Integrating proteomics and metabolomics to elucidate the regulatory mechanisms of pimpled egg production in chickens

Eggshells not only protect the contents of the egg from external damage but are also a key factor influencing consumer choice, second only to price. In the later stages of egg production, the incidence of pimpled eggs significantly increases, severely affecting the hatchability and food safety of th...

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Main Authors: Wenqiang Li, Xueying Ma, Xiaomin Li, Xuguang Zhang, Yifei Sun, Chao Ning, Qin Zhang, Dan Wang, Hui Tang
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:Poultry Science
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Online Access:http://www.sciencedirect.com/science/article/pii/S0032579125000550
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author Wenqiang Li
Xueying Ma
Xiaomin Li
Xuguang Zhang
Yifei Sun
Chao Ning
Qin Zhang
Dan Wang
Hui Tang
author_facet Wenqiang Li
Xueying Ma
Xiaomin Li
Xuguang Zhang
Yifei Sun
Chao Ning
Qin Zhang
Dan Wang
Hui Tang
author_sort Wenqiang Li
collection DOAJ
description Eggshells not only protect the contents of the egg from external damage but are also a key factor influencing consumer choice, second only to price. In the later stages of egg production, the incidence of pimpled eggs significantly increases, severely affecting the hatchability and food safety of the eggs. This study compares the differences in the uterine proteomes and metabolomes of hens producing pimpled eggs and those producing normal eggs, aiming to identify the proteins and metabolites that may play a crucial role in the formation of pimpled eggs. A total of 242 differentially expressed proteins (DEPs) were identified in uterine tissue, of which 116 were upregulated and 126 were downregulated. Enrichment analysis revealed that the DEPs were enriched in pathways related to ion transport, energy metabolism, and immune responses. The study found that in the normal eggs (NE) group, HCO₃⁻ was predominantly transported via SLC4A1, although other transport pathways may also play a role. In contrast, in the pimpled eggs (PE) group, bicarbonate ions (HCO₃⁻) was primarily transported through SLC4A4. Additionally, a total of 44 differentially metabolites (DMs) were identified in the uterus, with 5′-Adenylic acid (ATP) being significantly downregulated in the PE group. The ions and matrix proteins required for eggshell formation are transported from uterine cells to the uterine fluid against a concentration gradient, a process that consumes a substantial amount of energy. The decrease in ATP concentration in the PE group may be a significant factor influencing the formation of pimpled eggs. Subsequently, we found that the DEPs and DMs were jointly enriched in several signaling pathways, including the FoxO signaling pathway related to energy metabolism, nicotinate and nicotinamide metabolism, and tryptophan metabolism associated with immune response. Notably, the DMs involved in these signaling pathways were all downregulated in the PE group. Our research findings indicate that SLC4A1, SLC4A2, and ATP2B4 (DEPs), along with 5′-adenylic acid and trigonelline (DMs), influence the formation of eggshells through mechanisms related to energy metabolism, ion transport, and immune response. These DEPs and DMs may serve as potential biomarkers for the genetic improvement of eggshell quality.
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series Poultry Science
spelling doaj-art-b18982b17d0f410fb17681a3cc9fc4412025-01-19T06:23:48ZengElsevierPoultry Science0032-57912025-02-011042104818Integrating proteomics and metabolomics to elucidate the regulatory mechanisms of pimpled egg production in chickensWenqiang Li0Xueying Ma1Xiaomin Li2Xuguang Zhang3Yifei Sun4Chao Ning5Qin Zhang6Dan Wang7Hui Tang8Shandong Provincial Key laboratory for Livestock Germplasm Innovation & Utilization, College of Animal Science and Technology, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province 271018, PR ChinaShandong Provincial Key laboratory for Livestock Germplasm Innovation & Utilization, College of Animal Science and Technology, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province 271018, PR ChinaShandong Provincial Key laboratory for Livestock Germplasm Innovation & Utilization, College of Animal Science and Technology, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province 271018, PR ChinaShandong Provincial Key laboratory for Livestock Germplasm Innovation & Utilization, College of Animal Science and Technology, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province 271018, PR ChinaShandong Provincial Key laboratory for Livestock Germplasm Innovation & Utilization, College of Animal Science and Technology, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province 271018, PR ChinaShandong Provincial Key laboratory for Livestock Germplasm Innovation & Utilization, College of Animal Science and Technology, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province 271018, PR ChinaShandong Provincial Key laboratory for Livestock Germplasm Innovation & Utilization, College of Animal Science and Technology, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province 271018, PR ChinaShandong Provincial Key laboratory for Livestock Germplasm Innovation & Utilization, College of Animal Science and Technology, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province 271018, PR ChinaCorrespondence author at: No. 61, Daizong Street, Tai'an City, Shandong Province 271018, China.; Shandong Provincial Key laboratory for Livestock Germplasm Innovation & Utilization, College of Animal Science and Technology, Shandong Agricultural University, 61 Daizong Street, Taian City, Shandong Province 271018, PR ChinaEggshells not only protect the contents of the egg from external damage but are also a key factor influencing consumer choice, second only to price. In the later stages of egg production, the incidence of pimpled eggs significantly increases, severely affecting the hatchability and food safety of the eggs. This study compares the differences in the uterine proteomes and metabolomes of hens producing pimpled eggs and those producing normal eggs, aiming to identify the proteins and metabolites that may play a crucial role in the formation of pimpled eggs. A total of 242 differentially expressed proteins (DEPs) were identified in uterine tissue, of which 116 were upregulated and 126 were downregulated. Enrichment analysis revealed that the DEPs were enriched in pathways related to ion transport, energy metabolism, and immune responses. The study found that in the normal eggs (NE) group, HCO₃⁻ was predominantly transported via SLC4A1, although other transport pathways may also play a role. In contrast, in the pimpled eggs (PE) group, bicarbonate ions (HCO₃⁻) was primarily transported through SLC4A4. Additionally, a total of 44 differentially metabolites (DMs) were identified in the uterus, with 5′-Adenylic acid (ATP) being significantly downregulated in the PE group. The ions and matrix proteins required for eggshell formation are transported from uterine cells to the uterine fluid against a concentration gradient, a process that consumes a substantial amount of energy. The decrease in ATP concentration in the PE group may be a significant factor influencing the formation of pimpled eggs. Subsequently, we found that the DEPs and DMs were jointly enriched in several signaling pathways, including the FoxO signaling pathway related to energy metabolism, nicotinate and nicotinamide metabolism, and tryptophan metabolism associated with immune response. Notably, the DMs involved in these signaling pathways were all downregulated in the PE group. Our research findings indicate that SLC4A1, SLC4A2, and ATP2B4 (DEPs), along with 5′-adenylic acid and trigonelline (DMs), influence the formation of eggshells through mechanisms related to energy metabolism, ion transport, and immune response. These DEPs and DMs may serve as potential biomarkers for the genetic improvement of eggshell quality.http://www.sciencedirect.com/science/article/pii/S0032579125000550Pimpled eggChickenMetabolomicsProteomics
spellingShingle Wenqiang Li
Xueying Ma
Xiaomin Li
Xuguang Zhang
Yifei Sun
Chao Ning
Qin Zhang
Dan Wang
Hui Tang
Integrating proteomics and metabolomics to elucidate the regulatory mechanisms of pimpled egg production in chickens
Poultry Science
Pimpled egg
Chicken
Metabolomics
Proteomics
title Integrating proteomics and metabolomics to elucidate the regulatory mechanisms of pimpled egg production in chickens
title_full Integrating proteomics and metabolomics to elucidate the regulatory mechanisms of pimpled egg production in chickens
title_fullStr Integrating proteomics and metabolomics to elucidate the regulatory mechanisms of pimpled egg production in chickens
title_full_unstemmed Integrating proteomics and metabolomics to elucidate the regulatory mechanisms of pimpled egg production in chickens
title_short Integrating proteomics and metabolomics to elucidate the regulatory mechanisms of pimpled egg production in chickens
title_sort integrating proteomics and metabolomics to elucidate the regulatory mechanisms of pimpled egg production in chickens
topic Pimpled egg
Chicken
Metabolomics
Proteomics
url http://www.sciencedirect.com/science/article/pii/S0032579125000550
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