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:: Volume 28, Issue 3 (Scientific Journal of Kurdistan University of Medical Sciences 2023) ::
SJKU 2023, 28(3): 37-47 Back to browse issues page
Improvement of Sperm Parameters and Oxidative Stress by N-acetyl-cysteine in Adult Male Mice Treated with Zinc Oxide Nanoparticles
Niloufar Darbandi1 , Monireh Mahmoodi2 , Zahra Khosravi3
1- Asistant Professor, Department of Biology, Faculty of Sciences, Arak University, Arak, Iran
2- Asistant Professor, Department of Biology, Faculty of Sciences, Arak University, Arak, Iran. , m-mahmoodi@araku.ac.ir
3- Master of Science, Department of Biology, Faculty of Sciences, Arak University, Arak, Iran.
Abstract:   (1574 Views)
Background and Aim:  Zinc oxide nanoparticles are one of the nanoscale materials that by inducing the production of reactive oxygen species, DNA damage and apoptosis may have cytotoxic effects on the reproductive system and endanger male fertility. In the present study, we investigated the antioxidant effect of N-acetylcysteine on sperm and biochemical parameters in mice treated with zinc oxide nanoparticles.
Materials and Methods: 24 adult male NMRI mice with average weight (35.45 ± 2.11 g) were randomly divided into four groups (n = 6) of control, zinc oxide nanoparticles (50 mg/kg), N-acetylcysteine (150 mg/kg) and N-acetylcysteine + zinc oxide nanoparticles and treated intraperitoneally for 28 days. Then the mice were anesthetized and their left epididymis was used to evaluate sperm parameters (number, motility and viability). In addition, serum levels of testosterone, LH and FSH, malondialdehyde and total antioxidant capacity were measured. Using SPSS software, data were analyzed by one-way analysis of variance and Tukey's test. Differences among mean values were considered significant at p<0.05.
Results: We observed a significant decrease in the number, percentage of progressive motility and sperm viability, total antioxidant capacity, serum levels of testosterone, LH and FSH in the zinc oxide nanoparticles group compared to those in the control group (p<0.001). While the plasma malondialdehyde level showed a significant increase (p<0.001). Simultaneous treatment with N-acetylcysteine and zinc oxide nanoparticles improved the above parameters significantly. In N-acetylcysteine group, no significant difference was observed in these parameters compared to the control group (p<0.05).
Conclusion: These findings showed that acetylcysteine has a protective role against the destructive effects of zinc oxide nanoparticles on sperm parameters and biochemical factors by reducing oxidative stress, increasing the level of total antioxidant capacity and testosterone levels.
 
Keywords: N-acetylcysteine, Sex hormones, Sperm, Zinc oxide nanoparticles.
Full-Text [PDF 1295 kb]   (478 Downloads)    
Type of Study: Original Research | Subject: Biology of Reproduction
Received: 2022/09/5 | Accepted: 2023/01/18 | Published: 2023/07/31
References
1. 1. Yang D, Zhang M, Gan Y, Yang S, Wang J, Yu M, et al. Involvement of oxidative stress in ZnO NPs-induced apoptosis and autophagy of mouse GC-1 spg cells. Ecotoxicology and Environmental Safety. 2020;202:110960. [DOI:10.1016/j.ecoenv.2020.110960] [PMID]
2. Pinho AR, Rebelo S, Pereira MD. The impact of zinc oxide nanoparticles on male (in) fertility. Materials. 2020;13(4):849. [DOI:10.3390/ma13040849] [PMID] []
3. Tang Y, Chen B, Hong W, Chen L, Yao L, Zhao Y, et al. ZnO nanoparticles induced male reproductive toxicity based on the effects on the endoplasmic reticulum stress signaling pathway. International Journal of Nanomedicine. 2019;14:9563-76. [DOI:10.2147/IJN.S223318] [PMID] []
4. Mozaffari Z, Parivar K, Roodbari NH, Irani S. Histopathological evaluation of the toxic effects of zinc oxide (ZnO) nanoparticles on testicular tissue of NMRI adult mice. Adv. Stud. Biol. 2015;7(6):275-91. [DOI:10.12988/asb.2015.5425]
5. Han Z, Yan Q, Ge W, Liu ZG, Gurunathan S, De Felici M, et al. Cytotoxic effects of ZnO nanoparticles on mouse testicular cells. International Journal of Nanomedicine. 2016;11:5187-5203. [DOI:10.2147/IJN.S111447] [PMID] []
6. Talebi AR, Khorsandi L, Moridian M. The effect of zinc oxide nanoparticles on mouse spermatogenesis. Journal of assisted reproduction and genetics. 2013;30(9):1203-9. [DOI:10.1007/s10815-013-0078-y] [PMID] []
7. Gholamloo M, Jafari M. Study of Effect of N-Acetyl Cysteine on Reduction of Paraoxon-Induced Oxidative Stress in Brain and Heart Tissues. Health Research. 2017;2(2):77-85. [DOI:10.18869/acadpub.hrjbaq.2.2.77]
8. Kheradmandi R, Jorsaraei SG, Feizi F, Moghadamnia AA, Neamati N. Protective effect of N-acetyl cysteine on chlorpyrifos-induced testicular toxicity in mice. International journal of fertility & sterility. 2019;13(1):51-6.
9. Jannatifar R, Parivar K, Roodbari NH, Nasr-Esfahani MH. Effects of N-acetyl-cysteine supplementation on sperm quality, chromatin integrity and level of oxidative stress in infertile men. Reproductive Biology and Endocrinology. 2019;17(1):1-9. [DOI:10.1186/s12958-019-0468-9] [PMID] []
10. El-Maddawy ZK, El-Sayed YS. Comparative analysis of the protective effects of curcumin and N-acetyl cysteine against paracetamol-induced hepatic, renal, and testicular toxicity in Wistar rats. Environmental science and pollution research. 2018;25(4):3468-79. [DOI:10.1007/s11356-017-0750-3] [PMID]
11. Darbandi N, Khosravi S, Momeni HR. Effect of N-acetyl- cysteine on memory retrieval, hippocampal CA1 pyramidal neurons and some blood serum oxidative Stress factors in Male wistar Rats treated with zinc oxide nanoparticles. The Journal of Urmia University of Medical Sciences. 2018;29(6):450-63.
12. Abbasalipourkabir R, Moradi H, Zarei S, Asadi S, Salehzadeh A, Ghafourikhosroshahi A, Mortazavi M, Ziamajidi N. Toxicity of zinc oxide nanoparticles on adult male Wistar rats. Food and chemical toxicology. 2015;84:154-60. [DOI:10.1016/j.fct.2015.08.019] [PMID]
13. Feng D, Huang H, Yang Y, Yan T, Jin Y, Cheng X., Cui L. Ameliorative effects of N-acetylcysteine on fluoride-induced oxidative stress and DNA damage in male rats' testis. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2015;792:35-45. [DOI:10.1016/j.mrgentox.2015.09.004] [PMID]
14. Maheshwari A, Misro M, Aggarwal A, Sharma RK. N-acetyl-L-cysteine modulates multiple signaling pathways to rescue male germ cells from apoptosis induced by chronic hCG administration to rats. Apoptosis. 2012;17(6):551-65. [DOI:10.1007/s10495-012-0703-8] [PMID]
15. Kumari M, Singh P, Study on the reproductive organs and fertility of the male mice following administration of metronidazole. International journal of Fertility & Sterility. 2013; 7(3):225-38.‌
16. Mahmoodi M, Soleimani Mehranjani M, Kheradmand N. Protective Effect of Pentoxifylline on Sperm and Biochemical Parameters against Dexamethasone-Induced Toxicity in Mice. Journal of Mazandaran University of Medical Sciences. 2020;30(185):113-24.
17. Hassanzadeh A, Shahvaisi K, Hassanzadeh K, Izadpanah E, Amini A, Moloudi MR. Effects of rebamipide and encapsulating rebamipide with chitosan capsule on inflammatory mediators in rat experimental colitis. Scientific journal of Kurdistan university of medical sciences. 2015;20(3):94-104.
18. Shen J, Yang D, Zhou X, Wang Y, Tang S, Yin H, et al. Role of autophagy in zinc oxide Nanoparticles-induced apoptosis of mouse LEYDIG cells. International journal of molecular sciences. 2019; 20(16):4042. [DOI:10.3390/ijms20164042] [PMID] []
19. Srivastav AK, Kumar A, Prakash J, Singh D, Jagdale P, Shankar J, et al. Genotoxicity evaluation of zinc oxide nanoparticles in Swiss mice after oral administration using chromosomal aberration, micronuclei, semen analysis, and RAPD profile. Toxicology and Industrial Health. 2017;33(11):821-34. [DOI:10.1177/0748233717717842] [PMID]
20. Abbasalipourkabir R, Moradi H, Zarei S, Asadi S, Salehzadeh A, Ghafourikhosroshahi A. et al. Toxicity of zinc oxide nanoparticles on adult male Wistar rats. Food and chemical toxicology. 2015;84:154-60. [DOI:10.1016/j.fct.2015.08.019] [PMID]
21. Javadi A, Mokhtar S, Azimirad R, Esfandiari F, Gourabi H. Mechanisms of the Effects of Zinc Oxide Nanostructures on Living Cells. Journal of Fasa University of Medical Sciences. 2020;10(1):1998-2011.
22. Tremellen K. Oxidative stress and male infertility-a clinical perspective. Human reproduction update. 2008;14(3):243-58. [DOI:10.1093/humupd/dmn004] [PMID]
23. Nashwa A, Kawkab AA, Mouneir SM. The protective effect of ginger and N-acetyl cysteine on ciprofloxacin-induced reproductive toxicity in male rats. Journal of American Science. 2011;7(7):741-52.
24. Khoshtabiat L, Mahdavi M. The role of oxidative stress in proliferation and cell death. Journal of Mazandaran University of Medical Sciences. 2015;25(127):130-145.
25. Ozaras R, Tahan V, Aydin S, Uzun H, Kaya S, Senturk H. N-acetylcysteine attenuates alcohol-induced oxidative stress in he rat. World Journal of Gastroenterology. 2003;9(1):125. [DOI:10.3748/wjg.v9.i1.125] [PMID] []
26. Hussein MM, Ali HA, Saadeldin IM, Ahmed MM. Querectin alleviates zinc oxide nanoreprotoxicity in male albino rats. Journal of biochemical and molecular toxicology. 2016;30(10):489-96. [DOI:10.1002/jbt.21812] [PMID]
27. Singh S. Zinc oxide nanoparticles impacts: Cytotoxicity, genotoxicity, developmental toxicity, and neurotoxicity. Toxicology mechanisms and methods. 2019;29(4):300-11. [DOI:10.1080/15376516.2018.1553221] [PMID]
28. Chang YN, Zhang M, Xia L, Zhang J, Xing G. The toxic effects and mechanisms of CuO and ZnO nanoparticles. Materials. 2012;5(12):2850-71. [DOI:10.3390/ma5122850] []
29. Kirkinezos IG, Moraes CT. Reactive oxygen species and mitochondrial diseases. Seminars in cell & developmental biology. 2001;12(6):449-57. [DOI:10.1006/scdb.2001.0282] [PMID]
30. Valipour S, Hoseini SE, Vahdati A, Kesmati M. The effects of acute administration of zinc oxidenanoparticles on long term memory in the presence and absence of vitamin C in adult male rat. Adv. Environ. Biol. 2014;8:260-6.
31. Shirani M, Nouri M, Askari G. Effect of N-acetyl cysteine supplementation on sperm quality parameters and biochemical markers on the infertile people: A systematic review on clinical trials. KAUMS Journal (FEYZ). 2019;23(4):361-70.
32. Barekat F, Tavalaee M, Deemeh MR, Bahreinian M, Azadi L, Abbasi H. A Preliminary Study: N-acetyl-L-cysteine Improves Semen Quality following Varicocelectomy. Int J Fertil. 2016;10(1):120-6.
33. Mozafari Z, Hayati RN, Parivar K, Irani S. Investigation on the effect of Zinc Oxide Nanoparticle on LH, FSH, testosterone hormones in adult male NMRI mice. Journal of animal biology winter. 2016;8(2):65-73.
34. Chen C, Bu W, Ding H, Li Q, Wang D, Bi H, et al. Cytotoxic effect of zinc oxide nanoparticles on murine photoreceptor cells via potassium channel block and Na+/K+‐ATPase inhibition. Cell proliferation. 2017;50(3):1-9. [DOI:10.1111/cpr.12339] [PMID] []
35. Berk M, Samuni Y, Goldstein S, Dean OM. The chemistry and biological activities of N-acetylcysteine. 2013;1830(8):4117-29. [DOI:10.1016/j.bbagen.2013.04.016] [PMID]
36. Jahangiri Asl E, Soleimanzadeh A, Javadi SH, Asri Rezaei S. The effect of intratesticular injection of Zinc Oxide Nanoparticles on plasma concentrations of LH, FSH, Testosterone and Corticosterone in Rat. Veterinary Research and Biological Products. 2021;34(2):94-103.
37. Aldini G, Altomare A, Baron G, Vistoli G, Carini M, Borsani L, et al. N-Acetylcysteine as an antioxidant and disulphide breaking agent: the reasons why. Free radical research. 2018;52(7):751-62. [DOI:10.1080/10715762.2018.1468564] [PMID]
38. Yang D, Zhang M, Gan Y, Yang S, Wang J, Yu M, et al. Involvement of oxidative stress in ZnO NPs-induced apoptosis and autophagy of mouse GC-1 spg cells. Ecotoxicology and Environmental Safety. 2020;202:110960. [DOI:10.1016/j.ecoenv.2020.110960] [PMID]
39. Pinho AR, Rebelo S, Pereira MD. The impact of zinc oxide nanoparticles on male (in) fertility. Materials. 2020;13(4):849. [DOI:10.3390/ma13040849] [PMID] []
40. Tang Y, Chen B, Hong W, Chen L, Yao L, Zhao Y, et al. ZnO nanoparticles induced male reproductive toxicity based on the effects on the endoplasmic reticulum stress signaling pathway. International Journal of Nanomedicine. 2019;14:9563-76. [DOI:10.2147/IJN.S223318] [PMID] []
41. Mozaffari Z, Parivar K, Roodbari NH, Irani S. Histopathological evaluation of the toxic effects of zinc oxide (ZnO) nanoparticles on testicular tissue of NMRI adult mice. Adv. Stud. Biol. 2015;7(6):275-91. [DOI:10.12988/asb.2015.5425]
42. Han Z, Yan Q, Ge W, Liu ZG, Gurunathan S, De Felici M, et al. Cytotoxic effects of ZnO nanoparticles on mouse testicular cells. International Journal of Nanomedicine. 2016;11:5187-5203. [DOI:10.2147/IJN.S111447] [PMID] []
43. Talebi AR, Khorsandi L, Moridian M. The effect of zinc oxide nanoparticles on mouse spermatogenesis. Journal of assisted reproduction and genetics. 2013;30(9):1203-9. [DOI:10.1007/s10815-013-0078-y] [PMID] []
44. Gholamloo M, Jafari M. Study of Effect of N-Acetyl Cysteine on Reduction of Paraoxon-Induced Oxidative Stress in Brain and Heart Tissues. Health Research. 2017;2(2):77-85. [DOI:10.18869/acadpub.hrjbaq.2.2.77]
45. Kheradmandi R, Jorsaraei SG, Feizi F, Moghadamnia AA, Neamati N. Protective effect of N-acetyl cysteine on chlorpyrifos-induced testicular toxicity in mice. International journal of fertility & sterility. 2019;13(1):51-6.
46. Jannatifar R, Parivar K, Roodbari NH, Nasr-Esfahani MH. Effects of N-acetyl-cysteine supplementation on sperm quality, chromatin integrity and level of oxidative stress in infertile men. Reproductive Biology and Endocrinology. 2019;17(1):1-9. [DOI:10.1186/s12958-019-0468-9] [PMID] []
47. El-Maddawy ZK, El-Sayed YS. Comparative analysis of the protective effects of curcumin and N-acetyl cysteine against paracetamol-induced hepatic, renal, and testicular toxicity in Wistar rats. Environmental science and pollution research. 2018;25(4):3468-79. [DOI:10.1007/s11356-017-0750-3] [PMID]
48. Darbandi N, Khosravi S, Momeni HR. Effect of N-acetyl- cysteine on memory retrieval, hippocampal CA1 pyramidal neurons and some blood serum oxidative Stress factors in Male wistar Rats treated with zinc oxide nanoparticles. The Journal of Urmia University of Medical Sciences. 2018;29(6):450-63.
49. Abbasalipourkabir R, Moradi H, Zarei S, Asadi S, Salehzadeh A, Ghafourikhosroshahi A, Mortazavi M, Ziamajidi N. Toxicity of zinc oxide nanoparticles on adult male Wistar rats. Food and chemical toxicology. 2015;84:154-60. [DOI:10.1016/j.fct.2015.08.019] [PMID]
50. Feng D, Huang H, Yang Y, Yan T, Jin Y, Cheng X., Cui L. Ameliorative effects of N-acetylcysteine on fluoride-induced oxidative stress and DNA damage in male rats' testis. Mutation Research/Genetic Toxicology and Environmental Mutagenesis. 2015;792:35-45. [DOI:10.1016/j.mrgentox.2015.09.004] [PMID]
51. Maheshwari A, Misro M, Aggarwal A, Sharma RK. N-acetyl-L-cysteine modulates multiple signaling pathways to rescue male germ cells from apoptosis induced by chronic hCG administration to rats. Apoptosis. 2012;17(6):551-65. [DOI:10.1007/s10495-012-0703-8] [PMID]
52. Kumari M, Singh P, Study on the reproductive organs and fertility of the male mice following administration of metronidazole. International journal of Fertility & Sterility. 2013; 7(3):225-38.‌
53. Mahmoodi M, Soleimani Mehranjani M, Kheradmand N. Protective Effect of Pentoxifylline on Sperm and Biochemical Parameters against Dexamethasone-Induced Toxicity in Mice. Journal of Mazandaran University of Medical Sciences. 2020;30(185):113-24.
54. Hassanzadeh A, Shahvaisi K, Hassanzadeh K, Izadpanah E, Amini A, Moloudi MR. Effects of rebamipide and encapsulating rebamipide with chitosan capsule on inflammatory mediators in rat experimental colitis. Scientific journal of Kurdistan university of medical sciences. 2015;20(3):94-104.
55. Shen J, Yang D, Zhou X, Wang Y, Tang S, Yin H, et al. Role of autophagy in zinc oxide Nanoparticles-induced apoptosis of mouse LEYDIG cells. International journal of molecular sciences. 2019; 20(16):4042. [DOI:10.3390/ijms20164042] [PMID] []
56. Srivastav AK, Kumar A, Prakash J, Singh D, Jagdale P, Shankar J, et al. Genotoxicity evaluation of zinc oxide nanoparticles in Swiss mice after oral administration using chromosomal aberration, micronuclei, semen analysis, and RAPD profile. Toxicology and Industrial Health. 2017;33(11):821-34. [DOI:10.1177/0748233717717842] [PMID]
57. Abbasalipourkabir R, Moradi H, Zarei S, Asadi S, Salehzadeh A, Ghafourikhosroshahi A. et al. Toxicity of zinc oxide nanoparticles on adult male Wistar rats. Food and chemical toxicology. 2015;84:154-60. [DOI:10.1016/j.fct.2015.08.019] [PMID]
58. Javadi A, Mokhtar S, Azimirad R, Esfandiari F, Gourabi H. Mechanisms of the Effects of Zinc Oxide Nanostructures on Living Cells. Journal of Fasa University of Medical Sciences. 2020;10(1):1998-2011.
59. Tremellen K. Oxidative stress and male infertility-a clinical perspective. Human reproduction update. 2008;14(3):243-58. [DOI:10.1093/humupd/dmn004] [PMID]
60. Nashwa A, Kawkab AA, Mouneir SM. The protective effect of ginger and N-acetyl cysteine on ciprofloxacin-induced reproductive toxicity in male rats. Journal of American Science. 2011;7(7):741-52.
61. Khoshtabiat L, Mahdavi M. The role of oxidative stress in proliferation and cell death. Journal of Mazandaran University of Medical Sciences. 2015;25(127):130-145.
62. Ozaras R, Tahan V, Aydin S, Uzun H, Kaya S, Senturk H. N-acetylcysteine attenuates alcohol-induced oxidative stress in he rat. World Journal of Gastroenterology. 2003;9(1):125. [DOI:10.3748/wjg.v9.i1.125] [PMID] []
63. Hussein MM, Ali HA, Saadeldin IM, Ahmed MM. Querectin alleviates zinc oxide nanoreprotoxicity in male albino rats. Journal of biochemical and molecular toxicology. 2016;30(10):489-96. [DOI:10.1002/jbt.21812] [PMID]
64. Singh S. Zinc oxide nanoparticles impacts: Cytotoxicity, genotoxicity, developmental toxicity, and neurotoxicity. Toxicology mechanisms and methods. 2019;29(4):300-11. [DOI:10.1080/15376516.2018.1553221] [PMID]
65. Chang YN, Zhang M, Xia L, Zhang J, Xing G. The toxic effects and mechanisms of CuO and ZnO nanoparticles. Materials. 2012;5(12):2850-71. [DOI:10.3390/ma5122850] []
66. Kirkinezos IG, Moraes CT. Reactive oxygen species and mitochondrial diseases. Seminars in cell & developmental biology. 2001;12(6):449-57. [DOI:10.1006/scdb.2001.0282] [PMID]
67. Valipour S, Hoseini SE, Vahdati A, Kesmati M. The effects of acute administration of zinc oxidenanoparticles on long term memory in the presence and absence of vitamin C in adult male rat. Adv. Environ. Biol. 2014;8:260-6.
68. Shirani M, Nouri M, Askari G. Effect of N-acetyl cysteine supplementation on sperm quality parameters and biochemical markers on the infertile people: A systematic review on clinical trials. KAUMS Journal (FEYZ). 2019;23(4):361-70.
69. Barekat F, Tavalaee M, Deemeh MR, Bahreinian M, Azadi L, Abbasi H. A Preliminary Study: N-acetyl-L-cysteine Improves Semen Quality following Varicocelectomy. Int J Fertil. 2016;10(1):120-6.
70. Mozafari Z, Hayati RN, Parivar K, Irani S. Investigation on the effect of Zinc Oxide Nanoparticle on LH, FSH, testosterone hormones in adult male NMRI mice. Journal of animal biology winter. 2016;8(2):65-73.
71. Chen C, Bu W, Ding H, Li Q, Wang D, Bi H, et al. Cytotoxic effect of zinc oxide nanoparticles on murine photoreceptor cells via potassium channel block and Na+/K+‐ATPase inhibition. Cell proliferation. 2017;50(3):1-9. [DOI:10.1111/cpr.12339] [PMID] []
72. Berk M, Samuni Y, Goldstein S, Dean OM. The chemistry and biological activities of N-acetylcysteine. 2013;1830(8):4117-29. [DOI:10.1016/j.bbagen.2013.04.016] [PMID]
73. Jahangiri Asl E, Soleimanzadeh A, Javadi SH, Asri Rezaei S. The effect of intratesticular injection of Zinc Oxide Nanoparticles on plasma concentrations of LH, FSH, Testosterone and Corticosterone in Rat. Veterinary Research and Biological Products. 2021;34(2):94-103.
74. Aldini G, Altomare A, Baron G, Vistoli G, Carini M, Borsani L, et al. N-Acetylcysteine as an antioxidant and disulphide breaking agent: the reasons why. Free radical research. 2018;52(7):751-62. [DOI:10.1080/10715762.2018.1468564] [PMID]
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Darbandi N, Mahmoodi M, Khosravi Z. Improvement of Sperm Parameters and Oxidative Stress by N-acetyl-cysteine in Adult Male Mice Treated with Zinc Oxide Nanoparticles. SJKU 2023; 28 (3) :37-47
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Volume 28, Issue 3 (Scientific Journal of Kurdistan University of Medical Sciences 2023) Back to browse issues page
مجله علمی دانشگاه علوم پزشکی کردستان Scientific Journal of Kurdistan University of Medical Sciences
مجله علمی دانشگاه علوم پزشکی کردستان Scientific Journal of Kurdistan University of Medical Sciences
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