Journal Article

Binding of a C-type lectin’s coiled-coil domain to the Domeless receptor directly activates the JAK/STAT pathway in the shrimp immune response to bacterial infection

Zhao, Xiao-Fan, Vasta, Gerardo R., Sun, Jie-Jie, Lan, Jiang-Feng, Wang, Jin-Xing

2017

Overview

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.

• Publisher: Public Library of Science,Public Library of Science (PLoS)
• Subject: Analysis / Animals / Antibacterial agents / Antiinfectives and antibacterials / Antimicrobial peptides / Arthropod Proteins - immunology / Arthropod Proteins - metabolism / Bacteria / Bacterial diseases / Bacterial infections / Binding / Biology and Life Sciences / Carbohydrates / Cell death / Cell surface / Coils / Collagen / Crosslinking / Crustacea - metabolism / Crustacea - microbiology / Cytokines / Cytotoxicity / Developmental biology / DNA, Complementary - genetics / Dosage and administration / Drosophila / Fenneropenaeus chinensis / Gene expression / Growth factors / Health aspects / Immune response / Immune system / Infection / Infections / Insects / Invertebrates / Janus Kinases - metabolism / Laboratories / Lectins / Lectins, C-Type - chemistry / Lectins, C-Type - metabolism / Life sciences / Ligands / Lymphocytes T / Mannose / Mannose-binding lectin / Marsupenaeus japonicus / Medicine and Health Sciences / Microorganisms / Pathogens / Pattern recognition / Pattern recognition receptors / Peptides / Polysaccharides / Proteins / Receptors / Receptors, Pattern Recognition - metabolism / Signal Transduction / STAT Transcription Factors - metabolism / Supervision / Up-Regulation / Vertebrates