencephalo-habenulo-interpeduncular connections in the goldfish: a Dil study. Brain Behav Evol 48:205–212
Volkoff H, Canosa LF, Unniappan S, Cerda-Reverter JM, Bernier NJ, Kelly SP, Peter RE (2005) Neuropeptides and the control of food intake in fish. Gen Comp Endocrinol 142:3–19
Vulliemoz NR, Xiao E, Xia-Zhang L, Germond M, Rivier J, Ferin M (2004) Decrease in luteinizing hormone pulse frequency during a five-hour peripheral ghrelin infusion in the ovariectomized rhesus monkey. J Clin Endocrinol Metab 89:5718–5723
Walfish S (2006) A review of statistical outlier methods. Pharm Technol 30:82
Wang L, Saint-Pierre DH, Taché Y (2002) Peripheral ghrelin selectively increases Fos expression in neuropeptide Y–synthesizing neurons in mouse hypothalamic arcuate nucleus. Neurosci Lett 325:47–51
Wren AM, Bloom SR (2007) Gut hormones and appetite control. Gastroenterology 132:2116–2130
Wren A, Small C, Ward H, Murphy K, Dakin C, Taheri S, Kennedy A, Roberts G, Morgan D, Ghatei M (2000) The novel hypothalamic peptide ghrelin stimulates food intake and growth hormone secretion. Endocrinology 141:4325–4328
Yada T, Hirano T, Grau EG (1994) Changes in plasma levels of the two prolactins and growth hormone during adaptation to different salinities in the euryhaline tilapia, Oreochromis mossambicus. Gen Comp Endocrinol 93:214–223
Yamamoto N, Parhar IS, Sawai N, Oka Y, Ito H (1998) Preoptic gonadotropin-releasing hormone (GnRH) neurons innervate the pituitary in teleosts. Neurosci Res 31:31–38
Yañez J, Anadón R (1996) Afferent and efferent connections of the habenula in the rainbow trout (Oncorhynchus mykiss): an indocarbocyanine dye (DiI) study. J Comp Neurol 372:529–543
Zambrano D (1971) The nucleus lateralis tuberis system of the gobiid fish Gillichthys mirabilis: III Functional modifications of the neurons and gonadotropic cells. Gen Comp Endocrinol 17:164–182
Acknowledgements
The initial part of this project was conducted at the Nippon Medical School, Tokyo, Japan. The authors thank Mr. Hiroshi Uchida, Ms. Rachel Shalini Anthonysamy, Ms. Kai We Ng, Drs. Hideki Sato, Geeta Selvarajah and Tomoko Soga for their technical support. The authors also thank Prof. Yasuo Sakuma (University of Tokyo Health Sciences, Tokyo, Japan) for advice during the course of the study. This work was supported in part by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan; Grant number: 14580777 (to I.S.P.) and the Ministry of Health, Labour and Welfare; Grant number: H16-kagaku-002 (to I.S.P.) and Monash University Malaysia: MM-2-5-06, MM-7-07, MM-6-08, IP-09-01 (to I.S.P.) and M-2-1-06, M-2-07, M-4-08 (to S.O.). Additional support was provided by the National Research Initiative Competitive Grants Program/USDA award no. 2002-35206-11629 and 2004-05124 and USDA/ARS CRIS Project #1930-31000-003-00D (to B.S.S.) and Guangdong Marine Fishery Science and Technology Project, A201301B02 (to X.L.).
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This work was supported in part by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science and Technology of Japan; Grant number: 14580777 (to I.S.P.), the Ministry of Health, Labour and Welfare; Grant number: H16-kagaku-002 (to I.S.P.) and Monash University Malaysia: MM-2-5-06, MM-7-07, MM-6-08, IP-09-01 (to I.S.P.) and M-2-1-06, M-2-07, M-4-08 (to S.O.). Additional support was provided by the National Research Initiative Competitive Grants Program/USDA award no. 2002-35206-11629 and 2004-05124, and USDA/ARS CRIS Project #1930-31000-003-00D (to B.S.S.) and Guangdong Marine Fishery Science and Technology Project, A201301B02 (to X.L.).
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S.O., X.L. and B.S.S. performed the research; S.O. and I.S.P. designed the research study; S.O., B.S.S. and I.S.P. analyzed data; S.O., B.S.S. and I.S.P. wrote the paper.
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Ogawa, S., Liu, X., Shepherd, B.S. et al. Ghrelin stimulates growth hormone release from the pituitary via hypothalamic growth hormone-releasing hormone neurons in the cichlid, Oreochromis niloticus. Cell Tissue Res 374, 349–365 (2018). https://doi.org/10.1007/s00441-018-2870-6
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DOI: https://doi.org/10.1007/s00441-018-2870-6