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Spot Syndrome Virus Infection in Shrimp Lectin and Calreticulin Collaboration between a Soluble C-Type Lectin and Calreticulin Facilitates White Spot Syndrome Virus Infection in Shrimp This information is current as Xian-Wei Wang, Yi-Hui Xu, Ji-Dong Xu, Xiao-Fan Zhao of October 2, 2021. and Jin-Xing Wang J Immunol 2014; 193:2106-2117; Prepublished online 28 July 2014; doi: 10.4049/jimmunol.1400552 http://www.jimmunol.org/content/193/5/2106 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2014/07/26/jimmunol.140055 Material 2.DCSupplemental http://www.jimmunol.org/ References This article cites 51 articles, 17 of which you can access for free at: http://www.jimmunol.org/content/193/5/2106.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists by guest on October 2, 2021 • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2014 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Collaboration between a Soluble C-Type Lectin and Calreticulin Facilitates White Spot Syndrome Virus Infection in Shrimp Xian-Wei Wang, Yi-Hui Xu, Ji-Dong Xu, Xiao-Fan Zhao, and Jin-Xing Wang White spot syndrome virus (WSSV) mainly infects crustaceans through the digestive tract. Whether C-type lectins (CLs), which are important receptors for many viruses, participate in WSSV infection in the shrimp stomach remains unknown. In this study, we orally infected kuruma shrimp Marsupenaeus japonicus to model the natural transmission of WSSV and identified a CL (desig- nated as M. japonicus stomach virus–associated CL [MjsvCL]) that was significantly induced by virus infection in the stomach. Knockdown of MjsvCL expression by RNA interference suppressed the virus replication, whereas exogenous MjsvCL enhanced it. Further analysis by GST pull-down and coimmunoprecipitation showed that MjsvCL could bind to viral protein 28, the most abundant and functionally relevant envelope protein of WSSV. Furthermore, cell-surface calreticulin was identified as a receptor Downloaded from of MjsvCL, and the interaction between these proteins was a determinant for the viral infection–promoting activity of MjsvCL. The MjsvCL–calreticulin pathway facilitated virus entry likely in a cholesterol-dependent manner. This study provides insights into a mechanism by which soluble CLs capture and present virions to the cell-surface receptor to facilitate viral infection. The Journal of Immunology, 2014, 193: 2106–2117. hite spot syndrome virus (WSSV) is one of the most proteins of WSSV, viral protein 28 (VP28) and VP19, play im- http://www.jimmunol.org/ devastating pathogens threatening the shrimp aqua- portant roles in virus entry and systemic infection (9, 10). Al- W culture. As a dsDNA virus, WSSV belongs to the though some molecules from crustaceans were shown to be genus Whispovirus of the family Nimaviridae (1, 2). The WSSV involved in virus infection or antiviral responses (11–14), how genome consists of 30 M bp and is the largest among all animal WSSV is recognized by the host and how the virions enter the viruses sequenced until now (3). In addition, most proteins cells remain largely unknown. Thus, identification of critical encoded by the WSSV genome do not show any similarity to factors during WSSV infection, especially the early viral entry known proteins, further making functional studies of this virus stage, would be of great help in understanding the virus–host challenging (4, 5). The transmission of WSSV in the natural en- interaction and discovering the targets for disease control and by guest on October 2, 2021 vironment is mainly through oral ingestion (i.e., by healthy shrimp prevention. consuming dead or sick shrimp infected by the virus) (6, 7). Re- C-type lectins (CLs) are characterized by the C-type carbohy- cently, caveolae-mediated endocytosis was found to be likely drate recognition domain, which can bind to a wide range of critical for viral entry into shrimp cells (8). The principle envelope ligands, including glycans, proteins, lipids, and even inorganic compounds (15). Because of the “non–self-recognition” mediated by this binding ability, CLs play central roles in host defense. The Key Laboratory of Plant Cell Engineering and Germplasm Innovation of Many members of this family participate in virus infection, mainly Ministry of Education/Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Jinan, by recognizing virions and influencing their entry into host cells. Shandong 250100, China For example, the mammalian transmembrane CL DC-SIGN binds Received for publication March 5, 2014. Accepted for publication June 29, 2014. to HIV gp120 and mediates viral entry and dissemination (16). In This work was supported by the National Natural Science Foundation of China contrast, the soluble CL mannose binding lectin (MBL) can also (Grants 31130056 and 31302217), the National Basic Research Program of China (973 bind to gp120 and suppress the DC-SIGN–mediated uptake of Program, Grant 2012CB114405), the Ph.D. Programs Foundation of the Ministry of the virus (17). A member of the mosGCTLs family from Aedes Education of China (Grant 20110131130003), the Provincial Natural Science Foun- dation of Shandong, China (Grant ZR2011CM014), and the China Postdoctoral aegypti can bind to West Nile virus and then collaborate with Foundation (Grant 2013M540553) to J.X.W. and X.W.W. a protein tyrosine phosphatase to facilitate virus infection (18), The sequences presented in this article have been submitted to GenBank (http://www. whereas other members can bind to Dengue virus (DENV) to ncbi.nlm.nih.gov/nuccore/KF712277) under accession number KF712277. facilitate virus infection (19). A CL in Litopenaeus vannamei, Address correspondence and reprint requests to Dr. Jin-Xing Wang, School of Life LvCTL1, has been shown to protect shrimp from WSSV both Sciences, Shandong University, No. 27 Shanda South Road, Jinan, Shandong 250100, China. E-mail address: [email protected] in vivo and in vitro, and the protective function may be related to The online version of this article contains supplemental material. the interaction of LvCTL1 with several VPs (14). Although these CLs may have opposite functions in virus infection, the virus- Abbreviations used in this article: CL, C-type lectin; co-IP, coimmunoprecipitation; CRT, calreticulin; CTLD, CL domain; DENV, Dengue virus; ie1, immediate early 1; binding capacity is a common feature among them. Such an LvCTL1, CL in Litopenaeus vannamei;MbCD, methyl-b-cyclodextrin; MBL, man- ability allows CLs to participate in the recognition of virions or to nose binding lectin; MjsvCL, Marsupenaeus japonicus stomach virus–associated CL; MS, mass spectrometry; qRT-PCR, quantitative real-time PCR; rGST-MjsvCL, be hijacked for viral entry. rGST-tagged MjsvCL; RIPA, radioimmunoprecipitation assay; rMjsvCL, recombi- Therefore, our goal was to identify the CLs responding to WSSV nant MjsvCL; RNAi, RNA interference; VP, viral protein; WSSV, white spot syn- infection in the shrimp stomach, because this organ is first invaded drome virus. by the virus during natural transmission and may express such Copyright Ó 2014 by The American Association of Immunologists, Inc. 0022-1767/14/$16.00 molecules critical for the viral invasion or host defense. The virus www.jimmunol.org/cgi/doi/10.4049/jimmunol.1400552 The Journal of Immunology 2107 inoculum was delivered through the shrimp oral tract to model (M-MLV version; Takara, Dalian, China) following the manufacturer’s natural infection, and the expression of CLs in the stomach was instructions. Fourteen CLs (10098, 14945, 15188, 18420, 18765, 18947, analyzed. Among the CLs identified as induced by WSSV, one that 22501, 25392, 34742, 31681, 31996, 35574, 40058, and 47086), which were obtained from a transcriptome sequencing of kuruma shrimp stom- was mainly expressed in the stomach and responded most highly to ach, were selected for the screening. PCR was performed as described WSSV infection drew our attention and was subjected to further earlier using primers listed in Table I. Gene expression in each experi- investigation. The function of this CL, designated as Marsupenaeus mental stomach sample was normalized to that in the control and calcu- japonicus stomach virus–associated CL (MjsvCL), in virus in- lated as the fold change of expression induced by WSSV infection. Results are presented as the mean value 6 SD. fection was studied by both knockdown and overexpression of the protein. Moreover, the mechanism by which MjsvCL participates Identification of MjsvCL cDNA in WSSV infection was explored. The identification of a viral The CL 40058 (MjsvCL) was characterized as a WSSV-sensitive gene. The infection promoting CL in shrimp in this study will be helpful for fragment encoding the full open reading frame of MjsvCL was obtained understanding the molecular pathogenesis of WSSV and WSSV– from a transcriptome sequencing of kuruma shrimp by the Beijing shrimp interactions. Genomics Institute (BGI, Shenzhen, China). A pair of primers (MjsvCLGSF/R) was used to amplify the full-length cDNA of MjsvCL to confirm the correctness of the sequence. The SignalP 4.1 server (http:// Materials and Methods www.cbs.dtu.dk/services/SignalP/) was used to predict the signal peptide. Animals SMART (http://smart.embl-heidelberg.de/) and BLAST (http://blast.ncbi. ∼ nlm.nih.gov/Blast.cgi) programs were used to analyze the domain archi- Healthy kuruma shrimp M. japonicus ( 6–7 g) obtained from a farm in tecture.
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