DOI QR코드

DOI QR Code

The effects of sesame oil and different doses of estradiol on testicular structure, sperm parameters, and chromatin integrity in old mice

  • Mohammadzadeh, Masoomeh (Department of Reproductive Biology, Yazd Reproductive Sciences Institute, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences) ;
  • Pourentezari, Majid (Department of Biology and Anatomical Sciences, Shahid Sadoughi University of Medical Sciences) ;
  • Zare-Zardini, Hadi (Hematology and Oncology Research Center, Shahid Sadoughi University of Medical Sciences) ;
  • Nabi, Ali (Department of Reproductive Biology, Yazd Reproductive Sciences Institute, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences) ;
  • Esmailabad, Saeed Ghasemi (Department of Reproductive Biology, Yazd Reproductive Sciences Institute, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences) ;
  • Khodadadian, Ali (Department of Medical Genetics, Faculty of Medicine, Shahid Sadoughi University of Medical Sciences) ;
  • Talebi, Ali Reza (Department of Reproductive Biology, Yazd Reproductive Sciences Institute, Research and Clinical Center for Infertility, Shahid Sadoughi University of Medical Sciences)
  • Received : 2020.01.14
  • Accepted : 2020.04.25
  • Published : 2021.03.31

Abstract

Objective: Studies of the effects of estrogens on the male reproductive system have emphasized the role of these hormones in male fertility. Sesame oil has many phytoestrogenic compounds and may improve male fertility. This study investigated the effects of sesame oil and different concentrations of estrogen on sperm parameters and DNA integrity in male mice. Methods: Twenty old NMRI (The Naval Medical Research Institute) male mice (40 weeks; weight, 30-35 g) were treated with sesame oil or different concentrations of estrogen (estradiol, 1 and 10 μL/kg/day) or received no treatment (controls). After 35 days, sperm parameters and DNA integrity were assessed and analyzed. Results: Sperm count, progressive motility, and morphology were decreased in the group that received 10 μL/kg of estradiol. A remarkably lower percentage of DNA fragmentation and protamine deficiency were detected in the group that received 1 μL/kg of estradiol. In the groups that received sesame oil and 1 μL/kg of estradiol, the numbers of spermatogonia and Leydig cells were higher than in controls. The combination of sesame oil and 1 μL/kg of estradiol led to improved sperm parameters and chromatin and testicular structure. Conclusion: Based on this study, consumption of sesame oil and a low concentration of estradiol may improve testicular function in older mice.

Keywords

Acknowledgement

The authors would like to thank Yazd Reproductive Science Institute for financial support of the current study.

References

  1. Walker WH, Cheng J. FSH and testosterone signaling in Sertoli cells. Reproduction 2005;130:15-28. https://doi.org/10.1530/rep.1.00358
  2. O'Donnell L, Robertson KM, Jones ME, Simpson ER. Estrogen and spermatogenesis. Endocr Rev 2001;22:289-318. https://doi.org/10.1210/er.22.3.289
  3. Leavy M, Trottmann M, Liedl B, Reese S, Stief C, Freitag B, et al. Effects of elevated β-estradiol levels on the functional morphology of the testis: new insights. Sci Rep 2017;7:39931. https://doi.org/10.1038/srep39931
  4. Khaneshi F, Nasrolahi O, Azizi S, Nejati V. Sesame effects on testicular damage in streptozotocin-induced diabetes rats. Avicenna J Phytomed 2013;3:347-55.
  5. Shittu LA, Shittu RK, Olufemi O, Tayo AO, Osunubi AA. Hypoglycaemia and improved testicular parameters in Sesamum radiatum treated normo-glycaemic adult male Sprague Dawley rats. Afr J Biotechnol 2009;8:2878-86.
  6. National Research Council of the National Academies. Guide for the care and use of laboratory animals. Washington: The National Academies Press; 2010.
  7. Almeida S, Rato L, Sousa M, Alves MG, Oliveira PF. Fertility and sperm quality in the aging male. Curr Pharm Des 2017;23:4429-37.
  8. Alshahrani S, Agarwal A, Assidi M, Abuzenadah AM, Durairajanayagam D, Ayaz A, et al. Infertile men older than 40 years are at higher risk of sperm DNA damage. Reprod Biol Endocrinol 2014; 12:103. https://doi.org/10.1186/1477-7827-12-103
  9. Dostalova P, Zatecka E, Dvorakova-Hortova K. Of oestrogens and sperm: areview of the roles of oestrogens and oestrogen receptors in male reproduction. Int J Mol Sci 2017;18:904. https://doi.org/10.3390/ijms18050904
  10. Huang J, Chen L, Wan L, Yang JG, Wang H, Zhou XY, et al. An analysis of donor semen quality in Chongqing Human Sperm Bank. Zhonghua Nan Ke Xue 2018;24:700-4.
  11. Ge ZJ, Schatten H, Zhang CL, Sun QY. Oocyte ageing and epigenetics. Reproduction 2015;149:R103-14. https://doi.org/10.1530/REP-14-0242
  12. Hirakawa I, Miyagawa S, Katsu Y, Kagami Y, Tatarazako N, Kobayashi T, et al. Gene expression profiles in the testis associated with testis-ova in adult Japanese medaka (Oryziaslatipes) exposed to 17α-ethinylestradiol. Chemosphere 2012;87:668-74. https://doi.org/10.1016/j.chemosphere.2011.12.047
  13. Yamada S, Pokutta S, Drees F, Weis WI, Nelson WJ. Deconstructing the cadherin-catenin-actin complex. Cell 2005;123:889-901. https://doi.org/10.1016/j.cell.2005.09.020
  14. Rowlands TM, Symonds JM, Farookhi R, Blaschuk OW. Cadherins: crucial regulators of structure and function in reproductive tissues. Rev Reprod 2000;5:53-61. https://doi.org/10.1530/ror.0.0050053
  15. Purohit S, Brahmaraju M, Palta A, Shukla S, Laloraya M, Kumar PG. Impaired E-cadherin expression in human spermatozoa in a male factor infertility subset signifies E-cadherin-mediated adhesion mechanisms operative in sperm-oolemma interactions. Biochem Biophys Res Commun 2004;316:903-9. https://doi.org/10.1016/j.bbrc.2004.02.133
  16. Tsuchiya B, Sato Y, Kameya T, Okayasu I, Mukai K. Differential expression of N-cadherin and E-cadherin in normal human tissues. Arch Histol Cytol 2006;69:135-45. https://doi.org/10.1679/aohc.69.135
  17. Ha HK, Park HJ, Park NC. Expression of E-cadherin and α-catenin in a varicocele-induced infertility rat model. Asian J Androl 2011; 13:470-5. https://doi.org/10.1038/aja.2010.94
  18. Bandegi L, Anvari M, Vakili M, Khoradmehr A, Mirjalili A, Talebi AR. Effects of antidepressants on parameters, melondiadehyde, and diphenyl-2-picryl-hydrazyl levels in mice spermatozoa. Int J Reprod Biomed 2018;16:365-72. https://doi.org/10.29252/ijrm.16.6.365
  19. Pourmasumi S, Khoradmehr A, Rahiminia T, Sabeti P, Talebi AR, Ghasemzadeh J. Evaluation of sperm chromatin integrity using aniline blue and toluidine blue staining in infertile and normozoospermic men. J Reprod Infertil 2019;20:95-101.
  20. Nazar M, Talebi AR, Hosseini Sharifabad M, Abbasi A, Khoradmehr A, Danafar AH. Acute and chronic effects of gold nanoparticles on sperm parameters and chromatin structure in Mice. Int J Reprod Biomed 2016;14:637-42. https://doi.org/10.29252/ijrm.14.10.637
  21. Costa DS, Paula TA, Matta SL. The intertubular compartment morphometry in capybaras (Hydrochoerus hydrochaeris) testis. Anim Reprod Sci 2006;91:173-9. https://doi.org/10.1016/j.anireprosci.2005.03.013
  22. Stone BA, Alex A, Werlin LB, Marrs RP. Age thresholds for changes in semen parameters in men. Fertil Steril 2013;100:952-8. https://doi.org/10.1016/j.fertnstert.2013.05.046
  23. Kumar N, Singh AK, Choudhari AR. Impact of age on semen parameters in male partners of infertile couples in a rural tertiary care center of central India: a cross-sectional study. Int J Reprod Biomed 2017;15:497-502. https://doi.org/10.29252/ijrm.15.8.497
  24. Levitas E, Lunenfeld E, Weisz N, Friger M, Potashnik G. Relationship between age and semen parameters in men with normal sperm concentration: analysis of 6022 semen samples. Andrologia 2007;39:45-50. https://doi.org/10.1111/j.1439-0272.2007.00761.x
  25. Ryan E, Galvin K, O'Connor TP, Maguire AR, O'Brien NM. Phytosterol, squalene, tocopherol content and fatty acid profile of selected seeds, grains, and legumes. Plant Foods Hum Nutr 2007;62:85-91. https://doi.org/10.1007/s11130-007-0046-8
  26. Khani B, Bidgoli SR, Moattar F, Hassani H. Effect of sesame on sperm quality of infertile men. J Res Med Sci 2013;18:184-7.
  27. Agarwal A, Nallella KP, Allamaneni SS, Said TM. Role of antioxidants in treatment of male infertility: an overview of the literature. Reprod Biomed Online 2004;8:616-27. https://doi.org/10.1016/S1472-6483(10)61641-0
  28. Patel SR, Sigman M. Antioxidant therapy in male infertility. Urol Clin North Am 2008;35:319-30. https://doi.org/10.1016/j.ucl.2008.01.009
  29. Jeng KC, Hou RC. Sesamin and sesamolin: nature's therapeutic lignans. Curr Enzym Inhib 2005;1:11-20. https://doi.org/10.2174/1573408052952748
  30. Abbasi Z, Tabatabaei SR, Mazaheri Y, Barati F, Morovvati H. Effects of sesame oil on the reproductive parameters of diabetes mellitus-induced male rats. World J Mens Health 2013;31:141-9. https://doi.org/10.5534/wjmh.2013.31.2.141
  31. Lubbert H, Leo-Rossberg I, Hammerstein J. Effects of ethinyl estradiol on semen quality and various hormonal parameters in a eugonadal male. Fertil Steril 1992;58:603-8. https://doi.org/10.1016/S0015-0282(16)55271-6
  32. Patrao MT, Silva EJ, Avellar MC. Androgens and the male reproductive tract: an overview of classical roles and current perspectives. Arq Bras Endocrinol Metabol 2009;53:934-45. https://doi.org/10.1590/S0004-27302009000800006
  33. Belloc S, Hazout A, Zini A, Merviel P, Cabry R, Chahine H, et al. How to overcome male infertility after 40: influence of paternal age on fertility. Maturitas 2014;78:22-9. https://doi.org/10.1016/j.maturitas.2014.02.011
  34. Mirzazadeh M, Sadri-Ardekani H. Implications of ejaculatory sperm DNA fragmentation on male infertility management. Transl Androl Urol 2017;6(Suppl 4):S402-4. https://doi.org/10.21037/tau.2017.03.40
  35. Cho CL, Agarwal A. Role of sperm DNA fragmentation in male factor infertility: a systematic review. Arab J Urol 2017;16:21-34. https://doi.org/10.1016/j.aju.2017.11.002
  36. Ebrahimi M, Dehghani F, Farhadian N, Karimi M, Golmohammadzadeh S. Investigating the anti-apoptotic effect of sesame oil and honey in a novel nanostructure form for treatment of heart failure. Nanomed J 2017;4:245-53.
  37. Bianchi PG, Manicardi GC, Urner F, Campana A, Sakkas D. Chromatin packaging and morphology in ejaculated human spermatozoa: evidence of hidden anomalies in normal spermatozoa. Mol Hum Reprod 1996;2:139-44. https://doi.org/10.1093/molehr/2.3.139
  38. Balhorn R, Reed S, Tanphaichitr N. Aberrant protamine 1/protamine 2 ratios in sperm of infertile human males. Experientia 1988;44:52-5. https://doi.org/10.1007/BF01960243
  39. Bianchi PG, Manicardi GC, Bizzaro D, Bianchi U, Sakkas D. Effect of deoxyribonucleic acid protamination on fluorochrome staining and in situ nick-translation of murine and human mature spermatozoa. Biol Reprod 1993;49:1083-8. https://doi.org/10.1095/biolreprod49.5.1083
  40. Iranpour FG. The effects of protamine deficiency on ultrastructure of human sperm nucleus. Adv Biomed Res 2014;3:24. https://doi.org/10.4103/2277-9175.124666
  41. Weider K, Bergmann M, Brehm R. Connexin 43: its regulatory role in testicular junction dynamics and spermatogenesis. Histol Histopathol 2011;26:1343-52.
  42. Toyama Y, Hosoi I, Ichikawa S, Maruoka M, Yashiro E, Ito H, et al. Beta-estradiol 3-benzoate affects spermatogenesis in the adult mouse. Mol Cell Endocrinol 2001;178:161-8. https://doi.org/10.1016/S0303-7207(01)00419-1
  43. Nakamura N, Sloper DT, Del Valle PL. Evaluation of an in vitro mouse testis organ culture system for assessing male reproductive toxicity. Birth Defects Res 2019;111:70-7 https://doi.org/10.1002/bdr2.1431
  44. Senarat S, Kettratad J, Jiraungkoorskul W, Plumley FG, Tongmit K, Poolprasert P, et al. Identification of sbGnRH-GTHs system and estrogen receptor α (ER α) immunoreactivities in the mature testicular tissue in Rastrelliger brachysoma (Bleeker, 1851). Eurasia J Biosci 2018;12:385-92.
  45. Pentikainen V, Erkkila K, Suomalainen L, Parvinen M, Dunkel L. Estradiol acts as a germ cell survival factor in the human testis in vitro. J Clin Endocrinol Metab 2000;85:2057-67. https://doi.org/10.1210/jc.85.5.2057
  46. Lambard S, Carreau S. Aromatase and oestrogens in human male germ cells. Int J Androl 2005;28:254-9. https://doi.org/10.1111/j.1365-2605.2005.00546.x
  47. MacCalman CD, Getsios S, Farookhi R, Blaschuk OW. Estrogens potentiate the stimulatory effects of follicle-stimulating hormone on N-cadherin messenger ribonucleic acid levels in cultured mouse Sertoli cells. Endocrinology 1997;138:41-8. https://doi.org/10.1210/endo.138.1.4831
  48. Dorrington JH, Bendell JJ, Khan SA. Interactions between FSH, estradiol-17 beta and transforming growth factor-beta regulate growth and differentiation in the rat gonad. J Steroid Biochem Mol Biol 1993;44:441-7. https://doi.org/10.1016/0960-0760(93)90248-U
  49. Lucas TF, Lazari MF, Porto CS. Differential role of the estrogen receptors ESR1 and ESR2 on the regulation of proteins involved with proliferation and differentiation of Sertoli cells from 15-day-old rats. Mol Cell Endocrinol 2014;382:84-96. https://doi.org/10.1016/j.mce.2013.09.015
  50. Royer C, Lucas TF, Lazari MF, Porto CS. 17Beta-estradiol signaling and regulation of proliferation and apoptosis of rat Sertoli cells. Biol Reprod 2012;86:108.
  51. Sperling MA. Pediatric endocrinolog. Amsterdam: Elsevier Health Sciences; 2014.
  52. Shittu LA, Shittu RK, Osinubi AA, Ashiru OA. Stereological evidences of epithelial hypoplasia of Seminiferous tubules induced by mesterolone in adult Sprague-Dawley rats. Afr J Endocrinol Metab 2008;7:14-7.
  53. Oluyemi KA, Jimoh OR, Adesanya OA, Omotuyi IO, Josiah SJ, Oyesola TO. Effects of crude ethanolic extract of Garcinia cambogia on the reproductive system of male wistar rats (Rattus novergicus). Afr J Biotechnol 2007;6:1236-8.