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

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

doi:10.1007/s13105-024-01021-2

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

J Physiol Biochem. 2024 Apr 18. doi: 10.1007/s13105-024-01021-2. Online ahead of print.

Authors

Haibing Pei^{1

2

3}, Zhiyin Lin^{1

2

3}, Kexin Yao^{1

2

3}, Yeqing Luo^{1

2

3}, Ping Tong^{4

5}, Hongbing Chen^{1

3

6}, Yong Wu^{1

3

6}, Zhihua Wu^{1

3

6}, Jinyan Gao^{7

8}

Affiliations

¹ State Key Laboratory of Food Science and Resources, Nanchang University, Nanchang, 330047, P.R. China.
² College of Food Science & Technology, Nanchang University, Nanchang, 330047, P.R. China.
³ Jiangxi Province Key Laboratory of Food Allergy, Nanchang, 330047, P.R. China.
⁴ State Key Laboratory of Food Science and Resources, Nanchang University, Nanchang, 330047, P.R. China. tongping@ncu.edu.cn.
⁵ Jiangxi Province Key Laboratory of Food Allergy, Nanchang, 330047, P.R. China. tongping@ncu.edu.cn.
⁶ Sino-German Joint Research Institute, Nanchang University, Nanchang, 330047, P.R. China.
⁷ College of Food Science & Technology, Nanchang University, Nanchang, 330047, P.R. China. gaojy2013@ncu.edu.cn.
⁸ Jiangxi Province Key Laboratory of Food Allergy, Nanchang, 330047, P.R. China. gaojy2013@ncu.edu.cn.

PMID: 38632209
DOI: 10.1007/s13105-024-01021-2

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.

Keywords: Caenorhabditis elegans; DAF-16; Innate immunity; Insulin/IGF-1 signaling; Ovalbumin; SKN-1.