A C-type lectin isolated from the skin of Japanese bullhead shark (Heterodontus japonicus) binds a remarkably broad range of sugars and induces blood coagulation

Abstract

The aim of this study was to determine the physiological role of skin lectins of the Japanese bullhead shark (Heterodontus japonicus). A skin extract was subjected to affinity chromatography using seven different sugars as ligands. Molecular mass and N-terminal amino acid sequence analyses indicated elution of the same protein by each of the seven respective cognate ligands from sugar affinity columns. The predicted amino acid sequence encoded by the cDNA of this protein [designated as H. japonicus C-type-lectin (HjCL)] identified it as a novel fish subgroup VII C-type lectin evolutionarily related to snake venom lectins. HjCL was predicted to bind to mannose because of the presence of a Glu-Pro-Asn (EPN) motif; however, haemagglutination inhibition assays and glycoconjugate microarray analysis demonstrated its binding to numerous structurally diverse sugars. Competitive sugar-binding assays using affinity chromatography indicated that HjCL bound multiple sugars via a common carbohydrate-recognition domain. The mRNA encoding HjCL was specifically detected in the skin, and immunohistochemical analysis detected its expression in uncharacterized large cells in the epidermis. HjCL agglutinated the bacterial pathogen Edwardsiella tarda and promoted immediate clotting of shark blood, indicating that HjCL is involved in host defence on the skin surface especially when the shark is injured and bleeds.

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

“…These characteristics of MjGCTL fit the description of vertebrate type I mucosal immunity (6). Also belonging to mucosal type I mucosal immunity are C-type lectins isolated from fish respiratory organs (14)(15)(16)(17)(18)(19). Interestingly, two of these were isolated from gill mucus of the Japanese eel, A. japonica, and share the same tissue expression profile as MjGCTL (19).…”

“…PRRs are key components for surveillance of mucosal surfaces, and a huge group of extracellular PRRs found among metazoans belong to the Ca 2+ -dependent carbohydratebinding C-type lectin superfamily (13). C-type lectins have been isolated from fish mucus (skin, gut, and gill) and participate in fish mucosal immunity, recognizing a wide-array of microorganisms (14)(15)(16)(17)(18). Two C-type lectins highly expressed in the gills were isolated from gill mucus of the Japanese eel Anguilla japonica (19).…”

The skin microbiome of the common thresher shark (Alopias vulpinus) has low taxonomic and gene function β‐diversity

“…In addition to the biophysical constraints of shark skin on the microbiome, the thin mucus layer against the skin surface is a biochemical filter to microorganisms. A C‐type lectin was identified in the skin mucus of the Japanese bullhead shark ( Heterodontus japonicas ) (Tsutsui et al ., ) and another anti‐microbial peptide called Pentraxin was found from the skin mucus of the common skate ( Raja kenojei ) (Tsutsui et al ., ). Though the mucus of sharks has not been characterized, histochemical staining of the thin mucus layer shows a protein rich substrata (Meyer and Seegers, ).These observations support the hypothesis that skin mucus of sharks mediates microbial activity.…”

“…The mechanisms for the maintenance of a healthy shark skin microbiome may vary from distantly related teleost species. Sharks, like teleosts support a biologically active mucus layer (Luer et al ., ; Tsutsui et al ., ) at the skin interface, however mucus on sharks is inconspicuous relative to that of teleost fishes (Meyer and Seegers, ), suggesting sharks have reduced mucus secretion. Another difference between sharks and teleost fishes is that shark skin is textured (microscopic ridging) by dermal denticles that protrude through the epidermal and mucosal layer.…”

Photophore Distribution and Enzymatic Diversity Within the Photogenic Integument of the Cookie-Cutter Shark Isistius brasiliensis (Chondrichthyes: Dalatiidae)

“…In addition to its not so common "bioluminescence function, " shark skin is also known to be a pleiotropic tissue involved in a variety of functions such as senses (e.g., Fields, 2007;Hart and Collin, 2014), protection and hydrodynamics through the placoid scale squamation pattern (e.g., Wainwright et al, 1978;Reif, 1985;Meyer and Seegers, 2012;Oeffner and Lauder, 2012), immunity (e.g., Moore et al, 1993;Tsutsui et al, 2015), and color changes for camouflage or UV protection through melanophore pigment motion (e.g., Lowe and Goodman-Lowe, 1996;Visconti et al, 1999;Robbins and Fox, 2012).…”