Histomorphometric evaluation of the testis after administration of methionine-loaded zinc oxide nano-particles in mice

Document Type : Original Article

Authors

1 Department of Basic Sciences, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

2 Department of Pathobiology, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

3 Department of Clinical Sciences, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

Abstract

With the remarkable progress of nanotechnology in medicine, the use of nano supplements such as methionine in low doses can be a starting point for the optimization and strengthening of the compounds that protect the testes and, subsequently, the improvement of the fertility rate of the population. Excessive amounts of methionine, an essential amino acid in mammals, have toxic effects on body organs. The beneficial effects of widely used and inexpensive zinc oxide nanoparticles (ZnO-NPs) with high antioxidant properties have been shown on the male reproductive system. This study was conducted to examine the histopathologic and histomorphometric effects of methionine-loaded zinc oxide nanoparticles on mice testes. Adult male mice (N = 50) were assigned to five groups (n = 10 in each group) randomly. The groups included M50 (50 mg/kg methionine), M200 (200 mg/kg methionine), NM50 (50 mg/kg methionine-loaded zinc oxide nanoparticles), NM200 (200 mg/kg methionine-loaded zinc oxide nanoparticles), and Control. After 42 days, the left testes of the mice were assessed for Johnsen scores, seminiferous tubule epithelium height, seminiferous tubule diameter, meiotic index, rate of spermatogenesis, and histopathological features after euthanasia. The results showed that high doses of methionine (alone and attached to nano zinc oxide particles) have toxic effects on the testes. In comparison to the control group, the histopathological and histomorphometric indicators of the testis in the group receiving methionine at a dose of 50 mg/kg attached to nano zinc oxide particles had some increase (although insignificant), with better status compared to the M50 group. High doses of methionine could have undesirable effects on testes and significantly decrease the mentioned parameters. However, the results indicated that the histomorphometric indices of mice testis may benefit from zinc oxide nanoparticles loaded with methionine.

Keywords

References

  1. Pascoal GD, Geraldi M V, Maróstica MR, Ong TP (2022) Effect of Paternal Diet on Spermatogenesis and Offspring Health: Focus on Epigenetics and Interventions with Food Bioactive Compounds. Nutrients 14
  2. Shayakhmetova GM, Bondarenko LB, Voronina AK, Kovalenko VM (2017) Comparative investigation of methionine and novel formulation Metovitan protective effects in Wistar rats with testicular and epididymal toxicity induced by anti-tuberculosis drugs co-administration. Food Chem Toxicol 99:222–230.https://doi.org/https://doi.org/10.1016/j.fct.2016.12.001
  3. Mohamed DA, Abdelrahman SA (2019) The possible protective role of zinc oxide nanoparticles (ZnONPs) on testicular and epididymal structure and sperm parameters in nicotine-treated adult rats (a histological and biochemical study). Cell Tissue Res 375:543–558. https://doi.org/10.1007/s00441-018-2909-8
  4. Aledo JC (2019) Methionine in proteins: The Cinderella of the proteinogenic amino acids. Protein Sci 28:1785–1796. https://doi.org/https://doi.org/10.1002/pro.3698
  5. Becquet P, Vazquez-Anon M, Mercier Y, et al (2023) A systematic review of metabolism of methionine sources in animals: One parameter does not convey a comprehensive story. Anim Nutr 13:31–49. https://doi.org/https://doi.org/10.1016/j.aninu.2023.01.009
  6. Koz ST, Gouwy NT, Demir N, et al (2010) Effects of maternal hyperhomocysteinemia induced by methionine intake on oxidative stress and apoptosis in pup rat brain. Int J Dev Neurosci 28:325–329. https://doi.org/https://doi.org/10.1016/j.ijdevneu.2010.02.006
  7. Nazem MN, Aghamiri SM, Kheirandish R, Hakimy Z (2022) The effects of methionine administration during the beginning postnatal days on the ovarian structures in adult rats. Vet Med Sci 8:1174–1179. https://doi.org/https://doi.org/10.1002/vms3.750
  8. Soltani L, Samereh S, Mohammadi T (2022) Effects of different concentrations of zinc oxide nanoparticles on the quality of ram cauda epididymal spermatozoa during storage at 4°C. Reprod Domest Anim 57:864–875.https://doi.org/https://doi.org/10.1111/rda.14130
  9. Vickram S, Rohini K, Srinivasan S, et al (2021) Role of Zinc (Zn) in Human Reproduction: A Journey from Initial Spermatogenesis to Childbirth. Int. J. Mol. Sci. 22
  10. Prasad AS, Bao B (2019) Molecular Mechanisms of Zinc as a Pro-Antioxidant Mediator: Clinical Therapeutic Implications. Antioxidants 8
  11. Erfani Majd N, Hajirahimi A, Tabandeh MR, Molaei R (2021) Protective effects of green and chemical zinc oxide nanoparticles on testis histology, sperm parameters, oxidative stress markers and androgen production in rats treated with cisplatin. Cell Tissue Res 384:561–575. https://doi.org/10.1007/s00441-020-03350-2
  12. Ringu T, Ghosh S, Das A, Pramanik N (2022) Zinc oxide nanoparticles: an excellent biomaterial for bioengineering applications. Emergent Mater 5:1629–1648. https://doi.org/10.1007/s42247-022-00402-x
  13. Pinho AR, Rebelo S, Pereira MD (2020) The Impact of Zinc Oxide Nanoparticles on Male (In)Fertility. Materials (Basel). 13
  14. DO CARMO E SÁ M V, PEZZATO LE, BARROS MM, DE MAGALHÃES PADILHA P (2005) Relative bioavailability of zinc in supplemental inorganic and organic sources for Nile tilapia Oreochromis niloticus fingerlings. Aquac Nutr 11:273–281. https://doi.org/https://doi.org/10.1111/j.1365-2095.2005.00352.x
  15. Goma AA, Tohamy HG, El-Kazaz SE, et al (2021) Insight Study on the Comparison between Zinc Oxide Nanoparticles and Its Bulk Impact on Reproductive Performance, Antioxidant Levels, Gene Expression, and Histopathology of Testes in Male Rats. Antioxidants 10
  16. Tang Y, Chen B, Hong W, et al (2019) ZnO nanoparticles induced male reproductive toxicity based on the effects on the endoplasmic reticulum stress signaling pathway. Int J Nanomedicine 14:9563–9576. https://doi.org/10.2147/IJN.S223318
  17. Naidu ECS, Olojede SO, Lawal SK, et al (2021) Nanoparticle delivery system, highly active antiretroviral therapy, and testicular morphology: The role of stereology. Pharmacol Res Perspect 9:e00776
  18. Thakur M, Gupta H, Singh D, et al (2014) Histopathological and ultra structural effects of nanoparticles on rat testis following 90 days (Chronic study) of repeated oral administration. J Nanobiotechnology 12:1–13
  19. Rahimi Kalateh Shah Mohammad G, Karimi E, Oskoueian E, Homayouni-Tabrizi M (2020) Anticancer properties of green-synthesised zinc oxide nanoparticles using Hyssopus officinalis extract on prostate carcinoma cells and its effects on testicular damage and spermatogenesis in Balb/C mice. Andrologia 52:e13450. https://doi.org/https://doi.org/10.1111/and.13450
  20. Bara N, Eshwarmoorthy M, Subaharan K, Kaul G (2018) Mesoporous silica nanoparticle is comparatively safer than zinc oxide nanoparticle which can cause profound steroidogenic effects on pregnant mice and male offspring exposed in utero. Toxicol Ind Health 34:507–524. https://doi.org/10.1177/0748233718757641
  21. Yousef MI, Mutar TF, Kamel MAE-N (2019) Hepato-renal toxicity of oral sub-chronic exposure to aluminum oxide and/or zinc oxide nanoparticles in rats. Toxicol Reports 6:336–346. https://doi.org/https://doi.org/10.1016/j.toxrep.2019.04.003
  22. Johnsen SG (1970) Testicular Biopsy Score Count – A Method for Registration of Spermatogenesis in Human Testes: Normal Values and Results in 335 Hypogonadal Males. Horm Res Paediatr 1:2–25. https://doi.org/10.1159/000178170
  23. Ghanbari E, Nejati V, Khazaei M (2016) Antioxidant and protective effects of Royal jelly on histopathological changes in testis of diabetic rats. Int J Reprod Biomed 14:519–526
  24. Chin K, Toue S, Kawamata Y, et al (2015) A 4-Week Toxicity Study of Methionine in Male Rats. Int J Toxicol 34:233–241. https://doi.org/10.1177/1091581815583678
  25. Khushboo M, Murthy MK, Devi MS, et al (2018) Testicular toxicity and sperm quality following copper exposure in Wistar albino rats: ameliorative potentials of L-carnitine. Environ Sci Pollut Res 25:1837–1862. https://doi.org/10.1007/s11356-017-0624-8
  26. Lin S, Qiao N, Chen H, et al (2020) Integration of transcriptomic and metabolomic data reveals metabolic pathway alteration in mouse spermatogonia with the effect of copper exposure. Chemosphere 256:126974. https://doi.org/https://doi.org/10.1016/j.chemosphere.2020.126974
  27. Magnuson AD, Liu G, Sun T, et al (2020) Supplemental methionine and stocking density affect antioxidant status, fatty acid profiles, and growth performance of broiler chickens. J Anim Sci 98:. https://doi.org/10.1093/jas/skaa092
  28. Seyyedin S, Nazem MN (2017) Histomorphometric study of the effect of methionine on small intestine parameters in rat: An applied histologic study. Folia Morphol 76:620–629. https://doi.org/10.5603/FM.a2017.0044
  29. Nazem MN, Kheirandish R, Babaei H, Dehghan F (2017) Effect of short-term administration of methionine on the ovary and uterus in a rat. Comp Clin Path 26:867–873. https://doi.org/10.1007/s00580-017-2458-7
  30. Mohammed ET, Radi AM, Aleya L, Abdel-Daim MM (2020) Cynara scolymus leaves extract alleviates nandrolone decanoate-induced alterations in testicular function and sperm quality in albino rats. Environ Sci Pollut Res 27:5009–5017. https://doi.org/10.1007/s11356-019-07302-4
  31. Abu Elnaga NAM (2012) Effect of Cholesterol and /or Methionine on the Testis of Rats. Egypt J Hosp Med 49:857–878. https://doi.org/10.21608/ejhm.2012.16220
  32. Bin P, Huang R, Zhou X (2017) Oxidation Resistance of the Sulfur Amino Acids: Methionine and Cysteine. Biomed Res Int 2017:9584932.https://doi.org/10.1155/2017/9584932
  33. Gomez J, Caro P, Sanchez I, et al (2009) Effect of methionine dietary supplementation on mitochondrial oxygen radical generation and oxidative DNA damage in rat liver and heart. J Bioenerg Biomembr 41:309–321. https://doi.org/10.1007/s10863-009-9229-3
  34. Liao W, Cai M, Chen J, et al (2010) Hypobaric hypoxia causes deleterious effects on spermatogenesis in rats. Reproduction 139:1031–1038
  35. Toue S, Kodama R, Amao M, et al (2006) Screening of Toxicity Biomarkers for Methionine Excess in Rats. J Nutr 136:1716S-1721S. https://doi.org/10.1093/jn/136.6.1716S
  36. Jin N, Huang L, Hong J, et al (2021) Elevated homocysteine levels in patients with heart failure: A systematic review and meta-analysis. Medicine (Baltimore) 100:e26875. https://doi.org/10.1097/MD.0000000000026875
  37. dos Santos DP, Ribeiro DF, Frigoli GF, et al (2022) Voluntary Exercise Attenuates Hyperhomocysteinemia, But Does not Protect Against Hyperhomocysteinemia-Induced Testicular and Epididymal Disturbances. Reprod Sci 29:277–290. https://doi.org/10.1007/s43032-021-00704-1
  38. Nazem MN, Teymouri M, Jahantigh M (2016) The histomorphometric and histopathologic effect of methionine on the epidermis and dermis layers of skin in rat. Comp Clin Path 25:699–704
  39. Elsherbiny NM, Sharma I, Kira D, et al (2020) Homocysteine Induces Inflammation in Retina and Brain. Biomolecules 10
  40. Tiwari D, Rani A, Jha HC (2022) Homocysteine and Folic Acid Metabolism BT - Homocysteine Metabolism in Health and Disease. In: Dubey GP, Misra K, Kesharwani RK, Ojha RP (eds) Homocysteine Metabolism in Health and Disease. Springer Nature Singapore, Singapore, pp 3–36
  41. Kuszczyk M, Gordon-Krajcer W, Lazarewicz JW (2009) Homocysteine-induced acute excitotoxicity in cerebellar granule cells in vitro is accompanied by PP2A-mediated dephosphorylation of tau. Neurochem Int 55:174–180. https://doi.org/10.1016/j.neuint.2009.02.010
  42. Forges T, Monnier-Barbarino P, Alberto JM, et al (2007) Impact of folate and homocysteine metabolism on human reproductive health. Hum Reprod Update 13:225–238. https://doi.org/10.1093/humupd/dml063
  43. Jung JH, Seo JT (2014) Empirical medical therapy in idiopathic male infertility: Promise or panacea? Clin Exp Reprod Med 41:108–114. https://doi.org/10.5653/cerm.2014.41.3.108
  44. Torabi F, Malekzadeh Shafaroudi M, Rezaei N (2017) Combined protective effect of zinc oxide nanoparticles and melatonin on cyclophosphamide-induced toxicity in testicular histology and sperm parameters in adult Wistar rats. Int J Reprod Biomed 15:403–412
  45. Badkoobeh P, Parivar K, Kalantar SM, et al (2013) Effect of nano-zinc oxide on doxorubicin- induced oxidative stress and sperm disorders in adult male Wistar rats. Iran J Reprod Med 11:355–364
  46. Ghobadi E, Moloudizargari M, Asghari MH, Abdollahi M (2017) The mechanisms of cyclophosphamide-induced testicular toxicity and the protective agents. Expert Opin Drug Metab Toxicol 13:525–536. https://doi.org/10.1080/17425255.2017.1277205
  47. Faiz H, Zuberi A, Nazir S, et al (2015) Zinc oxide, zinc sulfate and zinc oxide nanoparticles as source of dietary zinc: comparative effects on growth and hematological indices of juvenile grass carp (Ctenopharyngodon idella). Int J Agric Biol 17:
  48. Dhivya R, Ranjani J, Rajendhran J, et al (2018) Enhancing the anti-gastric cancer activity of curcumin with biocompatible and pH sensitive PMMA-AA/ZnO nanoparticles. Mater Sci Eng C 82:182–189. https://doi.org/https://doi.org/10.1016/j.msec.2017.08.058
  49. Sayyar Z, Jafarizadeh-Malmiri H, Beheshtizadeh N (2022) A study on the anticancer and antimicrobial activity of Curcumin nanodispersion and synthesized ZnO nanoparticles. Process Biochem 121:18–25.https://doi.org/https://doi.org/10.1016/j.procbio.2022.06.033
  50. Anjum S, Hashim M, Malik SA, et al (2021) Recent Advances in Zinc Oxide Nanoparticles (ZnO NPs) for Cancer Diagnosis, Target Drug Delivery, and Treatment. Cancers (Basel). 13
  51. Keerthana S, Kumar A (2020) Potential risks and benefits of zinc oxide nanoparticles: a systematic review. Crit Rev Toxicol 50:47–71.https://doi.org/10.1080/10408444.2020.1726282
  52. El-Maddawy ZK, Abd El Naby WSH (2019) Protective effects of zinc oxide nanoparticles against doxorubicin induced testicular toxicity and DNA damage in male rats. Toxicol Res (Camb) 8:654–662. https://doi.org/10.1039/c9tx00052f
  53. Atef HA, Mansour MK, Ibrahim EM, et al (2016) Efficacy of zinc oxide nanoparticles and curcumin in amelioration the toxic effects in aflatoxicated rabbits. Int J Curr Microbiol Appl Sci 5:795–818
Veterinary and Comparative Biomedical Research
Volume 1, Issue 1
June 2024
Pages 1-11

Files

Share

How to cite

Statistics