Abstract
Intracerebroventricular (ICV) injection of melanin-concentrating hormone (MCH) influences feeding behavior in the goldfish and exerts an anorexigenic action in goldfish brain, unlike its orexigenic action in mammals. Despite a growing body of knowledge concerning MCH function in mammals, the role of MCH in appetite has not yet been well studied in fish. The aim of the present study was to investigate the involvement of endogenous MCH in the feeding behavior of the goldfish. We examined the distribution of MCH-like immunoreactivity (MCH-LI) in the goldfish brain and the effect of feeding status upon this distribution. Neuronal cell bodies containing MCH-LI were localized specifically to four areas of the hypothalamus. Nerve fibers with MCH-LI were found mainly in the neurohypophysis, with a few in the telencephalon, mesencephalon, and diencephalon. The number of neuronal cell bodies containing MCH-LI in the dorsal area adjoining the lateral recess of the third ventricle in the posterior and inferior lobes of the hypothalamus showed a significant decrease in fasted fish compared with that in normally fed fish, although other areas showed no evident differences. We also administered an antiserum against fish MCH (anti-MCH serum) by ICV injection and examined its immunoneutralizing effect on food intake by using an automatic monitoring system. Cumulative food intake was significantly increased by ICV injection of the anti-MCH serum. These results indicate that MCH potentially functions as an anorexigenic neuropeptide in the goldfish brain, and that the further study of the evolutionary background of the MCH system and its role in appetite is warranted.
Similar content being viewed by others
References
Amano M, Takahashi A, Oka Y, Yamanome T, Kawauchi H, Yamamori K (2003) Immunocytochemical localization and ontogenic development of melanin-concentrating hormone in the brain of a pleuronectiform fish, the barfin flounder. Cell Tissue Res 311:71–77
Amiya N, Amano M, Takahashi A, Yamanome T, Kawauchi H, Yamamori K (2005) Effects of tank color on melanin-concentrating hormone levels in the brain, pituitary gland, and plasma of the barfin flounder as revealed by a newly developed time-resolved fluoroimmunoassay. Gen Comp Endocrinol 143:251–256
Andersen AC, Pelletier G, Eberle AN, Leroux P, Jegou S, Vaudry H (1986) Localization of melanin-concentrating hormone-like immunoreactivity in the brain and pituitary of the frog Rana ridibunda. Peptides 7:941–951
Andersen AC, Jegou S, Eberle AN, Tonon MC, Pelletier G, Vaudry H (1987) Coexistence of melanin-concentrating hormone (MCH) and alpha-melanocyte-stimulating hormone (alpha-MSH) in the preoptic nucleus of the frog brain. Brain Res Bull 18:257–259
Baker BI, Bird DJ (2002) Neuronal organization of the melanin-concentrating hormone system in primitive actinopterygians: evolutionary changes leading to teleosts. J Comp Neurol 442:99–114
Baker B, Levy A, Hall L, Lightman S (1995) Cloning and expression of melanin-concentrating hormone genes in the rainbow trout brain. Mol Neuroendocrinol 61:67–76
Bird DJ, Potter IC, Sower SA, Baker BI (2001) The distribution of melanin-concentrating hormone in the lamprey brain. Gen Comp Endocrinol 121:232–241
Cardinaud B, Darre-Toulemonde F, Duhault J, Boutin JA, Nahon JL (2004) Comparative analysis of melanin-concentrating hormone structure and activity in fishes and mammals. Peptides 25:1623–1632
Cardot J, Griffond B, Risold PY, Blähser S, Fellmann D (1999) Melanin-concentrating hormone-producing neurons in birds. J Comp Neurol 411:239–256
Demski LS, Knigge KM (1971) The telencephalon and hypothalamus of the bluegill (Lepomis macrochirus): evoked feeding, aggressive and reproductive behavior with representative frontal sections. J Comp Neurol 143:1–16
Duarte G, Segura-Noguera MM, Martín del Río MP, Mancera JM (2001) The hypothalamo-hypophyseal system of the white seabream Diplodus sargus: immunocytochemical identification of arginine-vasotocin, isotocin, melanin-concentrating hormone and corticotropin-releasing factor. Histochem J 33:569–578
Gomori A, Ishihara A, Ito M, Mashiko S, Matsushita H, Yumoto M, Ito M, Tanaka T, Tokita S, Moriya M, Iwaasa H, Kanatani A (2003) Chronic intracerebroventricular infusion of MCH causes obesity in mice. Melanin-concentrating hormone. Am J Physiol Endocrinol Metab 284:E583–E588
Gröneveld D, Balm PHM, Wendelaar Bonga SE (1995a) Biphasic effect of MCH on α-MSH release from the tilapia (Oreochromis mossambicus) pituitary. Peptides 16:945–949
Gröneveld D, Eckhardt ERM, Coenen AJM, Martens GJM, Balm PHM, Wendelaar Bonga SE (1995b) Expression of tilapia prepro-melanin-concentrating hormone mRNA in hypothalamic and neurohypophysial cells. J Mol Endocrinol 14:199–207
Huesa G, Van den Pol AN, Finger TE (2005) Differential distribution of hypocretin (orexin) and melanin-concentrating hormone in the goldfish brain. J Comp Neurol 488:476–491
Kawauchi H, Baker BI (2004) Melanin–concentrating hormone signaling systems in fish. Peptides 25:1577–1584
Kawauchi H, Kawazoe I, Tsubokawa M, Kishida M, Baker BI (1983) Characterization of melanin-concentrating hormone in chum salmon pituitaries. Nature 305:321–323
Kawazoe I, Kawauchi H, Hirano T, Naito N (1987) Structure-activity relationships of melanin-concentrating hormone. Int J Pept Protein Res 29:714–721
Ludwig DS, Tritos NA, Mastaitis JW, Kulkarni R, Kokkotou E, Elmquist J, Lowell B, Flier JS, Maratos-Flier E (2001) Melanin-concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. J Clin Invest 107:379–386
Maruyama K, Miura T, Uchiyama M, Shioda S, Matsuda K (2006) Relationship between anorexigenic action of pituitary adenylate cyclase-activating polypeptide (PACAP) and that of corticotrophin-releasing hormone (CRH) in the goldfish, Carassius auratus. Peptides 27:1820–1826
Matsuda K, Maruyama K, Miura T, Uchiyama M, Shioda S (2005a) Anorexigenic action of pituitary adenylate cyclase-activating polypeptide (PACAP) in the goldfish: feeding-induced changes in the expression of mRNAs for PACAP and its receptors in the brain, and locomotor response to central injection. Neurosci Lett 386:9–13
Matsuda K, Maruyama K, Nakamachi T, Miura T, Uchiyama M, Shioda S (2005b) Inhibitory effects of pituitary adenylate cyclase-activating polypeptide (PACAP) and vasoactive intestinal peptide (VIP) on food intake in the goldfish, Carassius auratus. Peptides 26:1611–1616
Matsuda K, Miura T, Kaiya H, Maruyama K, Shimakura SI, Uchiyama M, Kangawa K, Shioda S (2006a) Regulation of food intake by acyl and des-acyl ghrelins in the goldfish. Peptides 27:2321–2325
Matsuda K, Miura T, Kaiya H, Maruyama K, Uchiyama M, Kangawa K, Shioda S (2006b) Stimulatory effect of n-octanoylated ghrelin on locomotor activity in the goldfish, Carassius auratus. Peptides 27:1335–1340
Matsuda K, Shimakura SI, Maruyama K, Miura T, Uchiyama M, Kawauchi H, Shioda S, Takahashi A (2006c) Central administration of melanin-concentrating hormone (MCH) suppresses food intake, but not locomotor activity, in the goldfish, Carassius auratus. Neurosci Lett 399:259–263
Naito N, Nakai Y, Kawauchi H, Hayashi Y (1985) Immunohistochemical identification of melanin-concentrating hormone in the brain and pituitary gland of teleost fishes Onchorhynchus keta and Salmo gairdneri. Cell Tissue Res 242:41–48
Nakamachi T, Matsuda K, Maruyama K, Miura T, Uchiyama M, Funahashi H, Sakurai T, Shioda S (2006) Regulation by orexin of feeding behavior and locomotor activity in the goldfish. J Neuroendocrinol 18:290–297
Pandolfi M, Canepa MM, Ravaglia MA, Maggese MC, Paz DA, Vissio PG (2003) Melanin-concentrating hormone system in the brain and skin of the cichlid fish Cichlasoma dimerus: anatomical localization, ontogeny and distribution in comparison to alpha-melanocyte-stimulating hormone-expressing cells. Cell Tissue Res 311:61–69
Pissios P, Bradley RL, Maratos-Flier E (2006) Expanding the scales: the multiple roles of MCH in regulating energy balance and biological functions. Endocr Rev 27:606–620
Qu D, Ludwig DS, Gammeltoft S, Piper M, Pelleymounter MA, Cullen MJ, Mathes WF, Przypek J, Kanarek R, Maratos-Flier E (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380:243–247
Roberts MG, Savage GE (1978) Effects of hypothalamic lesions on the food intake of the goldfish (Carassius auratus). Brain Behav Evol 15:150–164
Rossi M, Choi SJ, O’Shea D, Miyoshi T, Ghatei MA, Bloom SR (1997) Melanin-concentrating hormone acutely stimulates feeding, but chronic administration has no effect on body weight. Endocrinology 138:351–355
Savage GE, Roberts MG (1975) Behavioural effects of electrical stimulation of the hypothalamus of the goldfish (Carassius auratus). Brain Behav 12:42–56
Shi Y (2004) Beyond skin color: emerging roles of melanin-concentrating hormone in energy homeostasis and other physiological functions. Peptides 25:1605–1611
Shimada M, Tritos NA, Lowell BB, Flier JS, Maratos-Flier E (1998) Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature 396:670–674
Takahashi A, Tsuchiya K, Yamanome T, Amano M, Yasuda A, Yamamori K, Kawauchi H (2004) Possible involvement of melanin-concentrating hormone in food intake in a teleost fish, barfin flounder. Peptides 25:1613–1622
Unniappan S, Canosa LF, Peter RE (2003) Orexigenic actions of ghrelin in goldfish: feeding-induced changes in brain and gut mRNA expression and serum levels, and responses to central and peripheral injections. Neuroendocrinology 79:100–108
Vallarino M, Andersen AC, Delbende C, Ottonello I, Eberle AN, Vaudry H (1989a) Melanin-concentrating hormone (MCH) immunoreactivity in the brain and pituitary of the dogfish Scyliorhinus canicula. Peptides 10:375–382
Vallarino M, Trabucchi M, Chartrel N, Jaggin V, Eberle AN, Vaudry H (1989b) Melanin-concentrating hormone system in the brain of the lungfish Protopterus annectens. J Comp Neurol 390:41–51
Volkoff H, Bjorklund JM, Peter RE (1999) Stimulation of feeding behavior and food concumption in the goldfish, Carassius auratus, by orexin-A and orexin-B. Brain Res 846:204–209
Author information
Authors and Affiliations
Corresponding author
Additional information
This work was supported by Grants-in-Aid from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (K.M. and A.T.) and by a research grant from the Toyama Marine Biotechnology Association (K.M.).
Rights and permissions
About this article
Cite this article
Matsuda, K., Shimakura, SI., Miura, T. et al. Feeding-induced changes of melanin-concentrating hormone (MCH)-like immunoreactivity in goldfish brain. Cell Tissue Res 328, 375–382 (2007). https://doi.org/10.1007/s00441-006-0347-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00441-006-0347-5