Abstract
In this investigation, we examined the influence of alpha-melanocyte stimulating hormone (α-MSH), a proopiomelanocortin-derived peptide, along the hypothalamic-pituitary-gonad axis in a cichlid fish Oreochromis mossambicus. Administration of α-MSH (40 µg/0.1 ml saline) for 22 days did not affect the number of stage I (previtellogenic) follicles but caused significant reduction in the mean numbers of previtellogenic (stages II and III), vitellogenic (stage IV) and preovulatory (stage V) follicles compared to those of controls. While the gonadosomatic index was significantly lower, the rate of follicular atresia in stages II, III and IV remained significantly higher in α-MSH-treated fish compared to the controls. Furthermore, the mean percent area of gonadotropin-releasing hormone-immunoreactive (GnRH-ir) fibres and luteinizing hormone-immunoreactive (LH-ir) cells were significantly reduced in the proximal pars distalis of the pituitary gland in α-MSH-treated fish compared with the controls. Together, our findings suggest for the first time that the treatment of α-MSH blocks the follicular developmental process during the ovarian cycle, possibly through the inhibition of GnRH-LH pathway in teleosts.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
Code availability (software application or custom code)
Not applicable.
References
Alsop D, Ings JS, Vijayan MM (2009) Adrenocorticotropic hormone suppresses gonadotropin-stimulated estradiol release from zebrafish ovarian follicles. PLoS ONE 4(7):e6463. https://doi.org/10.1371/journal.pone.0006463
Amiya N, Amano M, Oka Y, Iigo M, Takahashi A, Yamamori K (2008) Interaction of orexin/hypocretin-like immunoreactive neurons with melanin-concentrating hormone and α-melanocyte-stimulating hormone neurons in brain of a pleuronectiform fish, barfin flounder. Fish Sci 74:1040–1046. https://doi.org/10.1111/j.1444-2906.2008.01622.x
Backholer K, Smith J, Clarke IJ (2009) Melanocortins may stimulate reproduction by activating orexin neurons in the dorsomedial hypothalamus and kisspeptin neurons in the preoptic area of the ewe. Endocrinology 150:5488–5497. https://doi.org/10.1210/en.2009-0604
Bhat SK, Ganesh CB (2020) Domperidone treatment attenuates stress-induced suppression of reproduction in viviparous mosquitofish Gambusia affinis. J Fish Biol 96:37–48. https://doi.org/10.1111/jfb.14183
Caquineau C, Len G, Guan XM, Jiang M, Van der Ploeg L, Douglas AJ (2006) Effects of alpha-melanocyte-stimulating hormone on magnocellular oxytocin neurones and their activation at intromission in male rats. J Neuroendocrinol 18:685–691. https://doi.org/10.1111/j.1365-2826.2006.01465.x
Catania A, Cutuli M, Garofalo L, Carlin A, Airaghi L, Barcellini W, Lipton, JM (2000) The Neuropeptide α-MSH in Host Defense. Ann N Y Acad Sci 917:227–231. https://doi.org/10.1111/j.1749-6632.2000.tb05387.x
Chabbi A, Ganesh CB (2012) Stress-induced inhibition of recruitment of ovarian follicles for vitellogenic growth and interruption of spawning cycle in the fish Oreochromis mossambicus. Fish Physiol Biochem 38:1521–1532. https://doi.org/10.1007/s10695-012-9643-z
Chabbi A, Ganesh CB (2013) β-endorphin-induced inhibition of vitellogenic follicular growth in the fish Oreochromis mossambicus evidence for opioidergic mediation of ovarian stress response. J Exp Zool A Ecol Genet Physiol 319:156–165. https://doi.org/10.1002/jez.1781
Chabbi A, Ganesh CB (2014) Glucocorticoid synthesis inhibitor metyrapone blocks stress-induced suppression along luteinizing hormone secreting cells–ovary axis in the fish Oreochromis mossambicus. J Exp Zool A Ecol Genet Physiol 321:125–134. https://doi.org/10.1002/jez.1842
Celis ME (1985) Release of LH in response to alpha-MSH administration. Acta Physiol Pharmacol Latinoam 35:281–290
Cone RD (2005) Anatomy and regulation of the central melanocortin system. Nat Neurosci 8:571–578
Cragnolini A, Scimonelli T, Celis M, Schiöth H (2000) The role of melanocotin receptors in sexual behavior in female rats. Neuropeptides 34:211–215. https://doi.org/10.1054/npep.2000.0815
Filadelfi AM, Castrucci AM (1994) Melatonin desensitizing effects on the in vitro responses to MCH, alpha-MSH, isoproterenol and melatonin in pigment cells of a fish (S. marmoratus), a toad (B. ictericus), a frog (R. pipiens) and a lizard (A. carolinensis), exposed to varying photoperiodic regimens. Comp Biochem Physiol A 109:1027–1037. https://doi.org/10.1016/0300-9629(94)90252-64
Flik G, Klaren PH, Van den Burg EH, Metz JR, Huising MO (2006) CRF and stress in fish. Gen Comp Endocrinol 146:36–44. https://doi.org/10.1016/j.ygcen.2005.11.005
Ganesh CB (2014) Follicular development status and profile of 17β estradiol and cortisol levels during the spawning cycle in Oreochromis mossambicus (Peters). Ind J Fish 61:45–51
Ganesh CB (2021) The stress—reproductive axis in fish: the involvement of functional neuroanatomical systems in the brain. J Chem Neuroanat 112:101904. https://doi.org/10.1016/j.jchemneu.2020.101904
Ganesh CB, Chabbi A (2013) Naltrexone attenuates stress-induced suppression of LH secretion in the pituitary gland in the cichlid fish Oreochromis mossambicus evidence for the opioidergic mediation of reproductive stress response. Fish Physiol Biochem 39:627–636. https://doi.org/10.1007/s10695-012-9725-y
Guraya SS (1986) The cell and molecular biology of fish oogenesis. In: Saver HW (ed) Monographs in developmental biology. Karger, New York, pp 1–223
Holmes R, Ball J (1974) The pituitary gland—a comparative account. Cambridge University Press, Cambridge
Ikari T, Kobayashi Y, Kitani Y, Sekiguchi T, Endo M, Kambegawa A, Asahina K, Hattori A, Tabuchi Y, Amornsakun T, Mizusawa K, Takahashi A, Suzuki N (2018) α-Melanocyte-stimulating hormone directly increases the plasma calcitonin level and involves calcium metabolism in goldfish. Int Aquat Res 10:283–292. https://doi.org/10.1007/s40071-018-0206-5
Israel DD, Sheffer-Babila S, de Luca C, Jo YH, Liu SM, Xia Q, Spergel DJ, Dun SL, Dun NJ, Chua SC Jr (2012) Effects of leptin and melanocortin signaling interactions on pubertal development and reproduction. Endocrinology 153(5):2408–2419. https://doi.org/10.1210/en.2011-1822
Kasper RS, Shved N, Takahashi A, Reinecke M, Eppler E (2006) A systematic immunohistochemical survey of the distribution patterns of GH prolactin somatolactin beta-TSH, beta-FSH, beta-LH, ACTH and alpha-MSH in the adenohypophysis of Oreochromis niloticus, the Nile tilapia. Cell Tissue Res 325:303–313. https://doi.org/10.1007/s00441-005-0119-7
Khorram O, DePalatis LR, McCann SM (1984) The effect and possible mode of action of alpha-melanocyte-stimulating hormone on gonadotropin release in the ovariectomized rat: an in vivo and in vitro analysis. Endocrinology 114(1):227–233. https://doi.org/10.1210/endo-114-1-227
Kumbar J, Ganesh CB (2021) Alpha-melanocyte stimulating hormone immunoreactivity in the brain of the cichlid fish Oreochromis mossambicus. Neuropeptides 87:102128. https://doi.org/10.1016/j.npep.2021.102128
Kwon HC, Hayashi S, Mugiya Y (1993) Vitellogenin induction by estradiol-17b in primary hepatocyte culture in the rainbow trout, Oncorhynchus mykiss. Comp Biochem Physiol 104B:381–396
Lamers AE, Ter Brugge PJ, Flik G, Wendelaar Bonga SE (1997) Acid stress induces a D1-like dopamine receptor in pituitary MSH cells of Oreochromis mossambicus. Am J Physiol 273:387–392
Limone P, Calvelli P, Altare F, Ajmone-Catt P, Lima T, Molinatti GM (1997) Evidence for an interaction between alpha-MSH and opioids in the regulation of gonadotropin secretion in man. J Endocrinol Invest 20:207–210. https://doi.org/10.1007/BF03346904
Lubzens E, Young G, Bobe J, Cerda J (2010) Oogenesis in teleosts: how fish eggs are formed. Gen Comp Endocrinol 165:367–389
Luger TA, Scholzen TE, Brzoska T, Bohm M (2003) New insights into the functions of alpha-MSH and related peptides in the immune system. Ann N Y Acad Sci 994:133–140
Matsuyama S, Ohkura S, Sakurai K, Tsukamura H, Maeda K, Okamura H (2005) Activation of melanocortin receptors accelerates the gonadotropin-releasing hormone pulse generator activity in goats. Neurosci Lett 383:289–294. https://doi.org/10.1016/j.neulet.2005.04.026
Mezey E, Kiss JZ, Mueller GP, Eskay R, O’Donohue TL, Palkovits M (1985) Distribution of the pro-opiomelanocortin derived peptides, adrenocorticotrope hormone, alpha-melanocyte-stimulating hormone and beta-endorphin (ACTH, alpha-MSH, beta-END) in the rat hypothalamus. Brain Res 328:341–347
Naftolin F, Horvath TL, Jakab RL, Leranth C, Harada N, Balthazart J (1996) Aromatase immunoreactivity in axon terminals of the vertebrate brain. An immunocytochemical study on quail, rat, monkey and human tissues. Neuroendocrinology 63:149–155
Newman CB, Wardlaw SL, Frantz AG (1985) Suppression of basal and stress-induced prolactin release and stimulation of luteinizing hormone secretion by α-melanocyte-stimulating hormone. Life Sci 36:1661–1668. https://doi.org/10.1016/0024-3205(85)90369-8
Olivereau M (1978) Serotonin and MSH secretion: effect of parachlorophenylalanine on the pituitary cytology of the eel. Cell Tissue Res 191:83–92. https://doi.org/10.1007/BF00223217
Pandolfi M, Cánepa 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. https://doi.org/10.1007/s00441-002-0654-4
Reid RL, Ling N, Yen SS (1984) Gonadotropin-releasing activity of alpha-melanocyte-stimulating hormone in normal subjects and in subjects with hypothalamic-pituitary dysfunction. J Clin Endocrinol Metab 58:773–777. https://doi.org/10.1210/jcem-58-5-773
Roa J, Herbison AE (2012) Direct regulation of GnRH neuron excitability by arcuate nucleus POMC and NPY neuron neuropeptides in female mice. Endocrinology 153:5587–5599
Rotllant J, Balm P, Wendelaar-Bonga S, Pérez-Sánchez J, Tort L (2000) A drop in ambient temperature results in a transient reduction of interrenal ACTH responsiveness in the gilthead sea bream (Sparus aurata, L.). Fish Physiol Biochem 23:265–273. https://doi.org/10.1023/A:1007873811975
Scimonelli T, Celis ME (1990) A central action of alpha-melanocyte-stimulating hormone on serum levels of LH and prolactin in rats. J Endocrinol 124:127–132. https://doi.org/10.1677/joe.0.1240127
Shahjahan M, Kitahashi T, Parhar IS (2014) Central pathways integrating metabolism and reproduction in teleosts. Front Endocrinol (Lausanne) 5:25–36. https://doi.org/10.3389/fendo.2014.00036
Smith CJ, Haley SR (1988) Steroid profiles of the female Tilapia, Oreochromis mossambicus, and correlation with oocyte growth and mouthbrooding behavior. Gen Comp Endocrinol 69:88–98
Swanson P, Dickey JT, Campbell B (2003) Biochemistry and physiology of fish gonadotropins. Fish Physiol Biochem 28:53–55
Thody AJ, Ridley K, Penny RJ, Chalmers R, Fisher C, Shuster S (1983) MSH peptides are present in mammalian skin. Peptides 4:813–816
Thody AJ, Wilson CA (1983) Melanocyte stimulating hormone and the inhibition of sexual behaviour in the female rat. Physiol Behav 31:67–72. https://doi.org/10.1016/0031-9384(83)90097-5
Vallarino M, Delbende C, Jegou S, Vaudry H (1988) Alpha-melanocyte-stimulating hormone (alpha-MSH) in the brain of the cartilaginous fish. Immunohistochemical localization and biochemical characterization. Peptides 9:899–907. https://doi.org/10.1016/0196-9781(88)90139-8
Vallarino M, Tranchand Bunel D, Vaudry H (1992) Alpha-melanocyte-stimulating hormone (alpha-MSH) in the brain of the African lungfish Protopterus annectens immunohistochemical localization and biochemical characterization. J Comp Neurol 322:266–274. https://doi.org/10.1002/cne.903220212
Vaudry H, Chartrel N, Desrues L, Galas L, Kikuyama S, Mor A, Nicolas P, Tonon MC (1999) The pituitary-skin connection in amphibians reciprocal regulation of melanotrope cells and dermal melanocytes. Ann N Y Acad Sci 885:2041–2056. https://doi.org/10.1111/j.1749-6632.1999.tb08664.x
Vijayalaxmi, Sakharkar AJ, Ganesh CB (2020) Leucine-enkephalin-immunoreactive neurons in the brain of the cichlid fish Oreochromis mossambicus. Neuropeptides 81:101999. https://doi.org/10.1016/j.npep.2019.101999
Funding
This study was supported by a grant from Science and Engineering Research Board, Department of Science and Technology (No. EEQ/2017/414), New Delhi, Government of India.
Author information
Authors and Affiliations
Contributions
Jyoti Kumbar conducted the study, analysed the results and prepared the draft. CBG was involved in conceptualization, funding acquisition and review and editing of the paper.
Corresponding author
Ethics declarations
Ethics approval
The experimental procedures were approved by an IAEC (No. 639/GO/Re/S/02/CPCSEA).
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Kumbar, J., Ganesh, C.B. The effect of α-MSH treatment on the hypothalamic-pituitary-gonad axis in the cichlid fish Oreochromis mossambicus. Fish Physiol Biochem 47, 1659–1668 (2021). https://doi.org/10.1007/s10695-021-01005-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-021-01005-9