Hepatic lectin of Nile tilapia (Oreochromis niloticus) is involved in the regulation of innate antibacterial immunity as a novel C-type lectin receptor

Abstract

Hepatic lectin, a type II member of the C-type lectin receptor (CLR) superfamily, plays a crucial role in the immune response and mediates multiple biological processes, including suppressing metastasis of hepatocellular carcinoma, modulating monocyte-to-macrophage differentiation, and regulating inflammation caused by SARS-CoV-2. Nonetheless, the roles of hepatic lectin in the teleost immune system remain unknown. This study identified a hepatic lectin molecule from Nile tilapia (Onhl) and uncovered its functions in the tilapia immunological response to bacteria. Onhl, a single-pass type II membrane protein, contains a protein of 237 amino acids that is encoded by an open reading frame of 711 bp with an extracellular C-type lectin domain (CTLD). The CTLD of Onhl was highly conserved compared to other hepatic lectins. The transcriptional level of Onhl was highest in the liver of healthy tilapia. Meanwhile, the transcriptional level of Onhl was increased dramatically after S. agalactiae and A. hydrophila infection. Moreover, Onhl participated in the recognition process of tilapia to multiple pathogens by binding and agglutinating gram-positive and gram-negative bacteria. Furthermore, Onhl was primarily expressed in nonspecific cytotoxic cells (NCC) and monocytes (Mo)/macrophages (Mφ) in tilapia head kidney leukocytes (HKLs) and widely involved in the phagocytosis of pathogens performed by Mφ. Finally, blocking Onhl had a great impact on the antibacterial immune responses of tilapia HKLs, including suppression inflammation, reducing the expression of perforin, inhibiting pyroptosis, and promoting apoptosis. In summarily, hepatic lectin functions as a novel CLR and is vital in regulating the innate immune responses in Nile tilapia.