Functional characterization of interleukin (IL)-22 and its inhibitor, IL-22 binding protein (IL-22BP) in Mandarin fish, Siniperca chuatsi

Hui Jun Huo; Shan Nan Chen; Li Li; Zubair Ahmed Laghari; Nan Li; Pin Nie

doi:10.1016/j.dci.2019.03.007

Functional characterization of interleukin (IL)-22 and its inhibitor, IL-22 binding protein (IL-22BP) in Mandarin fish, Siniperca chuatsi

Dev Comp Immunol. 2019 Aug:97:88-97. doi: 10.1016/j.dci.2019.03.007. Epub 2019 Mar 19.

Authors

Hui Jun Huo¹, Shan Nan Chen², Li Li², Zubair Ahmed Laghari², Nan Li², Pin Nie³

Affiliations

¹ State Key Laboratory of Freshwater Ecology and Biotechnology, and Key Laboratory of Aquaculture Disease Control, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei Province, 430072, China; University of Chinese Academy of Sciences, Beijing, 100049, China.
² State Key Laboratory of Freshwater Ecology and Biotechnology, and Key Laboratory of Aquaculture Disease Control, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei Province, 430072, China.
³ State Key Laboratory of Freshwater Ecology and Biotechnology, and Key Laboratory of Aquaculture Disease Control, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, Hubei Province, 430072, China; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, Shandong Province, 266237, China; School of Marine Science and Engineering, Qingdao Agricultural University, Qingdao, Shandong Province, 266109, China. Electronic address: pinnie@ihb.ac.cn.

PMID: 30902735
DOI: 10.1016/j.dci.2019.03.007

Abstract

As an important immune regulatory molecule, interleukin (IL)-22 has been reported in several species of fish, but its soluble receptor, IL-22 binding protein (IL-22BP), discovered as a natural antagonist of IL-22 in mammals, has not been functionally characterized in fish to date. In the present study, IL-22 and IL-22BP genes were cloned in mandarin fish Siniperca chuatsi. They all exhibited a high basal expression level in mucosa-enriched tissues, implying their possible roles in mucosal immunity. The IL-22 was found to show a potent response to LPS stimulation, acting as an inducer of antimicrobial peptide (AMP) genes, such as hepcidin and Liver-expressed antimicrobial peptide-2 (LEAP-2) in intestinal cells. IL-22BP, via co-incubation with IL-22, inhibited completely the induction of downstream genes by IL-22. Through a yeast two-hybrid assay, the interaction between IL-22BP and IL-22 was confirmed, which may account for the inhibitory effect of IL-22BP. Moreover, two hot spot residues for IL-22 binding, as reported in mammalian IL-22BP, were found to be conserved both in sequence location and function in mandarin fish IL-22BP, indicating that the interaction mode between IL-22 and IL-22BP may be also conserved in fish and mammals. In conclusion, the mandarin fish IL-22 and IL-22BP are conserved in their interaction and function with their mammalian orthologues, and these findings provide basis for future research on IL-22-IL-22BP axis in fish immunity.

Keywords: Hepcidin; IL-22; IL-22BP; LEAP-2; Mandarin fish.

Publication types

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

MeSH terms

Amino Acid Sequence
Animals
Fish Proteins / classification
Fish Proteins / genetics*
Fish Proteins / metabolism
Gene Expression Profiling / methods
Interleukin-22
Interleukins / classification
Interleukins / genetics*
Interleukins / metabolism
Perciformes / genetics*
Perciformes / metabolism
Phylogeny
Protein Binding
Receptors, Interleukin / classification
Receptors, Interleukin / genetics*
Receptors, Interleukin / metabolism
Sequence Homology, Amino Acid
Two-Hybrid System Techniques

Substances

Fish Proteins
Interleukins
Receptors, Interleukin
interleukin-22 receptor