The Sperm and In-Vitro Fertilization (IVF) of Mice with Phenylhydrazine-Induced Hemolytic Anemia; Ameliorating the Effect of Royal Jelly and Vitamin C

Document Type : Original Article (s)

Authors

1 PhD Student, Department of Basic Sciences, School of Veterinary Medicine, University of Tehran, Tehran, Iran

2 Associate Professor, Department of Basic Sciences, School of Veterinary Medicine, University of Tehran, Tehran, Iran

3 Assistant Professor, Department of Basic Sciences, School of Veterinary Medicine, Urmia University, Urmia, Iran

4 Professor, Department of Basic Sciences, School of Veterinary Medicine, Urmia University, Urmia, Iran

5 PhD Student, Department of Basic Sciences, School of Veterinary Medicine, Urmia University, Urmia , Iran

Abstract

Background: Hemolytic anemia induced by phenylhydrazine (PHZ), as a hemolytic compound, can cause disorders in spermatogenesis and fertility. The present study aimed to evaluate the effect of vitamin C (Vit C) and royal jelly (RJ) as effective antioxidant compounds against phenylhydrazine-induced hemolytic anemia.Methods: Adult male mice were randomly diveded into four groups of eight. The first group received 0.1 ml of normal saline intraperitonealy (IP). The second group received 60 mg/kg of phenylhydrazine in 48-hour intervals intraperitonealy. The third group received 60 mg/kg of phenylhydrazine along with 250 mg/kg of vitamin C intraperitonealy and100 mg/kg of royal jelly orally. The fourth group received the same doses of vitamin C and royal jelly as the third group. After 35 days, serum samples were taken, the sperms were collected from epididymis and in-vitro fertilization (IVF) was evaluated.Findings: Phenylhydrazine-induced hemolytic anemia significantly decreased serum testosterone concentration and increased damaged DNA and immature nuclear sperm. Moreover, phenylhydrazine decreased the number of fertilized oocytes, two-cell and four-cell embryos, morula and blastocyst and increased arrested embryos. However, administrating of royal jelly and vitamin C improved these parameters significantly.Conclusion: It seems that royal jelly and vitamin C, as free radicals scavengers, have the potential to decrease oxidative damages on reproductive organ in phenylhydrazine-induced hemolytic anemia.

Keywords

References

  1. Berger J. Phenylhydrazine haematotoxicity. J Appl Biomed 2007; 5(3): 125-30.
  2. Puntarulo S. Iron, oxidative stress and human health. Mol Aspects Med 2005; 26(4-5): 299-312.
  3. Ferrali M, Ciccoli L, Signorini C, Comporti M. Iron release and erythrocyte damage in allyl alcohol intoxication in mice. Biochem Pharmacol 1990; 40(7): 1485-90.
  4. Friedmann B, Jost J, Rating T, Weller E, Werle E, Eckardt KU, et al. Effects of iron supplementation on total body hemoglobin during endurance training at moderate altitude. Int J Sports Med 1999; 20(2): 78-85.
  5. Macome JC, Costa LE, Martin IH, Taquini AC. Steroid biosynthesis by gonads of rats submitted to chronic hypobaric hypoxia. Acta Physiol Lat Am 1977; 27(5): 249-57.
  6. Khmel'nitskii OK, Tararak TI. Morphological characteristics of the pituitary-gonad system in high altitude hypoxia. Biull Eksp Biol Med 1991; 111(4): 432-6. [In Russian].
  7. Rattner BA, Macmillan BT, Michael SD, Altland PD. Plasma gonadotrophins, prolactin and corticosterone concentrations in male mice exposed to high altitude. J Reprod Fertil 1980; 60(2): 431-6.
  8. McCluskey ES. Which vertebrates make vitamin C? Origins 1985; 12(2): 96-100.
  9. du Toit R, Volsteedt Y, Apostolides Z. Comparison of the antioxidant content of fruits, vegetables and teas measured as vitamin C equivalents. Toxicology 2001; 166(1-2): 63-9.
  10. Siddique YH, Beg T, Afzal M. Antigenotoxic effects of ascorbic acid against megestrol acetate-induced genotoxicity in mice. Hum Exp Toxicol 2005; 24(3): 121-7.
  11. Aly N, EL-Gendy K, Mahmoud F, El-Sebae AK. Protective effect of vitamin C against chlorpyrifos oxidative stress in male mice. Pest Biochem Physiol 2010; 97(1): 7-12.
  12. Taghiyar M, Ghiasvand R, Feizi A, Askari Gh, Shokri N. Effects of vitamins C and E supplementation on muscle damage and oxidative stress in female athletes: a double-blind clinical trial. J Isfahan Med Sch 2013; 30(216): 2113-24. [In Persian].
  13. Ramadan MF, Al-Ghamdi A. Bioactive compounds and health-promoting properties of royal jelly: A review. J Funct Foods 2012; 4(1): 39-52.
  14. Nakajima Y, Tsuruma K, Shimazawa M, Mishima S, Hara H. Comparison of bee products based on assays of antioxidant capacities. BMC Complement Altern Med 2009; 9: 4.
  15. Zamani Z, Reisi P, Alaei H, Pilehvarian AA. Effect of royal jelly on improving passive avoidance learning and spatial learning and memory in rats. J Shahid Sadoughi Univ Med Sci 2012; 20(2): 211-9. [In Persian].
  16. Shirzad H, Sedaghat A, Ghasemi S, Shirzad M. Effect of royal jelly on sterile wound healing in Balb/C mice. Armaghane-Danesh 2010; 15(1): 38-46. [In Persian].
  17. Yang A, Zhou M, Zhang L, Xie G, Chen H, Liu Z, et al. Influence of royal jelly on the reproductive function of puberty male rats. Food Chem Toxicol 2012; 50(6): 1834-40.
  18. Kalantari Hesari A, Shahrooz R, Ahmadi A, Malekinejad H, Saboory E. Crocin prevention of anemia-induced changes in structural and functional parameters of mice testes. ‎J Appl Biomed 2015; 13(3): 213-23.
  19. Yu F, Wang Z, Ju B, Wang Y, Wang J, Bai D. Apoptotic effect of organophosphorus insecticide chlorpyrifos on mouse retina in vivo via oxidative stress and protection of combination of vitamins C and E. Exp Toxicol Pathol 2008; 59(6): 415-23.
  20. Silici S, Ekmekcioglu O, Eraslan G, Demirtas A. Antioxidative effect of royal jelly in cisplatin-induced testes damage. Urology 2009; 74(3): 545-51.
  21. Sadeghi MR, Akhondi MA, Savadi Shirazi E, Hodjat M, Amirjanati N, Akhondi MA, et al. The comparison of four different sperm chromatin assays and their correlation with semen parameters. Tehran Univ Med J 2008; 65(Suppl 3): 33-41. [In Persian].
  22. Talebi AR, Sarcheshmeh AA, Khalili MA, Tabibnejad N. Effects of ethanol consumption on chromatin condensation and DNA integrity of epididymal spermatozoa in rat. Alcohol 2011; 45(4): 403-9.
  23. Sadeghi MR, Hodjat M, Lakpour N, Arefi S, Amirjannati N, Modarresi T, et al. Effects of sperm chromatin integrity on fertilization rate and embryo quality following intracytoplasmic sperm injection. Avicenna J Med Biotechnol 2009; 1(3): 173-80.
  24. Byers SL, Payson SJ, Taft RA. Performance of ten inbred mouse strains following assisted reproductive technologies (ARTs). Theriogenology 2006; 65(9): 1716-26.
  25. Ikeda T, Sofikitis N. Bilateral testicular consequences in the unilateral vasectomy of immature rats. Yonago Acta Medica 2000; 43(1): 1-9.
  26. Cebral E, Carrasco I, Vantman D, Smith R. Preimplantation embryotoxicity after mouse embryo exposition to reactive oxygen species. Biocell 2007; 31(1): 51-9.
  27. Zahra A, Gholamreza N, Farokhi F, Shalizar JA. Attenuation of cyclosporine-induced sperm impairment and embryotoxicity by crataegus monogyna fruit aqueous extract. Cell J 2013; 15(3): 198-205.
  28. Roque M, D´Anna C, Gatti Ch, Veuthey T. Hematological and morphological analysis of the erythropoietic regenerative response in phenylhydrazine-induced hemolytic anemia in mice. Scand J Lab Anim Sci 2008; 35(3): 181-90.
  29. Guyton AC, Hall JE. Textbook of medical physiology. 9th ed. Philadelphia, PA: Saunders; 1996.
  30. Ghanbari E, Nejati V, Najafi G, Khazaei M, Babaei M. Study on the effect of royal jelly on reproductive parameters in streptozotocin-induced diabetic rats. Int J Fertil Steril 2015; 9(1): 113-20.
  31. Mohammadi J, Chatrroz B, Delaviz H. The effect of hydroalcoholic extract of capparis spinosa on quality of sperm and rate of testosterone following induction of diabetes in rats. J Isfahan Med Sch 2014; 31(264): 2042-52. [In Persian].
  32. McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, de Kretser DM, Pratis K, et al. Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog Horm Res 2002; 57: 149-79.
  33. Shan L, Hardy DO, Catterall JF, Hardy MP. Effects of luteinizing hormone (LH) and androgen on steady state levels of messenger ribonucleic acid for LH receptors, androgen receptors, and steroidogenic enzymes in rat Leydig cell progenitors in vivo. Endocrinology 1995; 136(4): 1686-93.
  34. Yang J, Zhang Y, Wang Y, Cui S. Toxic effects of zearalenone and alpha-zearalenol on the regulation of steroidogenesis and testosterone production in mouse Leydig cells. Toxicol in Vitro 2007; 21(4): 558-65.
  35. Bairy KL, Kumar G, Rao Y. Effect of acyclovir on the sperm parameters of albino mice. Indian J Physiol Pharmacol 2009; 53(4): 327-33.
  36. Amirshahi T, Najafi G, Nejati V. Protective effect of royal jelly on fertility and biochemical parameters in bleomycin-induced male rats. Iran J Reprod Med 2014; 12(3): 209-16.
  37. Farias JG, Bustos-Obregon E, Orellana R, Bucarey JL, Quiroz E, Reyes JG. Effects of chronic hypobaric hypoxia on testis histology and round spermatid oxidative metabolism. Andrologia 2005; 37(1): 47-52.
  38. Fanaei H, Khayat S, Halvaei I, Ramezani V, Azizi Y, Kasaeian A, et al. Effects of ascorbic acid on sperm motility, viability, acrosome reaction and DNA integrity in teratozoospermic samples. Iran J Reprod Med 2014; 12(2): 103-10.
  39. Roqueta-Rivera M, Stroud CK, Haschek WM, Akare SJ, Segre M, Brush RS, et al. Docosahexaenoic acid supplementation fully restores fertility and spermatogenesis in male delta-6 desaturase-null mice. J Lipid Res 2010; 51(2): 360-7.
  40. Rezvanfar M, Sadrkhanlou R, 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(12): 901-10.
  41. Kalantari A, Shahrooz R, Ahmadi A, Malekinejad H. Evaluation of sperm quality in phenylhydrazine-induced hemolytic anemia impacts on mice and protective role of crocin. Iranian Veterinary Journal 2016; 77-84. [In Persian].
  42. Jalali AS, Hasanzadeh S, Malekinejad H. Achillea millefolium inflorescence aqueous extract ameliorates cyclophosphamide-induced toxicity in rat testis: stereological evidences. Chinese Journal of Natural Medicines 2012; 10(4): 247-54.
  43. Sharma RK, Agarwal A. Role of reactive oxygen species in male infertility. Urology 1996; 48(6): 835-50.
  44. Seli E, Sakkas D. Spermatozoal nuclear determinants of reproductive outcome: implications for ART. Hum Reprod Update 2005; 11(4): 337-49.
  45. Pons-Rejraji H, Sion B, Saez F, Brugnon F, Janny L, Grizard G. Role of reactive oxygen species (ROS) on human spermatozoa and male infertility. Gynecol Obstet Fertil 2009; 37(6): 529-35. [In French].
  46. Shalizar JA, Najafi G, Hosseinchi M, Sedighnia A. Royal jelly alleviates sperm toxicity and improves in vitro fertilization outcome in Stanozolol-treated mice. Iran J Reprod Med 2015; 13(1): 15-22.
  47. Takayama H, Kato H. Nitric oxide inhibits oocyte meiotic maturation. Biol Reprod 2002; 67(5): 1588-92.
  48. Hashimoto S, Minami N, Yamada M, Imai H. Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Mol Reprod Dev 2000; 56(4): 520-6.
  49. Aitken RJ. The Amoroso Lecture. The human spermatozoon--a cell in crisis? J Reprod Fertil 1999; 115(1): 1-7.
  50. Dalvit GC, Cetica PD, Beconi MT. Effect of alpha-tocopherol and ascorbic acid on bovine in vitro fertilization. Theriogenology 1998; 49(3): 619-27.
  51. Griesinger G, Franke K, Kinast C, Kutzelnigg A, Riedinger S, Kulin S, et al. Ascorbic acid supplement during luteal phase in IVF. J Assist Reprod Genet 2002; 19(4): 164-8.
  52. Jeong YW, Park SW, Hossein MS, Kim S, Kim JH, Lee SH, et al. Antiapoptotic and embryotrophic effects of alpha-tocopherol and L-ascorbic acid on porcine embryos derived from in vitro fertilization and somatic cell nuclear transfer. Theriogenology 2006; 66(9): 2104-12.
Journal of Isfahan Medical School
Volume 33, Issue 363 - Serial Number 363
November and December 2016
Pages 2193-2203

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History

  • Receive Date: 22 September 2015
  • Revise Date: 01 November 2024
  • Accept Date: 06 April 2022

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