Treatment of copper nanoparticles (CuNPs) for two spermatogenic cycles impairs testicular activity via down-regulating steroid receptors and inhibition of germ cell proliferation in a mice model

References

• Aboul-Soud, M. A., A. M Al Othman, G. E. El-Desoky, Z. A Al Othman, K. Yusuf, J. Ahmad, and A. A. Al-Khedhairy. 2011. “Hepatoprotective Effects of Vitamin E/Selenium against Malathion-Induced Injuries on the Antioxidant Status and Apoptosis-Related Gene Expression in Rats.” The Journal of Toxicological Sciences 36 (3): 285–296. doi:10.2131/jts.36.285.
   PubMed Web of Science ®Google Scholar
• Ancona, A., M. C. Sportelli, A. Trapani, R. A. Picca, C. Palazzo, E. Bonerba, F. P. Mezzapesa, G. Tantillo, G. Trapani, and N. Cioffi. 2014. “Synthesis and Characterization of Hybrid Copper–Chitosan Nano-Antimicrobials by Femtosecond Laser-Ablation in Liquids.” Materials Letters 136: 397–400. doi:10.1016/j.matlet.2014.08.083.
   Web of Science ®Google Scholar
• AL-Musawi, M., H. Al-Shmgani, and G. A. Al-Bairuty. 2022. “Histopathological and Biochemical Comparative Study of Copper Oxide Nanoparticles and Copper Sulphate Toxicity in Male Albino Mice Reproductive System.” International Journal of Biomaterials 2022: 1–12. doi:10.1155/2022/4877637.
   Web of Science ®Google Scholar
• Azenabor, A., A. O. Ekun, and O. Akinloye. 2015. “Impact of Inflammation on Male Reproductive Tract.” Journal of Reproduction & Infertility 16 (3): 123.
   PubMedGoogle Scholar
• Bancroft, J. D. and M. Gamble, eds. 2008. Theory and Practice of Histological Techniques. Elsevier Health Sciences.
   Google Scholar
• Bancroft, J. D, and M. Gamble. 2002. Theory and Practice of Histological Techniques, vol. 172, 593–620. Edinburgh. Churchill Livingstone Pub.
   Google Scholar
• Borm, P., F. C. Klaessig, T. D. Landry, B. Moudgil, J. Pauluhn, K. Thomas, R. Trottier, and S. Wood. 2006. “Research Strategies for Safety Evaluation of Nanomaterials, Part V: role of Dissolution in Biological Fate and Effects of Nanoscale Particles.” Toxicological Sciences 90 (1): 23–32. doi:10.1093/toxsci/kfj084.
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. 1976. “A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding.” Analytical Biochemistry 72 (1–2): 248–254. doi:10.1016/0003-2697(76)90527-3.
   PubMed Web of Science ®Google Scholar
• Carreau, S, and R. A. Hess. 2010. “Oestrogens and Spermatogenesis.” Philosophical Transactions of the Royal Society of London-Series B, Biological Sciences 365 (1546): 1517–1535. doi:10.1098/rstb.2009.0235.
   PubMed Web of Science ®Google Scholar
• Chen, L., Y. Tao, and Y. Jiang. 2015. “Apelin Activates the Expression of Inflammatory Cytokines in Microglial BV2 Cells via PI-3K/Akt and MEK/Erk Pathways.” Science China Life Sciences 58 (6): 531–540. doi:10.1007/s11427-015-4861-0.
   PubMed Web of Science ®Google Scholar
• Cometa, S., R. Iatta, M. A. Ricci, C. Ferretti, and E. De Giglio. 2013. “Analytical Characterization and Antimicrobial Properties of Novel Copper Nanoparticle–Loaded Electrosynthesized Hydrogel Coatings.” Journal of Bioactive and Compatible Polymers 28 (5): 508–522. doi:10.1177/0883911513498960.
   Web of Science ®Google Scholar
• Chen, H., Y. Wang, J. Luo, M. Kang, J. Hou, R. Tang, L. Zhao, et al. 2022. “Autophagy and Apoptosis Mediated Nano-Copper-Induced Testicular Damage.” Ecotoxicology and Environmental Safety 229: 113039. doi:10.1016/j.ecoenv.2021.113039.
   PubMed Web of Science ®Google Scholar
• Chimento, A., R. Sirianni, C. Delalande, D. Silandre, C. Bois, S. Andò, M. Maggiolini, S. Carreau, and V. Pezzi. 2010. “17β-estradiol Activates Rapid Signaling Pathways Involved in Rat Pachytene Spermatocytes Apoptosis through GPR30 and ERα.” Molecular and Cellular Endocrinology 320 (1–2): 136–144. doi:10.1016/j.mce.2010.01.035.
   PubMed Web of Science ®Google Scholar
• Das, M., L. Annie, K. V. Derkach, A. O. Shpakov, G. Gurusubramanian, and V. K. Roy. 2021. “Expression and Localization of Apelin and Its Receptor in the Testes of Diabetic Mice and Its Possible Role in Steroidogenesis.” Cytokine 144: 155554. doi:10.1016/j.cyto.2021.155554.
   PubMed Web of Science ®Google Scholar
• De Berardis, B., G. Civitelli, M. Condello, P. Lista, R. Pozzi, G. Arancia, and S. Meschini. 2010. “Exposure to ZnO Nanoparticles Induces Oxidative Stress and Cytotoxicity in Human Colon Carcinoma Cells.” Toxicology and Applied Pharmacology 246 (3): 116–127. doi:10.1016/j.taap.2010.04.012.
   PubMed Web of Science ®Google Scholar
• Dinçer, Y., C. Akkaya, T. Mutlu, S. Yavuzer, G. Erkol, M. Bozluolcay, and M. Guven. 2019. “DNA Repair Gene OGG1 Polymorphism and Its Relation with Oxidative DNA Damage in Patients with Alzheimer’s Disease.” Neuroscience Letters 709: 134362. doi:10.1016/j.neulet.2019.134362.
   PubMed Web of Science ®Google Scholar
• Dagher, S., Y. Haik, A. I. Ayesh, and N. Tit. 2014. “Synthesis and Optical Properties of Colloidal CuO Nanoparticles.” Journal of Luminescence 151: 149–154. doi:10.1016/j.jlumin.2014.02.015.
   Web of Science ®Google Scholar
• Durfey, C. L., D. D. Burnett, S. F. Liao, C. S. Steadman, M. A. Crenshaw, H. J. Clemente, S. T. Willard, P. L. Ryan, and J. M. Feugang. 2017. “Nanotechnology-Based Selection of Boar Spermatozoa: growth Development and Health Assessments of Produced Offspring.” Livestock Science 205: 137–142. doi:10.1016/j.livsci.2017.09.024.
   Web of Science ®Google Scholar
• Ema, M., K. S. Hougaard, A. Kishimoto, and K. Honda. 2016. “Reproductive and Developmental Toxicity of Carbon-Based Nanomaterials: A Literature Review.” Nanotoxicology 10 (4): 391–412. doi:10.3109/17435390.2015.1073811.
   PubMed Web of Science ®Google Scholar
• França, L. R., C. L. Godinho. 2003. “Testis morphometry, seminiferous epithelium cycle length, and daily sperm production in domestic cats (Felis catus).” Biology of Reproduction 68 (5): 1554–1561.
   Google Scholar
• Foussal, C., O. Lairez, D. Calise, A. Pathak, C. Guilbeau-Frugier, P. Valet, A. Parini, and O. Kunduzova. 2010. “Activation of Catalase by Apelin Prevents Oxidative Stress-Linked Cardiac Hypertrophy.” FEBS Letters 584 (11): 2363–2370. doi:10.1016/j.febslet.2010.04.025.
   PubMed Web of Science ®Google Scholar
• Guneli, E., K. Tugyan, H. Ozturk, M. Gumustekin, S. Cilaker, and N. Uysal. 2008. “Effect of Melatonin on Testicular Damage in Streptozotocin-Induced Diabetes Rats.” Europaische Chirurgische Forschung. Recherches Chirurgicales Europeennes [European Surgical Research] 40 (4): 354–360. doi:10.1159/000118032.
   PubMed Web of Science ®Google Scholar
• Guo, H., Y. Ouyang, J. Wang, H. Cui, H. Deng, X. Zhong, Z. Jian, et al. 2021. “Cu-Induced Spermatogenesis Disease is Related to Oxidative Stress-Mediated Germ Cell Apoptosis and DNA Damage.” Journal of Hazardous Materials 416 (416): 125903. doi:10.1016/j.jhazmat.2021.125903.
   PubMedGoogle Scholar
• Hou, J., L. Zhao, H. Tang, X. He, G. Ye, F. Shi, M. Kang, H. Chen, and Y. Li. 2021. “Silver Nanoparticles Induced Oxidative Stress and Mitochondrial Injuries Mediated Autophagy in HC11 Cells through Akt/AMPK/mTOR Pathway.” Biological Trace Element Research 199 (3): 1062–1073. doi:10.1007/s12011-020-02212-w.
   PubMed Web of Science ®Google Scholar
• Hejazy, M., M. K. Koohi, A. Bassiri Mohamad Pour, and D. Najafi. 2018. “Toxicity of Manufactured Copper nanoparticles-A Review.” Nanomedicine Research Journal 3 (1): 1–9.
   Google Scholar
• Habas, K., E. Demir, C. Guo, M. H. Brinkworth, and D. Anderson. 2021. “Toxicity Mechanisms of Nanoparticles in the Male Reproductive System.” Drug Metabolism Reviews 53 (4): 604–617. doi:10.1080/03602532.2021.1917597.
   PubMed Web of Science ®Google Scholar
• He, H., Z. Zou, B. Wang, G. Xu, C. Chen, X. Qin, C. Yu, and J. Zhang. 2020. “Copper Oxide Nanoparticles Induce Oxidative DNA Damage and Cell Death via Copper Ion-Mediated P38 MAPK Activation in Vascular Endothelial Cells.” International Journal of Nanomedicine 15: 3291–3302. doi:10.2147/IJN.S241157.
   PubMed Web of Science ®Google Scholar
• Hadwan, M. H. 2018. “Simple Spectrophotometric Assay for Measuring Catalase Activity in Biological Tissues.” BMC Biochemistry 19 (1): 1–8. doi:10.1186/s12858-018-0097-5.
   PubMedGoogle Scholar
• Han, P., W. Martens, E. R. Waclawik, S. Sarina, and H. Zhu. 2018. “Metal Nanoparticle Photocatalysts: Synthesis, Characterization, and Application.” Particle & Particle Systems Characterization 35 (6): 1700489. doi:10.1002/ppsc.201700489.
   Web of Science ®Google Scholar
• Han, J. W., J. K. Jeong, S. Gurunathan, Y. J. Choi, J. Das, D. N. Kwon, S. G. Cho, et al. 2016. “Male-and Female-Derived Somatic and Germ Cell-Specific Toxicity of Silver Nanoparticles in Mouse.” Nanotoxicology 10 (3): 361–373. doi:10.3109/17435390.2015.1073396.
   PubMed Web of Science ®Google Scholar
• Ingle, A. P., N. Duran, and M. Rai. 2014. “Bioactivity, Mechanism of Action, and Cytotoxicity of Copper-Based Nanoparticles: A Review.” Applied Microbiology and Biotechnology 98 (3): 1001–1009. doi:10.1007/s00253-013-5422-8.
   PubMed Web of Science ®Google Scholar
• Jeremy, M., G. Gurusubramanian, and V. K. Roy. 2019. “Vitamin D3 Mediated Regulation of Steroidogenesis Mitigates Testicular Activity in an Aged Rat Model.” The Journal of Steroid Biochemistry and Molecular Biology 190: 64–75. doi:10.1016/j.jsbmb.2019.03.016.
   PubMed Web of Science ®Google Scholar
• Jeremy, M., G. Gurusubramanian, and V. K. Roy. 2017. “Localization Pattern of Visfatin (NAMPT) in d-Galactose Induced Aged Rat Testis.” Anatomischer Anzeiger [Annals of Anatomy] 211: 46–54. doi:10.1016/j.aanat.2017.01.009.
   PubMed Web of Science ®Google Scholar
• Johnsen, S. G. 1970. “Testicular Biopsy Score Count–a Method for Registration of Spermatogenesis in Human Testes: normal Values and Results in 335 Hypogonadalmales.” Hormones 1 (1): 2–25. doi:10.1159/000178170.
   PubMedGoogle Scholar
• Kang, M., J. Luo, L. Zhao, F. Shi, G. Ye, X. He, S. Hao, et al. 2021. “Autophagy Was Activated against the Damages of Placentas Caused by Nano-Copper Oral Exposure.” Ecotoxicology and Environmental Safety 220: 112364. doi:10.1016/j.ecoenv.2021.112364.
   PubMed Web of Science ®Google Scholar
• Khan, I., K. Saeed, and I. Khan. 2019. “Nanoparticles: Properties, Applications and Toxicities.” Arabian Journal of Chemistry 12 (7): 908–931. doi:10.1016/j.arabjc.2017.05.011.
   Web of Science ®Google Scholar
• Khushboo, M., M. K. Murthy, M. S. Devi, S. Sanjeev, K. S. Ibrahim, N. S. Kumar, V. K. Roy, and G. Gurusubramanian. 2018. “Testicular Toxicity and Sperm Quality following Copper Exposure in Wistar Albino Rats: ameliorative Potentials of L-Carnitine.” Environmental Science and Pollution Research International 25 (2): 1837–1862. doi:10.1007/s11356-017-0624-8.
   PubMed Web of Science ®Google Scholar
• Kakkar, P., B. Das, and P. N. Viswanathan. 1984. “A Modified Spectrophotometric Assay of Superoxide Dismutase.” Indian Journal of Biochemistry & Biophysics 21 (2):130–132.
   Google Scholar
• Ko, J. W., E. T. Hong, I. C. Lee, S. H. Park, J. I. Park, N. W. Seong, J. S. Hong, H. I. Yun, and J. C. Kim. 2015. “Evaluation of 2-Week Repeated Oral Dose Toxicity of 100 nm Zinc Oxide Nanoparticles in Rats.” Laboratory Animal Research 31 (3): 139–147. doi:10.5625/lar.2015.31.3.139.
   PubMedGoogle Scholar
• Komatsu, T., M. Tabata, M. Kubo-Irie, T. Shimizu, K. I. Suzuki, Y. Nihei, and K. Takeda. 2008. “The Effects of Nanoparticles on Mouse Testis Leydig Cells in Vitro.” Toxicology in Vitro 22 (8): 1825–1831. doi:10.1016/j.tiv.2008.08.009.
   PubMed Web of Science ®Google Scholar
• Lee, I. C., J. W. Ko, S. H. Park, J. O. Lim, I. S. Shin, C. Moon, S. H. Kim, J. D. Heo, and J. C. Kim. 2016. “Comparative Toxicity and Biodistribution of Copper Nanoparticles and Cupric Ions in Rats.” International Journal of Nanomedicine 11: 2883–2900. doi:10.2147/IJN.S106346.
   PubMed Web of Science ®Google Scholar
• Lin, D, and B. Xing. 2007. “Phytotoxicity of Nanoparticles: inhibition of Seed Germination and Root Growth.” Environmental Pollution 150 (2): 243–250. doi:10.1016/j.envpol.2007.01.016.
   PubMed Web of Science ®Google Scholar
• Luo, J., S. Hao, L. Zhao, F. Shi, G. Ye, C. He, J. Lin, et al. 2020. “Oral Exposure of Pregnant Rats to Copper Nanoparticles Caused Nutritional Imbalance and Liver Dysfunction in Fetus.” Ecotoxicology and Environmental Safety 206: 111206. doi:10.1016/j.ecoenv.2020.111206.
   PubMed Web of Science ®Google Scholar
• Li, L., F. Li, F. Li, X. Mao, L. Yang, H. Huang, Y. Guo, L. Chen, and J. Li. 2011. “NOX4-Derived Reactive Oxygen Species Drive Apelin-13-Induced Vascular Smooth Muscle Cell Proliferation via the ERK Pathway.” International Journal of Peptide Research and Therapeutics 17 (4): 307–315. doi:10.1007/s10989-011-9269-5.
   Web of Science ®Google Scholar
• Murugananthkumar, R., D. Rajesh, and B. Senthilkumaran. 2016. “Copper Nanoparticles Differentially Target Testis of the Catfish.” Clariasbatrachus 4: 67.
   Google Scholar
• Mazzotta, H. C., W. A. Robbins, and C. S. Tsai. 2022. “An Analysis of Prenatal Exposure Factors and Offspring Health Outcomes in Rodents from Synthesized Nanoparticles.” Reproductive Toxicology 110: 60–67. doi:10.1016/j.reprotox.2022.03.014.
   PubMed Web of Science ®Google Scholar
• O'Donnell, L., P. Stanton, and D. M. de Kretser. 2017. “Endocrinology of the Male Reproductive System and Spermatogenesis.”In Feingold KR, Anawalt B, Boyce A, et al., editors. Endotext [Internet]. South Dartmouth (MA): MDText.com, Inc.; 2000-. Available from: https://www.ncbi.nlm.nih.gov/books/NBK279031/
   Google Scholar
• Ohkawa, H., N. Ohishi, and K. Yagi. 1979. “Assay for Lipid Peroxides in Animal Tissues by Thiobarbituric Acid Reaction.” Analytical Biochemistry 95 (2): 351–358. doi:10.1016/0003-2697(79)90738-3.
   PubMed Web of Science ®Google Scholar
• Ogunsuyi, O. M., O. L. Ogunsuyi, O. Akanni, O. A. Alabi, C. G. Alimba, O. A. Adaramoye, S. Cambier, S. Eswara, A. C. Gutleb, and A. A. Bakare. 2020. “Alteration of Sperm Parameters and Reproductive Hormones in Swiss Mice via Oxidative Stress after co‐Exposure to Titanium Dioxide and Zinc Oxide Nanoparticles.” Andrologia 52 (10): e13758. doi:10.1111/and.13758.
   PubMed Web of Science ®Google Scholar
• Oldereid, N. B., P. D. Angelis, R. Wiger, and O. P. Clausen. 2001. “Expression of Bcl-2 Family Proteins and Spontaneous Apoptosis in Normal Human Testis.” Molecular Human Reproduction 7 (5): 403–408. doi:10.1093/molehr/7.5.403.
   PubMed Web of Science ®Google Scholar
• Oztekin, Y., M. Tok, E. Bilici, L. Mikoliunaite, Z. Yazicigil, A. Ramanaviciene, and A. Ramanavicius. 2012. “Copper Nanoparticle Modified Carbon Electrode for Determination of Dopamine.” Electrochimica Acta 76: 201–207. doi:10.1016/j.electacta.2012.04.105.
   Web of Science ®Google Scholar
• Paglia, D. E, and W. N. Valentine. 1967. “Studies on the Quantitative and Qualitative Characterization of Erythrocyte Glutathione Peroxidase.” The Journal of Laboratory and Clinical Medicine 70 (1): 158–169.
   PubMed Web of Science ®Google Scholar
• Prabhu, B. M., S. F. Ali, R. C. Murdock, S. M. Hussain, and M. Srivatsan. 2010. “Copper Nanoparticles Exert Size and Concentration Dependent Toxicity on Somatosensory Neurons of Rat.” Nanotoxicology 4 (2): 150–160. doi:10.3109/17435390903337693.
   PubMed Web of Science ®Google Scholar
• Privalova, L., B. Katsnelson, N. Loginova, V. Gurvich, V. Shur, I. Valamina, O. Makeyev, et al. 2014. “Subchronic Toxicity of Copper Oxide Nanoparticles and Its Attenuation with the Help of a Combination of Bioprotectors.” International Journal of Molecular Sciences 15 (7): 12379–12406. doi:10.3390/ijms150712379.
   PubMed Web of Science ®Google Scholar
• Rai, M., A. P. Ingle, R. Pandit, P. Paralikar, S. Shende, I. Gupta, J. K. Biswas, and S. S. da Silva. 2018. “Copper and Copper Nanoparticles: Role in Management of Insect-Pests and Pathogenic Microbes.” Nanotechnology Reviews 7 (4): 303–315. doi:10.1515/ntrev-2018-0031.
   Web of Science ®Google Scholar
• Roychoudhury, S., S. Nath, P. Massanyi, R. Stawarz, M. Kacaniova, and A. Kolesarova. 2016. “Copper-Induced Changes in Reproductive Functions: In Vivo and in Vitro Effects.” Physiological Research 65 (1): 11–22. doi:10.33549/physiolres.933063.
   PubMed Web of Science ®Google Scholar
• Rempuia, V., B. Anima, M. Jeremy, G. Gurusubramanian, P. P. Pankaj, R. K. Kharwar, and V. K. Roy. 2022. “Effects of Metformin on the Uterus of d‐Galactose‐Induced Aging Mice: Histomorphometric, Immunohistochemical Localization (B‐Cell Lymphoma 2, Bcl2‐Associated X Protein, and Active capase3), and Oxidative Stress Study.” Journal of Experimental Zoology Part A 337 (6): 600–611. doi:10.1002/jez.2592.
   Google Scholar
• Seifermann, M., A. Ulges, T. Bopp, S. Melcea, A. Schäfer, S. Oka, Y. Nakabeppu, A. Klungland, C. Niehrs, and B. Epe. 2017. “Role of the DNA Repair Glycosylase OGG1 in the Activation of Murine Splenocytes.” DNA Repair 58: 13–20. doi:10.1016/j.dnarep.2017.08.005.
   PubMed Web of Science ®Google Scholar
• Schrans-Stassen, B. H., P. T. Saunders, H. J. Cooke, and D. G. de Rooij. 2001. “Nature of the Spermatogenic Arrest in Dazl−/− Mice.” Biology of Reproduction 65 (3): 771–776. doi:10.1095/biolreprod65.3.771.
   PubMed Web of Science ®Google Scholar
• Sinha, S., A. Dutta, S. N. Singh, and U. S. Ray. 2010. “Protein Nitration, Lipid Peroxidation and DNA Damage at High Altitude in Acclimatized Lowlanders and Native Highlanders: relation with Oxygen Consumption.” Respiratory Physiology & Neurobiology 171 (2): 115–121. doi:10.1016/j.resp.2010.03.002.
   PubMed Web of Science ®Google Scholar
• Smith, L. B, and W. H. Walker. 2014. “The Regulation of Spermatogenesis by Androgens.” Seminars in Cell & Developmental Biology 30: 2–13. doi: 10.1016/j.semcdb.2014.02.012.
   Google Scholar
• Sung, J. H., J. H. Ji, J. D. Park, J. U. Yoon, D. S. Kim, K. S. Jeon, M. Y. Song, et al. 2009. “Subchronic Inhalation Toxicity of Silver Nanoparticles.” Toxicological Sciences 108 (2): 452–461. doi:10.1093/toxsci/kfn246.
   PubMed Web of Science ®Google Scholar
• Shankar, S., L. F. Wang, and J. W. Rhim. 2017. “Preparation and Properties of Carbohydrate-Based Composite Films Incorporated with CuO Nanoparticles.” Carbohydrate Polymers 169: 264–271. doi:10.1016/j.carbpol.2017.04.025.
   PubMed Web of Science ®Google Scholar
• Tang, H., M. Xu, F. Shi, G. Ye, C. Lv, J. Luo, L. Zhao, and Y. Li. 2018. “Effects and Mechanism of Nano-Copper Exposure on Hepatic Cytochrome P450 Enzymes in Rats.” International Journal of Molecular Sciences 19 (7): 2140. doi:10.3390/ijms19072140.
   PubMed Web of Science ®Google Scholar
• Than, A., X. Zhang, M. K. S. Leow, C. L. Poh, S. K. Chong, and P. Chen. 2014. “Apelin Attenuates Oxidative Stress in Human Adipocytes.” The Journal of Biological Chemistry 289 (6): 3763–3774. doi:10.1074/jbc.M113.526210.
   PubMed Web of Science ®Google Scholar
• Umezu, M., S. Kagabu, and S. Sugawara. 1994. “Increase in Testis Weight of Hereditary Dwarf Rats (Rdw/Rdw) with Advancing Age.” Jikken Dobutsu 9Experimental Animals] 43 (4): 577–580. doi:10.1538/expanim1978.43.4_577.
   PubMed Web of Science ®Google Scholar
• Verma, H. P, and S. K. Singh. 2014. “Effect of Aqueous Leaf Extract of DalbergiasissooRoxb. on Spermatogenesis and Fertility in Male Mice.” The European Journal of Contraception & Reproductive Health Care 19 (6): 475–486. doi:10.3109/13625187.2014.945165.
   PubMed Web of Science ®Google Scholar
• Walczak–Jedrzejowska, R., J. K. Wolski, and J. Slowikowska–Hilczer. 2013. “The Role of Oxidative Stress and Antioxidants in Male Fertility.” Central European Journal of Urology 66 (1): 60–67. doi:10.5173/ceju.2013.01.art19.
   PubMedGoogle Scholar
• Wang, Y., H. Tang, M. Xu, J. Luo, L. Zhao, F. Shi, G. Ye, C. Lv, and Y. Li. 2019. “Effect of Copper Nanoparticles on Brain Cytochrome P450 Enzymes in Rats.” Molecular Medicine Reports 20 (1): 771–778. doi:10.3892/mmr.2019.10302.
   PubMed Web of Science ®Google Scholar
• Walker, W. H. 2011. “Testosterone Signaling and the Regulation of Spermatogenesis.” Spermatogenesis 1 (2): 116–120. doi:10.4161/spmg.1.2.16956.
   PubMedGoogle Scholar
• Xu, D., E. Li, B. Karmakar, N. S. Awwad, H. A. Ibrahium, H. E. Osman, A. F. El-Kott, and M. M. Abdel-Daim. 2022. “Green Preparation of Copper Nanoparticle-Loaded Chitosan/Alginate Bio-Composite: Investigation of Its Cytotoxicity, Antioxidant and anti-Human Breast Cancer Properties.” Arabian Journal of Chemistry 15 (3): 103638. doi:10.1016/j.arabjc.2021.103638.
   Web of Science ®Google Scholar
• Zhao, F., Y. Zhao, Y. Liu, X. Chang, C. Chen, and Y. Zhao. 2011. “Cellular Uptake, Intracellular Trafficking, and Cytotoxicity of Nanomaterials.” Small 7 (10): 1322–1337. doi:10.1002/smll.201100001.
   PubMed Web of Science ®Google Scholar
• Zhou, M., X. Ge, D. M. Ke, H. Tang, J. Z. Zhang, M. Calvaresi, B. Gao, L. Sun, Q. Su, and H. Wang. 2019. “The Bioavailability, Biodistribution, and Toxic Effects of Silica-Coated Upconversion Nanoparticles in Vivo.” Frontiers in Chemistry 10 (7): 218.
   Google Scholar