Clinical and Experimental Reproductive Medicine

The Korean Society for Reproductive Medicine (대한생식의학회)
권호 표지
DOI QR코드

DOI QR Code

The effects of Commiphora mukul extract on spermatogenesis and testosterone levels in male diabetic rats

  • Rezaei, Ali Akbar (Neurophysiology Research Center, Hamadan University of Medical Sciences) ;
  • Salehi, Iraj (Neurophysiology Research Center, Hamadan University of Medical Sciences) ;
  • Karimi, Seyed Asaad (Neurophysiology Research Center, Hamadan University of Medical Sciences) ;
  • Rahnama, Mehdi (Department of Physiology, Faculty of Science, Science and Research Branch, Islamic Azad University)
  • Received : 2019.08.04
  • Accepted : 2019.09.29
  • Published : 2020.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Objective: The strong antioxidant activity of Commiphora mukul prompted us to conduct the present study to explore whether treatment with C. mukul extract (CME) would have any protective influence on sperm parameters, testosterone levels, and plasma glucose levels in streptozotocin (STZ)-induced diabetic rats. Methods: Male Wistar rats were randomly divided into four groups: control, control animals treated with CME, diabetic animals, and diabetic animals treated with CME. CME extract (300 mg/kg) was administered for 60 days by daily gavage. Diabetes was induced by an intraperitoneal injection of 50 mg/kg STZ. The epididymal sperm count, weight, motility, morphology, viability, and serum testosterone and glucose levels were determined. Results: In the diabetic animals, CME decreased blood glucose levels (p< 0.05), increased the total sperm count (p< 0.05), and decreased the proportion of sperm with abnormal morphology (p< 0.05). Diabetes reduced sperm motility (p< 0.001), and CME supplementation partially reversed this effect of diabetes (p= 0.003). Furthermore, in diabetic animals, CME decreased the proportion of immotile sperm (p< 0.001). In rats, diabetes caused a significant decrease (p< 0.05) in serum testosterone levels (F[3, 28] = 3.283, p= 0.035), but treatment of diabetic animals with CME increased serum testosterone levels. Conclusion: The present study demonstrated that C. mukul possesses proandrogenic activity and exerts a beneficial effect on sperm parameters in diabetic rats.

Keywords

References

  1. American Diabetes Association. 2. Classification and diagnosis of diabetes. Diabetes Care 2016;39 Suppl 1:S13-22. https://doi.org/10.2337/dc16-S005
  2. La Vignera S, Condorelli R, Vicari E, D'Agata R, Calogero AE. Diabetes mellitus and sperm parameters. J Androl 2012;33:145-53. https://doi.org/10.2164/jandrol.111.013193
  3. Mallidis C, Czerwiec A, Filippi S, O'Neill J, Maggi M, McClure N. Spermatogenic and sperm quality differences in an experimental model of metabolic syndrome and hypogonadal hypogonadism. Reproduction 2011;142:63-71. https://doi.org/10.1530/REP-10-0472
  4. Sexton WJ, Jarow JP. Effect of diabetes mellitus upon male reproductive function. Urology 1997;49:508-13. https://doi.org/10.1016/S0090-4295(96)00573-0
  5. Volpe CM, Villar-Delfino PH, Dos Anjos PM, Nogueira-Machado JA. Cellular death, reactive oxygen species (ROS) and diabetic complications. Cell Death Dis 2018;9:119. https://doi.org/10.1038/s41419-017-0135-z
  6. Agarwal A. Role of oxidative stress in male infertility and antioxidant supplementation. US Kidney Urol Dis 2005;122.
  7. Agbaje IM, Rogers DA, McVicar CM, McClure N, Atkinson AB, Mallidis C, et al. Insulin dependant diabetes mellitus: implications for male reproductive function. Hum Reprod 2007;22:1871-7. https://doi.org/10.1093/humrep/dem077
  8. Mangoli E, Talebi AR, Anvari M, Pourentezari M. Effects of experimentally-induced diabetes on sperm parameters and chromatin quality in mice. Iran J Reprod Med 2013;11:53-60.
  9. Aitken RJ, Baker MA. Oxidative stress, sperm survival and fertility control. Mol Cell Endocrinol 2006;250:66-9. https://doi.org/10.1016/j.mce.2005.12.026
  10. Lewis SE. Is sperm evaluation useful in predicting human fertility? Reproduction 2007;134:31-40. https://doi.org/10.1530/REP-07-0152
  11. Hughes CM, Lewis SE, McKelvey-Martin VJ, Thompson W. The effects of antioxidant supplementation during Percoll preparation on human sperm DNA integrity. Hum Reprod 1998;13:1240-7. https://doi.org/10.1093/humrep/13.5.1240
  12. Bahmanzadeh M, Vahidinia A, Mehdinejadiani S, Shokri S, Alizadeh Z. Dietary supplementation with astaxanthin may ameliorate sperm parameters and DNA integrity in streptozotocin-induced diabetic rats. Clin Exp Reprod Med 2016;43:90-6. https://doi.org/10.5653/cerm.2016.43.2.90
  13. Ahangarpour A, Oroojan AA, Radan M. Effect of aqueous and hydro-alcoholic extracts of lettuce (Lactuca sativa) seed on testosterone level and spermatogenesis in NMRI mice. Iran J Reprod Med 2014;12:65-72.
  14. Bellamkonda R, Rasineni K, Singareddy SR, Kasetti RB, Pasurla R, Chippada AR, et al. Antihyperglycemic and antioxidant activities of alcoholic extract of Commiphora mukul gum resin in streptozotocin induced diabetic rats. Pathophysiology 2011;18:255-61. https://doi.org/10.1016/j.pathophys.2010.10.002
  15. Urizar NL, Moore DD. GUGULIPID: a natural cholesterol-lowering agent. Annu Rev Nutr 2003;23:303-13. https://doi.org/10.1146/annurev.nutr.23.011702.073102
  16. Institute of Laboratory Animal Resources (US), Committee on Care and Use of Laboratory Animals, National Institutes of Health (US), Division of Research Resources. Guide for the care and use of laboratory animals. Bethesda, MD: U.S. Department of Health and Human Services, Public Health Service, National Insititutes of Health; 1985.
  17. Salehi I, Taheraslani Z, Moradkhani S. Hydro-alcoholic extract of Commiphora mukul gum resin may improve cognitive impairments in diabetic rats. Avicenna J Med Biochem 2014;2:e24906.
  18. Moradkhani S, Salehi I, Abdolmaleki S, Komaki A. Effect of Calendula officinalis hydroalcoholic extract on passive avoidance learning and memory in streptozotocin-induced diabetic rats. Anc Sci Life 2015;34:156-61. https://doi.org/10.4103/0257-7941.157160
  19. Omidi G, Karimi SA, Rezvani-Kamran A, Monsef A, Shahidi S, Komaki A. Effect of coenzyme Q10 supplementation on diabetes induced memory deficits in rats. Metab Brain Dis 2019;34:833-40. https://doi.org/10.1007/s11011-019-00402-7
  20. Gheibi S, Jeddi S, Carlstrom M, Gholami H, Ghasemi A. Effects of long-term nitrate supplementation on carbohydrate metabolism, lipid profiles, oxidative stress, and inflammation in male obese type 2 diabetic rats. Nitric Oxide 2018;75:27-41. https://doi.org/10.1016/j.niox.2018.02.002
  21. Ramesh B, Karuna R, Sreenivasa Reddy S, Sudhakara G, Saralakumari D. Ethanolic extract of Commiphora mukul gum resin attenuates streptozotocin-induced alterations in carbohydrate and lipid metabolism in rats. EXCLI J 2013;12:556-68.
  22. Seed J, Chapin RE, Clegg ED, Dostal LA, Foote RH, Hurtt ME, et al. Methods for assessing sperm motility, morphology, and counts in the rat, rabbit, and dog: a consensus report. ILSI Risk Science Institute Expert Working Group on Sperm Evaluation. Reprod Toxicol 1996;10:237-44. https://doi.org/10.1016/0890-6238(96)00028-7
  23. Narayana K, Prashanthi N, Nayanatara A, Kumar HH, Abhilash K, Bairy KL. Effects of methyl parathion (o,o-dimethyl o-4-nitrophenyl phosphorothioate) on rat sperm morphology and sperm count, but not fertility, are associated with decreased ascorbic acid level in the testis. Mutat Res 2005;588:28-34. https://doi.org/10.1016/j.mrgentox.2005.08.012
  24. Bahmanzadeh M, Abolhasani F, Amidi F, Ejtemaeimehr S, Salehnia M, Abasi M. The effects of nitric oxide synthase inhibitor (L-NAME) on epididymal sperm count, motility, and morphology in varicocelized rat. DARU 2008;16:23-8.
  25. La Vignera S, Vicari E, Condorelli R, D'Agata R, Calogero AE. Ultrasound characterization of the seminal vesicles in infertile patients with type 2 diabetes mellitus. Eur J Radiol 2011;80:e64-7. https://doi.org/10.1016/j.ejrad.2010.08.001
  26. Ding GL, Liu Y, Liu ME, Pan JX, Guo MX, Sheng JZ, et al. The effects of diabetes on male fertility and epigenetic regulation during spermatogenesis. Asian J Androl 2015;17:948-53. https://doi.org/10.4103/1008-682X.150844
  27. Jangir RN, Jain GC. Diabetes mellitus induced impairment of male reproductive functions: a review. Curr Diabetes Rev 2014;10:147-57. https://doi.org/10.2174/1573399810666140606111745
  28. Karimi J, Goodarzi MT, Tavilani H, Khodadadi I, Amiri I. Increased receptor for advanced glycation end products in spermatozoa of diabetic men and its association with sperm nuclear DNA fragmentation. Andrologia 2012;44 Suppl 1:280-6. https://doi.org/10.1111/j.1439-0272.2011.01178.x
  29. Shrilatha B, Muralidhara. Early oxidative stress in testis and epididymal sperm in streptozotocin-induced diabetic mice: its progression and genotoxic consequences. Reprod Toxicol 2007;23:578-87. https://doi.org/10.1016/j.reprotox.2007.02.001
  30. Hisatomi A, Sakuma S, Fujiwara M, Seki J. Effect of tacrolimus on the cauda epididymis in rats: analysis of epididymal biochemical markers or antioxidant defense enzymes. Toxicology 2008;243:23-30. https://doi.org/10.1016/j.tox.2007.09.017
  31. Barve K. Herbs in the treatment of diabetes induced erectile dysfunction. J Pharm Phytother 2013;1:2-8.
  32. Matsuda H, Morikawa T, Ando S, Oominami H, Murakami T, Kimura I, et al. Absolute stereostructures of polypodane-type triterpenes, myrrhanol A and myrrhanone A, from guggul-gum resin (the resin of Balsamodendron mukul). Chem Pharm Bull (Tokyo) 2004;52:1200-3. https://doi.org/10.1248/cpb.52.1200
  33. Jasuja ND, Choudhary J, Sharma P, Sharma N, Joshi SC. A review on bioactive compounds and medicinal uses of Commiphora mukul. J Plant Sci 2012;7:113-37. https://doi.org/10.3923/jps.2012.113.137
  34. Cornick CL, Strongitharm BH, Sassano G, Rawlins C, Mayes AE, Joseph AN, et al. Identification of a novel agonist of peroxisome proliferator-activated receptors alpha and gamma that may contribute to the anti-diabetic activity of guggulipid in Lep(ob)/Lep(ob) mice. J Nutr Biochem 2009;20:806-15. https://doi.org/10.1016/j.jnutbio.2008.07.010
  35. Huang TH, Teoh AW, Lin BL, Lin DS, Roufogalis B. The role of herbal PPAR modulators in the treatment of cardiometabolic syndrome. Pharmacol Res 2009;60:195-206. https://doi.org/10.1016/j.phrs.2009.03.020
  36. Sharma B, Salunke R, Srivastava S, Majumder C, Roy P. Effects of guggulsterone isolated from Commiphora mukul in high fat diet induced diabetic rats. Food Chem Toxicol 2009;47:2631-9. https://doi.org/10.1016/j.fct.2009.07.021
  37. Bellamkonda R, Karuna R, Sasi Bhusana Rao B, Haritha K, Manjunatha B, Silpa S, et al. Beneficiary effect of Commiphora mukul ethanolic extract against high fructose diet induced abnormalities in carbohydrate and lipid metabolism in wistar rats. J Tradit Complement Med 2017;8:203-11.
  38. Ramesh B, Karuna R, Sreenivasa RS, Haritha K, Sai MD, Sasi BR, et al. Effect of Commiphora mukul gum resin on hepatic marker enzymes, lipid peroxidation and antioxidants status in pancreas and heart of streptozotocin induced diabetic rats. Asian Pac J Trop Biomed 2012;2:895-900. https://doi.org/10.1016/S2221-1691(12)60249-4
  39. Mahmoud AM, Alqahtani S, Othman SI, Germoush MO, Hussein OE, Al-Basher G, et al. Commiphora molmol modulates glutamate-nitric oxide-cGMP and Nrf2/ARE/HO-1 pathways and attenuates oxidative stress and hematological alterations in hyperammonemic rats. Oxid Med Cell Longev 2017;2017:7369671.
  40. De Lamirande E, Leclerc P, Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 1997;3:175-94. https://doi.org/10.1093/molehr/3.3.175
  41. Sikka SC. Oxidative stress and role of antioxidants in normal and abnormal sperm function. Front Biosci 1996;1:e78-86. https://doi.org/10.2741/A146
  42. Paick JS. Role of reactive oxygen species in male infertility. Korean J Androl 2003;21:1-11.
  43. Sharma RK, Agarwal A. Role of reactive oxygen species in male infertility. Urology 1996;48:835-50. https://doi.org/10.1016/S0090-4295(96)00313-5
  44. Rao RM, Khan ZA, Shah AH. Toxicity studies in mice of Commiphora molmol oleo-gum-resin. J Ethnopharmacol 2001;76:151-4. https://doi.org/10.1016/S0378-8741(01)00189-1
  45. Shah AH, Al-Shareef AH, Ageel AM, Qureshi S. Toxicity studies in mice of common spices, Cinnamomum zeylanicum bark and Piper longum fruits. Plant Foods Hum Nutr 1998;52:231-9. https://doi.org/10.1023/A:1008088323164