Abstract
For animals that breed seasonally, photoperiod is a key factor in controlling their behavior. Epididymal function is highly dependent on androgen. However, the effects of photoperiod on epididymal function and the regulatory mechanism of androgen in this process have not yet been reported. This study examined the effects of different photoperiods on androgen contents and the expression patterns of 5α-reductase, AR, and GPx-5 in the epididymis of Cricetulus barabensis to explore the role of androgens in photoperiod regulation of epididymal function and its mechanism in antioxidant stress. The results showed that in the caput epididymis, androgen content decreased with the shortening of light time, and the mRNA and protein levels of 5α-reductase 1 and androgen receptor (AR) in the long photoperiod (LP) group were significantly higher than those in the short photoperiod (SP) group. In the cauda epididymis, androgen content and the mRNA and protein level of GPx-5 were the lowest in the medium photoperiod (MP) group. In conclusion, these results suggest that androgens affected by the photoperiod may regulate the expression of GPx-5 through the androgen/AR pathway. The findings of this study will help to understand the physiological and biochemical status of the epididymis of seasonally breeding animals under different photoperiods.
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REFERENCES
Aitken, R.J., Harkiss, D., Knox, W., Paterson, M., and Irvine, D.S., A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation, J. Cell Sci., 1998, vol. 111, part 5, pp. 645–656.
Belleannée, C., Labas, V., Teixeira-Gomes, A.P., Gatti, J.L., Dacheux, J.L., and Dacheux, F., Identification of luminal and secreted proteins in bull epididymis, J. Proteomics, 2011, vol. 74, no. 1, pp. 59–78.
Belleannee, C., Legare, C., Calvo, E., Thimon, V., and Sullivan, R., microRNA signature is altered in both human epididymis and seminal microvesicles following vasectomy, Hum. Reprod., 2013, vol. 28, no. 6, pp. 1455–1467.
Berman, D.M., and Russell, D.W., Cell-type-specific expression of rat steroid 5 alpha-reductase isozymes, Proc. Natl. Acad. Sci. U. S. A., 1993, vol. 90, no. 20, pp. 9359–9363.
Bernard, R., Shayesta, S., Mahsa, H., and Sophie-Anne, L., Androgenic regulation of novel genes in the epididymis, Asian J. Androl., 2007, vol. 9, no. 4, pp. 545–553.
Breton, S., Ruan, Y.C., Park, Y.J., and Kim, B., Regulation of epithelial function, differentiation, and remodeling in the epididymis, Asian J. Androl., 2016, vol. 18, no. 1, pp. 3–9.
Brigelius-Flohe, R. and Maiorino, M., Glutathione peroxidases, Biochim. Biophys. Acta, Gen. Subj., 2013, vol. 1830, no. 5, pp. 3289–3303.
Burnstein, K.L., Maiorino, C.A., Dai, J.L., and Cameron, D.J., Androgen and glucocorticoid regulation of androgen receptor cDNA expression, Mol. Cell. Endocrinol., 1995, vol. 115, no. 2, pp. 177–186.
Chabory, E., Damon, C., Lenoir, A., Kauselmann, G., Kern, H., Zevnik, B., et al., Epididymis seleno-independent glutathione peroxidase 5 maintains sperm DNA integrity in mice, J. Clin. Invest., 2009, vol. 119, no. 7, pp. 2074–2085.
Chabory, E., Damon, C., Lenoir, A., Henry-Berger, J., Vernet, P., Cadet, R., et al., Mammalian glutathione peroxidases control acquisition and maintenance of spermatozoa integrity, J. Anim. Sci., 2010, vol. 88, no. 4, pp. 1321–1331.
Charles, R.G., Robinson, F.E., Hardin, R.T., Yu, M.W., Feddes, J., and Classen, H.L., Growth, body composition, and plasma androgen concentration of male broiler chickens subjected to different regimens of photoperiod and light intensity, Poultry Sci., 1992, vol. 71, no. 10, pp. 1595–1605.
Chauvin, T.R., Androgen-regulated genes in the murine epididymis, Biol. Reprod., 2004, vol. 71, no. 2, pp. 560–569.
Cooke, B.M., Hegstrom, C.D., and Breedlove, S.M., Photoperiod-dependent response to androgen in the medial amygdala of the Siberian hamster, Phodopus sungorus, J. Biol. Rhythms, 2002, vol. 17, no. 2, pp. 147–154.
Corbin, C.J., Legacki, E., Ball, B., Scoggin, K., and Conley, A.J., Equine 5α-reductase activity and expression in epididymis, J. Endocrinol., 2017, vol. 231, no. 1, pp. 23–33.
Cornwall, G.A., New insights into epididymal biology and function, Hum. Reprod. Update, 2009, vol. 15, no. 2, pp. 213–227.
Dai, J.L., Maiorino, C.A., Gkonos, P.J., and Burnstein, K.L., Androgenic up-regulation of androgen receptor cDNA expression in androgen-independent prostate cancer cells, Steroids, 1996, vol. 61, no. 9, pp. 531–539.
Dehm, S.M. and Tindall, D.J., Regulation of androgen receptor signaling in prostate cancer, Expert Rev. Anticancer Ther., 2005, vol. 5, no. 1, pp. 63–74.
Drevet, J.R., The antioxidant glutathione peroxidase family and spermatozoa: a complex story, Mol. Cell. Endocrinol., 2006, vol. 250, nos. 1–2, pp. 70–79.
El Allali, K., Sghiri, A., Bouaouda, H., Achaaban, M.R., Ouzir, M., Bothorel, B., et al., Effect of melatonin implants during the non-breeding season on the onset of ovarian activity and the plasma prolactin in dromedary camel, Front. Vet. Sci., 2018, vol. 5, p. 44.
Frungieri, M.B., Gonzalez-Calvar, S.I., Bartke, A., and Calandra, R.S., Influence of age and photoperiod on steroidogenic function of the testis in the golden hamster, Int. J. Androl., 1999, vol. 22, no. 4, pp. 243–252.
Ghyselinck, N.B., Dufaure, I., Lareyre, J.J., Rigaudiere, N., Mattei, M.G., and Dufaure, J.P., Structural organization and regulation of the gene for the androgen-dependent glutathione peroxidase-like protein specific to the mouse epididymis, Mol. Endocrinol. (Baltimore, Md.), 1993, vol. 7, no. 2, pp. 258–272.
Goncalves-de-Freitas, E., Carvalho, T.B., and Oliveira, R.F., Photoperiod modulation of aggressive behavior is independent of androgens in a tropical cichlid fish, Gen. Comp. Endocrinol., 2014, vol. 207, pp. 41–49.
González-Cadavid, N.F., Vernet, D., Navarro, A.F., Rodiguez, J., Swerdloff, R.S., and Rajfer, J., Up-regulation of the levels of androgen receptor and its mRNA by androgens in smooth-muscle cells from rat penis, Mol. Cell. Endocrinol., 1993, vol. 90, no. 2, pp. 219–229.
Griffiths, K., Eaton, C.L., Harper, M.E., Peeling, B., and Davies, P., Steroid hormones and the pathogenesis of benign prostatic hyperplasia, Eur. Urol., 1991, vol. 20, suppl. 1, no. 1, pp. 68–77.
Hegstrom, C.D., Jordan, C.L., and Breedlove, S.M., Photoperiod and androgens act independently to induce spinal nucleus of the bulbocavernosus neuromuscular plasticity in the Siberian hamster, Phodopus sungorus, J. Neuroendocrinol., 2002, vol. 14, no. 5, pp. 368–374.
James, E.R., Carrell, D.T., Aston, K.I., Jenkins, T.G., Yeste, M., and Salas-Huetos, A., The role of the epididymis and the contribution of epididymosomes to mammalian reproduction, Int. J. Mol. Sci., 2020, vol. 21, no. 15, p. 5377.
Koziorowska-Gilun, M., Koziorowski, M., StrzeEk, J., and Fraser, L., Seasonal changes in antioxidant defence systems in seminal plasma and fluids of the boar reproductive tract, Reprod. Biol., 2011, vol. 11, no. 1, pp. 37–47.
Kuenzel, W.J., Kang, S.W., and Zhou, Z.J., Exploring avian deep-brain photoreceptors and their role in activating the neuroendocrine regulation of gonadal development, Poultry Sci., 2015, vol. 94, no. 4, pp. 786–798.
Lee, D.K. and Chang, C., Endocrine mechanisms of disease: expression and degradation of androgen receptor: mechanism and clinical implication, J. Clin. Endocrinol. Metab., 2003, vol. 88, no. 9, pp. 4043–4054.
Lefranois, A.M., Jimenez, C., and Dufaure, J.P., Developmental expression and androgen regulation of 24 kDa secretory proteins by the murine epididymis, Int. J. Androl., 1993, vol. 16, no. 2, pp. 147–154.
Li, S.N., Xue, H.L., Zhang, Q., Xu, J.H., Wang, S., Chen, L., et al., Photoperiod regulates the differential expression of KiSS-1 and GPR54 in various tissues and sexes of striped hamster, Genet. Mol. Res., 2015a, vol. 14, no. 4, pp. 13894–13905.
Li, R.-I., Zhang, T., Fan, X.-m., Yang, X.-q.O., Zhang, C.-q., Cao, J.-w., et al., Study on expression of glutathione peroxidase type-5 (GPX5) and protein localization in epididymis of adult sheep, Sci. Agric. Sin., 2015b, vol. 48, no. 24, pp. 4989–4995.
Liu, C., Jiang, X.P., Liu, G.Q., Wassie, T., and Girmay, S., An ancient mutation in the TPH1 gene is consistent with the changes in mammalian reproductive rhythm, Int. J. Mol. Sci., 2019a, vol. 20, no. 23, p. 6065.
Liu, Q., Yu, W., Fan, S., Zhuang, H., and Weng, Q., Seasonal expressions of androgen receptor, estrogen receptors, 5α-reductases and P450arom in the epididymis of the male muskrat (Ondatra zibethicus), J. Steroid Biochem. Mol. Biol., 2019b, vol. 194, p. 105433.
Mahony, M.C., Swanlund, D.J., Billeter, M., Roberts, K.P., and Pryor, J.L., Regional distribution of 5α-reductase type 1 and type 2 mRNA along the human epididymis, Fertil. Steril., 1998, vol. 69, no. 6, p. 1116.
Mele, E., D’Auria, R., Scafuro, M., Marino, M., Fasano, S., Viggiano, A., et al., Differential expression of kisspeptin system and kisspeptin receptor trafficking during spermatozoa transit in the epididymis, Genes, 2022, vol. 13, no. 2, p. 295.
Morielli, T. and O’Flaherty, C., Oxidative stress impairs function and increases redox protein modifications in human spermatozoa, Reproduction, 2015, vol. 149, no. 1, pp. 113–123.
Mou, J.J., Xu, J.H., Wang, Z., Wang, C.L., Yang, X.Q., Wang, X.C., et al., Effects of photoperiod on morphology and function in testis and epididymis of Cricetulus barabensis, J. Cell. Physiol., 2021, vol. 236, no. 3, pp. 2109–2125.
O’Flaherty, C., Orchestrating the antioxidant defenses in the epididymis, Andrology, 2019, vol. 7, no. 5, pp. 662–668.
Pujol, A. and Bayard, F., Androgen receptors in the rat epididymis and their hormonal control, J. Reprod. Fertil., 1979, vol. 56, no. 1, p. 217.
Rejraji, H., Vernet, P., and Drevet, J.R., GPX5 is present in the mouse caput and cauda epididymidis lumen at three different locations, Mol. Reprod. Dev., 2002, vol. 63, no. 1, pp. 96–103.
Rigaudière, N., Ghyselinck, N.B., Faure, J., and Dufaure, J.P., Regulation of the epididymal glutathione peroxidase-like protein in the mouse: dependence upon androgens and testicular factors, Mol. Cell. Endocrinol., 1992, vol. 89, nos. 1–2, pp. 67–77.
Robaire, B. and Viger, R.S., Regulation of epididymal epithelial cell functions, Biol. Reprod., 1995, vol. 52, no. 2, pp. 226–236.
Robaire, B., Hinton, B.T., and Orgebin-Crist, M.C., The epididymis, in Knobil and Neill’s Physiology of Reproduction, 2006, vol. 1, 3rd ed., pp. 1071–1148.
Rył, A., Rotter, I., Grzywacz, A., et al., Molecular analysis of the SRD5A1 and SRD5A2 genes in patients with benign prostatic hyperplasia with regard to metabolic parameters and selected hormone levels, Int. J. Environ. Res. Public Health, 2017, vol. 14, no. 11, p. 1318.
Shan, L.X., Rodriguez, M.C., and Jänne, O., Regulation of androgen receptor protein and mRNA concentrations by androgens in rat ventral prostate and seminal vesicles and in human hepatoma cells, Mol. Endocrinol., 1990, vol. 4, no. 11, pp. 1636–1646.
Shoemaker, M.B. and Heideman, P.D., Reduced body mass, food intake, and testis size in response to short photoperiod in adult F344 rats, BMC Physiol., 2002, vol. 2, p. 11.
Silva, E.J.R., Queiroz, D.B.C., Honda, L., and Avellar, M.C.W., Glucocorticoid receptor in the rat epididymis: expression, cellmmular distribution and regulation by steroid hormones, Mol. Cell. Endocrinol., 2010, vol. 325, nos. 1–2, pp. 64–77.
Vernet, P., Rigaudire, N., Ghyselinck, N., et al., In vitro expression of a mouse tissue specific glutathione-peroxidase-like protein lacking the selenocysteine can protect stably transfected mammalian cells against oxidative damage, Biochem. Cell Biol., 1996, vol. 74, no. 1, pp. 125–131.
Vernet, P., Faure, J., Dufaure, J.P., and Drevet, J.R., Tissue and developmental distribution, dependence upon testicular factors and attachment to spermatozoa of GPX5, a murine epididymis-specific glutathione peroxidase, Mol. Reprod. Dev., 1997, vol. 47, no. 1, pp. 87–98.
Viger, R.S. and Robaire, B., The mRNAs for the steroid 5 alpha-reductase isozymes, types 1 and 2, are differentially regulated in the rat epididymis, J. Androl., 1996, vol. 17, no. 1, pp. 27–34.
Wang, J., Liu, Q., Qi, H., Wang, Y., Gao, Q., Gao, F., et al., Seasonal expressions of androgen receptor, P450arom and estrogen receptors in the epididymis of the wild ground squirrel (Citellus dauricus Brandt), Gen. Comp. Endocrinol., 2019, vol. 270, pp. 131–138.
Wang, C.L., Wang, Z., Mou, J.J., Wang, S., Zhao, X.Y., Feng, Y.Z., et al., Short photoperiod reduces oxidative stress by up-regulating the Nrf2-Keap1 signaling pathway in hamster kidneys, J. Evol. Biochem. Physiol., 2022, vol. 58, no. 2, pp. 418–429.
Xu, L.X., Xue, H.L., Li, S.N., Xu, J.H., and Chen, L., Seasonal differential expression of KiSS-1/GPR54 in the striped hamsters (Cricetulus barabensis) among different tissues, Integr. Zool., 2017, vol. 12, no. 3, pp. 260–268.
Yamashita, S., Localization of estrogen and androgen receptors in male reproductive tissues of mice and rats, Anat. Rec., Part A, 2004, vol. 279, no. 2, pp. 768–778.
Yu, W.Y., Zhang, Z.W., Liu, P., Yang, X.Y., Zhang, H.L., Yuan, Z.R., et al., Seasonal expressions of SPAG11A and androgen receptor in the epididymis of the wild ground squirrels (Spermophilus dauricus Brandt), Eur. J. Histochem., 2020, vol. 64, no. 2, pp. 120–128.
Zduńczyk, S., Janowski, T., Raś, A., and Barański, W., Activity of steroid sulphatase and estrogen sulphotransferase in the boar epididymis during the postpubertal period, Reprod. Biol., 2012, vol. 12, no. 4, pp. 374–378.
Zhang, T., Localization of plasminogen activator and inhibitor, LH and androgen receptors and inhibin subunits in monkey epididymis, Mol. Hum. Reprod., 1997, vol. 3, no. 11, pp. 945–952.
Zhao, X.Y., Wang, S., Xu, J.H., Wang, C.L., Feng, Y.Z., Xue, H.L., et al., Effects of short daylight and mild low temperature on mitochondrial degeneration in the testis of Cricetulus barabensis, Mol. Reprod. Dev., 2022, vol. 89, no. 9, pp. 413–422.
Zheng, W.M., Zhang, Y., Sun, C.Y., Ge, S.Y., Tan, Y.F., Shen, H.L., et al., A multi-omics study of human testis and epididymis, Molecules, 2021, vol. 26, no. 11, p. 3345.
Zhou, Z.X., Wong, C.I., Sar, M., and Wilson, E.M., The androgen receptor: an overview, Recent Prog. Horm. Res., 1994, vol. 49, no. 1, pp. 249–274.
ACKNOWLEDGMENTS
We thank Dr. Wang Zhe for his guidance and help in the experiment.
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This study was supported by the National Natural Science Foundation of China (nos. 32072436, 31770455, 31972283, 31800308).
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Yongzhen Feng and Shuo Wang contributed equally to this work.
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Statement on the welfare of animals. The animal study was reviewed and approved by the Biomedical Ethics Committee of Qufu Normal University (Permit no. dwsc2022060). All procedures followed the Laboratory Animal Guidelines for the Ethical Review of Animal Welfare (GB/T 35892-2018) This article does not contain any studies with human participants performed by any of the authors.
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Yongzhen Feng, Wang, S., Wang, X. et al. Photoperiod Regulates the Expression of GPx-5 in the Epididymis of Cricetulus barabensis through Androgen. Biol Bull Russ Acad Sci 50, 1316–1326 (2023). https://doi.org/10.1134/S1062359023602872
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DOI: https://doi.org/10.1134/S1062359023602872