1. The polymeric immunoglobulin receptor-like protein from Marsupenaeus japonicus is a receptor for white spot syndrome virus infection
- Author
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Jin-Xing Wang, Ming-Chong Yang, Zhong-Hua He, Xiao-Fan Zhao, Guo-Juan Niu, Ji-Dong Xu, Jie-Jie Sun, and Shuai Wang
- Subjects
Hemocytes ,Physiology ,Aquaculture ,Virus Replication ,Biochemistry ,Intracellular Receptors ,White Blood Cells ,RNA interference ,Viral Envelope Proteins ,Animal Cells ,Immune Physiology ,Medicine and Health Sciences ,Biology (General) ,Internalization ,media_common ,0303 health sciences ,Secretory Pathway ,Immune System Proteins ,biology ,030302 biochemistry & molecular biology ,Receptors, Polymeric Immunoglobulin ,Eukaryota ,Endocytosis ,Crustaceans ,Cell biology ,Shrimp ,Nucleic acids ,Genetic interference ,Cell Processes ,293T cells ,Cell lines ,Epigenetics ,Cellular Types ,Anatomy ,Biological cultures ,Research Article ,Signal Transduction ,Protein Binding ,Arthropoda ,QH301-705.5 ,Immune Cells ,media_common.quotation_subject ,Immunology ,Microbiology ,Clathrin ,Antibodies ,03 medical and health sciences ,White spot syndrome virus 1 ,Penaeidae ,Viral entry ,Virology ,Genetics ,Animals ,Molecular Biology ,030304 developmental biology ,Blood Cells ,Organisms ,DNA Viruses ,Biology and Life Sciences ,Proteins ,Cell Biology ,Receptor-mediated endocytosis ,Virus Internalization ,RC581-607 ,Invertebrates ,Gastrointestinal Tract ,Research and analysis methods ,Viral replication ,biology.protein ,RNA ,Immunoglobulin superfamily ,Parasitology ,Gene expression ,Immunologic diseases. Allergy ,Polymeric immunoglobulin receptor ,Digestive System - Abstract
Viral entry into the host cell is the first step towards successful infection. Viral entry starts with virion attachment, and binding to receptors. Receptor binding viruses either directly release their genome into the cell, or enter cells through endocytosis. For DNA viruses and a few RNA viruses, the endocytosed viruses will transport from cytoplasm into the nucleus followed by gene expression. Receptors on the cell membrane play a crucial role in viral infection. Although several attachment factors, or candidate receptors, for the infection of white spot syndrome virus (WSSV) were identified in shrimp, the authentic entry receptors for WSSV infection and the intracellular signaling triggering by interaction of WSSV with receptors remain unclear. In the present study, a receptor for WSSV infection in kuruma shrimp, Marsupenaeus japonicus, was identified. It is a member of the immunoglobulin superfamily (IgSF) with a transmembrane region, and is similar to the vertebrate polymeric immunoglobulin receptor (pIgR); therefore, it was designated as a pIgR-like protein (MjpIgR for short). MjpIgR was detected in all tissues tested, and its expression was significantly induced by WSSV infection at the mRNA and protein levels. Knockdown of MjpIgR, and blocking MjpIgR with its antibody inhibited WSSV infection in shrimp and overexpression of MjpIgR facilitated the invasion of WSSV. Further analyses indicated that MjpIgR could independently render non-permissive cells susceptible to WSSV infection. The extracellular domain of MjpIgR interacts with envelope protein VP24 of WSSV and the intracellular domain interacts with calmodulin (MjCaM). MjpIgR was oligomerized and internalized following WSSV infection and the internalization was associated with endocytosis of WSSV. The viral internalization facilitating ability of MjpIgR could be blocked using chlorpromazine, an inhibitor of clathrin dependent endocytosis. Knockdown of Mjclathrin and its adaptor protein AP-2 also inhibited WSSV internalization. All the results indicated that MjpIgR-mediated WSSV endocytosis was clathrin dependent. The results suggested that MjpIgR is a WSSV receptor, and that WSSV enters shrimp cells via the pIgR-CaM-Clathrin endocytosis pathway., Author summary White Spot Syndrome Virus (WSSV) is one of the most virulent pathogens in shrimp farming. Several viral candidate receptors, or attachment factors were reported in previous studies, however, most of them are not authentic transmembrane proteins. In particular, the protein receptor(s) required the intracellular signaling triggering by interaction of WSSV with receptors remain unclear. In the present study, a polymeric immunoglobulin receptor (pIgR) like protein, a bona fide transmembrane receptor, was identified in kuruma shrimp, Marsupenaeus japonicus (MjpIgR for short). Knockdown of MjpIgR by RNA interference, and blocking it by its antibody prevented WSSV infection in shrimp and overexpression of MjpIgR facilitated the invasion of WSSV. Further study found that MjpIgR could independently render non-permissive cells susceptible to WSSV infection. The extracellular cellular domain of MjpIgR interacts with envelope protein VP24 of WSSV and the intracellular domain interacts with calmodulin (MjCaM). MjpIgR was oligomerized and internalized following WSSV infection and the internalization was associated with endocytosis of WSSV. The viral internalization facilitating ability of MjpIgR could be blocked using chlorpromazine, an inhibitor of clathrin dependent endocytosis, indicating that MjpIgR-mediated WSSV endocytosis was clathrin dependent. The results suggested that MjpIgR is a WSSV receptor, and that WSSV enters shrimp cells via the pIgR-CaM-Clathrin endocytosis pathway. This study provides a new target for WSSV control in shrimp aquaculture.
- Published
- 2019