Protective effects of selenium on electromagnetic field-induced apoptosis, aromatase P450 activity, and leptin receptor expression in rat testis

Document Type : Original Article

Authors

1 Department of Anatomy and Cell Biology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

2 Department of Biology and Anatomical Sciences, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, Iran

3 Applied Biomedical Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

Abstract

Objective(s): Electromagnetic field (EMF) emitted by mobiles may affect the male reproductive system. Selenium, as an antioxidant, may protect against electromagnetic field-induced tissue damage. Theis study aimed to investigate the effects of selenium on rat testis exposed to electromagnetic fields.
Materials and Methods: Twenty-four male Wistar rats were divided into four groups, namely EM group (2100 MHZ), EM/SE group (2100 MHZ + selenium (0.2 mg/kg), SE group (selenium 0.2 mg/kg), CONT (control group). Serum LH, FSH, testosterone, leptin and aromatase levels, testis weight and volume index, sperm parameters (count and abnormal percent), seminiferous tubule diam‌eters, germinal epithelia thickness, immunoreactivity of leptin receptor and caspase-3 (for apoptotic cells in germinal epithelium) were investigated.
Results: Our results showed that serum LH, FSH, GnRH, testosterone level, sperm count, germinal epithelium thickness, and seminiferous tubule diameter were significantly declined in the EM group compared with the CONT group (p <0.05). However, in the EM group, the serum leptin level, sperm abnormality, aromatase enzyme level, apoptotic cells, and leptin receptor were increased compared with the CONT group (p <0.05). Furthermore, an increase in sperm count, germinal epithelium thickness, seminiferous diameters, serum LH, FSH, and GnRH, and testosterone levels, and a significant decrease in sperm abnormality, leptin receptor and apoptotic cells in the EM/SE group compared with the EM group were also observed (p <0.05).
Conclusion: This study showed that electromagnetic radiation may have detrimental impacts on the male reproductive system, which can be prevented by use of selenium.

Keywords


1. Singh T, Devi R, Kumar A, Jambagi SS, Singh B. Transmission of Electromagnetic Radiations from Mobile Phones: A Critical Analysis.  Smart Inno. Commu. Comput Sci Springer; 2019. p. 229-238.
2. Sharma AB, Lamba O. A review: source and effect of mobile communication radiation on human health. Adv Wirel Mob Commu 2017;10:423-435.
3. Ye W, Wang F, Zhang W, Fang N, Zhao W, Wang J. Effect of mobile phone radiation on cardiovascular development of chick embryo. Anatomia, histologia, embryologia. 2016;45:197-208.
4. Aydin B, Akar A. Effects of a 900-MHz electromagnetic field on oxidative stress parameters in rat lymphoid organs, polymorphonuclear leukocytes and plasma. Arch Med Res 2011;42:261-267.
5. Asl JF, Larijani B, Zakerkish M, Rahim F, Shirbandi K, Akbari R. The possible global hazard of cell phone radiation on thyroid cells and hormones: a systematic review of evidences. Environ. Sci Pollut Res 2019:1-15.
6. Nazıroğlu M, Yüksel M, Köse SA, Özkaya MO. Recent reports of Wi-Fi and mobile phone-induced radiation on oxidative stress and reproductive signaling pathways in females and males. Membr Biol 2013;246:869-875.
7. Hardell L, Carlberg M, Söderqvist F, Mild KH. Case-control study of the association between malignant brain tumours diagnosed between 2007 and 2009 and mobile and cordless phone use. Int J Oncol 2013;43:1833-1845.
8. Bin-Meferij MM, El-Kott AF. The radioprotective effects of Moringa oleifera against mobile phone electromagnetic radiation-induced infertility in rats. Int J Cli Exp Med 2015;8:12487-12497.
9. Salama N, Kishimoto T, Kanayama Ho. Retracted: Effects of exposure to a mobile phone on testicular function and structure in adult rabbit. Int J Androl 2010;33:88-94.
10. Gautam R, Singh KV, Nirala J, Murmu NN, Meena R, Rajamani P. Oxidative stress‐mediated alterations on sperm parameters in male Wistar rats exposed to 3G mobile phone radiation. Andrologia 2019;51:e13201.
11. Kesari KK, Behari J. Evidence for mobile phone radiation exposure effects on reproductive pattern of male rats: role of ROS. Elect Bio Med 2012;31:213-222.
12. Foresta C, Flohé L, Garolla A, Roveri A, Ursini F, Maiorino M. Male fertility is linked to the selenoprotein phospholipid hydroperoxide glutathione peroxidase. Bio Reprod 2002;67:967-971.
13. Biller-Takahashi JD, Takahashi LS, Mingatto FE, Urbinati EC. The immune system is limited by oxidative stress: dietary selenium promotes optimal antioxidative status and greatest immune defense in pacu Piaractus mesopotamicus. Fish Shellfish Immunol. 2015;47:360-367.
14. Rayman MP, Duntas LH. Selenium deficiency and thyroid disease.  The Thyroid and Its Diseases: Springer; 2019. p. 109-126.
15. Rayman MP. Is Adequate Selenium Important for Healthy Human Pregnancy?  Selenium: Springer; 2016. p. 353-364.
16. Watanabe LM, Júnior FB, Jordão AA, Navarro AM. Influence of HIV infection and the use of antiretroviral therapy on selenium and selenomethionine concentrations and antioxidant protection. Nutrition 2016;32:1238-1242.
17. de Oliveira Nascimento RGB, Hessel G, Cozzolino SMF, Vasques ACJ, de Sousa Almondes KG, Pimentel JAC, et al. Inflammatory process of patients receiving parenteral nutrition is not exclusively responsible for low selenium and glutathione peroxidase levels. Nutrition 2019;61:202-207.
18. Jamilian M, Razavi M, Fakhrie Kashan Z, Ghandi Y, Bagherian T, Asemi Z. Metabolic response to selenium supplementation in women with polycystic ovary syndrome: A randomized, double‐blind, placebo‐controlled trial. Clin. Endocrinol 2015;82:885-891.
19. Adegoke E, Wang X, Wang H, Wang C, Zhang H, Zhang G. Selenium (Na 2 SeO 3) upregulates expression of immune genes and blood–testis barrier constituent proteins of bovine sertoli cell in vitro. Biol Trace Elem Res 2018;185:332-343.
20. Shi L, Song R, Yao X, Ren Y. Effects of selenium on the proliferation, apoptosis and testosterone production of sheep Leydig cells. Theriogenol 2017;93:24-32.
21. Masuzaki H, Ogawa Y, Isse N, Satoh N, Okazaki T, Shigemoto M, et al. Human obese gene expression: adipocyte-specific expression and regional differences in the adipose tissue. Diabetes 1995;44:855-858.
22. Chavarro JE, Toth TL, Wright DL, Meeker JD, Hauser R. Body mass index in relation to semen quality, sperm DNA integrity, and serum reproductive hormone levels among men attending an infertility clinic. Fertil Steril 2010;93:2222-2231.
23. Hofny ER, Ali ME, Abdel-Hafez HZ, Kamal EE-D, Mohamed EE, El-Azeem HGA, et al. Semen parameters and hormonal profile in obese fertile and infertile males. Fertil Steril 2010;94:581-584.
24. Tena-Sempere M, Barreiro M. Leptin in male reproduction: the testis paradigm. Mol Cell Endocrinol 2002;188:9-13.
25. Carreau S, Delalande C, Silandre D, Bourguiba S, Lambard S. Aromatase and estrogen receptors in male reproduction. Mol. Cell. Endocrinol 2006;246:65-68.
26. O’donnell L, Robertson KM, Jones ME, Simpson ER. Estrogen and spermatogenesis. Endocr Rev 2001;22:289-318.
27. Durgun M, Dasdag S, Erbatur S, Yegin K, Durgun SO, Uzun C, et al. Effect of 2100 MHz mobile phone radiation on healing of mandibular fractures: an experimental study in rabbits. Biotechnol. Biotechnol Equip 2016;30:112-120.
28. Schwarz K. Essentiality and metabolic functions of selenium. Med. Clin. North Am. 1976;60:745-758.
29. Sehitoglu I, Tumkaya L, Kalkan Y, Bedir R, Cure MC, Zorba OU, et al. Biochemical and histopathological effects on the rat testis after exposure to electromagnetic field during fetal period. Arch Esp Urol 2015;68:562-568.
30. Jalilvand N, Hosseini M, Beheshti F, Ebrahimzadeh-Bideskan A. Protective effect of PPARγ agonist pioglitazone, on testicular tissue and sperm parameters in hypothyroid rats. Toxin Rev 2019:1-10.
31. Haeri P, Mohammadipour A, Heidari Z, Ebrahimzadeh-bideskan A. Neuroprotective effect of crocin on substantia nigra in MPTP-induced Parkinson’s disease model of mice. Anat Sci Int 2019;94:119-127.
32. Mobaraki F, Seghatoleslam M, Fazel A, Ebrahimzadeh-Bideskan A. Effects of MDMA (ecstasy) on apoptosis and heat shock protein (HSP70) expression in adult rat testis. Toxicol Mech Methods 2018;28:219-229.
33. Mohammadi S, Jalali M, Nikravesh MR, Fazel A, Ebrahimzadeh A, Gholamin M, et al. Effects of Vitamin-E treatment on CatSper genes expression and sperm quality in the testis of the aging mouse. Iran J Reprod Med 2013;11:989-1000.
34. Bakhtiary Z, Shahrooz R, Ahmadi A, Zarei L, Editors. Evaluation of antioxidant effects of crocin on sperm quality in cyclophosphamide treated adult mice. Veterinary research forum: a. Int Quar J; 2014: Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.
35. Darbandi M, Darbandi S, Agarwal A, Sengupta P, Durairajanayagam D, Henkel R, et al. Reactive oxygen species and male reproductive hormones. Reprod Bio Endocrinol 2018;16:1-14.
36. Kaur M, Khera K. impact of cell phone radiations on pituitary gland and biochemical parameters in albino rat. Octa J Biosci 2018;6.
37. Al‐Akhras MdA, Darmani H, Elbetieha A. Influence of 50 Hz magnetic field on sex hormones and other fertility parameters of adult male rats. Bioelectromagnetics: J.  Bioelect. Soci,  Soci. Physical Regul.  Biol Med European Bioelect Assoc 2006;27:127-131.
38. Lukusa K, Lehloenya K. Selenium supplementation improves testicular characteristics and semen quality of Saanen bucks. Small Rumin 2017;151:52-58.
39. Malik IA, Durairajanayagam D, Singh HJ. Leptin and its actions on reproduction in males. Asian J. Androl. 2019;21:296.
40. Zhang J, Gong M. Review of the role of leptin in the regulation of male reproductive function. Andrologia 2018;50:e12965.
41. Ahn SY, Yang SW, Lee HJ, Byun JS, Om JY, Shin CH. Excess of leptin inhibits hypothalamic KiSS-1 expression in pubertal mice. Korean J Pediatr 2012;55:337-343.
42. Mahdavi SM, Sahraei H, Yaghmaei P, Tavakoli H. Effects of electromagnetic radiation exposure on stress-related behaviors and stress hormones in male wistar rats. Biomol Ther 2014;22:570-576.
43. Wabitsch M, Jensen PB, Blum WF, Christoffersen CT, Englaro P, Heinze E, et al. Insulin and cortisol promote leptin production in cultured human fat cells. Diabetes 1996;45:1435-1438.
44. Kim CY, Kim G-N, Wiacek JL, Chen C-Y, Kim K-H. Selenate inhibits adipogenesis through induction of transforming growth factor-β1 (TGF-β1) signaling. Biochem. Biophys Res Commun 2012;426:551-557.
45. Ishikawa T, Fujioka H, Ishimura T, Takenaka A, Fujisawa M. Expression of leptin and leptin receptor in the testis of fertile and infertile patients. Andrologia 2007;39:22-27.
46. Carreau S, Genissel C, Bilinska B, Levallet J. Sources of oestrogen in the testis and reproductive tract of the male. Int J Androl 1999;22:211-223.
47. D’Souza R, Gill-Sharma MK, Pathak S, Kedia N, Kumar R, Balasinor N. Effect of high intratesticular estrogen on the seminiferous epithelium in adult male rats. Mol Cell Endocrinol 2005;241:41-48.
48. Tunc O, Bakos H, Tremellen K. Impact of body mass index on seminal oxidative stress. Andrologia 2011;43:121-128.
49. Zhang Y, Zhou Y, Tang Q, Hu F, Feng L, Shen J, et al. The protective effects of selenium-enriched spirulina on the reproductive system of male zebrafish (Danio rerio) exposed to beta-cypermethrin. Food Funct 2018;9:5791-5804.
50. Chen YB, Li J, Liu JY, Zeng LH, Wan Y, Li YR, et al. Effect of Electromagnetic Pulses (EMP) on associative learning in mice and a preliminary study of mechanism. Int J Radiat Biol 2011;87:1147-1154.
51. Hancı H, Odacı E, Kaya H, Aliyazıcıoğlu Y, Turan İ, Demir S, et al. The effect of prenatal exposure to 900-MHz electromagnetic field on the 21-old-day rat testicle. Reprod. Toxicol 2013;42:203-209.
52. Kilgallon SJ, Simmons LW. Image content influences men’s semen quality. Bio Lett 2005;1:253-255.
53. Khalid A, Khudhair N, He H, Peng Z, Yaguang T, Guixue Z. Effects of dietary selenium supplementation on seminiferous tubules and SelW, GPx4, LHCGR, and ACE expression in chicken testis. Biol. Trace Elem Res 2016;173:202-209.
54. Wan N, Xu Z, Chi Q, Hu X, Pan T, Liu T, et al. microRNA‐33‐3p involved in selenium deficiency‐induced apoptosis via targeting ADAM10 in the chicken kidney. J Cell Physiol 2019;234:13693-13704.
55. Zeng R, Liang Y, Farooq MU, Zhang Y, Ei HH, Tang Z, et al. Alterations in transcriptome and antioxidant activity of naturally aged mice exposed to selenium-rich rice. Environ. Sci Pollut Res 2019:1-11.
56. Gao J, Wang Y, Xu G, Wei J, Chang K, Tian X, et al. Selenium attenuates apoptosis and p-AMPK expressions in fluoride-induced NRK-52E cells. Environ Sci Pollut Res 2019;26:15685-15697.
57. Makker K, Varghese A, Desai NR, Mouradi R, Agarwal A. Cell phones: modern man’s nemesis?  Reprod BioMed Online 2009;18:148-157.
58. Agarwal A, Deepinder F, Sharma RK, Ranga G, Li J. Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertil Steril 2008;89:124-128.
59. Rezaeian-Tabrizi M, Sadeghi A. Plasma antioxidant capacity, sexual and thyroid hormones levels, sperm quantity and quality parameters in stressed male rats received nano-particle of selenium. Asian Pac J Reprod 2017;6:29-34.