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MD-2 Homologue Recognizes the White Spot Syndrome Virus Lipid Component and Induces Antiviral Molecule Expression in Shrimp

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MD-2 Homologue Recognizes the White Spot Syndrome Virus Lipid Component and Induces Antiviral Molecule Expression in Shrimp MD-2 Homologue Recognizes the White Spot Syndrome Virus Lipid Component and Induces Antiviral Molecule Expression in Shrimp This information is current as of October 1, 2021. Jie Gao, Jin-Xing Wang and Xian-Wei Wang J Immunol 2019; 203:1131-1141; Prepublished online 22 July 2019; doi: 10.4049/jimmunol.1900268 http://www.jimmunol.org/content/203/5/1131 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2019/07/20/jimmunol.190026 Material 8.DCSupplemental http://www.jimmunol.org/ References This article cites 38 articles, 18 of which you can access for free at: http://www.jimmunol.org/content/203/5/1131.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on October 1, 2021 • No Triage! Every submission reviewed by practicing scientists • 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 © 2019 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology MD-2 Homologue Recognizes the White Spot Syndrome Virus Lipid Component and Induces Antiviral Molecule Expression in Shrimp Jie Gao,* Jin-Xing Wang,*,†,‡ and Xian-Wei Wang*,†,‡ The myeloid differentiation factor 2 (MD-2)–related lipid-recognition (ML) domain is found in multiple proteins, including MD-2, MD-1, Niemann–Pick disease type C2, and mite major allergen proteins. The significance of ML proteins in antibacterial signal transduction and in lipid metabolism has been well studied. However, their function in host–virus interaction remains poorly understood. In the current study, we found that the ML protein family is involved in resistance against white spot syndrome virus in kuruma shrimp, Marsupenaeus japonicus. One member, which showed a high similarity to mammalian MD-2/MD-1 and was designated as ML1, participated in the antiviral response by recognizing cholesta-3,5-diene (CD), a lipid component of the white spot syndrome virus envelope. After recognizing CD, ML1 induced the translocation of Rel family NF-kB transcription factor Downloaded from Dorsal into the nucleus, resulting in the expression of Vago, an IFN-like antiviral cytokine in arthropods. Overall, this study revealed the significance of an MD-2 homologue as an immune recognition protein for virus lipids. The identification and characterization of CD–ML1–Dorsal–Vago signaling provided new insights into invertebrate antiviral immunity. The Journal of Immunology, 2019, 203: 1131–1141. yeloid differentiation factor 2 (MD-2)–related lipid- with MD-2 and Niemann–Pick disease type C2 (NPC2), respec- http://www.jimmunol.org/ recognition (ML) family proteins are characterized tively, as representatives for the two typical roles. M by the presence of an ML domain. Comprising ∼150 MD-2 was identified as an accessory receptor accompanying residues, the ML domain shows an overall structure of two anti- TLR4 in LPS sensing (2). MD-2 is coexpressed with TLR4, and parallel b sheets that are built from multiple b strands. The two the TLR4/MD-2 heterodimer forms before LPS binding (3). The sheets enclose a cavity to accommodate lipids or lipid-like mol- hydrophobic cavity of MD-2 provides a site for five of six acyl ecules. The hydrophobic residues in the binding pocket are mainly chains of LPS. The remaining exposed acyl chain of LPS interacts responsible for interacting with the side chains of lipids. A high with the conserved hydrophobic phenylalanines located in the C degree of sequence variation in the ligand-binding site, especially terminus of the extracellular domain of a second TLR4, leading by guest on October 1, 2021 the hydrophobic residues, allows the ML domain to recognize a to dimerization of two TLR4–MD-2 complexes (4, 5). The close variety of lipids (1). Through interacting with specific lipids origi- proximity of the TLR4 intracellular domains results in the re- nated from nonself or self via the ML domain, the ML family is cruitment of downstream adaptors, the initiation of an immune mainly involved in antibacterial immunity and lipid metabolism, signaling cascade, and finally, the expression of inflammatory cytokines (6). MD-1, an ortholog of MD-2 sharing ∼20% se- quence homology with MD-2, is also involved in LPS signaling *Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology, together with radioprotective 105, which shares 30% sequence School of Life Sciences, Shandong University, Qingdao, Shandong 266237, China; †Laboratory for Marine Biology and Biotechnology, Qingdao National Labora- identity with TLR4 (7, 8). The radioprotective 105/MD-1 com- tory for Marine Science and Technology, Qingdao, Shandong 266237, China; and plex promotes LPS-induced cell growth and Ab production in ‡ State Key Laboratory of Microbial Technology, Shandong University, Qingdao, B cells and suppresses LPS-induced immune signaling in den- Shandong 266237, China dritic cells and macrophages by interacting with the TLR4/MD-2 Received for publication March 4, 2019. Accepted for publication June 22, 2019. complex (9, 10). This work was supported by the National Science Foundation of China (Grants NPC2 was named for its involvement in the NPC2, which is a 31622058 and 31873043), the National Key Research and Development Program of China (2018YFD0900505), and the Young Scholars Program of Shandong Uni- neurodegenerative lysosomal lipid storage disorder (11). Mutation of versity (Grant 2015WLJH26) (to X.-W.W.). the NPC2 gene would lead to the impairment of egress of choles- The sequences presented in this article have been submitted to GenBank under terol from lysosomes. The NPC2 protein is secreted, recaptured accession numbers MK993577, MK993578, MK993579, MK993580, MK993581, from extracellular sites, and transported into lysosomes. By bind- and MK993582. ing and transferring cholesterol in late endosomes or lysosomes to Address correspondence and reprint requests to Dr. Xian-Wei Wang, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, China. E-mail address: NPC1, another important participator in cholesterol trafficking, [email protected] NPC2 plays an important role in regulating intracellular cholesterol The online version of this article contains supplemental material. homeostasis (12). The structural basis of NPC2-cholesterol bind- Abbreviations used in this article: CD, cholesta-3,5-diene; ChIP, chromatin immu- ing has been revealed. Unliganded bovine NPC2 adopts an overall noprecipitation; F, fusion; GM2A, GM2 activator; ITC, isothermal titration calorim- Ig-like b-sandwich structure, similar to other ML proteins. The etry; MD-2, myeloid differentiation factor 2; ML, MD-2–related lipid-recognition; NPC2, Niemann–Pick disease type C2; qRT-PCR, quantitative real-time RT-PCR; hydrophobic interior core of bovine NPC2 provides a site to RNAi, RNA interference; RSV, respiratory syncytial virus; siRNA, small interfering accommodate cholesterol (13). Similar to NPC2, GM2 activator RNA; SPR, surface plasmon resonance; WNV, West Nile virus; WSSV, white spot (GM2A) is also a small protein involved in lipid metabolism (14). syndrome virus. Through its lipid-binding ability, GM2A functions as a cofactor for Copyright Ó 2019 by The American Association of Immunologists, Inc. 0022-1767/19/$37.50 b-hexosaminidase A, which converts ganglioside GM2 to GM3. www.jimmunol.org/cgi/doi/10.4049/jimmunol.1900268 1132 MD-2 HOMOLOGUE RECOGNIZES VIRUS LIPID IN SHRIMP Deficiency or functional impairment of GM2A leads to GM2 ac- Expression profile analysis cumulation and neuronal disease (15). Semiquantitative RT-PCR was performed to study the tissue distribution of In addition to LPS signaling and lipid metabolism, studies have MjML mRNAs using the gene-specific primers listed in Table I, following suggested the importance of the ML family in host–virus inter- a conventional procedure: 94˚C for 3 min; 30 cycles of 94˚C for 15 s, 54˚C action. For example, mouse mammary tumor virus enhances its for 30 s and 72˚C for 30 s; and a final 72˚C for 10 min, using the EasyTaq infectivity by acquiring host LPS binding factors, including CD14, PCR SuperMix (TransGen Biotech, Beijing, China). PCR products were analyzed using 1.5% agarose gel electrophoresis. Quantitative real-time TLR4, and MD-2, to exploit LPS from commensal bacteria (16). RT-PCR (qRT-PCR) was performed to determine the expression profiles Human MD-2 interacts with the respiratory syncytial virus (RSV) of MjML mRNAs upon WSSV challenge using the iQ SYBR Green fusion (F) protein to activate TLR4–NF-kB–mediated cytokine Supermix (Bio-Rad Laboratories, Hercules, CA) and the CFX96 Real- expression (17). Loss of host NPC2 greatly increased the cho- Time System (Bio-Rad Laboratories), using the same primers used for RT-PCR. The PCR procedure was as follows: 94˚C for 5 min, followed lesterol level in late endosomes/lysosomes and enhanced HIV by 40 cycles of 94˚C for 10 s and 60˚C for 1 min, and a final melting from infectivity (18). The involvement of ML proteins in host–virus 65˚C to 95˚C. PCR data were analyzed using the 22OOCt method. b-Actin interaction was also observed in invertebrates. Silencing of a was used as the internal reference for both semiquantitative RT-PCR and dengue virus–inducible ML protein in Aedes aegypti, AaegML33, qRT-PCR. The expression level was normalized to the control group at resulted in a significantly lower dengue virus titer in the mosquito each time point. Three independent experiments were performed, and the results represented the mean 6 SD.
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