Abstract

C-type lectins (CTLs) are characterized by the presence of a C-type carbohydrate recognition domain (CTLD) that by recognizing microbial glycans, is responsible for their roles as pattern recognition receptors in the immune response to bacterial infection. In addition to the CTLD, however, some CTLs display additional domains that can carry out effector functions, such as the collagenous domain of the mannose-binding lectin. While in vertebrates, the mechanisms involved in these effector functions have been characterized in considerable detail, in invertebrates they remain poorly understood. In this study, we identified in the kuruma shrimp (Marsupenaeus japonicus) a structurally novel CTL (MjCC-CL) that in addition to the canonical CTLD, contains a coiled-coil domain (CCD) responsible for the effector functions that are key to the shrimp’s antibacterial response mediated by antimicrobial peptides (AMPs). By the use of in vitro and in vivo experimental approaches we elucidated the mechanism by which the recognition of bacterial glycans by the CTLD of MjCC-CL leads to activation of the JAK/STAT pathway via interaction of the CCD with the surface receptor Domeless, and upregulation of AMP expression. Thus, our study of the shrimp MjCC-CL revealed a striking functional difference with vertebrates, in which the JAK/STAT pathway is indirectly activated by cell death and stress signals through cytokines or growth factors. Instead, by cross-linking microbial pathogens with the cell surface receptor Domeless, a lectin directly activates the JAK/STAT pathway, which plays a central role in the shrimp antibacterial immune responses by upregulating expression of selected AMPs.

Highlights

  • Like other invertebrates, the shrimp’s defense against microbial pathogens relies on innate immune responses, which generally encompass their recognition, killing and disposal through humoral and cellular mechanisms

  • We identified core components of Janus kinases (JAKs)/signal transducers and activators of transcription (STATs) pathway in shrimp and found the pathway had an important function in antibacterial immunity

  • Working as a cytokine like ligand, the MjCC-CL binds to polysaccharides from bacteria and the interleukin receptor (ILR) domain of Domeless, induces STAT phosphorylation and translocation into the nucleus, and expression of several antimicrobial peptides (AMPs)

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Summary

Introduction

The shrimp’s defense against microbial pathogens relies on innate immune responses, which generally encompass their recognition, killing and disposal through humoral and cellular mechanisms. The CTLD is responsible for the CTLs’ roles as pattern recognition receptors (PRRs) in the innate immune response to bacterial infection of both vertebrates and invertebrates. During the past few years, we have focused on the roles of CTLs in the shrimp immune response to bacterial infection [7,8,9]. Based on their domain organization, at present time the shrimp CTLs can be classified in three distinct groups: (1) CTLs that contain only one CTLD, (2) CTLs with two CTLDs, and (3)

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