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Ovalbumin promotes innate immune response of Caenorhabditis elegans through DAF-16 and SKN-1 pathways in insulin/IGF-1 signaling

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Abstract

Ovalbumin (OVA) is a major allergen in eggs and could induce severe allergic reactions in sensitive individuals, where the innate immune system works as a regulator. The mechanism of how innate immunity adjusts to food allergy is relatively well-studied, however, the effects of allergen uptake on the innate immune system remain unclear. Therefore, the Caenorhabditis elegans (C. elegans) model was utilized to assess the effects of OVA on its innate immune system. OVA enhanced the immune response of C. elegans with higher survival rates under Pseudomonas aeruginosa infection. Moreover, sustaining OVA treatment improved the health states that were reflected in the prolonged lifespan, alleviated oxidative stress, accelerated growth, and promoted motility. RNA-sequencing analysis and the slow-killing assays in the mutants of insulin/IGF-1 signaling (IIS)-related genes confirmed that IIS was necessary for OVA to regulate innate immunity. Besides, OVA activated SKN-1 temporarily and facilitated the nuclear localization of DAF-16 for improving immunity and health status in C. elegans. Together, OVA could enhance the innate immune responses via DAF-16 and SKN-1 pathways in the IIS of C. elegans, and this work will provide novel insights into the regulation of innate immunity by OVA in higher organisms.

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Acknowledgments

This work was supported by the National Natural Science Foundation of China (No. 32072339). The authors also thank Guangxi Key Laboratory of Marine Drugs for providing Pseudomonas aeruginosa strains and the Caenorhabditis Genetics Center (CGC, University of Minnesota, USA) for providing the worm strains.

Funding

This work was supported by the National Natural Science Foundation of China (No. 32072339).

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Authors and Affiliations

  1. State Key Laboratory of Food Science and Resources, Nanchang University, Nanchang, 330047, P.R. China

    Haibing Pei, Zhiyin Lin, Kexin Yao, Yeqing Luo, Ping Tong, Hongbing Chen, Yong Wu & Zhihua Wu

  2. College of Food Science & Technology, Nanchang University, Nanchang, 330047, P.R. China

    Haibing Pei, Zhiyin Lin, Kexin Yao, Yeqing Luo & Jinyan Gao

  3. Jiangxi Province Key Laboratory of Food Allergy, Nanchang, 330047, P.R. China

    Haibing Pei, Zhiyin Lin, Kexin Yao, Yeqing Luo, Ping Tong, Hongbing Chen, Yong Wu, Zhihua Wu & Jinyan Gao

  4. Sino-German Joint Research Institute, Nanchang University, Nanchang, 330047, P.R. China

    Hongbing Chen, Yong Wu & Zhihua Wu

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Contributions

P T designed the study. HB P, ZY L, KX Y, and YQ L conducted experiments and analyzed the data. Y W developed the methodology. All authors participated in writing the original draft. P T, ZH W, and JY G critically revised the manuscript. HB C supervised the research. All authors have read and approved the final manuscript. The authors declare that all data were generated in-house and that no paper mill was used.

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Correspondence to Ping Tong or Jinyan Gao.

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Key points

1. OVA enhanced the innate immune responses of C. elegans.

2. Sustaining OVA treatment brought health and life-promoting benefits to C. elegans.

3. Insulin/IGF-1 signaling is involved in the innate immune responses of C. elegans with OVA treatment.

4. OVA differently regulates DAF-16 and SKN-1 nuclear translocation for enhancing immune responses and improving health status in C. elegans.

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Pei, H., Lin, Z., Yao, K. et al. Ovalbumin promotes innate immune response of Caenorhabditis elegans through DAF-16 and SKN-1 pathways in insulin/IGF-1 signaling. J Physiol Biochem (2024). https://doi.org/10.1007/s13105-024-01021-2

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