Dietary α-ketoglutarate alleviates glycinin and β-conglycinin induced damage in the intestine of mirror carp (Cyprinus carpio)

Qiaohua Luo; Rendong Qian; Zongsheng Qiu; Fernando Y Yamamoto; Yingying Du; Xiaowen Lin; Jianhua Zhao; Qiyou Xu

doi:10.3389/fimmu.2023.1140012

Dietary α-ketoglutarate alleviates glycinin and β-conglycinin induced damage in the intestine of mirror carp (Cyprinus carpio)

Front Immunol. 2023 Apr 28:14:1140012. doi: 10.3389/fimmu.2023.1140012. eCollection 2023.

Authors

Qiaohua Luo^{1

2}, Rendong Qian^{1

2}, Zongsheng Qiu^{1

2}, Fernando Y Yamamoto^{3

4}, Yingying Du^{1

2}, Xiaowen Lin^{1

2}, Jianhua Zhao^{1

2}, Qiyou Xu^{1

2}

Affiliations

¹ College of Life Science, Huzhou University, Huzhou, China.
² Nation Local Joint Engineering Laboratory of Aquatic Animal Genetic Breeding and Nutrition, Zhejiang Provincial Key Laboratory of Aquatic Bioresource Conservation and Development Technology, Huzhou, China.
³ Thad Cochran National Warmwater Aquaculture Center Agriculture and Forestry Experiment Station, Mississippi State University, Starkville, MS, United States.
⁴ Department of Wildlife, Fisheries and Aquaculture, Mississippi State University, Starkville, MS, United States.

Abstract

This study investigated the glycinin and β-conglycinin induced intestinal damage and α-ketoglutarate alleviating the damage of glycinin and β-conglycinin in intestine. Carp were randomly divided into six dietary groups: containing fish meal (FM) as the protein source, soybean meal (SM), glycinin (FMG), β-conglycinin (FMc), glycinin+1.0% α-ketoglutarate (AKG) (FMGA), β-conglycinin+1.0% AKG (FMcA). The intestines were collected on 7^th, and the hepatopancreas and intestines were collected on 56^th. Fish treated with SM and FMc displayed reduced weight gain, specific growth rate, and protein efficiency. On 56^th day, Fish fed on SM, FMG and FMc presented lower superoxide dismutase (SOD) activities. FMGA and FMcA had higher SOD activity than those fed on the FMG and FMc, respectively. In intestine, fish fed on the SM diets collected on 7^th presented upregulated the expression of transforming growth factor beta (TGFβ1), AMP-activated protein kinase beta (AMPKβ), AMPKγ, and acetyl-CoA carboxylase (ACC). Fish fed FMG presented upregulated expression of tumor necrosis factor alpha (TNF-α), caspase9, and AMPKγ, while downregulated the expression of claudin7 and AMPKα. FMc group presented upregulated expression of TGFβ1, caspase3, caspase8, and ACC. Fish fed FMGA showed upregulated expression of TGFβ1, claudin3c, claudin7, while downregulating the expression of TNF-α and AMPKγ when compared to fish fed FMG diet. FMcA upregulated the expression of TGFβ1, claudin3c than fed on the FMc. In intestine, the villus height and mucosal thickness of the proximal intestine (PI) and the distal intestine (DI) were decreased and crypt depth of the PI and mid intestine (MI) were increased in SM, FMG and FMc. In addition, fish fed on SM, FMG and FMc presented lower citrate synthase (CS), isocitrate dehydrogenase (ICD), α-ketoglutarate dehydrogenase complex (α-KGDHC) Na⁺/K⁺-ATPase activity in DI. FMGA had higher CS, ICD, α-KGDHC, and Na⁺/K⁺-ATPase activity in PI and MI than those fed on the FMG. FMcA had higher Na⁺/K⁺-ATPase activity in MI. In conclusion, dietary soybean meal destroys the intestine's health, the adverse effects are related to the presence of β-conglycinin and glycinin, especially glycinin. AKG may regulate intestinal energy via tricarboxylic acid cycle, thereby alleviating the damage intestinal morphology caused by the dietary soybean antigen proteins.

Keywords: Cyprinus carpio; glycinin; intestine immunity; α-ketoglutarate; β-conglycinin.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adenosine Triphosphatases
Animals
Carps*
Diet
Glycine max
Intestines
Ketoglutaric Acids / pharmacology
Superoxide Dismutase
Tumor Necrosis Factor-alpha / pharmacology

Substances

glycinin
beta-conglycinin protein, Glycine max
Ketoglutaric Acids
Tumor Necrosis Factor-alpha
Superoxide Dismutase
Adenosine Triphosphatases

Grants and funding

This work was financially supported by the Natural Science Foundation of China, NSFC (31972800), and the China Agriculture Research System of MOF and MARA.