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Animal Models

Paternal obesity induces subfertility in male offspring by modulating the oxidative stress-related transcriptional network

International Journal of Obesity (2024)Cite this article

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Abstract

Background/objective

The effects of fathers’ high-fat diet (HFD) on the reproductive health of their male offspring (HFD- F1) remain to be elucidated. Parental obesity is known to have a negative effect on offspring fertility, but there are few relevant studies on the effects of HFD-F1 on reproductive function.

Methods

We first succeeded in establishing the HFD model, which provides a scientific basis in the analysis of HFD-F1 reproductive health. Next, we assessed biometric indices, intratesticular cellular status, seminiferous tubules and testicular transcriptomic homeostasis in HFD-F1. Finally, we examined epididymal (sperm-containing) apoptosis, as well as antioxidant properties, motility, plasma membrane oxidation, DNA damage, and sperm-egg binding in the epididymal sperm.

Results

Our initial results showed that HFD-F1 mice had characteristics similar to individuals with obesity, including higher body weight and altered organ size. Despite no major changes in the types of testicular cells, we found decreased activity of important genes and noticed the presence of abnormally shaped sperm at seminiferous tubule lumen. Further analysis of HFD-F1 testes suggests that these changes might be caused by increased vulnerability to oxidative stress. Finally, we measured several sperm parameters, these results presented HFD-F1 offspring exhibited a deficiency in antioxidant properties, resulting in damaged sperm mitochondrial membrane potential, insufficient ATP content, increased DNA fragmentation, heightened plasma membrane oxidation, apoptosis-prone and decreased capacity for sperm-oocyte binding during fertilization.

Conclusion

HFD- F1 subfertility arises from the susceptibility of the transcriptional network to oxidative stress, resulting in reduced antioxidant properties, motility, sperm-egg binding, and elevated DNA damage.

Schematic representation of the HFD-F1 oxidative stress susceptibility to subfertility. Notably, excessive accumulation of ROS surpasses the physiological threshold, thereby damaging PUFAs within the sperm plasma membrane. This oxidative assault affects crucial components such as mitochondria and DNA. Consequently, the sperm’s antioxidant defense mechanisms become compromised, leading to a decline in vitality, motility, and fertility.

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Fig. 1: Detection of biological characteristics of HFD mice.
Fig. 2: Assessment of biological features of mouse.
Fig. 3: Detection of different cell populations and antioxidant markers in the testis.
Fig. 4: Transcriptome data of testis of HFD-F1 and NC-F1.
Fig. 5: Evaluation of sperm oxidation index and oxidation properties index.
Fig. 6: CASA assesses sperm motility.
Fig. 7: Detection of sperm DNA damage by 8-OHdG and γ‐H2AX.
Fig. 8: Evaluate the expression of BAX, BCL2, CASP3 apoptosis-related proteins.
Fig. 9: Evaluation of sperm plasma membrane oxidation, phosphorylation and sperm-egg binding.

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All data will be made available on request.

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Acknowledgements

We acknowledge the assisted by the Northwest A&F University, the reproductive biology and cell engineering team at college of animal science and technology, and Ankang R&D Center of Se-enriched Products. This work was supported by grant from National Natural Science Foundation of China (Grant No. C1704-32172737) for financial support.

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  1. These authors contributed equally: Long Li, Yuxuan Ma, Chao Zhu.

Authors and Affiliations

  1. College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, 712100, P.R. China

    Long Li, Yuxuan Ma, Chao Zhu, Yan Li, Heran Cao, Zifang Wu, Tianqi Jin, Yang Wang, Shaoxian Chen & Wuzi Dong

  2. Biology Research Centre of Qin Mountains Wildlife, Northwest A&F University, Yangling, Shaanxi, 712100, China

    Yuxuan Ma & Wuzi Dong

  3. Ankang R&D Center of Se-enriched Products, Ankang, Shaanxi, 725000, China

    Chao Zhu

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Contributions

The completion of this study is mainly divided into four parts, and all the authors undertake the corresponding tasks in one or more parts. Part I, experimental design (LL and WZD), and part II, the collection and specific execution of experimental materials (YXM, YL, HRC, ZFW, TQJ, and YW); Part III, statistical analysis of data and manuscript writing (LL and YXM); The fourth part IV, final proofreading of the article (LL, ZC, SXC, and WZD). The authors read and agreed with the eventual manuscript for publication.

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Correspondence to Wuzi Dong.

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Li, L., Ma, Y., Zhu, C. et al. Paternal obesity induces subfertility in male offspring by modulating the oxidative stress-related transcriptional network. Int J Obes (2024). https://doi.org/10.1038/s41366-024-01562-y

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