A Hint of Primitive Mucosal Immunity in Shrimp through Marsupenaeus japonicus Gill C-Type Lectin

• Published in: The Journal of immunology (1950) 2019-10, Vol.203 (8), p.2310-2318
• Main Authors: Alenton, Rod Russel R, Koiwai, Keiichiro, Nakamura, Rika, Thawonsuwan, Jumroensri, Kondo, Hidehiro, Hirono, Ikuo
• Format: Article
• Language: English
• Subjects: Animals; Gills - immunology; Immunity, Mucosal - immunology; Lectins, C-Type - immunology; Lectins, C-Type - isolation & purification; Penaeidae - immunology
• ISSN: 0022-1767; 1550-6606
• DOI: 10.4049/jimmunol.1900156

Lectins are found in most living organisms, providing immune surveillance by binding to carbohydrate ligands. In fishes, C-type lectins were isolated from mucus of respiratory organs (skin and gills), where they aid the mucosal immune response in regulating microbiota and suppressing pathogens. In shrimp, however, no mucosal immunity or any form of gill-specific immune defense has been reported, and most identified C-type lectins are associated with hemocyte cellular and humoral responses. Interestingly, our microarray analysis revealed the localization of highly expressed novel biodefense genes in gills, among which is gill C-type lectin (MjGCTL), which we previously reported. Gill mucus collected from displayed similar bacterial agglutination ability as observed with recombinant MjGCTL. This agglutinating ability can be attributed to endogenous MjGCTL (nMjGCTL) detected in gill mucus, which was confirmed with an agglutination assay using purified nMjGCTL from gills. In addition, nMjGCTL also promoted in vivo bacterial phagocytosis by hemocytes. In vivo knockdown of MjGCTL resulted in a compromised immune system, which was manifested by impaired agglutination capacity of gill mucus and downregulation of the gill antimicrobial peptides, crustin and penaeidin. Shrimp immunocompromised by MjCGTL knockdown, apparently lost the ability to respond to attaching and penetrating bacteria. This was evident as increased total bacteria and counts in both gills and hemolymph, which were correlated with low survival during a bacterial challenge. These results reveal immune defense by shrimp gills resembling a primitive form of mucosal immunity.