Volume 13, Issue 1 (1-2015)                   IJRM 2015, 13(1): 15-22 | Back to browse issues page

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Shalizar Jalali A, Najafi G, Hosseinchi M, Sedighnia A. Royal Jelly alleviates sperm toxicity and improves in vitro fertilization outcome in Stanozolol-treated mice. IJRM 2015; 13 (1) :15-22
URL: http://ijrm.ir/article-1-586-en.html
1- Department of Basic Sciences, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran , ali_shalizar@yahoo.com
2- Department of Basic Sciences, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran
3- Department of Basic Sciences, Faculty of Veterinary Medicine, Urmia Branch, Islamic Azad University, Urmia, Iran
Abstract:   (2609 Views)
Background: Stanozolol (ST) is a synthetic anabolic-androgenic steroid often abused by athletes. An increasing body of evidence points towards the role of ST misuses in the pathogenesis of a wide range of adverse effects including reprotoxicity.
Objective: The aim of this study was to analyze the possible reproprotective effect of royal jelly (RJ) as an efficient antioxidant in ST-treated mice.
Materials and Methods: Adult male mice were divided into four groups (n=5). Two groups of mice received ST (4.6 mg/kg/day) via gavage for 35 days. RJ was given orally to one of these groups at the dose level of 100 mg/kg body weight per day synchronously. Untreated control group and RJ-only treated group were also included. Epididymal sperm characteristics and in vitro fertilizing capacity were evaluated after 35 days.
Results: ST treatment caused a significant (p<0.05) decrease in sperm count and motility and fertilization rate along with poor blastocyst formation and increased sperm DNA damage. Moreover, the incidence of apoptosis and abnormality in spermatozoa was significantly (p<0.05) higher in ST-exposed mice than those of control. The above-mentioned parameters were restored to near normal level by RJ co-administration.
Conclusion: Data from the current study suggest that RJ has a potential repro-protective action against ST-induced reproductive toxicity in mice. However, clinical studies are warranted to investigate such an effect in human subjects.
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Type of Study: Original Article |

References
1. Shahidi NT. A review of the chemistry, biological action, and clinical applications of anabolic-androgenic steroids. Clin Ther 2001; 23: 1355- 1390. [DOI:10.1016/S0149-2918(01)80114-4]
2. Yesalis CE, Bahrke MS. Doping among adolescent athletes. Clin Endocrinol Metab 2000; 14: 25-35. [DOI:10.1053/beem.2000.0051]
3. Yavari A. Abuse of anabolic androgenic steroids. J Stress Physiol Biochem 2009; 5: 22-32.
4. Pavlatos AM, Fultz O, Monberg MJ, Vootkur A. Review of oxymetholone: a 17α-alkylated anabolic-androgenic steroid. Clin Ther 2001; 23: 789-801. [DOI:10.1016/S0149-2918(01)80070-9]
5. Hengge UR, Stocks K, Wiehler H, Faulkner S, Esser S, Lorenz C, et al. Double-blind, randomized, placebo-controlled phase III trial of oxymetholone for the treatment of HIV wasting. AIDS 2003; 28: 699-710. [DOI:10.1097/00002030-200303280-00008]
6. Hosseinimehr SJ, Zakaryaee V, Froughizadeh M. Oral oxymetholone reduces mortality induced by gamma irradiation in mice through stimulation of hematopoietic cells. Mol Cell Biochem 2006; 287: 193-199. [DOI:10.1007/s11010-005-9111-5]
7. Dickerman RD, Pertusi RM, Zachariah NY, Dufour DR, McConathy WJ. Anabolic steroid-induced hepatotoxicity: Is it overstated? Clin J Sport Med 1999; 9: 34-39. [DOI:10.1097/00042752-199901000-00007]
8. Fineschi V, Baroldi G, Monciotti F, Paglicci Reattelli L, Turillazzi E. Anabolic steroid abuse and cardiac sudden death: a pathologic study. Arch Pathol Lab Med 2001; 125: 253-255.
9. Torres-Calleja J, González-Unzaga M, DeCelis-Carrillo R, Calzada-Sánchez L, Pedrón N. Effect of androgenic anabolic steroids on sperm quality and serum hormone levels in adult male bodybuilders. Life Sci 2001; 68: 1769-1774. [DOI:10.1016/S0024-3205(01)00972-9]
10. Clark AS, Kelton MC, Whitney AC. Chronic administration of anabolic steroids disrupts pubertal onset and estrous cyclicity in rats. Biol Reprod 2003; 68: 465-471. [DOI:10.1095/biolreprod.102.008078]
11. Hall RC, Hall RC, Champan MJ. Psychiatric complications of anabolic steroid abuse. Psychosomatics 2005; 46: 285-290. [DOI:10.1176/appi.psy.46.4.285]
12. Small M, Beastall GH, Semple CG, Cowan RA, Forbes CD. Alteration of hormone levels in normal males given the anabolic steroid stanozolol. Clin Endocrinol (Oxf) 1984; 21: 49-55. [DOI:10.1111/j.1365-2265.1984.tb00135.x]
13. Whitney AC, Clark AS. Effects of acute stanozolol treatment on puberty in female rats. Biol Reprod 2001; 64: 1460-1465. [DOI:10.1095/biolreprod64.5.1460]
14. Mutalip SSM, Singh GKS, Shah AM, Mohamad M, Mani V, Hussin SN. Histological changes in testes of rats treated with testosterone, nandrolone, and stanozolol. Iran J Reprod Med 2013; 11: 653-658.
15. Ergüder IB, Çetin R, Devrim E, Kiliçoğlu B, Avci A, Durak I. Effects of cyclosporine on oxidant/antioxidant status in rat ovary tissues: protective role of black grape extract. Int Immunopharmacol 2005; 5: 1311-1315. [DOI:10.1016/j.intimp.2005.03.016]
16. Rezvanfar MA, Sadrkhanlou RA, Ahmadi A, Shojaei-Sadee H, Rezvanfar M, Mohammadirad A, et al. Protection of cyclophosphamide-induced toxicity in reproductive tract histology, sperm characteristics, and DNA damage by an herbal source; evidence for role of free-radical toxic stress. Hum Exp Toxicol 2008; 27: 901-910. [DOI:10.1177/0960327108102046]
17. Sato K, Sueoka K, Tanigaki R, Tajima H, Nakabayashi A, Yoshimura Y, et al. Green tea extracts attenuate doxorubicin-induced spermatogenic disorders in conjunction with higher telomerase activity in mice. J Assist Reprod Genet 2010: 27: 501-508. [DOI:10.1007/s10815-010-9438-z]
18. El-Nekeety AA, El-Kholy W, Abbas NF, Ebaid A, Amra HA, Abdel-Wahhab AA. Efficacy of royal jelly against the oxidative stress of fumonisin in rats. Toxicon 2007; 50: 256–269. [DOI:10.1016/j.toxicon.2007.03.017]
19. Guo H, Ekusa A, Iwai K, Yonekura M, Takahata Y, Morimatsu F. Royal jelly peptides inhibit lipid peroxidation in vitro and in vivo. J Nutr Sci Vitaminol (Tokyo) 2008; 54: 191-195. [DOI:10.3177/jnsv.54.191]
20. Sver L, Orsolic N, Tadic Z, Njari B, Valpotic I. A royal jelly as a new potential immunomodulator in rats and mice. Comp Immunol Microbial Infect Dis 1996; 19: 31-38. [DOI:10.1016/0147-9571(95)00020-8]
21. Fujiwara S, Imai J, Fujiwara M, Yaeshima T, Kawashima T, Kobayashi K. A potent antibacterial protein in royal jelly. Purification and determination of the primary structure of royalisin. Peptides 2004; 25: 919-928.
22. Kohno K, Okamoto I, Sano O, Arai N, Iwaki K, Ikeda M, et al. Royal jelly inhibits the production of pro-inflammatory cytokines by activated macrophages. Biosci Biotechnol Biochem 2004; 68: 138-145. [DOI:10.1271/bbb.68.138]
23. Oršolić N, Terzić S, Šver L, Bašić I. Honeybee products in prevention and/or therapy of murine transplantable tumours. J Sci Food Agric 2005; 85: 363-370. [DOI:10.1002/jsfa.2041]
24. Kato A, Onodera M, Ishijima Y. Effect of royal jelly on development of genital organ in male mice. J Tokyo Vet Anim Sci 1988; 35: 1-4.
25. Abdelhafiz AT, Muhamad JA. Midcycle pericoital intravaginal bee honey and royal jelly for male factor infertility. Int J Gynaecol Obstet 2008; 101: 146-149. [DOI:10.1016/j.ijgo.2007.11.012]
26. Lionikas A, Blizard DA. Diverse effects of stanozolol in C57BL/6J and A/J mouse strains. Eur J Appl Physiol 2008; 103: 333-341. [DOI:10.1007/s00421-008-0708-8]
27. Silici S, Ekmekcioglu O, Eraslan G, Demirtas A. Antioxidative effect of royal jelly in cisplatin-induced testes damage. Urology 2009; 74: 545-551. [DOI:10.1016/j.urology.2009.05.024]
28. Selvakumar E, Prahalathan C, Sudharsan PT, Varalakshmi P. Chemoprotective effect of lipoic acid against cyclophosphamide-induced changes in the rat sperm. Toxicology 2006; 217: 71-78. [DOI:10.1016/j.tox.2005.08.020]
29. Zambrano E, Rodriguez-Gonzalez GL, Guzman C, Garcia-Becerra R, Boeck L, Menjivar M, et al. 2005. A maternal low protein diet during pregnancy and lactation in the rat impairs male reproductive development. J Physiol 2005; 563; 275-284. [DOI:10.1113/jphysiol.2004.078543]
30. Erenpreiss J, Bars J, Lipatnikova V, Erenpreisa J, Zalkalns J. 2001. Comprative study of cytochemical tests for sperm chromatin integrity. J Androl 2001; 22; 45-53.
31. Wyrobek AJ, Gordon LA, Burkhart JG, Francis MW, Kapp RW Jr, Letz G, et al. An evaluation of the mouse sperm morphology test and other sperm tests in nonhuman mammals. A report of the US environmental protection agency gene-tox program. Mutat Res 1983; 115: 1-72. [DOI:10.1016/0165-1110(83)90014-3]
32. Menkveld R, Wong WY, Lombard CJ, Wetzels AM, Thomas CM, Merkus HM, et al. Semen parameters, including WHO and strict criteria morphology, in a fertile and subfertile population: an effort towards standardization of in-vivo thresholds. Hum Reprod 2001; 16: 1165-1171. [DOI:10.1093/humrep/16.6.1165]
33. Wu Y, Tibrewal N, Birge RB. Phosphatidylserine recognition by phagocytes: a view to a kill. Trends Cell Biol 2006; 16: 189-197. [DOI:10.1016/j.tcb.2006.02.003]
34. Van Heerde WL, de Groot PG, Reutelingsperger CP. The complexity of the phospholipid binding protein Annexin V. Thromb Haemost 1995; 73: 172-179.
35. Mahfouz RZ, Sharma RK, Said TM, Erenpreiss J, Agarwal A. Association of sperm apoptosis and DNA ploidy with sperm chromatin quality in human spermatozoa. Fertil Steril 2009; 91: 1110-1118. [DOI:10.1016/j.fertnstert.2008.01.047]
36. Byers SL, Payson SJ, Taft RA. Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). Theriogenology 2006; 65: 1716-1726. [DOI:10.1016/j.theriogenology.2005.09.016]
37. González R, Ruiz-León Y, Gomendio M, Roldan ER. The effect of glucocorticoids on mouse oocyte in vitro maturation and subsequent fertilization and embryo development. Toxicol In vitro 2010; 24: 108-115. [DOI:10.1016/j.tiv.2009.08.025]
38. Kaki T, Sofikitis N. Effects of unilateral cryptorchidism on contralateral epididymal sperm quality, quantity and fertilizing capacity. Yonago Acta Med 1999; 42: 79-86.
39. Wang X, Falcone T, Attaran M, Goldberg JM, Agarwal A, Sharma RK. Vitamin C and Vitamin E supplementation reduce oxidative stress–induced embryo toxicity and improve the blastocyst development rate. Fertil steril 2002; 78: 1272-1277. [DOI:10.1016/S0015-0282(02)04236-X]
40. Chailert C, Sanmee U, Piromlertamorn W, Samchimchom S, Vutyavanich T. Effects of partial or complete laser-assisted hatching on the hatching of mouse blastocysts and their cell numbers. Reprod Biol Endocrinol 2013; 11: 21. [DOI:10.1186/1477-7827-11-21]
41. Bahrke MS, Yesalis CE. Abuse of anabolic androgenic steroids and related substances in sport and exercise. Curr opin pharmacol 2004; 4: 614-620. [DOI:10.1016/j.coph.2004.05.006]
42. Feinberg MJ, Lumia AR, McGinnis MY. The effect of anabolicandrogenic steroids on sexual behavior and reproductive tissues in male rats. Physiol Behav 1997; 62: 23–30. [DOI:10.1016/S0031-9384(97)00105-4]
43. Takahashi M, Tatsugi Y, Kohno T. Endocrinological and pathological effects of anabolic-androgenic steroid in male rats. Endocr J 2004; 51: 425-434. [DOI:10.1507/endocrj.51.425]
44. Torres-Calleja J, González-Unzaga M, DeCelis-Carrillo R, Calzada-Sánchez L, Pedrón N. Effect of androgenic anabolic steroids on sperm quality and serum hormone levels in adult male bodybuilders. Life Sci 2001; 68: 1769-1774. [DOI:10.1016/S0024-3205(01)00972-9]
45. Karila T, Hovatta O, Seppala T. Concomitant abuse of anabolic androgenic steroids and human chorionic gonadotrophin impairs spermatogenesis in power athletes. Int J Sports Med 2004; 25: 257-263. [DOI:10.1055/s-2004-819936]
46. Hess RA, Cooke PS, Hofmann MC, Murphy KM. Mechanistic insights into the regulation of the spermatogonial stem cell niche. Cell Cycle 2006; 5: 1164-1170. [DOI:10.4161/cc.5.11.2775]
47. Mruk, DD, Cheng, CY. Sertoli-Sertoli and Sertoli-germ cell interactions and their significance in germ cell movement in the seminiferous epithelium during spermatogenesis. Endocr Rev 2004; 25: 747–806. [DOI:10.1210/er.2003-0022]
48. Sader MA, Griffiths KA, McCredie RJ, Handelsman DJ, Celermajer DS. Androgenic anabolic steroids and arterial structure and function in male bodybuilders. J Am Coll Cardiol 2001; 37: 224-230. [DOI:10.1016/S0735-1097(00)01083-4]
49. Pey A, Saborido A, Blazquez I, Delgado J, Megias A. Effects of prolonged stanozolol treatment on antioxidant enzyme activities, oxidative stress markers, and heat shock protein HSP72 levels in rat liver. J Steroid Biochem Mol Biol 2003; 87: 269-277. [DOI:10.1016/j.jsbmb.2003.09.001]
50. Agarwal A, Makker K, Sharma R. Clinical relevance of oxidative stress in male factor infertility: an update. Am J Reprod Immunol 2008; 59: 2-11. [DOI:10.1111/j.1600-0897.2007.00559.x]
51. Agarwal A, Sharma RK, Desai NR, Prabakaran S, Tavares A, Sabanegh E. Role of oxidative stress in pathogenesis of varicocele and infertility. Urology 2009; 73: 461-469. [DOI:10.1016/j.urology.2008.07.053]
52. Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 2003; 79: 829-843. [DOI:10.1016/S0015-0282(02)04948-8]
53. Virro MR, Larson-Cook KL, Evenson DP. Sperm chromatin structure assay (SCSA®) related to blastocyst rate, pregnancy rate and spontaneous abortion in IVF and ICSI cycles. Fertil Steril 2004; 8: 1289-1295. [DOI:10.1016/j.fertnstert.2003.09.063]
54. Agarwal A, Sharma RK, Nallella KP, Thomas AJ Jr, Alvarez JG, Sikka SC. Reactive oxygen species as an independent marker of male factor infertility. Fertil Steril 2006; 86: 878-885. [DOI:10.1016/j.fertnstert.2006.02.111]
55. Collins JA, Barnhart KT, Schlegel PN. Do sperm DNA fragmentation tests predict pregnancy with in vitro fertilization? Fertil Steril 2008; 89: 823-831. [DOI:10.1016/j.fertnstert.2007.04.055]
56. Gil-Guzman E, Ollero M, Lopez MC, Sharma RK, Alvarez JG, Thomas AJ Jr, et al. Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Hum Reprod 2001; 16: 1922-1930. [DOI:10.1093/humrep/16.9.1922]
57. Nagai T, Inoue R. Preparation and the functional properties of water extract and alkaline extract of royal jelly. Food Chem 2004; 84: 181-186. [DOI:10.1016/S0308-8146(03)00198-5]
58. Silici S, Ekmekcioglu O, Eraslan G, Demirtas A. Antioxidative effect of royal jelly in cisplatin-induced testes damage. Urology 2009; 74: 545-551. [DOI:10.1016/j.urology.2009.05.024]
59. Elnagar SA. Royal jelly counteracts bucks' "summer infertility". Anim Reprod Sci 2010; 121: 174-180. [DOI:10.1016/j.anireprosci.2010.05.008]
60. Najafi G, Nejati V, Jalali AS, Zahmatkesh E. Protective role of royal jelly in oxymetholone-induced oxidative injury in mouse testis. Iran J Toxicol 2014; 8: 1073-1080.

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