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Differential analysis of ovarian tissue between high and low-yielded laying hens in the late laying stage and the effect of LECT2 gene on follicular granulosa cells proliferation

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Abstract

The ovaries of high-yield laying hens exhibited signs of aging beyond 400 days of age, subsequently resulting in a decline in both egg production and egg quality. Oxidative stress, characterized by an increase in the production of reactive oxygen species (ROS), stands as one of the principal processes contributing to ovarian aging. Elevated ROS levels are implicated in the induction of apoptosis in granulosa cells (GCs), provoking mitochondrial impairment, and diminishing the capacity of the antioxidant defense system. This investigation stratified laying hens into two distinct groups, predicated upon their egg production levels: high-yield hens (HH) and low-yield hens (LL). The study focused on evaluating oxidative stress markers and identifying differentially expressed genes between these two groups. The findings revealed that the LL group exhibited follicular atresia, mitochondrial disruptions, and apoptotic occurrences in ovarian GCs. Notably, ROS levels, Malondialdehyde (MDA) concentrations, and 8-hydroxy-2'-deoxyguanosine (8-OHdG) concentrations in ovarian tissue and follicular GCs were substantially higher in the HH group. Furthermore, the RNA-sequencing results unveiled differential expression of the LECT2 gene between the HH and LL groups. Consequently, an overexpression vector for the LECT2 gene was successfully constructed and introduced into GCs. The quantitative polymerase chain reaction (QPCR) analysis exhibited significant downregulation (p < 0.01) of key apoptotic genes such as Caspase-3 and C-myc and significant upregulation (p < 0.01) of BCL2 following the overexpression of the LECT2 gene in GCs. In conclusion, oxidative stress emerges as a pivotal factor influencing the laying traits of both high and low-yield laying hens. The accumulation of reactive oxygen species (ROS) within the ovaries precipitates apoptosis in GCs, subsequently leading to follicular atresia and a reduction in egg production. Furthermore, we employed RNA sequencing technology to examine the ovarian matrix tissue in high and low laying hens during the late phase of egg laying. Our analysis revealed a substantial upregulation of the LECT2 gene in the ovarian matrix tissue of high laying hens. This observation implies that the LECT2 gene exerts a pivotal influence on driving the proliferation and differentiation of follicular GCs, thereby exerting a crucial regulatory role in follicular development.

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Funding

This work was supported by the National Key Research and Development Program of China (2022YFD1300100), China Agriculture Research System of MOF and MARA (CARS-40, CARS-41).

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Author notes

  1. Lin Chen and Xianqiang Li have contributed equally to this work.

Authors and Affiliations

  1. Animal Husbandry and Veterinary Research Institute, Hubei Key Laboratory of Animal Embryo and Molecular Breeding, Hubei Academy of Agricultural Sciences, Wuhan, 430000, China

    Lin Chen, Xianqiang Li, Yan Wu & Jinsong Pi

  2. College of Animal Science, Yangtze University, Jingzhou, 434000, China

    Lin Chen, Xianqiang Li & Jiaxiang Wang

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  1. Lin Chen
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  3. Yan Wu
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Contributions

The project’s conceptualization was initiated by LC and XL. LC took charge of the research execution and subsequent data analysis. All authors collaborated in the composition of the manuscript. The ultimate responsibility for the final manuscript rested with YW. All authors diligently reviewed and granted their approval for the concluding version of the manuscript.

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Correspondence to Yan Wu.

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All studies involving animals were conducted according to the regulation (No. 5 proclaim of the Standing Committee of Hubei People’s Congress) approved by the Standing Committee of Hubei People’s Congress, P. R. China. Sample collection was approved by the ethics committee of Hubei Academy of Agricultural Sciences. Animals were humanely sacrificed as necessary to ameliorate suffering.

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Chen, L., Li, X., Wu, Y. et al. Differential analysis of ovarian tissue between high and low-yielded laying hens in the late laying stage and the effect of LECT2 gene on follicular granulosa cells proliferation. Mol Biol Rep 51, 240 (2024). https://doi.org/10.1007/s11033-024-09260-8

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