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Rotavirus-Infected Intestinal Epithelium a Protective IFN Response in RIG-I/MDA5/MAVS Are Required to Signal

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Rotavirus-Infected Intestinal Epithelium a Protective IFN Response in RIG-I/MDA5/MAVS Are Required to Signal RIG-I/MDA5/MAVS Are Required To Signal a Protective IFN Response in Rotavirus-Infected Intestinal Epithelium This information is current as Alexis H. Broquet, Yoshihiro Hirata, Christopher S. of September 26, 2021. McAllister and Martin F. Kagnoff J Immunol 2011; 186:1618-1626; Prepublished online 27 December 2010; doi: 10.4049/jimmunol.1002862 http://www.jimmunol.org/content/186/3/1618 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2010/12/27/jimmunol.100286 Material 2.DC1 http://www.jimmunol.org/ References This article cites 69 articles, 33 of which you can access for free at: http://www.jimmunol.org/content/186/3/1618.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 26, 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 © 2011 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology RIG-I/MDA5/MAVS Are Required To Signal a Protective IFN Response in Rotavirus-Infected Intestinal Epithelium Alexis H. Broquet,* Yoshihiro Hirata,* Christopher S. McAllister,* and Martin F. Kagnoff*,† Rotavirus is a dsRNAvirus that infects epithelial cells that line the surface of the small intestine. It causes severe diarrheal illness in children and ∼500,000 deaths per year worldwide. We studied the mechanisms by which intestinal epithelial cells (IECs) sense rotavirus infection and signal IFN-b production, and investigated the importance of IFN-b production by IECs for controlling rotavirus production by intestinal epithelium and virus excretion in the feces. In contrast with most RNA viruses, which interact with either retinoic acid-inducible gene I (RIG-I) or melanoma differentiation-associated gene 5 (MDA5) inside cells, rotavirus was sensed by both RIG-I and MDA5, alone and in combination. Rotavirus did not signal IFN-b through either of the dsRNA sensors TLR3 or dsRNA-activated protein kinase (PKR). Silencing RIG-I or MDA5, or their common adaptor protein mitochon- Downloaded from drial antiviral signaling protein (MAVS), significantly decreased IFN-b production and increased rotavirus titers in infected IECs. Overexpression of laboratory of genetics and physiology 2, a RIG-I–like receptor that interacts with viral RNA but lacks the caspase activation and recruitment domains required for signaling through MAVS, significantly decreased IFN-b production and increased rotavirus titers in infected IECs. Rotavirus-infected mice lacking MAVS, but not those lacking TLR3, TRIF, or PKR, produced significantly less IFN-b and increased amounts of virus in the intestinal epithelium, and shed increased quantities of virus in the feces. We conclude that RIG-I or MDA5 signaling through MAVS is required for the activation of IFN-b production http://www.jimmunol.org/ by rotavirus-infected IECs and has a functionally important role in determining the magnitude of rotavirus replication in the intestinal epithelium. The Journal of Immunology, 2011, 186: 1618–1626. pithelial cells that line the intestinal mucosal surface are a signature of virus infection, via RNA-dependent RNA synthesis. a first line of defense against enteric pathogens (1–5). dsRNA activates cell type-specific pattern recognition receptors, E Microbial pathogens that infect the intestinal tract can which signal host cellular responses (10–13). For example, on in- cause structural and functional modifications of the epithelial teracting with dsRNA, dsRNA-activated protein kinase (PKR), barrier that are associated with diarrhea and systemic infection. a Ser/Thr kinase with dsRNA binding motifs in its N terminus, is by guest on September 26, 2021 Rotavirus, a dsRNA icosahedral RNA virus, is a major cause of activated (14). PKR phosphorylates eIF-2a and inhibits translation severe diarrhea and results in significant morbidity, especially in initiation (15). Although PKR is an IFN-regulated gene and infants and young children, with ∼500,000 deaths worldwide an- can regulate apoptotic pathways important for eliminating virus- nually (2, 6, 7). Severe rotavirus diarrhea also is more common infected cells (16), it is not known to have a direct role in increas- in the elderly and immunocompromised. ing the production of type I IFN that is important for host defense Rotavirus infection of the small intestine most markedly dam- to virus infection (17). ages epithelial cells located in the upper portion of intestinal villi Several host cellular proteins that interact with dsRNA signal (8, 9). After cell entry, RNA viruses generate dsRNA, which is host innate immune responses (10–13, 18, 19). For example, TLR3 is a pathogen recognition receptor (PRR) that transduces a signal to the adaptor molecule TRIF, which, in turn, signals the activation *Laboratory of Mucosal Immunology, Department of Medicine, University of Cal- of IFN regulatory factor 3 (IRF3), type I IFN, and NF-kB (20). ifornia, San Diego, La Jolla, CA 92093; and †Department of Pediatrics, University of California, San Diego, La Jolla, CA 92093 Mice genetically deficient in TRIF signaling have increased sus- ceptibility to certain viral infections (e.g., mouse cytomegalovi- Received for publication August 24, 2010. Accepted for publication November 22, 2010. rus), indicating a significant role for the TLR3–TRIF signaling This work was supported by the National Institutes of Health (Grant DK35108), the pathway in host-viral pathogenesis (20). However, signaling William K. Warren Foundation, and a fellowship from the Fondation pour la Re- through the TLR–TRIF pathway is not essential for developing cherche Me´dicale (France) (to A.H.B.). type I IFN responses because mice defective in TLR3–TRIF sig- Address correspondence and reprint requests to Prof. Martin F. Kagnoff, University naling can produce type I IFN responses to virus infection (21). of California, San Diego, 9500 Gilman Drive, Mail Code 0623D, La Jolla CA 92093- 0623. E-mail address: [email protected] Currently, there is no evidence whether TLR3 has a role in signaling The online version of this article contains supplemental material. type I IFN production in rotavirus-infected intestinal epithelial cells (IECs). Further, how dsRNA produced in the cytoplasm during Abbreviations used in this article: CARD, caspase activation and recruitment domain; ctrl, control; DN, dominant negative; IEC, intestinal epithelial cell; IRF3, IFN reg- virus replication would access TLR3 is an open question, because ulatory factor 3; ISRE, IFN-stimulated response element; LGP2, laboratory of ge- TLR3 is localized in the endosomal membrane in many cell types, netics and physiology 2; MAVS, mitochondrial antiviral signaling protein; MDA5, melanoma differentiation-associated gene 5; PKR, dsRNA-activated protein kinase; including IECs (22). poly(I:C), polyinosinic-polycytidylic acid; PRR, pathogen recognition receptor; RIG- Two members of the RIG-I–like receptor (RLR) family were I, retinoic acid-inducible gene I; RLR, RIG-I–like receptors; RRV, rhesus rotavirus; recognized more recently as important for cell signaling activated siRNA, small interfering RNA; WT, wild type. by dsRNA (23, 24). These RNA helicases, retinoic acid-inducible Copyright Ó 2011 by The American Association of Immunologists, Inc. 0022-1767/11/$16.00 gene I (RIG-I) and melanoma differentiation-associated gene 5 www.jimmunol.org/cgi/doi/10.4049/jimmunol.1002862 The Journal of Immunology 1619 (MDA5, also known as helicard or IFIH1), each contain a C- Mice terminal DExD/H box RNA helicase domain that is a character- Wild type (WT) C57BL/6J (B6) mice were from The Jackson Laboratory. istic amino acid signature motif of many RNA binding proteins, PKR2/2 (B6 background) and TLR32/2 (B6 background) mice were as well as two N-terminal caspase activation and recruitment provided by Dr. E. Raz (University of California, San Diego [UCSD], 2/2 domains (CARDs). Interaction of the DExD/H box RNA helicase La Jolla, CA). TRIF (B6 background) mice were provided by Dr. 2/2 domain with viral dsRNA induces the unwinding of RNAs by B. Beutler (The Scripps Research Institute, La Jolla, CA). MAVS mice (C57BL/6J/129 mixed background) (42) and the corresponding WT mice means of energy derived from ATP hydrolysis and, at the same were provided by Dr. Chen (University of Texas Southwestern Medical time, induces conformational changes in RIG-I and MDA5 that Center, Dallas, TX). All mouse strains were maintained at the UCSD. All promote the CARD-mediated downstream signaling cascade. This animal studies were approved by the UCSD Institutional Animal Care and leads to the activation of the adaptor molecule mitochondrial anti- Use Committee. viral signaling protein (MAVS; also termed IPS-1/Cardif/VISA) Reagents (25–29). Definitive evidence for the role of RIG-I and MDA5 in Trypsin (type IX-S, from porcine pancreas, 13–20 U/mg benzoyl L-arginine signaling activated by dsRNA viruses was obtained using
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