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Protective efficacy of Nerium oleander extract on spermatogenesis in streptozotocin-induced diabetic rats

Published online by Cambridge University Press:  29 January 2024

Afrooz Karimi
Affiliation:
Department of Radiology, School of Paramedical Sciences, Shiraz University of Medical Sciences, Shiraz, Iran
Farhad Kohpeyma
Affiliation:
Endocrine and Metabolism Research Center, Shiraz University of Medical Science, Shiraz, Iran
Ebrahim Asadi
Affiliation:
Department of Biology, University of Saskatchewan, Saskatoon, SK S7N 5E2, Canada
Maryam ziyaee
Affiliation:
Abadan University of Medical Science, Abadan, Iran
Samaneh Karimi*
Affiliation:
Department of Anatomical Sciences, School of Medicine, Abadan University of Medical Sciences, Abadan, Iran
*
Corresponding author: Samaneh Karimi; Emails: Samaneh_k_500@yahoo.com;s.karimi@abadanums.ac.ir

Summary

Men with diabetes frequently experience spermatogenic dysfunction, which is the most significant sign that diabetes has harmed their ability to reproduce. The effect of various doses of the hydro-alcoholic extract of Nerium oleander leaves on the pituitary–gonadal axis, sperm motility and number, antioxidant system, changes in testicular tissue structure, and spermatogenesis in healthy and diabetic rats has been examined in the current study. Eighty male rats that had been streptozotocin-induced diabetic and healthy were divided into eight groups: (1) control, (2) Nerium (50 mg/kg), (3) Nerium (100 mg/kg), (4) Nerium (200 mg/kg), (5) DM (6) DM+Nerium (50 mg/kg), (7) DM+Nerium (100 mg/kg) and (8) DM+Nerium (200 mg/kg) and were administered orally for 48 days consecutive. Following the studies, analysis of the testicular tissues’ antioxidant capacity as well as sperm parameters, Johnsen’s scoring and morphometric evaluation, histology, biochemical and stereology studies were performed.

The outcomes showed that Nerium 50 and 100 mg/kg considerably enhanced the testicular morphology, sperm parameters, and reproductive organs to varying degrees in diabetic rats. After Nerium 50 mg/kg administration, glutathione peroxidase (GPX) and catalase (CAT) levels in the testicular tissue were increased whereas malondialdehyde (MDA) levels were markedly decreased. Nerium may help protect against diabetic-induced spermatogenic dysfunction in male rats by enhancing the activities of antioxidant enzymes in lower dosages.

Type
Research Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press

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References

Agarwal, A., Mulgund, A., Alshahrani, S., Assidi, M., Abuzenadah, A. M., Sharma, R. and Sabanegh, E. (2014). Reactive oxygen species and sperm DNA damage in infertile men presenting with low level leukocytospermia. Reproductive Biology and Endocrinology: RB&E, 12, 126. doi: 10.1186/1477-7827-12-126 CrossRefGoogle ScholarPubMed
Anastasiou, I. A., Eleftheriadou, I., Tentolouris, A., Koliaki, C., Kosta, O. A. and Tentolouris, N. (2021). The effect of oxidative stress and antioxidant therapies on pancreatic β-cell dysfunction: Results from in vitro and in vivo studies. Current Medicinal Chemistry, 28(7), 13281346. doi: 10.2174/0929867327666200526135642 CrossRefGoogle ScholarPubMed
Anwar, S., Khan, S., Almatroudi, A., Khan, A. A., Alsahli, M. A., Almatroodi, S. A. and Rahmani, A. H. (2021). A review on mechanism of inhibition of advanced glycation end products formation by plant derived polyphenolic compounds. Molecular Biology Reports, 48(1), 787805. doi: 10.1007/s11033-020-06084-0 CrossRefGoogle ScholarPubMed
Armagan, A., Uz, E., Yilmaz, H. R., Soyupek, S., Oksay, T. and Ozcelik, N. (2006). Effects of melatonin on lipid peroxidation and antioxidant enzymes in streptozotocin-induced diabetic rat testis. Asian Journal of Andrology, 8(5), 595600. doi: 10.1111/j.1745-7262.2006.00177.x CrossRefGoogle ScholarPubMed
Barku, V. Y. A. (2019). Wound healing: Contributions from plant secondary metabolite antioxidants. In Wound Healing – Current Perspectives. Dogan, K. H. (ed.). IntechOpen. doi: 10.5772/intechopen.81208 Google Scholar
Bas, A. L., Demirci, S., Yazihan, N., Uney, K. and Ermis Kaya, E. E. (2012). Nerium oleander distillate improves fat and glucose metabolism in high-fat diet-fed streptozotocin-induced diabetic rats. International Journal of Endocrinology, 2012, 947187. doi: 10.1155/2012/947187 CrossRefGoogle ScholarPubMed
Bondy, S. C. (2023). The hormesis concept: Strengths and shortcomings. Biomolecules, 13(10), 1512. doi: 10.3390/biom13101512 CrossRefGoogle ScholarPubMed
Chainy, G. B. N. and Sahoo, D. K. (2020). Hormones and oxidative stress: An overview. Free Radical Research, 54(1), 126. doi: 10.1080/10715762.2019.1702656 CrossRefGoogle ScholarPubMed
Cheng, Y., Yang, Z., Shi, J., Yang, J., Zhao, J., He, Y. and Qi, M. (2020). Total flavonoids of Epimedium ameliorates testicular damage in streptozotocin-induced diabetic rats by suppressing inflammation and oxidative stress. Environmental Toxicology, 35(2), 268276. doi: 10.1002/tox.22864 CrossRefGoogle ScholarPubMed
Das, B., Biswas, B., Ghosh, A., Pakhira, B. P. and Ghosh, D. (2017). Ameliorative role of ethyl-acetate fraction of methanolic leaf extract of Camellia sinensis (green tea) on streptozotocin-induced diabetes linked testicular hypofunction in albino rat: A dose-dependent biochemical and genomic transection study. Journal of Complementary and Integrative Medicine, 14(4), 20160084. doi: 10.1515/jcim-2016-0084 CrossRefGoogle Scholar
Dey, P., Dutta, S., Biswas-Raha, A., Sarkar, M. P. and Chaudhuri, T. K. (2016). Haloalkane induced hepatic insult in murine model: Amelioration by oleander through antioxidant and anti-inflammatory activities, an in vitro and in vivo study. BMC Complementary and Alternative Medicine, 16(1), 280. doi: 10.1186/s12906-016-1260-4 CrossRefGoogle ScholarPubMed
Dey, P., Saha, M. R., Chowdhuri, S. R., Sen, A., Sarkar, M. P., Haldar, B. and Chaudhuri, T. K. (2015). Assessment of anti-diabetic activity of an ethnopharmacological plant Nerium oleander through alloxan induced diabetes in mice. Journal of Ethnopharmacology, 161, 128137. doi: 10.1016/j.jep.2014.12.012 CrossRefGoogle ScholarPubMed
Dey, P., Saha, M. R., Roy Choudhuri, S., Sarkar, I., Halder, B., Poddar-Sarkar, M., Sen, A. and Chaudhuri, T. K. (2019). Oleander stem and root standardized extracts mitigate acute hyperglycaemia by limiting systemic oxidative stress response in diabetic mice. Advances in Pharmacological Sciences, 2019, 7865359. doi: 10.1155/2019/7865359 CrossRefGoogle ScholarPubMed
Ellman, G. L. (1959). Tissue sulfhydryl groups. Archives of Biochemistry and Biophysics, 82(1), 7077. doi: 10.1016/0003-9861(59)90090-6 CrossRefGoogle ScholarPubMed
Forouzandeh, H. and Ghavamizadeh, M. (2020 ). Protective effects of zinc supplement on chromatin deficiency and sperm parameters in streptozotocin-induced diabetic rats. International Medical Journal, 27(5), 545.Google Scholar
Ghaffari, R., Di Bona, K. R., Riley, C. L. and Richburg, J. H. (2019). Copper transporter 1 (CTR1) expression by mouse testicular germ cells, but not Sertoli cells, is essential for functional spermatogenesis. PLOS ONE, 14(4), e0215522. doi: 10.1371/journal.pone.0215522 CrossRefGoogle Scholar
Goodson, S. G., Zhang, Z., Tsuruta, J. K., Wang, W. and O'Brien, D. A. (2011). Classification of mouse sperm motility patterns using an automated multiclass support vector machines model. Biology of Reproduction, 84(6), 12071215. doi: 10.1095/biolreprod.110.088989 CrossRefGoogle ScholarPubMed
Hajshafiha, M., Ghareaghaji, R., Salemi, S., Sadegh-Asadi, N. and Sadeghi-Bazargani, H. (2013). Association of body mass index with some fertility markers among male partners of infertile couples. International Journal of General Medicine, 6, 447451. doi: 10.2147/IJGM.S41341 Google ScholarPubMed
Han, X. X., Jiang, Y.-P. J., Liu, N., Wu, J., Yang, J. M., Li, Y.-X., Sun, M., Sun, T., Zheng, P. and Jian-qiang, Y. (2019). Protective effects of astragalin on spermatogenesis in streptozotocin-induced diabetes in male mice by improving antioxidant activity and inhibiting inflammation. Biomedicine and Pharmacotherapy, 110, 561570. doi: 10.1016/j.biopha.2018.12.012 CrossRefGoogle ScholarPubMed
Hong, X., Shao, N., Yin, L., Li, C., Tao, G., Sun, Y., Qian, K., Yang, J., Xiao, P., Yu, X. and Zhou, Z. (2022). Exposure to zinc oxide nanoparticles affects testicular structure, reproductive development and spermatogenesis in parental and offspring male rats. Annals of Translational Medicine, 10(13), 751. doi: 10.21037/atm-22-3047 CrossRefGoogle ScholarPubMed
Johnsen, S. G. (1970). Testicular biopsy score count--a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males. Hormones, 1, 225.Google ScholarPubMed
Khordad, E., Nikravesh, M. R., Jalali, M., Fazel, A. R., Sankian, M. and Alipour, F. (2020). Diabetes up-regulated collagen IV and laminin α5 genes in mRNA and protein levels in seminiferous tubules of C57BL/6 adult mice. Cellular and Molecular Biology, 66(5), 162168. doi: 10.14715/cmb/2020.66.5.28 CrossRefGoogle ScholarPubMed
Kolettis, P. N., Ross, J. H., Kay, R. and Thomas, A. J. (1999). Sperm retrieval and intracytoplasmic sperm injection in patients with prune-belly syndrome. Fertility and Sterility, 72, 948949.CrossRefGoogle ScholarPubMed
Koroliuk, M. A., Ivanova, L. I., Ma&ibreve;orova, I. G. and Tokarev, V. E. (1988). A method of determining catalase activity. Laboratornoe Delo, (1), 1619.Google ScholarPubMed
Kumar, M. (2019). Triterpenoids of Nerium oleander shows antifertility effect in male albino rats. Journal of Advanced Laboratory Research in Biology, 10(4), 104110.Google Scholar
Liu, H., Lin, S., Lv, Q., Yang, Q., Wu, G., Hu, J. and Yang, J. (2017). Taurine recovers testicular steroidogenesis and spermatogenesis in streptozotocin-induced diabetic rats. In 10 (Springer). Advances in Experimental Medicine and Biology, 801811. doi: 10.1007/978-94-024-1079-2_62 CrossRefGoogle Scholar
Maciejewski, R., Radzikowska-Büchner, E., Flieger, W., Kulczycka, K., Baj, J., Forma, A. and Flieger, J. (2022). An overview of essential microelements and common metallic nanoparticles and their effects on male fertility. International Journal of Environmental Research and Public Health, 19(17), 11066. doi: 10.3390/ijerph191711066 CrossRefGoogle ScholarPubMed
Maiorino, M. I., Bellastella, G. and Esposito, K. (2014). Diabetes and sexual dysfunction: Current perspectives. Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy, 7, 95105. doi: 10.2147/DMSO.S36455 Google ScholarPubMed
Mardanshahi, T., Rezaei, N., Zare, Z., Malekzadeh Shafaroudi, M. M. and Mohammadi, H. (2019). Effects of L-carnitine on the sperm parameters disorders, apoptosis of spermatogenic cells and testis histopathology in diabetic Rats. International Journal of Reproductive Biomedicine, 17(5), 325336. doi: 10.18502/ijrm.v17i5.4600 Google ScholarPubMed
Maresch, C. C., Stute, D. C., Alves, M. G., Oliveira, P. F., de Kretser, D. M. and Linn, T. (2018). Diabetes-induced hyperglycemia impairs male reproductive function: A systematic review. Human Reproduction Update, 24(1), 86105. doi: 10.1093/humupd/dmx033 CrossRefGoogle ScholarPubMed
Ohkawa, H., Ohishi, N. and Yagi, K. (1979). Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95(2), 351358. doi: 10.1016/0003-2697(79)90738-3 CrossRefGoogle ScholarPubMed
Pereira, S. C., Oliveira, P. F., Oliveira, S. R., Pereira, M. L. and Alves, M. G. (2021). Impact of environmental and lifestyle use of chromium on male fertility: Focus on antioxidant activity and oxidative stress. Antioxidants, 10(9), 1365. doi: 10.3390/antiox10091365 CrossRefGoogle ScholarPubMed
Rodríguez De Luna, S. L., Ramírez-Garza, R. E. and Serna Saldívar, S. O. (2020). Environmentally friendly methods for flavonoid extraction from plant material: impact of their operating conditions on yield and antioxidant properties. The Scientific World Journal, 2020, 6792069. doi: 10.1155/2020/6792069 CrossRefGoogle ScholarPubMed
Rohayem, J., Zitzmann, M., Laurentino, S., Kliesch, S., Nieschlag, E., Holterhus, P.-M. and Kulle, A. (2021). The role of gonadotropins in testicular and adrenal androgen biosynthesis pathways-Insights from males with congenital hypogonadotropic hypogonadism on hCG/rFSH and on testosterone replacement. Clinical Endocrinology, 94(1), 90101. doi: 10.1111/cen.14324 CrossRefGoogle ScholarPubMed
Roshankhah, S., Jalili, C. and Salahshoor, M. R. (2019). Effects of crocin on sperm parameters and seminiferous tubules in diabetic rats. Advanced Biomedical Research, 8, 4. doi: 10.4103/abr.abr_124_18 Google ScholarPubMed
Sathyaseelan, L., Thodi, R. C. and Sukumaran, S. T. (2020). Ethnomedicine and role of plant metabolites. In: Sukumaran, S. T., Sugathan, S., Abdulhameed, S. (eds) Plant Metabolites: Methods, Applications and Prospects. Springer, Singapore. doi: 10.1007/978-981-15-5136-9_9 Google Scholar
Shi, G. J., Zheng, J., Wu, J., Qiao, H. Q., Chang, Q., Niu, Y., Sun, T., Li, Y. X. and Yu, J. Q. (2017). Beneficial effects of Lycium barbarum polysaccharide on spermatogenesis by improving antioxidant activity and inhibiting apoptosis in streptozotocin-induced diabetic male mice. Food and Function, 8(3), 12151226. doi: 10.1039/c6fo01575a CrossRefGoogle ScholarPubMed
Sikarwar, M. S., Patil, M. B., Kokate, C. K., Sharma, S. and Bhat, V. (2009). Antidiabetic activity of Nerium indicum leaf extract in alloxan-induced diabetic rats. Journal of Young Pharmacists, 1(4), 330. doi: 10.4103/0975-1483.59323 CrossRefGoogle Scholar
Sudharshan, S. J., Krishna Narayanan, A., Princilly, J., Dyavaiah, M. and Nagegowda, D. A. (2022). Betulinic acid mitigates oxidative stress-mediated apoptosis and enhances longevity in the yeast Saccharomyces cerevisiae model. Free Radical Research, 56(11-12), 699712. doi: 10.1080/10715762.2023.2166505 CrossRefGoogle ScholarPubMed
Sun, X., Wu, B., Geng, L., Zhang, J. and Qin, G. (2021). Xiaokang Liuwei Dihuang decoction ameliorates the immune infertility of male rats induced by lipopolysaccharide through regulating the levels of sex hormones, reactive oxygen species, pro-apoptotic and immune factors. Biomedicine and Pharmacotherapy, 139, 111514. doi: 10.1016/j.biopha.2021.111514 CrossRefGoogle ScholarPubMed
Zhao, L., Zhao, J., Dong, Z., Xu, S. and Wang, D. (2023). Mechanisms underlying impaired spermatogenic function in orchitis induced by busulfan. Reproductive Toxicology (Elmsford, N.Y.), 115, 17. doi: 10.1016/j.reprotox.2022.11.002 CrossRefGoogle ScholarPubMed
Zhu, Z., Kawai, T., Umehara, T., Hoque, S. A. M., Zeng, W. and Shimada, M. (2019). Negative effects of ROS generated during linear sperm motility on gene expression and ATP generation in boar sperm mitochondria. Free Radical Biology and Medicine, 141, 159171. doi: 10.1016/j.freeradbiomed.2019.06.018 CrossRefGoogle ScholarPubMed