Novel Pattern Recognition Receptor Protects Shrimp by Preventing Bacterial Colonization and Promoting Phagocytosis

• Published in: The Journal of immunology (1950) 2017-04, Vol.198 (8), p.3045-3057
• Main Authors: Wang, Xian-Wei, Gao, Jie, Xu, Yi-Hui, Xu, Ji-Dong, Fan, Zhen-Xu, Zhao, Xiao-Fan, Wang, Jin-Xing
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; Animals; Arthropod Proteins - genetics; Arthropod Proteins - immunology; Bacteria; Blotting, Western; Calcium; Colonization; Decapoda; Division of labor; Enzyme-Linked Immunosorbent Assay; Flagellin; Hepatopancreas; Lectins, C-Type - immunology; Leucine; Lipopolysaccharides; Marsupenaeus japonicus; Pathogens; Pattern recognition; Pattern recognition receptors; Penaeidae - immunology; Penaeidae - microbiology; Penaeus japonicus; Phagocytosis; Polymerase Chain Reaction; Receptors, Pattern Recognition - immunology; Vibrio; Waterborne diseases
• ISSN: 0022-1767; 1550-6606
• DOI: 10.4049/jimmunol.1602002

The recognition of pathogen-associated molecular patterns is accomplished by the recognition modules of pattern recognition receptors (PRRs). Leucine-rich repeats (LRRs) and C-type lectin-like domain (CTLD) represent the two most universal categories of recognition modules. In the current study, we identified a novel soluble and bacteria-inducible PRR comprising LRRs and a CTLD from the hepatopancreas of kuruma shrimp and named it Leulectin. The module arrangement of Leulectin is unique among all organisms. Both modules, together with the whole molecule, protected shrimp against infection. By screening the pathogen-associated molecular patterns that shrimp might encounter, Leulectin was found to sense flagellin through the LRRs and to recognize LPS through CTLD. The LRR-flagellin interaction was confirmed by pull-down and far-Western assays and was found to rely on the fourth LRR of Leulectin and the N terminus of flagellin. The recognition of LPS was determined by the long loop region of CTLD in a calcium-independent manner. By sensing the flagellin, LRRs could prevent its attachment to shrimp cells, thereby inhibiting colonization. With the ability to recognize LPS, CTLD could agglutinate the bacteria and promote hemocytic phagocytosis. Our study clearly showed the division of labor and the synergy between different recognition modules and provided new insights into the concept of pattern recognition and the function of soluble PRRs in the antibacterial response.