Irisin may have a role in pubertal development and regulation of reproductive function in rats

in Reproduction

Correspondence should be addressed to S Canpolat; Email: sinancanpolat@firat.edu.tr
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Physical exercise and body muscle/fat mass are known to affect the endocrine system, puberty onset and reproductive health. However, the potential effects of irisin, an adipo-myokine and exercise-induced hormone, have not yet been fully elucidated on reproductive maturation. Therefore, the present study aimed to determine the effects of irisin administration on pubertal maturation and reproductive system in female and male rats. Daily i.p. injection of irisin (100 ng/kg; from postnatal day 21 for about 10 weeks) delayed the ages at the vaginal opening (as an external index of puberty onset) and first estrus. Furthermore, continuous administration of irisin to female rats caused a significant decrease in serum follicle-stimulating hormone levels and an increase in serum luteinizing hormone and 17β-estradiol levels, as well as causing histopathological changes in the ovarian tissue. On the contrary, irisin administration to male rats did not modify the timing of puberty, as estimated by age at preputial separation. However, chronic exposure to irisin produced significant increases in serum luteinizing hormone and testosterone levels and also sperm concentration and seminiferous tubule diameter in male rats. In conclusion, irisin exposure has different effects on both pubertal maturation and reproductive system in female and male rats. The present findings reveal that chronic irisin exposure may lead to disorders in the female reproductive system and may have androgenic potential on the hypothalamic-pituitary-gonadal axis in males.

 

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  • AllouhMZ 2015 Effects of swimming activity on the copulatory behavior of sexually active male rats. International Journal of Impotence Research 27 113117. (https://doi.org/10.1038/ijir.2014.42)

    • Search Google Scholar
    • Export Citation
  • AnastasilakisADPolyzosSASaridakisZGKynigopoulosGSkouvaklidouECMolyvasDVasiloglouMFApostolouAKaragiozoglou-LampoudiTSiopiA 2014 Circulating irisin in healthy, young individuals: day-night rhythm, effects of food intake and exercise, and associations with gender, physical activity, diet, and body composition. Journal of Clinical Endocrinology and Metabolism 99 32473255. (https://doi.org/10.1210/jc.2014-1367)

    • Search Google Scholar
    • Export Citation
  • ArtaşGPalaŞKuloğluTAtilganRYavuzkirŞAkyolA 2018 The effects of sclerotherapy with 5% trichloroacetic acid on the cyst diameter and ovarian tissue in the rat ovarian cyst model. Journal of Obstetrics and Gynaecology 38 686692. (https://doi.org/10.1080/01443615.2017.1399991)

    • Search Google Scholar
    • Export Citation
  • AydinSKulogluTAydinSKalayciMYilmazMCakmakTAlbayrakSGungorSColakogluNOzercanIH 2014 A comprehensive immunohistochemical examination of the distribution of the fat-burning protein irisin in biological tissues. Peptides 61 130136. (https://doi.org/10.1016/j.peptides.2014.09.014)

    • Search Google Scholar
    • Export Citation
  • BawazirAE 2010 Investigations on the chronic effect of Talbina (Barly water) on hormone (cortisol and testosterone), reproductive system and some neurotransmitter. American-Eurasian Journal of Scientific Research 5 134142.

    • Search Google Scholar
    • Export Citation
  • BenianAGuralpOUzunDDOkyarASahmayS 2013 The effect of repeated administration of methotrexate (MTX) on rat ovary: measurement of serum antiMullerian hormone (AMH) levels. Gynecological Endocrinology 29 226229. (https://doi.org/10.3109/09513590.2012.738725)

    • Search Google Scholar
    • Export Citation
  • BlüherSPanagiotouGPetroffDMarkertJWagnerAKlemmTFilippaiosAKellerAMantzorosCS 2014 Effects of a 1‐year exercise and lifestyle intervention on irisin, adipokines, and inflammatory markers in obese children. Obesity 22 17011708. (https://doi.org/10.1002/oby.20739)

    • Search Google Scholar
    • Export Citation
  • BoströmPWuJJedrychowskiMPKordeAYeLLoJCRasbachKABoströmEAChoiJHLongJZ 2012 A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481 463468. (https://doi.org/10.1038/nature10777)

    • Search Google Scholar
    • Export Citation
  • CanpolatSUlkerNYardimciABulmusOOzdemirGSahinZErcanZSerhatliogluIKacarEOzcanM 2016 Studies on the reproductive effects of chronic treatment with agomelatine in the rat. European Journal of Pharmacology 770 3339. (https://doi.org/10.1016/j.ejphar.2015.11.054)

    • Search Google Scholar
    • Export Citation
  • ChauhanNSDixitVK 2010 Effects of Bryonia laciniosa seeds on sexual behaviour of male rats. International Journal of Impotence Research 22 190195. (https://doi.org/10.1038/ijir.2009.62)

    • Search Google Scholar
    • Export Citation
  • DohertyEPakarinenPTiitinenAKiilavuoriAHuhtaniemiIForrestSAittomäkiK 2002 A novel mutation in the FSH receptor inhibiting signal transduction and causing primary ovarian failure. Journal of Clinical Endocrinology and Metabolism 87 11511155. (https://doi.org/10.1210/jcem.87.3.8319)

    • Search Google Scholar
    • Export Citation
  • EneaCBoisseauNFargeas-GluckMADiazVDugueB 2011 Circulating androgens in women: exercise-induced changes. Sports Medicine 41 115. (https://doi.org/10.2165/11536920-000000000-00000)

    • Search Google Scholar
    • Export Citation
  • EsserKAHarpoleCEPrinsGSDiamondAM 2009 Physical activity reduces prostate carcinogenesis in a transgenic model. Prostate 69 13721377. (https://doi.org/10.1002/pros.20987)

    • Search Google Scholar
    • Export Citation
  • FerranteCOrlandoGRecinellaLLeoneSChiavaroliADi NisioCShohrehRManippaFRicciutiAVaccaM 2016 Central inhibitory effects on feeding induced by the adipo-myokine irisin. European Journal of Pharmacology 791 389394. (https://doi.org/10.1016/j.ejphar.2016.09.011)

    • Search Google Scholar
    • Export Citation
  • GeorgopoulosNARoupasND 2016 Impact of intense physical activity on puberty and reproductive potential of young athletes. In Exercise and Human Reproduction pp. 239251. Eds VaamondeDdu PlessisS & AgarwalA. New York, NY: Springer.

    • Search Google Scholar
    • Export Citation
  • Gossell-WilliamsMDavisAO’ConnorN 2006 Inhibition of testosterone-induced hyperplasia of the prostate of Sprague-Dawley rats by pumpkin seed oil. Journal of Medicinal Food 9 284286. (https://doi.org/10.1089/jmf.2006.9.284)

    • Search Google Scholar
    • Export Citation
  • GuéritatJLefeuvre-OrfilaLVincentSCrétualARavanatJLGratas-DelamarcheARannou-BekonoFRébillardA 2014 Exercise training combined with antioxidant supplementation prevents the antiproliferative activity of their single treatment in prostate cancer through inhibition of redox adaptation. Free Radical Biology and Medicine 77 95105. (https://doi.org/10.1016/j.freeradbiomed.2014.09.009)

    • Search Google Scholar
    • Export Citation
  • GurdBKlentrouP 2003 Physical and pubertal development in young male gymnasts. Journal of Applied Physiology 95 10111015. (https://doi.org/10.1152/japplphysiol.00483.2003)

    • Search Google Scholar
    • Export Citation
  • JangHBKimHJKangJHParkSIParkKHLeeHJ 2017 Association of circulating irisin levels with metabolic and metabolite profiles of Korean adolescents. Metabolism: Clinical and Experimental 73 100108. (https://doi.org/10.1016/j.metabol.2017.05.007)

    • Search Google Scholar
    • Export Citation
  • JewoPIDuruFIFadeyibiIOSaaluLCNoronhaCC 2012 The protective role of ascorbic acid in burn-induced testicular damage in rats. Burns 38 113119. (https://doi.org/10.1016/j.burns.2011.02.009)

    • Search Google Scholar
    • Export Citation
  • JiangQZhangQLianAXuY 2017 Irisin stimulates gonadotropins gene expression in tilapia (Oreochromis niloticus) pituitary cells. Animal Reproduction Science 185 140147. (https://doi.org/10.1016/j.anireprosci.2017.06.018)

    • Search Google Scholar
    • Export Citation
  • JonesSLFarrellSGregoryJGPfausJG 2013 Sensitization of sexual behavior in ovariectomized rats by chronic estradiol treatment. Hormones and Behavior 64 818. (https://doi.org/10.1016/j.yhbeh.2013.04.012)

    • Search Google Scholar
    • Export Citation
  • KimHSShinJHMoonHJKimTSKangIHSeokJHKimIYParkKLHanSY 2002 Evaluation of the 20-day pubertal female assay in Sprague-Dawley rats treated with DES, tamoxifen, testosterone, and flutamide. Toxicological Sciences 67 5262. (https://doi.org/10.1093/toxsci/67.1.52)

    • Search Google Scholar
    • Export Citation
  • KorenbrotCCHuhtaniemiITWeinerRI 1977 Preputial separation as an external sign of pubertal development in the male rat. Biology of Reproduction 17 298303. (https://doi.org/10.1095/biolreprod17.2.298)

    • Search Google Scholar
    • Export Citation
  • La MarcaAGrisendiVGriesingerG 2013 How much does AMH really vary in normal women? International Journal of Endocrinology 2013 959487. (https://doi.org/10.1155/2013/959487)

    • Search Google Scholar
    • Export Citation
  • Leal-CerroAGippiniAAmayaMJLageMMatoJADieguezCCasanuevaFF 2003 Mechanisms underlying the neuroendocrine response to physical exercise. Journal of Endocrinological Investigation 26 879885. (https://doi.org/10.1007/BF03345239)

    • Search Google Scholar
    • Export Citation
  • LeePLindermanJDSmithSBrychtaRJWangJIdelsonCPerronRMWernerCDPhanGQKammulaUS 2014 Irisin and FGF21 are cold-induced endocrine activators of brown fat function in humans. Cell Metabolism 19 302309. (https://doi.org/10.1016/j.cmet.2013.12.017)

    • Search Google Scholar
    • Export Citation
  • LiuSDuFLiXWangMDuanRZhangJWuYZhangQ 2017 Effects and underlying mechanisms of irisin on the proliferation and apoptosis of pancreatic β cells. PLoS ONE 12 e0175498. (https://doi.org/10.1371/journal.pone.0175498)

    • Search Google Scholar
    • Export Citation
  • LouisGMBGrayLEMarcusMOjedaSRPescovitzOHWitchelSFSippellWAbbottDHSotoATylRW 2008 Environmental factors and puberty timing: expert panel research needs. Pediatrics 121 (Supplement 3) S192S207. (https://doi.org/10.1542/peds.1813E)

    • Search Google Scholar
    • Export Citation
  • MacklonNSFauserBC 2001 Follicle-stimulating hormone and advanced follicle development in the human. Archives of Medical Research 32 595600. (https://doi.org/10.1016/s0188-4409(01)00327-7)

    • Search Google Scholar
    • Export Citation
  • MannaIJanaKSamantaPK 2004 Intensive swimming exercise-induced oxidative stress and reproductive dysfunction in male Wistar rats: protective role of α-tocopherol succinate. Canadian Journal of Applied Physiologye 29 172185. (https://doi.org/10.1139/h04-013)

    • Search Google Scholar
    • Export Citation
  • MarcondesFKBianchiFJTannoAP 2002 Determination of the estrous cycle phases of rats: some helpful considerations. Brazilian Journal of Biology 62 609614. (https://doi.org/10.1590/s1519-69842002000400008)

    • Search Google Scholar
    • Export Citation
  • Martos-MorenoGAChowenJAArgenteJ 2010 Metabolic signals in human puberty: effects of over and undernutrition. Molecular and Cellular Endocrinology 324 7081. (https://doi.org/10.1016/j.mce.2009.12.017)

    • Search Google Scholar
    • Export Citation
  • OjedaSRUrbanskiHF 1994 Puberty in the rat. In The Physiology of Reproduction pp. 363410. Eds KnobilE & NeillJD. New York, NY: Raven Press.

    • Search Google Scholar
    • Export Citation
  • OzcanSUlkerNBulmusOYardimciAOzcanMCanpolatS 2020 The modulatory effects of irisin on Asprosin, leptin, glucose levels and lipid profile in healthy and obese male and female rats. Archives of Physiology and Biochemistry in press. (https://doi.org/10.1080/13813455.2020.1722706)

    • Search Google Scholar
    • Export Citation
  • ParandinRYousofvandNGhorbaniR 2012 The enhancing effects of alcoholic extract of Nigella sativa seed on fertility potential, plasma gonadotropins and testosterone in male rats. Iranian Journal of Reproductive Medicine 10 355362.

    • Search Google Scholar
    • Export Citation
  • PattonGCVinerR 2007 Pubertal transitions in health. Lancet 369 11301139. (https://doi.org/10.1016/S0140-6736(07)60366-3)

  • PoretskyLIslamJAvtanskiDLinYKShenYLHirthYLesserMRosenwaksZSeto-YoungD 2017 Reproductive effects of irisin: initial in vitro studies. Reproductive Biology 17 285288. (https://doi.org/10.1016/j.repbio.2017.05.011)

    • Search Google Scholar
    • Export Citation
  • ReinehrTElfersCLassNRothCL 2015 Irisin and its relation to insulin resistance and puberty in obese children: a longitudinal analysis. Journal of Clinical Endocrinology and Metabolism 100 21232130. (https://doi.org/10.1210/jc.2015-1208)

    • Search Google Scholar
    • Export Citation
  • RoaJTena-SempereM 2014 Connecting metabolism and reproduction: roles of central energy sensors and key molecular mediators. Molecular and Cellular Endocrinology 397 414. (https://doi.org/10.1016/j.mce.2014.09.027)

    • Search Google Scholar
    • Export Citation
  • ShiortaMKawashimaJNakamuraTOgawaYKamiieJYasunoKShirotaKYoshidaM 2012 Delayed effects of single neonatal subcutaneous exposure of low-dose 17α-ethynylestradiol on reproductive function in female rats. Journal of Toxicological Sciences 37 681690. (https://doi.org/10.2131/jts.37.681)

    • Search Google Scholar
    • Export Citation
  • ShokriSAitkenRJAbdolvahhabiMAbolhasaniFGhasemiFMKashaniIEjtemaeimehrSAhmadianSMinaeiBNaraghiMA 2010 Exercise and supraphysiological dose of nandrolone deconoate increase apoptosis in spermatogenic cells. Basic and Clinical Pharmacology and Toxicology 106 324330. (https://doi.org/10.1111/j.1742-7843.2009.00495.x)

    • Search Google Scholar
    • Export Citation
  • TanakaYNakadaKMoriyoshiMSawamukaiY 2001 Appearance and number of follicles and change in the concentration of serum FSH in female bovine fetuses. Reproduction 121 777782. (https://doi.org/10.1530/rep.0.1210777)

    • Search Google Scholar
    • Export Citation
  • TekinSBeyturAErdenYBeyturACigremisYVardiNTurkozYTekedereliISandalS 2019 Effects of intracerebroventricular administration of irisin on the hypothalamus–pituitary–gonadal axis in male rats. Journal of Cellular Physiology 234 88158824. (https://doi.org/10.1002/jcp.27541)

    • Search Google Scholar
    • Export Citation
  • TymchukCNBarnardRJHeberDAronsonWJ 2001 Evidence of an inhibitory effect of diet and exercise on prostate cancer cell growth. Journal of Urology 166 11851189. (https://doi.org/10.1016/S0022-5347(05)65943-5)

    • Search Google Scholar
    • Export Citation
  • VisserJASchipperILavenJSThemmenAP 2012 Anti-Müllerian hormone: an ovarian reserve marker in primary ovarian insufficiency. Nature Reviews: Endocrinology 8 331341. (https://doi.org/10.1038/nrendo.2011.224)

    • Search Google Scholar
    • Export Citation
  • WahabFShahabMBehrR 2016 Hypothesis: irisin is a metabolic trigger for the activation of the neurohormonal axis governing puberty onset. Medical Hypotheses 95 14. (https://doi.org/10.1016/j.mehy.2016.08.003)

    • Search Google Scholar
    • Export Citation
  • WitkośJWróbelP 2019 Menstrual disorders in amateur dancers. BMC Women’s Health 19 87. (https://doi.org/10.1186/s12905-019-0779-1)

  • YakubuMTAkanjiMAOladijiATAdesokanAA 2008 Androgenic potentials of aqueous extract of Massularia acuminata (G. Don) Bullock ex Hoyl. stem in male Wistar rats. Journal of Ethnopharmacology 118 508513. (https://doi.org/10.1016/j.jep.2008.05.020)

    • Search Google Scholar
    • Export Citation
  • YüceATürkGÇeribaşiSSönmezMÇiftçiMGüvençM 2013 Effects of cinnamon (C innamomum zeylanicum) bark oil on testicular antioxidant values, apoptotic germ cell and sperm quality. Andrologia 45 248255. (https://doi.org/10.1111/and.12000)

    • Search Google Scholar
    • Export Citation
  • ZhangQLinYZhangXYWangDH 2015 Cold exposure inhibits hypothalamic Kiss-1 gene expression, serum leptin concentration, and delays reproductive development in male Brandt’s vole (Lasiopodomys brandtii). International Journal of Biometeorology 59 679691. (https://doi.org/10.1007/s00484-014-0879-4)

    • Search Google Scholar
    • Export Citation