Royal Jelly Administration Recover Spermatogenesis and Sexual Hormones Levels in a Busulfan-injured Rat Model
Subject Areas :
Tayebeh Sadeghi
1
*
,
Seyed Ebrahim Hosseini
2
,
Mohammad Khaksari
3
,
Abbas Mortazaeizadeh
4
1 - Faculty of Medicine, Ke.C., Islamic Azad University, Kerman, Iran
2 - Department of Biology, Faculty of Science, Zand Institute of Higher Education, Shiraz, Iran
3 - Department of Physiology and Pharmacology, Kerman University of Medical Sciences, Kerman, Iran
4 - Pathology and Stem Cells Research Centre, Kerman University of Medical Sciences, Kerman, Iran
Keywords: Busulfan, Sex hormones, Rat, Spermatogenesis, Royal jelly,
Abstract :
The role of the busulfan-mediated pathway in its anti-estrogenic effects and resulting changes of spermatogenesis is still unknown, while royal jelly may improve spermatogenesis. Our objective was to determine the effects of royal jelly on the recovery of spermatogenesis, histology testis and sexual hormones and in of a busulfan-injured rat model. Sixty adult rats were randomly assigned to three treatment groups, consisting of four replicates with five rats in each replicate. Animals received a tow intraperitoneal vehicle (control) or 10 mg/kg busulfan injection (at 0 and 21 day), and 35 days after, the animals received orally 100 mg/kg royal jelly for 14, 28 and 56 days. One day after, blood plasma was obtained for hormone analysis, sperm was recovered from epididymis, and testes were processed for histology. The weight of the body and testis were recorded. Body and testis weights were significantly lower in the busulfan- vehicle group comparing to the other treatments (P<0.05). Whereas, this decrease was recovered in the royal jelly+ busulfan rat. Control groups did not show significant changes in most parameters, but busulfan decreased sperm counts, motility and normal morphology, induced seminiferous tubule depletion, intertubular space and decreased blood testosterone, FSH and LH. Royal jelly treatments partially recovered spermatogenesis, decreasing tubular atrophy. The royal jelly treatments in the busulfan-treated animals significantly increased sex hormones levels and sperm parameters, but, except for sperm motility and normal morphology at 56 d, they did not recover up to the values in the no-busulfan group (p<0.05). Royal jelly was the most efficient treatment, also increasing the concentration of sexual hormones close to no-busulfan levels. The royal jelly treatments reverted spermatogenesis, hormonal levels and histology similar to controls, however not attaining the same sperm quality than controls busulfan.
Amirshahi T, Najafi G, Nejati G. 2013. Protective effect of royal jelly on fertility and biochemical parameters in bleomycin- induced male rats. Iran J Reprod Med, 12(3), 209-216.
Saberivand A, Pashapour S, Noghani AE, Namvar Z. Synergistic effect of royal jelly in combination with glycerol and dimethyl sulfoxide on cryoprotection of Romanov ram sperm. Cryobiology. 2022 Feb;104:87-97. doi: 10.1016/j.cryobiol.2021.05.006. Epub 2021 May 30. PMID: 34077710
Chen X, Liang M, Wang D. 2018. Progress on the study of the mechanism of busulfan cytotoxicity. Cytotechnology. 70(2): 497-502. https://doi.org/10.1007/s10616-018-0189-5.
Khazaei F, Ghanbari E, Khazaei M. Protective Effect of Royal Jelly against Cyclophosphamide-Induced Thrombocytopenia and Spleen and Bone Marrow Damages in Rats. Cell J. 2020 Oct;22(3):302-309. doi: 10.22074/cellj.2020.6703. Epub 2019 Dec 15. PMID: 31863655; PMCID: PMC6947013.
Chi, H., Chun, K., Son, H., Kim, J., Kim, G., Roh, S. 2013. Effect of genistein administration on the recovery of spermatogenesis in the busulfan-treated rat testis. Clinical Experimental Reproductive Medicine 40(2), 60–66. https://doi.org/10.5653/cerm.2013.40.2.60
Miryan M, Moradi S, Soleimani D, Pasdar Y, Jangjoo A, Bagherniya M, Guest PC, Ashari S, Sahebkar A. The Potential Effect of Royal Jelly on Biomarkers Related to COVID-19 Infection and Severe Progression. Adv Exp Med Biol. 2023;1412:443-455. doi: 10.1007/978-3-031-28012-2_24. PMID: 37378782.
Dehghani F, Sotoude N, Bordbar H, Panjeshahin MR, Karbalay-Doust S. 2018. The use of platelet-rich plasma (PRP) to improve structural impairment of rat testis induced by busulfan, Platelets, DOI:10.1080/09537104.2018.1478400.
Delkhoshe-Kasmaie F, Malekinejad H, Khoramjouy M, Rezaei-Golmisheh A, Janbaze-Acyabar H. 2014. Royal jelly protects from taxol-induced testicular damages via improvement of antioxidant status and up-regulation of E2f1. Syst Biol Reprod Med, 60(2): 80–88. DOI: 10.3109/19396368.2013.852271.
Abdelnour SA, Abd El-Hack ME, Alagawany M, Taha AE, Elnesr SS, Abd Elmonem OM, Swelum AA. Useful impacts of royal jelly on reproductive sides, fertility rate and sperm traits of animals. J Anim Physiol Anim Nutr (Berl). 2020 Nov;104(6):1798-1808. doi: 10.1111/jpn.13303. Epub 2020 Jan 9. PMID: 31916638.
Dumasia K, Kumar A, Kadam L, Balasinor NH. 2015. Effect of estrogen receptor-subtype specific ligands on fertility in adult male rats. J Endocrinol, 225: 169–180. http://dx.doi:joe.endocrinology-journals.org.
Raut S, Kumar AV, Khambata K, Deshpande S, Balasinor NH. Genome-wide identification of estrogen receptor binding sites reveals novel estrogen-responsive pathways in adult male germ cells. Biochem J. 2020 Jun 26;477(12):2115-2131. doi: 10.1042/BCJ20190946. PMID: 32478811.
Jafarian, A., Sadeghi, M. R., Pejhan, N., Salehkhou, S., Lakpour, N., Akhondi, M. M. 2014. Regeneration of spermatogenesis in a mouse model of azoospermia by follicle-stimulating hormone and oestradiol. Andrologia, 46(10), 1098–1106. https://doi.org/10.1111/and.12198.
Kolahian, S., Sadri, H., Larijani, A., Hamidian, G., Davasaz, A. 2016. Supplementation of Diabetic Rats with Leucine, Zinc, and Chromium: Effects on Function and Histological Structure of Testes. International Journal of Vitamin Nutrition Research, 85(5-6), 311-321. https://doi.org/10.1024/0300-9831/a000244.
Zavvari Oskuye Z, Mirzaei Bavil F, Hamidian GR, Mehri K, Qadiri A, Ahmadi M, Oghbaei H, Vatankhah AM, Keyhanmanesh R. Troxerutin affects the male fertility in prepubertal type 1 diabetic male rats. Iran J Basic Med Sci. 2019 Feb;22(2):197-205. doi: 10.22038/ijbms.2018.32678.7814. PMID: 30834086; PMCID: PMC6396992.
Najafi G, Nejati V, Shalizar Jalali A, Zahmatkesh E. 2014. Protective Role of Royal Jelly in Oxymetholone-induced Oxidative Injury in Mouse Testis. Iranian Journal of Toxicology, 8 (25), 1073-1080.
F. Azad (MSc)*1, V. Nejati (PhD)1, A. Shalizar Jalali (PhD)2, Gh. Najafi (PhD)2, F. Rahmani (PhD)1The Protective Effect of Royal Jelly on Testicular Tissue and SpermParameters in Adult Mice Treated with Nicotine.Original Article J Babol Univ Med Sci،Vol 20, Issu 3; Mar 2018. P:50-58
Nagai, T. and Inoue, R. 2004. Preparation and functional properties of water extract and alkaline extract of royal jelly. Food Chem, 84, 181–186.
Shakib Khoob M, Hosseini SM, Kazemi S. In Vitro and In Vivo Antioxidant and Anticancer Potentials of Royal Jelly for Dimethylhydrazine-Induced Colorectal Cancer in Wistar Rats. Oxid Med Cell Longev. 2022 Jul 21;2022:9506026. doi: 10.1155/2022/9506026. PMID: 35910834; PMCID: PMC9334054.
Sakhaee, E., Emadi, L., Abshenas, J., Kheirandish, R., Azari, O., Amiri, E. 2012. Evaluation of epididymal sperm quality following experimentally induced copper poisoning in male rats. Andrologia, 44(Suppl1), 110–116. https://doi.org/10.1111/j.1439-0272.2010.01147.x.
Sarawi WS, Alhusaini AM, Fadda LM, Alomar HA, Albaker AB, Alghibiwi HK, Aljrboa AS, Alotaibi AM, Hasan IH, Mahmoud AM. Nano-Curcumin Prevents Copper Reproductive Toxicity by Attenuating Oxidative Stress and Inflammation and Improving Nrf2/HO-1 Signaling and Pituitary-Gonadal Axis in Male Rats. Toxics. 2022 Jun 30;10(7):356. doi: 10.3390/toxics10070356. PMID: 35878260; PMCID: PMC9316697
Sarkar D, Chowdhury Jayita P, Singh Shio K. 2016. Effect of polybrominated diphenyl ether (BDE-209) on testicular steroidogenesis and spermatogenesis through altered thyroid status in adult mice. Gen Comp Endocrinol, 239, 50–61. http://dx.doi.org/10.1016/j.ygcen.2015.11.009.
Arowolo O, Pilsner JR, Sergeyev O, Suvorov A. Mechanisms of Male ReproductiveToxicity of Polybrominated Diphenyl Ethers. Int J Mol Sci. 2022 Nov:17;23(22):14229. doi: 10.3390/ijms232214229. PMID: 36430706; PMCID: PMC9693139.
Sasso-Cerri, E., Oliveira, B., de Santi, F., Beltrame, F. L., Caneguim, B. H., Cerri, P.S. 2017. The antineoplastic busulphan impairs peritubular and Leydig cells, and vitamin B12 stimulates spermatogonia proliferation and prevents busulfan-induced germ cell death. Biomedicine & Pharmacotherapy, 95, 1619–1630. https://doi.org/10.1016/j.biopha.2017.08.131.
Silici, S., Ekmekcioglu, O., Ersalan, G., Demirtas, S. 2009. Antioxidative effect of royal jelly in cisplatin-induced testes damage. Urology, 74, 545–551.
Zhou W, Bolden-Tiller Olga U, Shao Shan H, Weng Connie C, Shetty G, AbuElhija M, Pakarinen P, Huhtaniemi I, Momin Amin A, Wang J, Stivers David N, Liu Z, Meistrich Marvin L. 2011. Estrogen-Regulated Genes in Rat Testes and Their Relationship to Recovery of Spermatogenesis after Irradiation. Biol Reprod, 85, 823–833. http://dx.doi:10.1095/biolreprod.111.091611