Repeated administrations of Mn₃O₄ nanoparticles cause testis damage and fertility decrease through PPAR-signaling pathway

References

• Adhikari, A., N. Polley, S. Darbar, D. Bagchi, and S. K. Pal. 2016. “Citrate Functionalized Mn3O4 in Nanotherapy of Hepatic Fbrosis by Oral Administration.” Future Science OA 2: 146. doi:10.4155/fsoa-2016-0029.
   Web of Science ®Google Scholar
• Adhikari, A., N. Polley, S. Darbar, and S. K. Pal. 2017. “Therapeutic Potential of Surface Functionalized Mn3O4 Nanoparticles against Chronic Liver Diseases in Murine Model.” Materials Focus 6 (3): 280–289. doi:10.1166/mat.2017.1403.
   Google Scholar
• Aly, H. A. A., and R. M. Khafagy. 2014. “Taurine Reverses Endosulfan-Induced Oxidative Stress and Apoptosis in Adult Rat Testis.” Food and Chemical Toxicology 64: 1–9. doi:10.1016/j.fct.2013.11.007.
   PubMed Web of Science ®Google Scholar
• Bae, E., H.-J. Park, J. Lee, Y. Kim, J. Yoon, K. Park, K. Choi, et al. 2010. “Bacterial Cytotoxicity of the Silver Nanoparticle Related to Physicochemical Metrics and Agglomeration Properties.” Environmental Toxicology and Chemistry 29 (10): 2154–2160. doi:10.1002/etc.278.
   PubMed Web of Science ®Google Scholar
• Deonandan, R., and M. Jaleel. 2012. “Global Decline in Semen Quality: ignoring the Developing World Introduces Selection Bias.” International Journal of General Medicine 5: 303–306. doi:10.2147/IJGM.S30673.
   PubMedGoogle Scholar
• El-Demerdash, F. M. 2011. “Lipid Peroxidation, Oxidative Stress and Acetylcholinesterase in Rat Brain Exposed to Organophosphate and Pyrethroid Insecticides.” Food and Chemical Toxicology : An International Journal Published for the British Industrial Biological Research Association 49 (6): 1346–1352. doi:10.1016/j.fct.2011.03.018.
   PubMed Web of Science ®Google Scholar
• Ema, M., N. Kobayashi, M. Naya, S. Hanai, and J. Nakanishi. 2010. “Reproductive and Developmental Toxicity Studies of Manufactured Nanomaterials.” Reproductive Toxicology 30 (3): 343–352. doi:10.1016/j.reprotox.2010.06.002.
   PubMed Web of Science ®Google Scholar
• Farombi, E. O., I. A. Adedara, G. E. Forcados, O. O. Anao, A. Agbowo, and A. K. Patlolla. 2016. “Responses of Testis, Epididymis, and Sperm of Pubertal Rats Exposed to Functionalized Multiwalled Carbon Nanotubes.” Environmental Toxicology 31 (5): 543–551. doi:10.1002/tox.22067.
   PubMed Web of Science ®Google Scholar
• Giri, A., N. Goswami, M. Pal, M. T. Zar Myint, S. Al-Harthi, A. Singha, B. Ghosh, et al. 2013. “Rational Surface Modification of Mn3O4 Nanoparticles to Induce Multiple Photoluminescence and Room Temperature Ferromagnetism.” Journal of Materials Chemistry C 1 (9): 1885–1895. doi:10.1039/c3tc00709j.
   PubMed Web of Science ®Google Scholar
• Hong, F., W. Si, X. Zhao, L. Wang, Y. Zhou, M. Chen, Y. Ge, et al. 2015a. “TiO2 Nanoparticle Exposure Decreases Spermatogenesis via Biochemical Dysfunctions in the Testis of Male Mice.” Journal of Agricultural and Food Chemistry 63 (31): 7084–7092. doi:10.1021/acs.jafc.5b02652.
   PubMed Web of Science ®Google Scholar
• Hong, F., X. Zhao, W. Si, Y. Ze, L. Wang, Y. Zhou, J. Hong, et al. 2015b. “Decreased Spermatogenesis Led to Alterations of Testis-Specific Gene Expression in Male Mice following nano-TiO2 Exposure.” Journal of Hazardous Materials 300: 718–728. doi:10.1016/j.jhazmat.2015.08.010.
   PubMed Web of Science ®Google Scholar
• Huang, C., B. Li, K. Xu, D. Liu, J. Hu, Y. Yang, H. C. Nie, et al. 2017. “Decline in Semen Quality among 30,636 Young Chinese Men from 2001 to 2015.” Fertility and Sterility 107 (1): 83–88. doi:10.1016/j.fertnstert.2016.09.035.
   PubMed Web of Science ®Google Scholar
• Huleihel, M., and E. Lunenfeld. 2004. “Regulation of Spermatogenesis by Paracrine/Autocrine Testicular Factors.” Asian Journal of Andrology 6 (3): 259–268.
   PubMed Web of Science ®Google Scholar
• Kim, B., G. Han, B. J. Toley, C. K. Kim, V. M. Rotello, and N. S. Forbes. 2010. “Tuning Payload Delivery in Tumour Cylindroids Using Gold Nanoparticles.” Nature Nanotechnology 5 (6): 465–472. doi:10.1038/nnano.2010.58.
   PubMed Web of Science ®Google Scholar
• Kong, L., M. Tang, T. Zhang, D. Wang, K. Hu, W. Lu, C. Wei, et al. 2014. “Nickel Nanoparticles Exposure and Reproductive Toxicity in Healthy Adult Rats.” International Journal of Molecular Sciences 15 (11): 21253–21269. doi:10.3390/ijms151121253.
   PubMed Web of Science ®Google Scholar
• Lei, S. J., K. B. Tang, Z. Fang, and H. G. Zheng. 2006. “Ultrasonic-Assisted Synthesis of Colloidal Mn3O4 Nanoparticles at Normal Temperature and Pressure.” Crystal Growth and Design 6 (8): 1757–1760. doi:10.1021/cg050402o.
   Web of Science ®Google Scholar
• Li, W. Q., F. Wang, Z. M. Liu, Y. C. Wang, J. Wang, and F. Sun. 2013. “Gold Nanoparticles Elevate Plasma Testosterone Levels in Male Mice without Affecting Fertility.” Small 9 (9-10): 1708–1714. doi:10.1002/smll.201201079.
   PubMed Web of Science ®Google Scholar
• Li, X., X. Yang, L. Yuwen, W. Yang, L. Weng, Z. Teng, L. Wang, et al. 2016. “Evaluation of Toxic Effects of CdTe Quantum Dots on the Reproductive System in Adult Male Mice.” Biomaterials 96: 24–32. doi:10.1016/j.biomaterials.2016.04.014.
   PubMed Web of Science ®Google Scholar
• Liu, J. J., D. W. Li, K. Zhang, M. X. Yang, H. C. Sun, and B. Yang. 2018. “One-Step Hydrothermal Synthesis of Nitrogen-Doped Conjugated Carbonized Polymer Dots with 31% Efficient Red Emission for in Vivo Imaging.” Small 14 (15): 1703919. doi:10.1002/smll.201703919.
   Web of Science ®Google Scholar
• Liu, J. N., W. B. Bu, and J. L. Shi. 2017. “Chemical Design and Synthesis of Functionalized Probes for Imaging and Treating Tumor Hypoxia.” Chemical Reviews 117 (9): 6160–6224. doi:10.1021/acs.chemrev.6b00525.
   PubMed Web of Science ®Google Scholar
• Liu, X., M. Wu, Q. Hu, H. Bai, S. Zhang, Y. Shen, G. Tang, et al. 2016. “Redox-Activated Light-up Nanomicelle for Precise Imaging-Guided Cancer Therapy and Real-Time Pharmacokinetic Monitoring.” ACS Nano 10 (12): 11385–11396. doi:10.1021/acsnano.6b06688.
   PubMed Web of Science ®Google Scholar
• Meena, R., K. Kajal, and R. Paulraj. 2015. “Cytotoxic and Genotoxic Effects of Titanium Dioxide Nanoparticles in Testicular Cells of Male Wistar Rat.” Applied Biochemistry and Biotechnology 175 (2): 825–840. doi:10.1007/s12010-014-1299-y.
   PubMed Web of Science ®Google Scholar
• Murugesan, P., T. Muthusamy, K. Balasubramanian, and J. Arunakaran. 2005. “Studies on the Protective Role of Vitamin C and E against Polychlorinated Biphenyl (Aroclor 1254)-Induced Oxidative Damage in Leydig Cells.” Free Radical Research 39 (11): 1259–1272. doi:10.1080/10715760500308154.
   PubMed Web of Science ®Google Scholar
• Nafiujjaman, M., M. Nurunnabi, S. H. Kang, G. R. Reeck, H. A. Khan, and Y. K. Lee. 2015. “Ternary Graphene Quantum Dot-polydopamine-Mn3O4 Nanoparticles for Optical Imaging Guided Photodynamic Therapy and T-1-Weighted Magnetic Resonance Imaging.” Journal of Materials Chemistry B 3 (28): 5815–5823. doi:10.1039/C5TB00479A.
   Web of Science ®Google Scholar
• Oliva, R., and J. Castillo. 2011. “Proteomics and the Genetics of Sperm Chromatin Condensation.” Asian Journal of Andrology 13 (1): 24–30. doi:10.1038/aja.2010.65.
   PubMed Web of Science ®Google Scholar
• Polley, N., S. Saha, A. Adhikari, S. Banerjee, S. Darbar, S. Das, S. K. Pal, et al. 2015. “Safe and Symptomatic Medicinal Use of Surface-Functionalized Mn3O4 Nanoparticles for Hyperbilirubinemia Treatment in Mice.” Nanomedicine 10 (15): 2349–2363. doi:10.2217/nnm.15.83.
   PubMed Web of Science ®Google Scholar
• Purvis, K., and E. Christiansen. 1992. “Male Infertility: current Concepts.” Annals of Medicine 24 (4): 259–272. doi:10.3109/07853899209149953.
   PubMed Web of Science ®Google Scholar
• Rahaman, H., A. Nath, R. Paul, M. Sengupta, and S. K. Ghosh. 2016. “Fe3O4-Mn3O4 Nanocomposites with Moderate Magnetism for in Vitro Cytotoxicity Studies on Macrophages.” RSC Advances 6 (86): 83146–83153. doi:10.1039/C6RA17493K.
   Web of Science ®Google Scholar
• Saha, A., S. C. Mohanta, K. Deka, P. Deb, and P. S. Devi. 2017. “Surface-Engineered Multifunctional Eu: Gd2O3 Nanopiates for Targeted and pH-Responsive Drug Delivery and Imaging Applications.” ACS Applied Materials & Interfaces 9 (4): 4126–4141. doi:10.1021/acsami.6b12804.
   PubMed Web of Science ®Google Scholar
• Saleh, R. A., and A. Agarwal. 2002. “Oxidative Stress and Male Infertility: From Research Bench to Clinical Practice.” Journal of Andrology 23 (6): 737–752.
   PubMedGoogle Scholar
• Sanchez, R., C. Cheuqueman, J. Risopatron, R. Felmer, J. Alvarez, and T. Mogas. 2013. “Modulation of Oxidative Stress during in Vitro Fertilization in Bovine: Effects of Melatonin on Sperm Function and Subsequent Embryo Development.” Fertility and Sterility 100: 426–427.
   Web of Science ®Google Scholar
• Shi, J. P., X. Sun, S. H. Zheng, J. L. Li, X. Y. Fu, and H. W. Zhang. 2018. “A New near-Infrared Persistent Luminescence Nanoparticle as a Multifunctional Nanoplatform for Multimodal Imaging and Cancer Therapy.” Biomaterials 152: 15–23. doi:10.1016/j.biomaterials.2017.10.032.
   PubMed Web of Science ®Google Scholar
• Sofikitis, N., N. Giotitsas, P. Tsounapi, D. Baltogiannis, D. Giannakis, and N. Pardalidis. 2008. “Hormonal Regulation of Spermatogenesis and Spermiogenesis.” The Journal of Steroid Biochemistry and Molecular Biology 109 (3-5): 323–330. doi:10.1016/j.jsbmb.2008.03.004.
   PubMed Web of Science ®Google Scholar
• Sreelatha, S., P. R. Padma, and M. Umadevi. 2009. “Protective Effects of Coriandrum Sativum Extracts on Carbon Tetrachloride-Induced Hepatotoxicity in Rats.” Food and Chemical Toxicology 47 (4): 702–708. doi:10.1016/j.fct.2008.12.022.
   PubMed Web of Science ®Google Scholar
• Thomas, K. H., D. Y. Sung, X. Chen, R. Gibbs, J. McCarrey, and W. Walker. 2011. “Developmental Patterns of PPAR/RXR Gene Expression during Spermatogenesis.” Frontiers in Bioscience 3: 1209–1220. doi:10.2741/e324.
   Google Scholar
• Tremellen, K. 2008. “Oxidative Stress and Male Infertility-a Clinical Perspective.” Human Reproduction Update 14 (3): 243–258. doi:10.1093/humupd/dmn004.
   PubMed Web of Science ®Google Scholar
• Vernet, P., R. J. Aitken, and J. R. Drevet. 2004. “Antioxidant Strategies in the Epididymis.” Molecular and Cellular Endocrinology 216 (1-2): 31–39. doi:10.1016/j.mce.2003.10.069.
   PubMed Web of Science ®Google Scholar
• Wu, J., C. Wang, J. Sun, and Y. Xue. 2011. “Neurotoxicity of silica nanoparticles: brain localization and dopaminergic neurons damage pathways.” ACS Nano 5 (6): 4476–4489. doi:10.1021/nn103530b.
   Google Scholar
• Xu, Y., N. Wang, Y. Yu, Y. Li, Y. B. Li, Y. B. Yu, X. Q. Zhou, and Z. W. Sun. 2014. “Exposure to silica nanoparticles causes reversible damage of the spermatogenic process in Mice.” PLOS ONE 9 (7): e101572. doi:10.1371/journal.pone.0101572.
   Google Scholar
• Yi, X., W. Zhao, J. Li, B. Zhang, Q. Yu, and M. Li. 2017. “Mn3O4 Nanoparticles Cause Endoplasmic Reticulum Stress-Dependent Toxicity to Saccharomyces cerevisiae.” RSC Advances. 7 (73): 46028–46035. doi:10.1039/C7RA07458A.
   Web of Science ®Google Scholar
• Yi, Z. J., Y. R. Fu, M. Li, K. S. Gao, and X. G. Zhang. 2009. “Effect of LTA Isolated from Bifidobacteria on D-Galactose-Induced Aging.” Experimental Gerontology 44 (12): 760–765. doi:10.1016/j.exger.2009.08.011.
   PubMed Web of Science ®Google Scholar
• Yu, Q., Y. M. Zhang, Y. H. Liu, and Y. Liu. 2019. “Magnetic Supramolecular Nanofibers of Gold Nanorods for Photothermal Therapy.” Advanced Therapeutics 2 (4): 1800137. doi:10.1002/adtp.201800137.
   Google Scholar
• Yu, Q., Y. M. Zhang, Y. H. Liu, X. Xu, and Y. Liu. 2018. “Magnetism and Photo Dual-Controlled Supramolecular Assembly for Suppression of Tumor Invasion and Metastasis.” Science Advances 4 (9): eaat2297. doi:10.1126/sciadv.aat2297.
   PubMed Web of Science ®Google Scholar
• Yu, Q. Y., S. M. Fang, W. D. Zuo, F. Y. Dai, Z. Zhang, and C. Lu. 2011. “Effect of Organophosphate Phoxim Exposure on Certain Oxidative Stress Biomarkers in the Silkworm.” Journal of Economic Entomology 104 (1): 101–106. doi:10.1603/EC10260.
   PubMed Web of Science ®Google Scholar
• Zhang, H., Q. L. Li, H. Y. Lin, Q. Yang, H. M. Wang, and C. Zhu. 2007. “Role of PPAR Gamma and Its Gonadotrophic Regulation in Rat Ovarian Granulosa Cells in Vitro.” Neuro Endocrinology Letters 28 (3): 289–294.
   PubMed Web of Science ®Google Scholar
• Zhang, L. W., S. Gao, F. Zhang, K. Yang, Q. J. Ma, and L. Zhu. 2014. “Activatable Hyaluronic Acid Nanoparticle as a Theranostic Agent for Optical/Photoacoustic Image-Guided Photothermal Therapy.” ACS Nano 8 (12): 12250–12258. doi:10.1021/nn506130t.
   PubMed Web of Science ®Google Scholar
• Zhang, P., Y. Zhan, B. Cai, C. Hao, J. Wang, C. Liu, Z. Meng, et al. 2010. “Shape-Controlled Synthesis of Mn3O4 Nanocrystals and Their Catalysis of the Degradation of Methylene Blue.” Nano Research 3 (4): 235–243. doi:10.1007/s12274-010-1026-0.
   Web of Science ®Google Scholar
• Zook, J. M., R. I. MacCuspie, L. E. Locascio, M. D. Halter, and J. T. Elliott. 2011. “Stable Nanoparticle Aggregates/Agglomerates of Different Sizes and the Effect of Their Size on Hemolytic Cytotoxicity.” Nanotoxicology 5 (4): 517–530. doi:10.3109/17435390.2010.536615.
   PubMed Web of Science ®Google Scholar