Genome-wide identification, immune response profile and functional characterization of IL-10 from spotted knifejaw (Oplegnathus punctatus) during host defense against bacterial and viral infection

• Published in: Fish & shellfish immunology Vol. 124; pp. 513 - 524
• Main Authors: Wang, Jie, Chen, Zhangfan, Li, Ming, Ziwei zhang, Song, Yu, Xu, Wenteng, Wang, Lei, Chen, Songlin
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 01.05.2022
• Subjects: Animals; Bass - metabolism; Epinephelus lanceolatus; family; fish; Fish Diseases; Fish Proteins; Gene Expression Regulation; genome; immune response; Immunity; Innate immune response; Interleukin-10; Interleukin-10 - genetics; Interleukin-10 - metabolism; interleukin-12; interleukin-6; interleukin-8; intestines; intracellular signaling peptides and proteins; Iridovirus; kidneys; liver; NF-kappa B - metabolism; Notolabrus; Oplegnathus; Oplegnathus punctatus; Phylogeny; polyinosinic-polycytidylic acid; shellfish; spleen; Spotted knifejaw iridovirus; Vibrio harveyi; Virus Diseases; Oplegnathus punctatus; Interleukin-10; Vibrio harveyi; Spotted knifejaw iridovirus; Innate immune response
• ISSN: 1050-4648; 1095-9947; 1095-9947
• DOI: 10.1016/j.fsi.2022.04.026

Interleukin 10 (IL-10), a pleiotropic cytokine, plays an essential role in multiple immunity responses. In the current study, the sequences of IL-10 family were identified from spotted knifejaw (Oplegnathus punctatus) whole genome, and O. punctatus IL-10 (OpIL-10) was cloned and characterized. OpIL-10 encodes 187 amino acids with a typical IL-10 family signature motif and predicted α-helices. It shared high identities with Notolabrus celidotus IL-10 and Epinephelus Lanceolatus IL-10. OpIL-10 was widely detected in healthy tissues, with the abundant expression in liver and skin. It was significantly up-regulated in the six immune-related tissues (liver, spleen, kidney, intestine, gill and skin) after infection against Vibrio harveyi and spotted knifejaw iridovirus (SKIV). Dual-luciferase analysis showed that OpIL-10 overexpression could suppress the activity of NF-κB. Meanwhile, OpIL-10 knockdown caused the down-regulation of five immune-related genes in JAK2/STAT3 signaling pathway and NF-κB signaling pathway, including IL-10R2, TYK2, STAT3, NOD2, and IκB. In addition, LPS and poly I:C stimulated expression of pro-inflammatory cytokines, including IL-6, IL-1β, IL-8, and IL-12, were lower with recombinant OpIL-10 (rOp IL-10) than the control group, indicating the anti-inflammatory roles of rOpIL-10. Taken together, these results indicated OpIL-10 as a negative regulator in the inflammatory responses of spotted knifejaw against bacterial and viral infection, which would help us better understand the role of IL-10 in teleost immunity. •OpIL-10 was identified and characterized from spotted knifejaw (Oplegnathus punctatus).•OpIL-10 was expressed in multiple tissues and upregulated in six immune-related tissues after bacterial and viral infection.•OpIL-10 could regulate JAK2/STAT3 signaling pathway and NF-κB signaling pathway.•Recombinant OpIL-10 protein had an inhibitory effect on the expression of proinflammatory cytokines.•OpIL-10 plays a negatively regulator in the immune response against bacterial and viral infection in spotted knifejaw.