Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2022-0038
Animal Reproduction (AR)
ORIGINAL ARTICLE

Effects of melatonin on testicular function in adult male mice under different photoperiods

Dan-li Jiang; Yang-long Xu; Jian-qiu Pan; Di Fan; Xu Shen; Wan-yan Li; Hong-jia Ou-Yang; Dan-ning Xu; Yun-bo Tian; Yun-mao Huang

Downloads: 0
Views: 6

Abstract

Photoperiod is an important environmental factor affecting animal physiological function. Melatonin is an endogenous hormone that plays an important role in circadian and seasonal (or cyclical) rhythms and seasonal reproduction in mammals. To investigate the effects of melatonin on the reproductive performance of adult male mice under different photoperiods, sixty mice were randomly allotted to six groups: control (Light Dark, 12 L:12 D), control plus melatonin (MLD, 12 L:12 D), 24-hour continuous light (LL, 24 L:0 D), 24-hour continuous light plus melatonin (MLL 24 L:0 D), constant darkness (DD, 0 L:24 D), and constant darkness plus melatonin (MDD, 0 L:24 D). Normal saline (100 μL) was injected into the LD, LL, and DD groups at noon each day; the MLD, MLL, and MDD groups were injected with melatonin (1 mg/mL; 2 mg/kg·body weigh). After 24 hours of prolonged light exposure, testis morphology decreased, convoluted seminiferous tubules became sparse, the diameter of convoluted seminiferous tubules decreased, and the level of sex hormones decreased. After the administration of exogenous melatonin, testicular morphology and sex hormone levels decreased in the MLD group under normal light conditions. In the MLL group, the testicular tissue morphology returned to normal, the diameter of convoluted tubules increased, the hormone levels of LH (Luteinizing hormone) and MTL (melatonin) significantly increased (P<0.05), and th0e gene expressions of LHβ and Mtnr1A (Melatonin receptors 1A) increased. There was almost no difference in the MDD group under continuous darkness. In conclusion, melatonin can damage the reproductive performance of male mice under normal light conditions, while exogenous melatonin can alleviate and protect the testicular injury of male mice under continuous light conditions.

Keywords

photoperiod, melatonin, reproductive function, testicular function

References

Abecia JA, Chemineau P, Keller M, Delgadillo JA. Extended day length in late winter/early spring, with a return to natural day length of shorter duration, increased plasma testosterone and sexual performance in rams with or without melatonin implants. Reprod Domest Anim. 2017;52(5):851-6. http://dx.doi.org/10.1111/rda.12988. PMid:28455947.

Ahmad R, Haldar C. Effect of intra-testicular melatonin injection on testicular functions, local and general immunity of a tropical rodent Funambulus pennanti. Endocrine. 2010;37(3):479-88. http://dx.doi.org/10.1007/s12020-010-9331-7. PMid:20960172.

Akhtar MF, Wei Q, Zhu H, Chen Z, Ahmad E, Zhendan S, Shi F. The role of active immunization against inhibin α-subunit on testicular development, testosterone concentration and relevant genes expressions in testis, hypothalamus and pituitary glands in Yangzhou goose ganders. Theriogenology. 2019;128:122-32. http://dx.doi.org/10.1016/j.theriogenology.2019.01.039. PMid:30743101.

Ansel L, Bentsen AH, Ancel C, Bolborea M, Klosen P, Mikkelsen JD, Simonneaux V. Peripheral kisspeptin reverses short photoperiod-induced gonadal regression in Syrian hamsters by promoting GNRH release. Reproduction. 2011;142(3):417-25. http://dx.doi.org/10.1530/REP-10-0313. PMid:21670127.

Blank JL, Freeman DA. Differential reproductive response to short photoperiod in deer mice: role of melatonin. J Comp Physiol A. 1991;169(4):501-6. http://dx.doi.org/10.1007/BF00197662. PMid:1779421.

Charif SE, Inserra PIF, Schmidt AR, Cortasa SA, Proietto S, Corso MC, Halperin J, Giorgio NP, Lux-Lantos V, Vitullo AD, Dorfman VB. Melatonin is involved in the modulation of the hypothalamic and pituitary activity in the South American plains vizcacha, Lagostomus maximus. J Comp Physiol B. 2022;192(1):141-59. http://dx.doi.org/10.1007/s00360-021-01405-6. PMid:34459966.

Choi D. Continuous melatonin attenuates the regressing activities of short photoperiod in male golden hamsters. Dev Reprod. 2013;17(2):111-9. http://dx.doi.org/10.12717/DR.2013.17.2.111. PMid:25949127.

Dominoni D, Quetting M, Partecke J. Artificial light at night advances avian reproductive physiology. Proc Biol Sci. 2013;280(1756):20123017. http://dx.doi.org/10.1098/rspb.2012.3017. PMid:23407836.

Dubocovich ML, Markowska M. Functional MT1 and MT2 melatonin receptors in mammals. Endocrine. 2005;27(2):101-10. http://dx.doi.org/10.1385/ENDO:27:2:101. PMid:16217123.

Frungieri MB, Mayerhofer A, Zitta K, Pignataro OP, Calandra RS, Gonzalez-Calvar SI. Direct effect of melatonin on Syrian hamster testes: melatonin subtype 1a receptors, inhibition of androgen production, and interaction with the local corticotropin-releasing hormone system. Endocrinology. 2005;146(3):1541-52. http://dx.doi.org/10.1210/en.2004-0990. PMid:15550508.

Gao Y, Wu X, Zhao S, Zhang Y, Ma H, Yang Z, Yang W, Zhao C, Wang L, Zhang Q. Melatonin receptor depletion suppressed hCG-induced testosterone expression in mouse Leydig cells. Cell Mol Biol Lett. 2019;24(1):21. http://dx.doi.org/10.1186/s11658-019-0147-z. PMid:30915128.

Kelestimur H, Ozcan M, Kacar E, Alcin E, Yılmaz B, Ayar A. Melatonin elicits protein kinase C-mediated calcium response in immortalized GT1-7 GnRH neurons. Brain Res. 2012;1435:24-8. http://dx.doi.org/10.1016/j.brainres.2011.11.040. PMid:22177776.

Lateef OM, Akintubosun MO. Sleep and reproductive health. J Circadian Rhythms. 2020;18(1):1. http://dx.doi.org/10.5334/jcr.190. PMid:32256630.

Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402-8. http://dx.doi.org/10.1006/meth.2001.1262. PMid:11846609.

Majrashi KA, Barakat IA, Al-Himaidi AR, Adham KG. Effect of exogenous melatonin treatment on the reproductive characteristics and progeny of male rats exposed to different periods from light and darkness. Physiol Res. 2017;66(3):507-18. http://dx.doi.org/10.33549/physiolres.933556. PMid:28248544.

Malpaux B, Migaud M, Tricoire H, Chemineau P. Biology of mammalian photoperiodism and the critical role of the pineal gland and melatonin. J Biol Rhythms. 2001;16(4):336-47. http://dx.doi.org/10.1177/074873001129002051. PMid:11506379.

Malpaux B, Thiery JC, Chemineau P. Melatonin and the seasonal control of reproduction. Reprod Nutr Dev. 1999;39(3):355-66. http://dx.doi.org/10.1051/rnd:19990308. PMid:10420438.

Martin JE, McKellar S, Klein DC. Melatonin inhibition of the in vivo pituitary response to luteinizing hormone-releasing hormone in the neonatal rat. Neuroendocrinology. 1980;31(1):13-7. http://dx.doi.org/10.1159/000123044. PMid:6993981.

McGuire NL, Kangas K, Bentley GE. Effects of melatonin on peripheral reproductive function: regulation of testicular GnIH and testosterone. Endocrinology. 2011;152(9):3461-70. http://dx.doi.org/10.1210/en.2011-1053. PMid:21771888.

Miera CS, Beymer M, Routledge K, Krol E, Selman C, Hazlerigg DG, Simonneaux V. Photoperiodic regulation in a wild-derived mouse strain. J Exp Biol. 2020;223(Pt 6):jeb217687. PMid:32098881.

Mirhoseini M, Gatabi ZR, Saeedi M, Morteza-Semnani K, Amiri FT, Kelidari HR, Malekshah AAK. Protective effects of melatonin solid lipid nanoparticles on testis histology after testicular trauma in rats. Res Pharm Sci. 2019;14(3):201-8. http://dx.doi.org/10.4103/1735-5362.258486. PMid:31160897.

Mukherjee A, Haldar C. Effect of Naltrexone on photoperiodic regulation of testicular steroidogenesis in adult golden hamster, Mesocricetus auratus. Gen Comp Endocrinol. 2016;239:89-96. http://dx.doi.org/10.1016/j.ygcen.2015.10.001. PMid:26449162.

Olivares AN, Valladares LE, Bustos-Obregón E, Núñez SM. Testicular function of sexually immature rats chronically treated with melatonin. Arch Biol Med Exp. 1989;22(4):387-93. PMid:2488537.

Ono H, Hoshino Y, Yasuo S, Watanabe M, Nakane Y, Murai A, Ebihara S, Korf HW, Yoshimura T. Involvement of thyrotropin in photoperiodic signal transduction in mice. Proc Natl Acad Sci USA. 2008;105(47):18238-42. http://dx.doi.org/10.1073/pnas.0808952105. PMid:19015516.

Otálora BB, Madrid JA, Alvarez N, Vicente V, Rol MA. Effects of exogenous melatonin and circadian synchronization on tumor progression in melanoma-bearing C57BL6 mice. J Pineal Res. 2008;44(3):307-15. http://dx.doi.org/10.1111/j.1600-079X.2007.00531.x. PMid:18339126.

Pitrosky B, Pévet P. The photoperiodic response in Syrian hamsters depends upon a melatonin-driven rhythm of sensitivity to melatonin. Biol Signals. 1997;6(4-6):264-71. http://dx.doi.org/10.1159/000109137. PMid:9500665.

Qin F, Zhang J, Zan L, Guo W, Wang J, Chen L, Cao Y, Shen O, Tong J. Inhibitory effect of melatonin on testosterone synthesis is mediated via GATA-4/SF-1 transcription factors. Reprod Biomed Online. 2015;31(5):638-46. http://dx.doi.org/10.1016/j.rbmo.2015.07.009. PMid:26386639.

Robert KA, Lesku JA, Partecke J, Chambers B. Artificial light at night desynchronizes strictly seasonal reproduction in a wild mammal. Proc Biol Sci. 2015;282(1816):20151745. http://dx.doi.org/10.1098/rspb.2015.1745. PMid:26423847.

Russart KLG, Nelson RJ. Artificial light at night alters behavior in laboratory and wild animals. J Exp Zool A Ecol Integr Physiol. 2018;329(8-9):401-8. http://dx.doi.org/10.1002/jez.2173. PMid:29806740.

Saide M, Ozen SAD, Arzu KA, Suna O, Kazime GA. The protective role of melatonin and curcumin in the testis of young and aged rats. Andrologia. 2019;51(3):e13203. http://dx.doi.org/10.1111/and.13203. PMid:30467869.

Shi L, Li N, Bo L, Xu Z. Melatonin and hypothalamic-pituitary-gonadal axis. Curr Med Chem. 2013;20(15):2017-31. http://dx.doi.org/10.2174/09298673113209990114. PMid:23410151.

Simonneaux V, Ansel L, Revel F, Klosen P, Pévet P, Mikkelsen J. Kisspeptin and the seasonal control of reproduction in hamsters. Peptides. 2009;30(1):146-53. http://dx.doi.org/10.1016/j.peptides.2008.06.006. PMid:18619505.

Sinhasane SV, Joshi BN. Exposure to different spectra of light, continuous light and treatment with melatonin affect reproduction in the Indian desert Gerbil Meriones hurrianae (Jerdon). Biol Signals Recept. 1998;7(3):179-87. http://dx.doi.org/10.1159/000014543. PMid:9672760.

Sogorescu EZS, Anghel A, Nadolu D, Dobrin N. Pattern of testosterone secretion, testicular volume and sperm production after applied the photoperiod treatments on Carpathian bucks. Ann Rom Soc Cell Biol. 2012;17(1):284-91.

Spaliviero JA, Jimenez M, Allan CM, Handelsman DJ. Luteinizing hormone receptor-mediated effects on initiation of spermatogenesis in gonadotropin-deficient (hpg) mice are replicated by testosterone. Biol Reprod. 2004;70(1):32-8. http://dx.doi.org/10.1095/biolreprod.103.019398. PMid:12954730.

Talpur HS, Chandio IB, Brohi RD, Worku T, Rehman Z, Bhattarai D, Ullah F, JiaJia L, Yang L. Research progress on the role of melatonin and its receptors in animal reproduction: a comprehensive review. Reprod Domest Anim. 2018;53(4):831-49. http://dx.doi.org/10.1111/rda.13188. PMid:29663591.

Tan DX, Zheng X, Kong J, Manchester LC, Hardeland R, Kim SJ, Xu X, Reiter RJ. Fundamental issues related to the origin of melatonin and melatonin isomers during evolution: relation to their biological functions. Int J Mol Sci. 2014;15(9):15858-90. http://dx.doi.org/10.3390/ijms150915858. PMid:25207599.

Tian X, Wang F, Zhang L, He C, Ji P, Wang J, Zhang Z, Lv D, Abulizi W, Wang X, Lian Z, Liu G. Beneficial effects of melatonin on the in vitro maturation of sheep oocytes and its relation to melatonin receptors. Int J Mol Sci. 2017;18(4):834. http://dx.doi.org/10.3390/ijms18040834. PMid:28420163.

Touitou Y, Arendt J, Pévet P. Melatonin and the pineal gland: from basic science to clinical application. Psychopharmacology. 1992;106(2):288. http://dx.doi.org/10.1007/BF02801987.

Valenti S, Guido R, Giusti M, Giordano G. In vitro acute and prolonged effects of melatonin on purified rat Leydig cell steroidogenesis and adenosine 3′,5′-monophosphate production. Endocrinology. 1995;136(12):5357-62. http://dx.doi.org/10.1210/endo.136.12.7588282. PMid:7588282.

Vivid D, Bentley GE. Seasonal reproduction in vertebrates: melatonin synthesis, binding, and functionality using Tinbergen’s four questions. Molecules. 2018;23(3):652. PMid:29534047.

Wang X, Guo G, Zhang X, Li M, Xiao K, Hu C, Li X. Effect of RFRP-3, the mammalian ortholog of GnIH, on the epididymis of male rats. Theriogenology. 2018;118:196-202. http://dx.doi.org/10.1016/j.theriogenology.2018.05.029. PMid:29913425.

Yao J, Chiba T, Sakai J, Hirose K, Yamamoto M, Hada A, Kuramoto K, Higuchi K, Mori M. Mouse testis transcriptome revealed using serial analysis of gene expression. Mamm Genome. 2004;15(6):433-51. http://dx.doi.org/10.1007/s00335-004-2347-7. PMid:15181536.

Yu K, Deng SL, Sun TC, Li YY, Liu YX. Melatonin regulates the synthesis of steroid hormones on male reproduction: a review. Molecules. 2018;23(2):447. http://dx.doi.org/10.3390/molecules23020447. PMid:29462985.

Zhang P, Zheng Y, Lv Y, Li F, Su L, Qin Y, Zeng W. Melatonin protects the mouse testis against heat-induced damage. Mol Hum Reprod. 2020;26(2):65-79. http://dx.doi.org/10.1093/molehr/gaaa002. PMid:31943111.
 


Submitted date:
03/23/2022

Accepted date:
08/26/2022

632b035aa953954620243d02 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections