Abstract
Galectins are a lectin family characterized by a conserved sequence motif in the carbohydrate recognition domain, which preferential binds to galactosyl moieties. However, few studies about the biological roles of galectins in invertebrates have been reported except for the galectin (CvGal1) from the eastern oyster Crassostrea virginica. Furthermore, galectins have been described in only a few crustacean species, and no functional studies have been reported so far. In this study, we identified and functionally characterized a galectin from the kuruma shrimp Marsupenaeus japonicus, which we designated MjGal. Upon Vibrio anguillarum challenge, expression of MjGal was up-regulated mostly in hemocytes and hepatopancreas, and the protein bound to both Gram-positive and Gram-negative bacteria through the recognition of lipoteichoic acid (LTA) or lipopolysaccharide (LPS), respectively. By also binding to the shrimp hemocyte surface, MjGal functions as an opsonin for microbial pathogens, promoting their phagocytosis. Further, as shown by RNA interference, MjGal participates in clearance of bacteria from circulation, and thereby contributes to the shrimp’s immune defense against infectious challenge. Elucidation of functional and mechanistic aspects of shrimp immunity will enable the development of novel strategies for intervention in infectious diseases currently affecting the shrimp farming industry worldwide.
Highlights
Invertebrates lack the typical adaptive immune responses of vertebrates but are endowed with effective defense mechanisms against infectious challenge [1]
The results showed that recombinant MjGal (rMjGal) bound strongly to the selected bacterial species tested, that the binding takes place via the carbohydrate binding domains (CRDs), and that lactose could not inhibit or displace the binding of the galectin to bacteria, both lipoteichoic acid (LTA) and LPS could function as effective binding inhibitors
Galectins were initially described as developmentally regulated in their expression and playing key roles in early embryogenesis, cell differentiation, and tissue organization, in recent years evidence has accumulated in support of their participation in regulation of immune homeostasis by modulating inflammation and multiple aspects of innate and adaptive immunity, including leukocyte chemotaxis, migration and activation [29], B cell development [9,30], T cell apoptosis [8,31], and other regulatory aspects of the immune responses of vertebrates [7,8,9,10,11,12]
Summary
Invertebrates lack the typical adaptive immune responses of vertebrates but are endowed with effective defense mechanisms against infectious challenge [1]. They comprise both cellular and humoral responses mediated by multiple soluble factors and cellassociated receptors that can recognize pathogens and lead to effector functions, including opsonization, phagocytosis, coagulation cascades and expression of antimicrobial peptides [2,3]. Pathogen recognition functions that involve protein-carbohydrate interactions are mostly mediated by both soluble and cellassociated lectins, which are critical components of the innate immune responses in both vertebrates and invertebrates [4] Based on their carbohydrate specificity, divalent cation requirements, presence of conserved sequence motifs in their carbohydrate binding domains (CRDs), and most recently their structural folds, animal lectins have classified into several families such as C-, F-, Iand P- type lectins, ficolins and galectins. Up to 15 distinct galectins (galectin-1 to 15) have been described that fall into three structural types: proto type, with one CRD per subunit and mostly form noncovalently-bound dimers, the chimera type, with one CRD and an N-terminal polypeptide extension that enables subunit oligomerization into trimers and pentamers, and the tandem repeat type, in which two CRDs are covalently joined by a linker peptide [6]
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