Identification of two pIgR-like molecules in teleost fish with opposite roles in mucosal immunity against bacterial infection

• Published in: Water Biology and Security 2023-10, Vol.2 (4), p.100209, Article 100209
• Main Authors: Xu, Haoyue, Wang, Zixuan, Huang, Zhenyu, Chen, Xiaoyun, Lin, Ruiqi, Yu, Yongyao, Xu, Zhen
• Format: Article
• Language: English
• Subjects: Edwardsiella piscicida; Inflammatory response; Mucosal immunity; pIgR-like; Zebrafish
• ISSN: 2772-7351; 2772-7351
• DOI: 10.1016/j.watbs.2023.100209

Polymeric immunoglobulin (Ig) receptor-like (pIgRL) molecules have been identified in teleost fish. However, compared to functional studies of their related genes (e.g., mammalian CD300 family) in eliminating pathogen invasion while preserving homeostasis, the roles of pIgRL in teleost fish remain unclear. In this study, we demonstrated that a pair of pIgRL molecules in zebrafish, pIgRL3.5 and pIgRL4.2, were highly expressed in the intestine and immune cells. Moreover, we constructed an Edwardsiella piscicida infection model, which induced strong inflammatory responses in the zebrafish intestine. Interestingly, pIgRL3.5 and pIgRL4.2 exhibited opposite inducible expression patterns in response to bacterial infection, suggesting that they perform different roles. More importantly, by conducting overexpression and knockdown experiments, our findings demonstrated that zebrafish pIgRL3.5 played a protective role in host defense against E. piscicida infection by inhibiting excessive inflammatory responses. In contrast, pIgRL4.2 facilitated pathogen growth and dissemination in zebrafish intestine. Collectively, our findings are the first to demonstrate that a pair of pIgRL molecules in teleost fish play opposite roles in mucosal immune response to bacterial infection. Therefore, our results provide crucial insights into the conserved role of pIgRL molecules in immune regulatory functions throughout vertebrate evolution. •Fish pIgRL molecules share similar structure and function with mammalian CD300.•PIgRL3.5 and pIgRL4.2 exhibit different inducible expression patterns in response to bacterial infection.•PIgRL3.5 and pIgRL4.2 play opposite roles in mucosal immunity by inhibiting or promoting inflammatory responses.