Abstract
Although the involvement of β-endorphin (β-ERP) in vertebrate reproduction has been suggested, its role in testicular activity is not clear in fish. We describe the influence of β-ERP on spermatogenesis in a cichlid fish in the present paper. In comparison to the control group, the administration of β-ERP (3 µg) caused a significant increase in the number of spermatogonia-A and spermatids. Following treatment with β-ERP (6 µg), a significant increase in the number of spermatogonia-A was observed, whereas the numbers of all the other germ cells, excluding spermatogonia-B, significantly decreased in comparison to those in the control group. In addition, treatment of fish with 6 µg β-ERP resulted in a significant reduction in the dimensions of the lumen and seminiferous lobules, the level of immunopositive androgen receptor (AR) expression in Sertoli cells, and the percentage of luteinizing hormone (LH) immunolabeled in the pituitary compared to those in the control group or the group treated with 3 µg β-ERP. In contrast, the intensity of AR immunoreactivity and the percentage of LH immunolabeling were substantially increased in fish treated with 3 µg β-ERP compared to those in the control group. These findings reveal for the first time that a low dose of β-ERP stimulates the recruitment of spermatogonia as well as spermateleosis, whereas a high concentration affects the recruitment of germ cells prior to meiotic division in tilapia. These results suggest that β-ERP exerts modulatory effects at the testicular and hypophysial levels through alterations in AR expression and LH secretory activity, respectively, in teleosts.
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References
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
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(3):156–165. https://doi.org/10.1002/jez.1781
Chabbi A, Ganesh CB (2016) Neuroanatomical evidence for the involvement of β-endorphin during reproductive stress response in the fish Oreochromis mossambicus. J Chem Neuroanat 77:161–168. https://doi.org/10.1016/j.jchemneu.2016.07.002
Chandrashekar V, Bartke A (1992) The influence of beta-endorphin on testicular endocrine function in adult rats. Biol Reprod 47(1):1–5. https://doi.org/10.1095/biolreprod47.1.1
Chaube R, Sharma S, Senthilkumaran B, Bhat SG, Joy KP (2022) Kisspeptins stimulate the hypothalamus - pituitary - ovarian axis and induce final oocyte maturation and ovulation in female stinging catfish (Heteropneustes fossilis): Evidence from in vivo and in vitro studies. Aquac 548(2):737734. https://doi.org/10.1016/j.aquaculture.2021.737734
Chen WP, Witkin JW, Silverman AJ (1989) Beta-endorphin and gonadotropin-releasing hormone synaptic input to gonadotropin-releasing hormone neurosecretory cells in the male rat. J Comp Neurol 286(1):85–95. https://doi.org/10.1002/cne.902860106
Ciarcia G, Cardone A, Paolucci M, Botte V (1996) In vitro effects of beta-endorphin on testicular release of androgens in the lizard Podarcis sicula Raf. Mol Reprod Dev 45(3):308–312. https://doi.org/10.1002/(sici)1098-2795(199611)45:3%3C308::aid-mrd7%3E3.0.co;2-w
Contijoch AM, Malamed S, Sarkar DK, Advis JP (1993) Beta-endorphin regulation of LHRH release at the median eminence level: immunocytochemical and physiological evidence in hens. Neuroendocrinology 57:365–373. https://doi.org/10.1159/000126381
El-Haggar S, El-Ashmawy S, Attia A, Mostafa T, Roaiah MM, Fayez A, Ghazi S, Zohdy W, Roshdy N (2006) Beta-endorphin in serum and seminal plasma in infertile men. Asian J Androl 8(6):709–712. https://doi.org/10.1111/j.1745-7262.2006.00180.x
Elias AN, Iyer K, Pandian MR, Weathersbee P, Stone S, Tobis J (1986) Betaendorphin/beta-lipotropin release and gonadotropin secretion after acute exercise in normal males. J Appl Physiol (Bethesda, Md.:1985) 61(6):2045–2049. https://doi.org/10.1152/jappl.1986.61.6.2045
Escobar S, Servili A, Espigares F, Gueguen MM, Brocal I, Felip A, Gómez A, Carrillo M, Zanuy S, Kah O (2013) Expression of kisspeptins and kiss receptors suggests a large range of functions for kisspeptin systems in the brain of the European sea bass. PLos One 8(7):e70177. https://doi.org/10.1371/journal.pone.0070177
Estomba H, Muñoa-Hoyos I, Gianzo M, Urizar-Arenaza I, Casis L, Irazusta J, Subirán N (2016) Expression and localization of opioid receptors in male germ cells and the implication for mouse spermatogenesis. PLos One 11(3):e0152162. https://doi.org/10.1371/journal.pone.0152162
Fabbri A, Dufau ML (1988) Hormonal regulation of β-endorphin in the testis. J Steroid Biochem 30(1–6):347–352. https://doi.org/10.1016/0022-4731(88)90121-5
Fabbri A, Knox G, Buczko E, Dufau ML (1988) Beta-endorphin production by the fetal Leydig cell: regulation and implications for paracrine control of Sertoli cell function. Endocrinology 122(2):749–755. https://doi.org/10.1210/endo-122-2-749
Facchinetti F, Genazzani AR, Vallarino M, Pestarino M, Polzonetti-Magni A, Carnevali O, Ciarcia G, Fasano S, D’Antonio M, Pierantoni R (1993) Opioids and testicular activity in the frog Rana esculenta. J Endocrinol 137:49–57. https://doi.org/10.1677/joe.0.1370049
Faletti A, Jawerbaum A, Viggiano J, Gimeno MA (1997) Naltrexone enhances ovulation and prostaglandin synthesis in the rat ovary. Prostaglandins 54:665–675. https://doi.org/10.1016/s0090-6980(97)00132-9
Faletti AG, Mastronardi CA, Lomniczi A, Seilicovich A, Gimeno M, McCann SM, Rettori V (1999) β-Endorphin blocks luteinizing hormone-releasing hormone release by inhibiting the nitricoxidergic pathway controlling its release. Proc Natl Acad Sci USA 96:1722–1726. https://doi.org/10.1073/pnas.96.4.1722
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(3):627–636. https://doi.org/10.1007/s10695-012-9725-y
Kanda S, Akazome Y, Mitani Y, Okubo K, Oka Y (2013) Neuroanatomical evidence that kisspeptin directly regulates isotocin and vasotocin neurons. PLos One 8(4):e62776. https://doi.org/10.1371/journal.pone.0062776
Kant PA, Saxena RN (1995) Effect of beta-endorphin and naloxone on rat testicular steroidogenesis. Ind J Exp Biol 33(3):165–168
Kilpatrick DL, Millette CF (1986) Expression of proenkephalin messenger RNA by mouse spermatogenic cells. Proc Natl Acad Sci U S A 83(14):5015–5018. https://doi.org/10.1073/pnas.83.14.5015
Knotts LK, Glass JD (1988) Effects of photoperiod, beta-endorphin, and naloxone on in vivo secretion of testosterone in white-footed mouse (Peronyscus leucopus) testes. Biol Reprod 39:205–212. https://doi.org/10.1095/biolreprod39.1.205
Konkal P, Ganesh CB (2018) Exposure to low or high light intensity affects pituitary-testicular activity in the fish Oreochromis mossambicus. Aquaculture 497:109–116. https://doi.org/10.1016/j.aquaculture.2018.07.043
Laxmi NA, Vijayan E (1998) Effects of chronic systemic administration of opioid peptides, naloxone and N-acetyl β-endorphin antiserum on gonadotropins and testicular functions in the rat. Ind J Exp Biol 36:361–366
Leadem CA, Kalra SP (1985) Effects of endogenous opioid peptides and opiates on luteinizing hormone and prolactin secretion in ovariectomized rats. Neuroendocrinology 41:342–352. https://doi.org/10.1159/000124199
Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38(2):217–229
Pintar JE, Schachter BS, Herman AB, Durgerian S, Krieger DT (1984) Characterization and localization of proopiomelanocortin messenger RNA in the adult rat testis. Science 225(4662):632–634. https://doi.org/10.1126/science.6740329
Polzonetti-Magni A, Facchinetti F, Carnevali O, Mosconi G, Pestarino M, Vallarino M, Ciarcia G (1994) Presence and steroidogenic activity of beta-endorphin in the ovary of the lizard Podarcis sicula sicula (Raf.). Biol Reprod 50:1059–1065. https://doi.org/10.1095/biolreprod50.5.1059
Sabbieti MG, Marchetti L, Menghi G, Yamamoto K, Kikuyama S, Vaudry H, Polzonetti-Magni A (2003) Occurrence of β-endorphin binding sites in the pituitary of the frog Rana esculenta: effect of β-endorphin on luteinizing hormone secretion. Gen Comp Endocrinol 132(3):391–398. https://doi.org/10.1016/s0016-6480(03)00102-3
Sakharkar AJ, Singru PS, Mazumdar M, Subhedar N (2006) Reproduction phase-related expression of β-endorphin-like immunoreactivity in the nucleus lateralis tuberis of the female Indian major carp Cirrhinus mrigala: correlation with the luteinising hormone cells-ovary axis. J Neuroendocrinol 18(5):319–329. https://doi.org/10.1111/j.1365-2826.2006.01421.x
Sarkar S, Subhedar N (2000) β-Endorphin and gonadotropin-releasing hormone in the forebrain and pituitary of the female catfish, Clarias batrachus: double-immunolabeling study. Gen Comp Endocrinol 118(1):39–47. https://doi.org/10.1006/gcen.1999.7437
Shinde D, Ganesh CB (2022) Chronic exposure to aquacultural stressors affects pituitary-testis axis in the Mozambique tilapia Oreochromis mossambicus. Fish Physiol Biochem 48(2):437–448. https://doi.org/10.1007/s10695-022-01061-9
Somoza GM, Mechaly AS, Trudeau VL (2020) Kisspeptin and GnRH interactions in the reproductive brain of teleosts. Gen Comp Endocrinol 298:113568. https://doi.org/10.1016/j.ygcen.2020.113568
Tang H, Liu Y, Luo D, Ogawa S, Yin Y, Li S, Zhang Y, Hu W, Parhar IS, Lin H, Liu X, Cheng CH (2015) The kiss/kissr systems are dispensable for zebrafish reproduction: evidence from gene knockout studies. Endocrinology 156(2):589–599. https://doi.org/10.1210/en.2014-1204
Taya K, Sasamoto S (1989) Inhibitory effects of corticotrophin releasing factor and β-endorphin on LH and FSH secretion in the lactating rat. J Endocrinol 120:509–515. https://doi.org/10.1677/joe.0.1200509
Tsong SD, Phillips D, Halmi N, Liotta AS, Margioris A, Bardin CW, Krieger DT (1982) ACTH and beta-endorphin-related peptides are present in multiple sites in the reproductive tract of the male rat. Endocrinology 110(6):2204–2206. https://doi.org/10.1210/endo-110-6-2204
Uenoyama Y, Nagae M, Tsuchida H, Inoue N, Tsukamura H (2021) Role of KNDy neurons expressing kisspeptin, neurokinin B, and dynorphin A as a GnRH pulse generator controlling mammalian reproduction. Front Endocrinol 12:724632. https://doi.org/10.3389/fendo.2021.724632
Uenoyama Y, Tsuchida H, Nagae M, Inoue N, Tsukamura H (2022) Opioidergic pathways and kisspeptin in the regulation of female reproduction in mammals. Front Neurosci 16:958377. https://doi.org/10.3389/fnins.2022.958377
Urizar-Arenaza I, Estomba H, Muñoa-Hoyos I, Matorras R, Esposito A, Candenas L, Pinto FM, Valdivia A, Irazusta J, Subirán N (2016) The opioid peptide beta-endorphin stimulates acrosome reaction in human spermatozoa. Andrology 4(1):143–151. https://doi.org/10.1111/andr.12133
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
Xiong X, Zhang L, Fan M, Han L, Wu Q, Liu S, Miao J, Liu L, Wang X, Guo B, Tong D, Ni L, Yang J, Huang C (2019) β-Endorphin induction by psychological stress promotes Leydig cell apoptosis through p38 MAPK pathway in male rats. Cells 8(10):1265. https://doi.org/10.3390/cells8101265
Zerani M, Gobbetti A (1992) In vivo and in vitro studies on effects of beta-endorphin and naloxone on sex steroids in the water frog Rana esculenta. Acta Physiol Scand 146:271–279. https://doi.org/10.1111/j.1748-1716.1992.tb09416.x
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The first author expresses gratitude towards Karnatak University, Dharwad, for conferring a University Research Scholarship (URS). The authors express their gratitude for the infrastructural assistance extended by the Science and Engineering Research Board–Department of Science and Technology (SERB–DST), New Delhi, India.
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This work was supported by a grant from UGC-SAP (No. 18/2015/DSA-I), New Delhi.
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D.S. conducted the experiment and performed data analysis. S.K.B. helped in the data analysis and preparation of manuscript draft. C.B.G. was responsible for conceptualization, acquisition of funding, and review and editing of the manuscript.
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Shinde, D., Bhat, S.K. & Ganesh, C.B. The opioid peptide β-endorphin interferes with the pituitary-testis axis in the Mozambique tilapia Oreochromis mossambicus. Fish Physiol Biochem 50, 733–743 (2024). https://doi.org/10.1007/s10695-024-01302-z
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DOI: https://doi.org/10.1007/s10695-024-01302-z