Royal jelly protects male mice against nicotine-induced reproductive failure

Document Type: Original Article

Authors

1 Department of Biology, Faculty of Sciences, Urmia University, Urmia, Iran

2 Department of Basic Sciences, Faculty of Veterinary Medicine, Urmia University, Urmia, Iran

Abstract

This study evaluated the possible protective effect of royal jelly (RJ) on sperm parameters and sperm malondialdehyde (MDA) concentration and in vitro fertilizing potential in nicotine (NIC) exposed male mice. Thrtiy-six male BALB/c mice were randomly divided into six groups (n = 6). Group 1 received normal saline, group 2 received 100 mg kg-1 per day RJ, groups 3 and 4 received NIC at doses of 0.50 and 1.00 mg kg-1 per day, respectively and groups 5 and 6 received NIC at doses of 0.50 and 1.00 mg kg-1 per day, respectively plus RJ. Caudal epididymal sperm characteristics, lipid peroxidation and in vitro fertilizing capacity and embryo development were evaluated after 35 days. The NIC treatment caused a significant decrease in sperm motility and viability and fertilization rate along with poor blastocyst formation and increased sperm DNA damage and MDA levels. Moreover, the incidences of chromatin abnormality in spermatozoa were significantly higher in NIC-exposed mice than those of control. Nevertheless, RJ treatment improved sperm parameters and in vitro fertilization outcome as well as sperm lipid peroxidation level. Data from the current study suggest that RJ has a potential repro-protective action against NIC-induced sperm abnormalities and embryotoxicity in mice.

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  1. McLachlan RI, de Kretser DM. Male infertility: The case for continued research. Med J Aust 2001; 174(3): 116-117.
  2. Oyeyipo IP, Raji Y, Emikpe BO, et al. Effects of nicotine on sperm characteristics and fertility profile in adult male rats: A possible role of cessation. J Reprod Infertil 2011; 12(3): 201-207.
  3. Jana K, Samanta PK, De DK. Nicotine diminishes testicular gametogenesis, steroidogenesis, and steroidogenic acute regulatory protein expression in adult albino rats: Possible influence on pituitary gonadotropins and alteration of testicular antioxidant status. Toxicol Sci 2010; 116(2): 647-659.
  4. Nesseim W, Haroun H, Mostafa E, et al. Effect of nicotine on spermatogenesis in adult albino rats. Andrologia 2011; 43(6): 398-404.
  5. Kavitharaj N, Vijayammal P. Nicotine administration induced changes in the gonadal functions in male rats. Pharmacology 1999; 58(1): 2-7.
  6. Aydos K, Güven M, Can B, et al. Nicotine toxicity to the ultrastructure of the testis in rats. BJU Int 2001; 88(6): 622-626.
  7. Yildiz D, Ercal N, Armstrong DW. Nicotine enantiomers and oxidative stress. Toxicology 1998; 130(2):155-165.
  8. Arabi M. Nicotinic infertility: Assessing DNA and plasma membrane integrity of human spermatozoa. Andrologia 2004; 36(5): 305-310.
  9. Han B, Li C, Zhang L, et al. Novel royal jelly proteins identified by gel-based and gel-free proteomics. J Agric Food Chem. 2011; 59(18):10346-10355.
  10. Hattori N, Nomoto H, Fukumitsu H, et al. Royal jelly and its unique fatty acid, 10-hydroxy-trans-2-decenoic acid, promote neurogenesis by neural stem/progenitor cells in vitro. Biomed Res 2007; 28(5): 261-266.
  11. Abdelhafiz AT, Muhamad JA. Midcycle pericoital intravaginal bee honey and royal jelly for male factor infertility. Int J Gynecol Obstet 2008; 101(2):146-149.
  12. Edwards R, Steptoe P, Purdy J. Fertilization and cleavage in vitro of preovulator human oocytes. Nature 1970; 227(5265): 1307-1309.
  13. Trounson A. Current perspectives of in vitro fertilization and embryo transfer. Clin Reprod Fertil 1982; 1(1): 55-65.
  14. Shalizar Jalali A, Najafi G, Hosseinchi M, et al. Royal jelly alleviates sperm toxicity and improves in vitro fertilization outcome in Stanozolol-treated mice. Iran J Reprod Med 2015; 13(1):15-22.
  15. Khosh AH, Hasanzadeh S, Shalizar Jalali A. Ameliorative effects of Achillea millefolium inflorescences alcoholic extract on nicotine-induced reproductive toxicity in male rat: Apoptotic and biochemical evidences. Vet Res Forum 2017; 8(2): 97-104.
  16. Jin L, Xue HY, Jin LJ, et al. Antioxidant and pancreas-protective effect of aucubin on rats with streptozotocin-induced diabetes. Eur J Pharmacol 2008; 582(1): 162-167.
  17. Wyrobek AJ, Gordon LA, Burkhart JG, 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): 1-72.
  18. Jalali AS, Najafi G, Rahimzadeh P. Summer savory (Satureja hortensis) can reduce spermatotoxic effects of doxorubicin in rats. Caspian J Reprod Med 2015; 1(1): 2-7.
  19. Aziz N, Said T, Paasch U, et al. The relationship between human sperm apoptosis, morphology and the sperm deformity index. Hum Reprod 2007; 22(5): 1413-1419.
  20. Talebi AR, Ghasemzadeh J, Khalili MA, et al. Sperm chromatin quality and DNA integrity in partial versus total globozoospermia. Andrologia 2018;50(1). doi: 10.1111/and.12823. Epub 2017 May 18.
  21. Kazerooni T, Asadi N, Jadid L. Evaluation of sperm's chromatin quality with acridin orange test, Chromomycine A3 and aniline blue staining in couple with recurrent abortion. Fertil Steril 2009; 92(3): S206.
  22. Erenpreiss J, Bars J, Lipatnikova V, et al. Comprative study of cytochemical tests for sperm chromatin integrity. J Androl 2001; 22; 45-53.
  23. Janero DR. Malondialdehyde and thiobarbituric acid-reactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radic Biol Med 1990; 9(6): 515-540.
  24. Byers SL, Payson SJ, Taft RA. Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). Theriogenology 2006; 65(9): 1716-1726.
  25. González R, Ruiz-León Y, Gomendio M, et al. The effect of glucocorticoids on mouse oocyte in vitro maturation and subsequent fertilization and embryo development. Toxicol In Vitro 2010; 24(1): 108-115.
  26. Wang X, Falcone T, Attaran M, et al. Vitamin C and vitamin E supplementation reduce oxidative stress- induced embryo toxicity and improve the blastocyst development rate. Fertil Steril 2002; 78(6): 1272-1277.
  27. Silici S, Ekmekcioglu O, Eraslan G, et al. Antioxidative effect of royal jelly in cisplatin-induced testes damage. Urology 2009; 74(3): 545-551.
  28. Guo H, Ekusa A, Iwai K, et al. Royal jelly peptides inhibit lipid peroxidation in vitro and in vivo. J Nutr Sci Vitaminol (Tokyo) 2008; 54(3): 191-195.
  29. Elnagar SA. Royal jelly counteracts bucks’ “summer infertility”. Anim Reprod Sci 2010; 121(1): 174-180.
  30. Winrow V, Winyard P, Morris C, et al. Free radicals in inflammation: Second messengers and mediators of tissue destruction. Br Med Bull 1993; 49(3): 506-522.
  31. Sankako MK, Garcia PC, Piffer RC, et al. Semen and reproductive parameters during some abstinence periods after cigarette smoke exposure in male rats. Braz Arch Biol Technol 2013; 56(1): 93-100.
  32. Jorsaraei SGA, Shibahara H. The in-vitro effects of nicotine, cotinine and leptin on sperm parameters analyzed by CASA system. Iran J Reprod Med 2008; 6(3): 157-165.
  33. Barrios F, Filipponi D, Pellegrini M, et al. Opposing effects of retinoic acid and FGF9 on Nanos2 expression and meiotic entry of mouse germ cells. J Cell Sci 2010; 123(6): 871-880.
  34. Aitken RJ. Free radicals, lipid peroxidation and sperm function. Reprod Fertil Dev 1995; 7(4): 659-668.
  35. Sikka SC. Andrology lab corner: Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. J androl 2004; 25(1): 5-18.
  36. Pacifici R, Altieri I, Gandini L, et al. Environmental tobacco-smoke-nicotine and cotinine concentration in semen. Environ Res 1995; 68(1):69-72.
  37. Goss D, Oyeyipo IP, Skosana BT, et al. Ameliorative potentials of quercetin against cotinine-induced toxic effects on human spermatozoa. Asian Pac J Reprod 2016; 5(3):193-197.
  38. Shen HM, Ong CN. Detection of oxidative DNA damage in human sperm and its association with sperm function and male infertility. Free Radic Biol Med 2000; 28(4): 529-536.
  39. Moazamian R, Polhemus A, Connaughton H, et al. Oxidative stress and human spermatozoa: Diagnostic and functional significance of aldehydes generated as a result of lipid peroxidation. Mol Hum Reprod 2015; 21(6): 502-515.
  40. Saleh RA, Agarwal A, Sharma RK, et al. Effect of cigarette smoking on levels of seminal oxidative stress in infertile men: A prospective study. Fertil Steril 2002; 78(3): 491-499.
  41. Schulte RT, Ohl DA, Sigman M, et al. Sperm DNA damage in male infertility: Etiologies, assays, and outcomes. J Assist Reprod Genet 2010; 27(1): 3-12.
  42. La Maestra S, de Flora S, Micale RT. Effect of cigarette smoke on DNA damage, oxidative stress, and morphological alterations in mouse testis and spermatozoa. Int J Hyg Environ Health 2015; 218(1):117-122.
  43. Sadeghi MR, Hodjat M, Lakpour N, et al. Effects of sperm chromatin integrity on fertilization rate and embryo quality following intracytoplasmic sperm injection. Avicenna J Med Biotechnol 2009; 1(3): 173-180.
  44. Cho C, Jung-Ha H, Willis WD, et al. Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice. Biol Reprod 2003; 69(1): 211-217.
  45. Sharma R, Said T, Agarwal A. Sperm DNA damage and its clinical relevance in assessing reproductive outcome. Asian J Androl 2004; 6(2):139-148.
  46. Yamamoto Y, Isoyama E, Sofikitis N, et al. Effects of smoking on testicular function and fertilizing potential in rats. Urol Res 1998; 26(1): 45-48.
  47. Wang J, Wilcken DE, Wang XL. Cigarette smoke activates caspase-3 to induce apoptosis of human umbilical venous endothelial cells. Mol Genet Metab 2001; 72(1): 82-88.
  48. Ghanbari E, Nejati V, Khazaei M. Antioxidant and protective effects of royal jelly on histopathological changes in testis of diabetic rats. Int J Reprod Biomed 2016; 14(8): 519-526.
  49. Pourmoradian S, Mahdavi R, Mobasseri M, et al. Effects of royal jelly supplementation on glycemic control and oxidative stress factors in type 2 diabetic female: A randomized clinical trial. Chin J Integr Med 2014; 20(5): 347-352.
  50. Shahzad Q, Mehmood MU, Khan H, et al. Royal jelly supplementation in semen extender enhances post-thaw quality and fertility of Nili-Ravi buffalo bull sperm. Anim Reprod Sci 2016; 167:83-88.