Exploration of the immune response of grass carp (Ctenopharyngodon idellus) erythrocytes during bacterial infection

Shiyi Yang; Yanhan Bai; Junjie Tao; Chengming Tu; Bing Chen; Xiaoman Huang; Linpeng Zhang; Lihan Liu; Lin Li; Zhendong Qin

doi:10.1016/j.fsi.2024.109526

Exploration of the immune response of grass carp (Ctenopharyngodon idellus) erythrocytes during bacterial infection

Fish Shellfish Immunol. 2024 Mar 28:149:109526. doi: 10.1016/j.fsi.2024.109526. Online ahead of print.

Authors

Shiyi Yang¹, Yanhan Bai¹, Junjie Tao¹, Chengming Tu¹, Bing Chen², Xiaoman Huang¹, Linpeng Zhang¹, Lihan Liu¹, Lin Li³, Zhendong Qin⁴

Affiliations

¹ Guangdong Provincial Water Environment and Aquatic Products Security Engineering Technology Research Center, Guangzhou Key Laboratory of Aquatic Animal Diseases and Waterfowl Breeding, College of Animal Sciences and Technology, Zhongkai University of Agriculture and Engineering, Guangzhou, Guangdong Province, 510222, China.
² Laboratory of Animal Nutrition and Feed Science in South China, Ministry of Agriculture and Rural Affairs, Guangdong Key Laboratory of Animal Breeding and Nutrition, Institute of Animal Science, Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, China. Electronic address: chenbing114@163.com.
³ Guangdong Provincial Water Environment and Aquatic Products Security Engineering Technology Research Center, Guangzhou Key Laboratory of Aquatic Animal Diseases and Waterfowl Breeding, College of Animal Sciences and Technology, Zhongkai University of Agriculture and Engineering, Guangzhou, Guangdong Province, 510222, China. Electronic address: linli@zhku.edu.cn.
⁴ Guangdong Provincial Water Environment and Aquatic Products Security Engineering Technology Research Center, Guangzhou Key Laboratory of Aquatic Animal Diseases and Waterfowl Breeding, College of Animal Sciences and Technology, Zhongkai University of Agriculture and Engineering, Guangzhou, Guangdong Province, 510222, China. Electronic address: qinzhendongsc@163.com.

PMID: 38554743
DOI: 10.1016/j.fsi.2024.109526

Abstract

In teleost blood, red blood cells (RBCs) are the most common type of cell, and they differ from mammalian RBCs in having a nucleus and other organelles. As nucleated cells, teleost RBCs contribute to the immune response against pathogens, but their antibacterial mechanism remains unclear. Here, we utilized RNA-Seq to analyze gene expression patterns of grass carp (Ctenopharyngodon idellus) RBCs (GcRBCs) stimulated by Aeromonas hydrophila, Escherichia coli, and Staphylococcus aureus. Our transcriptomic data showed that bacterial stimulation generated many differentially expressed genes (DEGs). Furthermore, several inflammatory pathways responded to bacterial activation, and the TLR, IL-17, and tumor necrosis factor (TNF) signaling pathways were significantly activated based on Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis. Furthermore, the findings of qRT-PCR showed markedly elevated expression of various cytokines, including IL-1β, IL4, IL6, IL8, IL12, and TNFα, in GcRBCs after incubation with bacteria. Reactive oxygen species (ROS) production in GcRBCs was markedly increased after the cells were stimulated with the three bacteria, and the expression of superoxide dismutase, glutathione peroxidase, and antioxidant enzymes, including catalase, was altered. Flow cytometry analysis showed that the apoptosis rate of GcRBCs was enhanced after stimulation with the three bacteria for different times. In summary, our findings reveal that bacterial stimulation activates the immune response of GcRBCs by regulating ROS release, cytokine expression, and the antioxidant system, leading to apoptosis of GcRBCs.

Keywords: Antioxidant system; Apoptosis; GcRBCs; Inflammation; ROS.