Skip to main content
Log in

Molecular Regulatory Mechanism of Nano-Se Against Copper-Induced Spermatogenesis Disorder

  • Research
  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

Selenium nanoparticle (Nano-Se) is a new type of selenium supplement, which can improve the deficiency of traditional selenium supplements and maintain its physiological activity. Due to industrial pollution and irrational use in agriculture, Cu overexposure often occurs in animals and humans. In this study, Nano-Se alleviated CuSO4-induced testicular Cu accumulation, serum testosterone level decrease, testicular structural damage, and decrease in sperm quality. Meanwhile, Nano-Se reduced the ROS content in mice testis and enhanced the activities of T-AOC, GSH, SOD, and CAT compared with CuSO4 group. Furthermore, Nano-Se alleviated CuSO4-induced apoptosis by increasing the protein expression of Cleaved-Caspase-3, Cleaved-Caspase-9, Cleaved-Caspase-12, and Bax/Bcl-2 compared with CuSO4 group. At the same time, Nano-Se reversed CuSO4-induced increase of γ-H2AX protein expression in mice testis. In conclusion, this study confirmed that Nano-Se could alleviate oxidative stress, apoptosis, and DNA damage in the testis of mice with Cu excess, thereby protecting the spermatogenesis disorder induced by Cu.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data Availability

The data that support the findings of this study are available from the corresponding author upon reasonable.

References

  1. Tumer Z, Moller LB (2010) Menkes disease. Eur J Hum Genet 18(5):511–518

    Article  PubMed  Google Scholar 

  2. Pierson H, Yang H, Lutsenko S ( 2019) Copper transport and disease: what can we learn from organoids?. Annu Rev Nutr 39:75–94

  3. Ogórek M et al (2017) Atp7a and Atp7b regulate copper homeostasis in developing male germ cells in mice. Metallomics 9(9):1288–1303

    Article  PubMed  Google Scholar 

  4. Han LF et al (2017) Pollution characteristics and source identification of trace metals in riparian soils of Miyun Reservoir China. Ecotoxicol Environ Saf 144:321–329

    Article  CAS  PubMed  Google Scholar 

  5. Brewer GJ (2009) The risks of copper toxicity contributing to cognitive decline in the aging population and to Alzheimer’s disease. J Am Coll Nutr 28(3):238–242

    Article  PubMed  Google Scholar 

  6. Miska-Schramm A, Kruczek M, Kapusta J (2014) Effect of copper exposure on reproductive ability in the bank vole (Myodes glareolus). Ecotoxicology 23(8):1546–1554

    Article  CAS  PubMed  Google Scholar 

  7. Wang T et al (2022) Copper deposition in Wilson’s disease causes male fertility decline by impairing reproductive hormone release through inducing apoptosis and inhibiting ERK signal in hypothalamic-pituitary of mice. Front Endocrinol (Lausanne) 13:961748

    Article  PubMed  Google Scholar 

  8. Zhang ZW et al (2016) Copper-induced spermatozoa head malformation is related to oxidative damage to testes in CD-1 mice. Biol Trace Elem Res 173(2):427–432

    Article  CAS  PubMed  Google Scholar 

  9. Chen H et al (2020) Chronic copper exposure induces hypospermatogenesis in mice by increasing apoptosis without affecting testosterone secretion. Biol Trace Elem Res 195(2):472–480

    Article  CAS  PubMed  Google Scholar 

  10. Chen H et al (2022) Autophagy and apoptosis mediated nano-copper-induced testicular damage. Ecotoxicol Environ Saf 229:113039

    Article  CAS  PubMed  Google Scholar 

  11. Forman HJ, Zhang H (2021) Targeting oxidative stress in disease: promise and limitations of antioxidant therapy. Nat Rev Drug Discov 20(9):689–709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Dröge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82(1):47–95

    Article  PubMed  Google Scholar 

  13. Jomova K, Valko M (2011) Advances in metal-induced oxidative stress and human disease. Toxicology 283(2):65–87

    Article  CAS  PubMed  Google Scholar 

  14. Liu H et al (2020) Copper induces oxidative stress and apoptosis in the mouse liver. Oxid Med Cell Longev 2020:1359164

    PubMed  PubMed Central  Google Scholar 

  15. Guo H et al (2021) Cu-induced spermatogenesis disease is related to oxidative stress-mediated germ cell apoptosis and DNA damage. J Hazard Mater 416:125903

    Article  CAS  PubMed  Google Scholar 

  16. Wang N et al (2017) Supplementation of micronutrient selenium in metabolic diseases: its role as an antioxidant. Oxid Med Cell Longev 2017:7478523

    Article  PubMed  PubMed Central  Google Scholar 

  17. Maiyo F, Singh M (2017) Selenium nanoparticles: potential in cancer gene and drug delivery. Nanomedicine (Lond) 12(9):1075–1089

    Article  CAS  PubMed  Google Scholar 

  18. Forootanfar H et al (2014) Antioxidant and cytotoxic effect of biologically synthesized selenium nanoparticles in comparison to selenium dioxide. J Trace Elem Med Biol 28(1):75–79

    Article  CAS  PubMed  Google Scholar 

  19. Zhai X et al (2017) Antioxidant capacities of the selenium nanoparticles stabilized by chitosan. J Nanobiotechnology 15(1):4

    Article  PubMed  PubMed Central  Google Scholar 

  20. Sadek KM et al (2017) Neuro- and nephrotoxicity of subchronic cadmium chloride exposure and the potential chemoprotective effects of selenium nanoparticles. Metab Brain Dis 32(5):1659–1673

    Article  CAS  PubMed  Google Scholar 

  21. Hassanin KM, Abd El-Kawi SH, and Hashem KS (2013) The prospective protective effect of selenium nanoparticles against chromium-induced oxidative and cellular damage in rat thyroid. Int J Nanomedicine 8:1713–20

  22. Shi LG et al (2010) Effect of elemental nano-selenium on semen quality, glutathione peroxidase activity, and testis ultrastructure in male Boer goats. Anim Reprod Sci 118(2–4):248–254

    Article  CAS  PubMed  Google Scholar 

  23. Yang Y et al (2021) Nickel chloride induces spermatogenesis disorder by testicular damage and hypothalamic-pituitary-testis axis disruption in mice. Ecotoxicol Environ Saf 225:112718

    Article  CAS  PubMed  Google Scholar 

  24. Moghadam MT, Dadfar R, Khorsandi L (2021) The effects of ozone and melatonin on busulfan-induced testicular damage in mice. JBRA Assist Reprod 25(2):176–184

    Article  PubMed  PubMed Central  Google Scholar 

  25. Mehdi Y et al (2013) Selenium in the environment, metabolism and involvement in body functions. Molecules 18(3):3292–3311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Zhang J, Spallholz JE (2011) Toxicity of selenium compounds and Nano‐Selenium particles. Gen Appl Syst Toxicol. https://doi.org/10.1002/9780470744307.GAT243

  27. Chiou Y-D, Hsu Y-J (2011) Room-temperature synthesis of single-crystalline Se nanorods with remarkable photocatalytic properties. Appl Catal B 105(1):211–219

    Article  CAS  Google Scholar 

  28. Mandal T et al (2020) Structural and functional diversity among the members of CTR, the membrane copper transporter family. J Membr Biol 253(5):459–468

    Article  PubMed  PubMed Central  Google Scholar 

  29. Öhrvik H, Thiele DJ (2015) The role of Ctr1 and Ctr2 in mammalian copper homeostasis and platinum-based chemotherapy. J Trace Elem Med Biol 31:178–182

    Article  PubMed  Google Scholar 

  30. Liu H et al (2021) Copper induces hepatocyte autophagy via the mammalian targets of the rapamycin signaling pathway in mice. Ecotoxicol Environ Saf 208:111656

    Article  CAS  PubMed  Google Scholar 

  31. Chen N, Yao P, Zhang W, et al (2023) Selenium nanoparticles: Enhanced nutrition and beyond. Crit Rev Food Sci Nutr 63(33):12360–12371.

  32. Olivari FA, Hernández PP, Allende ML (2008) Acute copper exposure induces oxidative stress and cell death in lateral line hair cells of zebrafish larvae. Brain Res 1244:1–12

    Article  CAS  PubMed  Google Scholar 

  33. Krumschnabel G et al (2005) Oxidative stress, mitochondrial permeability transition, and cell death in Cu-exposed trout hepatocytes. Toxicol Appl Pharmacol 209(1):62–73

    Article  CAS  PubMed  Google Scholar 

  34. Arafa MH et al (2019) Protective effects of Tribulus terrestris extract and angiotensin blockers on testis steroidogenesis in copper overloaded rats. Ecotoxicol Environ Saf 178:113–122

    Article  CAS  PubMed  Google Scholar 

  35. Kheirandish R, Askari N, Babaei H (2014) Zinc therapy improves deleterious effects of chronic copper administration on mice testes: histopathological evaluation. Andrologia 46(2):80–85

    Article  CAS  PubMed  Google Scholar 

  36. Xiao Y et al (2017) Construction of a Cordyceps sinensis exopolysaccharide-conjugated selenium nanoparticles and enhancement of their antioxidant activities. Int J Biol Macromol 99:483–491

    Article  CAS  PubMed  Google Scholar 

  37. Amin KA et al (2017) Antioxidant and hepatoprotective efficiency of selenium nanoparticles against acetaminophen-induced hepatic damage. Biol Trace Elem Res 175(1):136–145

    Article  PubMed  Google Scholar 

  38. Luo M et al (2019) Effect of selenium nanoparticles against abnormal fatty acid metabolism induced by hexavalent chromium in chicken’s liver. Environ Sci Pollut Res Int 26(21):21828–21834

    Article  CAS  PubMed  Google Scholar 

  39. Shao Y et al (2019) Copper-mediated mitochondrial fission/fusion is associated with intrinsic apoptosis and autophagy in the testis tissues of chicken. Biol Trace Elem Res 188(2):468–477

    Article  CAS  PubMed  Google Scholar 

  40. Sarkar A et al (2011) Nano-copper induces oxidative stress and apoptosis in kidney via both extrinsic and intrinsic pathways. Toxicology 290(2):208–217

    Article  PubMed  Google Scholar 

  41. Guo H, Liu H, Wu H, et al (2019) Nickel Carcinogenesis Mechanism: DNA Damage. Int J Mol Sci 20(19):4690

  42. Linder MC (2012) The relationship of copper to DNA damage and damage prevention in humans. Mutat Res/Fundam. Mol. Mech. Mutagen 733(1):83–91

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the national key research and development project (2022YFD1601600), China Agriculture Research System of MOF and MARA (Beef Cattle/Yak, CARS-37), and Innovative Team for Beef Cattle Low-Carbon Production (2022–2024).

Author information

Authors and Affiliations

Authors

Contributions

Yujuan Ouyang: methodology, investigation, formal analysis, and writing—original draft. Yanbing Lou: methodology, investigation, formal analysis, and writing—original draft. Yanqiu Zhu: methodology, investigation, formal analysis, and writing—original draft. Yihan Wang: methodology. Song Zhu: methodology. Lin Jing: methodology. Tingting Yang: methodology. Hengmin Cui: methodology. Huidan Deng: methodology. Zhicai Zuo: methodology. Jing Fang: writing—review and editing and project administration. Hongrui Guo: conceptualization, experiment design, writing—review and editing, and funding acquisition.

Corresponding author

Correspondence to Hongrui Guo.

Ethics declarations

Competing interests

The authors declare no competing interests.

Conflict of Interest

The authors declare no conflict of interest.

Ethics Approval

All procedures related to animals were conducted in accordance with the guidelines of the Animal Care and the Ethics Committee of Sichuan Agricultural University (Approval No: 2012–024, Chengdu, China).

Consent for Publication

All the authors have consented to the publication of this research.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 4179 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ouyang, Y., Lou, Y., Zhu, Y. et al. Molecular Regulatory Mechanism of Nano-Se Against Copper-Induced Spermatogenesis Disorder. Biol Trace Elem Res (2024). https://doi.org/10.1007/s12011-024-04153-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12011-024-04153-0

Keywords

Navigation