Impact of absolute food deprivation on the reproductive system in male goldfish exposed to sex steroids

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid38880793

Grantová podpora
CENAKVA: LM2018099 and LM2023038 Ministerstvo Školství, Mládeže a Tělovýchovy
QK21010141 Národní Agentura pro Zemědělský Výzkum
Natural Sciences and Engineering Research Council of Canada Natural Sciences and Engineering Research Council of Canada
None Saskatchewan Health Research Foundation
None CIHR - Canada
None University of Tehran
None CIHR - Canada

Odkazy

PubMed 38880793
DOI 10.1007/s00360-024-01570-4
PII: 10.1007/s00360-024-01570-4
Knihovny.cz E-zdroje

There is a link between metabolism and reproduction as metabolic hormones affect hypothalamus-pituitary-testis (HPT) hormonal functions and vice versa. The aim of the present study was to investigate the effects of negative energy balance on the reproductive system in male goldfish exposed to testosterone (T) and 17β-estradiol (E2). Following 7 days of food deprivation (FD), ANOVA models showed significant FD × sex steroid interactions on sperm quality and circulating sex steroid levels. When FD effects were investigated, 11-ketotestosterone (11-KT) level and sperm motility and velocity decreased in food-deprived goldfish in the control group. In E2-exposed goldfish, FD decreased sperm production in addition to sperm motility and velocity that coincided with an elevation of circulating E2 level. However, FD did not significantly impact sex steroids and sperm quality in T-exposed goldfish. ANOVA models showed non-significant FD × sex steroid interactions for HSI, GSI, circulating luteinizing hormone (Lh) level, and metabolic (preproghrelin, goat and nucb2) and reproductive (kiss1, gpr54 and gnrh3) mRNAs. Furthermore, results showed that FD decreased HSI, and increased Lh levels and testicular preproghrelin and goat mRNAs, while sex steroids increased mid-brain nucb2, kiss1 and gpr54 mRNAs. Together, our results suggest that FD-induced inhibition of androgenesis resulted in diminished sperm quality associated with activation of the testicular ghrelinergic system, and negative feedback of 11-KT increased Lh level. The FD-induced testicular metabolic and hormonal system was impacted in goldfish exposed to sex steroids. However, the negative effects of FD on sperm quality were accelerated in E2-exposed goldfish due to estrogenic activity. This study provides novel information to better understand metabolic-associated reproductive disorders in fish.

Zobrazit více v PubMed

Alavi SMH, Barzegar-Fallah S, Rahdar P, Ahmadi MM, Yavari M, Hatef A, Golshan M, Linhart O (2021) A review on environmental contaminants-related fertility threat in male fishes: effects and possible mechanisms of action learned from wildlife and laboratory studies. Animals 11(10):2817. https://doi.org/10.3390/ani11102817 PubMed DOI PMC

Ankley GT, Bencic DC, Breen MS, Collette TW, Conolly RB, Denslow ND, Edwards SW, Ekman DR, Garcia-Reyero N, Jensen KM, Lazorchak JM, Martinović D, Miller DH, Perkins EJ, Orlando EF, Villeneuve DL, Wang RL, Watanabe KH (2009) Endocrine disrupting chemicals in fish: developing exposure indicators and predictive models of effects based on mechanism of action. Aquat Toxicol 92:168–178. https://doi.org/10.1016/j.aquatox.2009.01.013 PubMed DOI

Bertucci JI, Blanco AM, Canosa LF, Unniappan S (2016) Estradiol and testosterone modulate the tissue-specific expression of ghrelin, ghs-r, goat and nucb2 in goldfish. Gen Comp Endocrinol 228:17–23. https://doi.org/10.1016/j.ygcen.2016.01.006 PubMed DOI

Billard R (1986) Spermatogenesis and spermatology of some teleost fish species. Reprod Nutr Develop 26:877–920. https://doi.org/10.1051/rnd:19860601 DOI

Castellano JM, Navarro VM, Fernández-Fernández R, Nogueiras R, Tovar S, Roa J, Vazquez MJ, Vigo E, Casanueva FF, Aguilar E, Pinilla L, Dieguez C, Tena-Sempere M (2005) Changes in hypothalamic KiSS-1 system and restoration of pubertal activation of the reproductive axis by kisspeptin in undernutrition. Endocrinology 146(9):3917–3925. https://doi.org/10.1210/en.2005-0337 PubMed DOI

Chang B, Song C, Gao H, Ma T, Li T, Ma Q, Yao T, Wang M, Li J, Yi X, Tang D, Cao S (2021) Leptin and inflammatory factors play a synergistic role in the regulation of reproduction in male mice through hypothalamic kisspeptin-mediated energy balance. Reprod Biol Endocrinol 19(1):12. https://doi.org/10.1186/s12958-021-00698-0 PubMed DOI PMC

Chatzifotis S, Papadaki M, Despoti S, Roufidou C, Antonopoulou E (2011) Effect of starvation and re-feeding on reproductive indices, body weight, plasma metabolites and oxidative enzymes of sea bass (Dicentrarchus labrax). Aquaculture 316:53–59. https://doi.org/10.1016/j.aquaculture.2011.02.044 DOI

Compagnucci C, Compagnucci GE, Lomniczi A, Mohn C, Vacas I, Cebral E, Elverdin JC, Friedman SM, Rettori V, Boyer PM (2002) Effect of nutritional stress on the hypothalamo-pituitary-gonadal axis in the growing male rat. Neuroimmunomodulation 10(3):153–162. https://doi.org/10.1159/000067177 PubMed DOI

Dickey JT, Swanson P (1998) Effects of sex steroids on gonadotropin (FSH and LH) regulation in coho salmon (Oncorhynchus kisutch). J Mol Endocrinol 21(3):291–306. https://doi.org/10.1677/jme.0.0210291 PubMed DOI

Dore R, Levata L, Lehnert H, Schulz C (2017) Nesfatin-1: functions and physiology of a novel regulatory peptide. J Endocrinol 232:R45–65. https://doi.org/10.1530/JOE-16-0361 PubMed DOI

Dufour S, Quérat B, Tostivint H, Pasqualini C, Vaudry H, Rousseau K (2020) Origin and evolution of the neuroendocrine control of reproduction in vertebrates, with special focus on genome and gene duplications. Physiol Rev 100:869–943. https://doi.org/10.1152/physrev.00009.2019 PubMed DOI

Escobar S, Felip A, Salah M, Zanuy S, Carrillo M (2014) Long-term feeding restriction in prepubertal male sea bass (Dicentrarchus labrax L.) increases the number of apoptotic cells in the testis and affects the onset of puberty and certain reproductive parameters. Aquaculture 433:504–512. https://doi.org/10.1016/j.aquaculture.2014.07.008 DOI

Fontaine R, Royan MR, von Krogh K, Weltzien F-A, Dianne M, Baker DM (2020) Direct and indirect effects of sex steroids on gonadotrope cell plasticity in the teleost fish pituitary. Front Endocrinol 11:605068. https://doi.org/10.3389/fendo.2020.605068 DOI

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 luteinizing hormone secretion in the female rat. Neurosci Lett 460(2):143–147. https://doi.org/10.1016/j.neulet.2009.05.060 PubMed DOI

Gao X, Zhang K, Song M, Li X, Luo L, Tian Y, Zhang Y, Li Y, Zhang X, Ling Y, Fang F, Liu Y (2016) Role of nesfatin-1 in the reproductive axis of male rat. Sci Rep 6:32877. https://doi.org/10.1038/srep32877 PubMed DOI PMC

Golshan M, Hatef A, Zare A, Socha M, Milla S, Gosiewski G, Fontaine P, Sokołowska-Mikołajczyk M, Habibi HR, Alavi SMH (2014) Alternations in neuroendocrine and endocrine regulation of reproduction in male goldfish (Carassius auratus) following an acute and chronic exposure to vinclozolin, in vivo. Aquat Toxicol 155:73–83. https://doi.org/10.1016/j.aquatox.2014.06.004 PubMed DOI

Golshan M, Hatef A, Kazori N, Socha M, Sokołowska-Mikołajczyk M, Habibi HR, Linhart O, Alavi SMH (2022) A chronic exposure to bisphenol A reduces sperm quality in goldfish associated with increases in kiss2, gpr54 and gnrh3 mRNA and circulatory LH levels at environmentally relevant concentrations. Comp Biochem Physiol C Toxicol Pharmacol 257:109342. https://doi.org/10.1016/j.cbpc.2022.109342

Gonzalez R, Kerbel B, Chun A, Unniappan S (2010) Molecular, cellular and physiological evidences for the anorexigenic actions of nesfatin-1 in goldfish. PLoS ONE 5(12):e15201. https://doi.org/10.1371/journal.pone.0015201 PubMed DOI PMC

Grizard G, Artonne C, Grizard J, Boucher D (1997) Effect of short-term starvation on Leydig cell function in adult rats. Arch Androl 38(3):207–214. https://doi.org/10.3109/01485019708994879 PubMed DOI

Hatef A, Unniappan S (2019) Metabolic hormones and the regulation of spermatogenesis in fishes. Theriogenology 134:121–128. https://doi.org/10.1016/j.theriogenology.2019.05.021 PubMed DOI

Hatef A, Alavi SMH, Linhartova Z, Rodina M, Policar T, Linhart O (2010) In vitro effects of Bisphenol A on sperm motility characteristics in Perca fluviatilis L. (Percidae; Teleostei). J Appl Ichthyol 26(5):696–701. https://doi.org/10.1111/j.1439-0426.2010.01543.x

Hatef A, Shajan S, Unniappan S (2015) Nutrient status modulates the expression of nesfatin-1 encoding nucleobindin 2A and 2B mRNAs in zebrafish gut, liver and brain. Gen Comp Endocrinol 215:51–60. https://doi.org/10.1016/j.ygcen.2014.09.009 PubMed DOI

Hevrøy EM, Azpeleta C, Shimizu M, Lanzén A, Kaiya H, Espe M, Olsvik PA (2011) Effects of short-term starvation on ghrelin, GH-IGF system, and IGF-binding proteins in Atlantic salmon. Fish Physiol Biochem 37:217–232. https://doi.org/10.1007/s10695-010-9434-3 PubMed DOI

Hill JW, Elias CF (2018) Neuroanatomical framework of the metabolic control of reproduction. Physiol Rev 98(4):2349–2380. https://doi.org/10.1152/physrev.00033.2017 PubMed DOI PMC

Kah O, Pontet A, Nunez Rodriguez J, Calas A, Breton B (1989) Development of an enzyme-linked immunosorbent assay for goldfish gonadotropin. Biol Reprod 41(1):68–73. https://doi.org/10.1095/biolreprod41.1.68 PubMed DOI

Kobayashi MA, Sohn YC, Yoshiura Y, Aida K (2000) Effects of sex steroids on the mRNA levels of gonadotropin subunits in juvenile and ovariectomized goldfish Carassius auratus. Fish Sci 66(2):223–231. https://doi.org/10.1046/j.1444-2906.2000.00038.x DOI

Kobayashi M, Sorensen PW, Stacey NE (2002) Hormonal and pheromonal control of spawning behavior in the goldfish. Fish Physiol Biochem 26:71–84. https://doi.org/10.1023/A:1023375931734 DOI

Kojima M, Hosoda H, Date Y, Nakazato M, Matuso H, Kangawa K (1999) Ghrelin is a growth-hormone-releasing acylated peptide. Nature 402:656–660. https://doi.org/10.1038/45230 PubMed DOI

Lahnsteiner F, Berger B, Kletzl M, Weismann T (2006) Effect of 17β-estradiol on gamete quality and maturation in two salmonid species. Aquat Toxicol 79:124–131. https://doi.org/10.1016/j.aquatox.2006.05.011 PubMed DOI

Leonhardt S, Shahab M, Luft H, Wuttke W, Jarry H (1999) Reduction of luteinizing hormone secretion induced by long-term feed restriction in male rats is associated with increased expression of GABA-synthesizing enzymes without alterations of GnRH gene expression. J Neuroendocrinol 11(8):613–619. https://doi.org/10.1046/j.1365-2826.1999.00377.x PubMed DOI

Levavi-Sivan B, Biran J, Fireman E (2006) Sex steroids are involved in the regulation of gonadotropin-releasing hormone and dopamine D2 receptors in female tilapia pituitary. Biol Reprod 75(4):642–650. https://doi.org/10.1095/biolreprod.106.051540 PubMed DOI

Lin F, Zhou C, Chen H, Wu H, Xin Z, Liu J, Gao Y, Yuan D, Wang T, Wei R, Chen D, Yang S, Wang Y, Pu Y, Li Z (2014) Molecular characterization, tissue distribution and feeding related changes of NUCB2A/nesfatin-1 in Ya-fish (Schizothorax prenanti). Gene 536(2):238–246. https://doi.org/10.1016/j.gene.2013.12.031 PubMed DOI

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-∆∆CT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262 PubMed DOI

Martini AC, Fernández-Fernández RS, Tovar S, Navarro VM, Vigo E, Vazquez MJ, Davies JS, Thompson NM, Aguilar E, Pinilla L, Wells T, Dieguez C, Tena-Sempere M (2006) Comparative analysis of the effects of ghrelin and unacylated ghrelin on luteinizing hormone secretion in male rats. Endocrinology 147(5):2374–2382. https://doi.org/10.1210/en.2005-1422 PubMed DOI

Matsubara M, Sakata I, Wada R, Yamazaki M, Inoue K, Sakai T (2004) Estrogen modulates ghrelin expression in the female rat stomach. Peptides 25:289–297. https://doi.org/10.1016/j.peptides.2003.12.020 PubMed DOI

Mechaly AS, Tovar Bohórquez MO, Mechaly AE, Suku E, Pérez MR, Giorgetti A, Ortí G, Viñas J, Somoza GM (2018) Evidence of alternative splicing as a regulatory mechanism for Kissr2 in pejerrey fish. Front Endocrinol 9:604. https://doi.org/10.3389/fendo.2018.00604 DOI

Nagahama Y (1994) Endocrine regulation of gametogenesis in fish. Int J Dev Biol 38:217–229. https://doi.org/10.1387/ijdb.7981031 PubMed DOI

Oh-IS, Shimizu H, Satoh T, Okada S, Adachi S, Inoue K, Eguchi H, Yamamoto M, Imaki T, Hashimoto K, Tsuchiya T, Monden T, Horiguchi K, Yamada M, Mori M (2006) Identification of nesfatin-1 as a satiety molecule in the hypothalamus. Nature 443(7112):709–712. https://doi.org/10.1038/nature05162 DOI

Omolaso BO, Akanbi CO, Akintayo CO, Oluwole FS (2012) Evaluation of the effects of fasting on fertility in adult male Wistar rats. J Pharmacol Biol Sci 3(4):2–5

Palmer NO, Bakos HW, Fullston T, Lane M (2012) Impact of obesity on male fertility, sperm function and molecular competition. Spermatogenesis 2(4):253–263. https://doi.org/10.4161/spmg.21362 PubMed DOI PMC

Pikle RP, Jatiger RM, Ganesh CB (2017) Food-deprivation-induced suppression of pituitary–testicular-axis in the tilapia Oreochromis mossambicus. Int Aquat Res 9:203–213. https://doi.org/10.1007/s40071-017-0169-y DOI

Poretti MB, Frautschi C, Luque E, Bianconi S, Martini AC, Stutz G, Vincenti L, Santillán ME, Ponzio M, Schiöth HB, de Fiol M, Carlini VP (2018) Reproductive performance of male mice after hypothalamic ghrelin administration. Reproduction 156(2):121–132. https://doi.org/10.1530/REP-17-0535 PubMed DOI

Rajeswari JJ, Unniappan S (2020) Nesfatin-1 suppresses fish reproductive axis and gonadal steroidogenesis. Reproduction 160:445–454. https://doi.org/10.1530/REP-20-0068 PubMed DOI

Rajeswari JJ, Hatef A, Golshan M, Alavi SMH, Unniappan S (2019) Metabolic stress leads to divergent changes in the ghrelinergic system in goldfish (Carassius auratus) gonads. Comp Biochem Physiol Mol Integr Physiol 235:112–120. https://doi.org/10.1016/j.cbpa.2019.05.027 DOI

Rehm S, White TE, Zahalka EA, Stanislaus DJ, Boyce RW, Wier PJ (2008) Effects of food restriction on testis and accessory sex glands in maturing rats. Toxicol Pathol 36(5):687–694. https://doi.org/10.1177/0192623308320275 PubMed DOI

Sales CF, Pinheiro APB, Ribeiro YM, Weber AA, de Oliveira Paes-Leme F, Luz RK, Bazzoli N, Rizzo E, Melo RMC (2020) Effects of starvation and refeeding cycles on spermatogenesis and sex steroids in the Nile tilapia Oreochromis Niloticus. Mol Cell Endocrinol 500:110643. https://doi.org/10.1016/j.mce.2019.110643 PubMed DOI

Samuel SA, Francis AO, Denen A, Anthony OO (2015) Effects of prolonged fasting on sperm count. J Mol Pathophysiol 4(3):99–102. https://doi.org/10.5455/jmp.20150915011928 DOI

Sánchez-Bretaño A, Blanco AM, Unniappan S, Kah O, Gueguen MM, 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(10):e0141043. https://doi.org/10.1371/journal.pone.0141043 PubMed DOI PMC

Schalla MA, Stengel A (2021) The role of the gastric hormones ghrelin and nesfatin-1 in reproduction. Int J Mol Sci 22:11059. https://doi.org/10.3390/ijms222011059 PubMed DOI PMC

Seon S, Jeon D, Kim H, Chung Y, Choi N, Yang H (2017) Testosterone regulates NUCB2 mRNA expression in male mouse hypothalamus and pituitary gland. Dev Reprod 21(1):71–78. https://doi.org/10.12717/DR.2017.21.1.071 PubMed DOI PMC

Sharpe RL, Woodhouse A, Moon TW, Trudeau VL, MacLatchy DL (2007) β-Sitosterol and 17β-estradiol alter gonadal steroidogenic acute regulatory protein (StAR) expression in goldfish, Carassius auratus. Gen Comp Endocrinol 151:34–41. https://doi.org/10.1016/j.ygcen.2006.11.005 PubMed DOI

Shepperd E, Peng C, Unniappan S (2012) Ghrelinergic system in fish ovaries and ghrelin inhibition of germinal vesicle breakdown in zebrafish oocytes. Gen Comp Endocrinol 176(3):426–431. https://doi.org/10.1016/j.ygcen.2012.01.014 PubMed DOI

Sirotkin AV, Chrenková M, Nitrayová S, Patras P, Darlak K, Valenzuela F, Pinilla L, Tena-Sempere M (2008) Effects of chronic food restriction and treatments with leptin or ghrelin on different reproductive parameters of male rats. Peptides 29:1362–1368. https://doi.org/10.1016/j.peptides.2008.03.011 PubMed DOI

Sivalingam M, Parhar IS (2022) Hypothalamic kisspeptin and kisspeptin receptors: species variation in reproduction and reproductive behaviours. Front Neuroendocrinol 64:100951. https://doi.org/10.1016/j.yfrne.2021.100951 PubMed DOI

Sokołowska-Mikołajczyk M, Socha M, Szczerbik P, Epler P (2009) The effects of ghrelin on the in vitro spontaneous and sGnRH-A stimulated luteinizing hormone (LH) release from the pituitary cells of common carp (Cyprinus carpio L). Comp Biochem Physiol Mol Integr Physiol 153:386–390. https://doi.org/10.1016/j.cbpa.2009.03.012 DOI

Tena-Sempere M, Barreiro ML, González LC, Gaytán F, Zhang FP, Caminos JE, Pinilla L, Casanueva FF, Diéguez C, Aguilar E (2002) Novel expression and functional role of ghrelin in rat testis. Endocrinology 143(2):717–725. https://doi.org/10.1210/endo.143.2.8646 PubMed DOI

Unniappan S, Peter RE (2004) In vitro and in vivo effects of ghrelin on luteinizing hormone and growth hormone release in goldfish. Am J Physiol Regul Integr Comp Physiol 286(6):R1093–R1101. https://doi.org/10.1152/ajpregu.00669.2003 PubMed DOI

Unniappan S, Canosa LF, Peter RE (2004) 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. https://doi.org/10.1159/000076634 PubMed DOI

Volkoff H (2015) Cloning, tissue distribution and effects of fasting on mRNA expression levels of leptin and ghrelin in red-bellied piranha (Pygocentrus nattereri). Gen Comp Endocrinol 217–218:20–27. https://doi.org/10.1016/j.ygcen.2015.05.004 PubMed DOI

FAO, IFAD, UNICEF, WFP, WHO (2020) The State of Food Security and Nutrition in the World 2020. Transforming food systems for affordable healthy diets. Rome, FAO. https://doi.org/10.4060/ca9692en DOI

Yamaguchi S, Gen K, Okuzawa K, Matsuyama M, Kagawa H (2006) Influence of estradiol-17β, testosterone, and 11-ketotestosterone on testicular development serum steroid hormone, and gonadotropin secretion in male red sea bream Pagrus major. Fish Sci 72:835–845. https://doi.org/10.1111/j.1444-2906.2006.01225.x DOI

Yang J, Brown MS, Liang G, Grishin NV, Goldstein JL (2008) Identification of the acyltransferase that octanoylates ghrelin, an appetite-stimulating peptide hormone. Cell 132(3):387–396. https://doi.org/10.1016/j.cell.2008.01.017 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...