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Recognition TLR7 Signaling Beyond Endosomal Dendritic Cells Flavivirus Activation of Plasmacytoid Dendritic Cells Delineates Key Elements of TLR7 Signaling beyond Endosomal Recognition This information is current as of September 29, 2021. Jennifer P. Wang, Ping Liu, Eicke Latz, Douglas T. Golenbock, Robert W. Finberg and Daniel H. Libraty J Immunol 2006; 177:7114-7121; ; doi: 10.4049/jimmunol.177.10.7114 http://www.jimmunol.org/content/177/10/7114 Downloaded from References This article cites 38 articles, 21 of which you can access for free at: http://www.jimmunol.org/content/177/10/7114.full#ref-list-1 http://www.jimmunol.org/ Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication by guest on September 29, 2021 *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 © 2006 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Flavivirus Activation of Plasmacytoid Dendritic Cells Delineates Key Elements of TLR7 Signaling beyond Endosomal Recognition1 Jennifer P. Wang,2* Ping Liu,† Eicke Latz,* Douglas T. Golenbock,* Robert W. Finberg,* and Daniel H. Libraty† TLR7 senses RNA in endosomal compartments. TLR7 expression and signaling have been demonstrated in plasmacytoid and myeloid dendritic cells, B cells, and T cells. The regulation of TLR7 signaling can play a crucial role in shaping the immune response to RNA viruses with different cellular tropisms, and in developing adjuvants capable of promoting balanced humoral and cell-mediated immunity. We used unique characteristics of two ssRNA viruses, dengue virus and influenza virus, to delineate factors that regulate viral RNA-human TLR7 signaling beyond recognition in endosomal compartments. Our data show that Downloaded from TLR7 recognition of enveloped RNA virus genomes is linked to virus fusion or uncoating from the endosome. The signaling threshold required to activate TLR7-type I IFN production is greater than that required to activate TLR7-NF-␬B-IL-8 produc- tion. The higher order structure of viral RNA appears to be an important determinant of TLR7-signaling potency. A greater understanding of viral RNA-TLR7 activity relationships will promote rational approaches to interventional and vaccine strategies for important human viral pathogens. The Journal of Immunology, 2006, 177: 7114–7121. http://www.jimmunol.org/ nduction of the type I IFN pathway is a critical aspect of Human pDCs express high levels of TLR7, whereas human mDCs innate immunity to many viral infections. Nearly all cell express intermediate levels of both TLR7 and TLR8 (2, 9). TLR7 types can produce some type I IFN in response to viruses, expression and signaling function have also been demonstrated in I ϩ and several mechanisms of viral recognition leading to type I IFN naive B cells (10), and naive and effector memory CD4 T cells production have been identified (1). The amount, kinetics, and reg- (11). This makes TLR7 activation potentially important in shaping ulation of type I IFN in dendritic cells (DCs)3 play a central role the immune responses to RNA viruses with different cellular tro- in shaping antiviral innate immune responses. In particular, plas- pisms. It also raises interest in potent TLR7 agonists as vaccine macytoid DCs (pDCs) are highly specialized cells that produce adjuvants capable of directly targeting all cells involved in gener- large amounts of IFN-␣ in response to a wide range of enveloped ating effective humoral and cell-mediated immunity. by guest on September 29, 2021 viruses and other microbial stimuli (2, 3). They likely play an TLR7 recognizes and is activated by RNA, either uridine-con- important role in controlling systemic infections with enveloped taining ssRNA (12, 13) or synthetic guanosine-like compounds, viruses such as HIV-1, dengue, and HSV (4–6). Through IFN-␣ such as resiquimod (R-848) (14, 15). Spatial recognition of RNA secretion and other effects, pDCs interact with surrounding my- within endosomes is a key regulator of TLR7 activation. Acidifi- eloid DCs (mDCs) to induce innate antiviral immunity and shape cation of endosomal compartments is required for RNA virus- effective adaptive antiviral responses (2, 7). TLR7 signaling (16). Beyond spatial recognition, little is known pDCs and mDCs have several potential mechanisms to recog- about other factors regulating TLR7 signaling and determinants of nize viruses and trigger activation (1, 8). For RNA viruses, TLRs TLR7 agonist potency. Differences in TLR7-signaling capacity 7 and 8 are important mediators of recognition and innate immune have been reported between ssRNA and monomeric ligands (17), activation. TLRs 7 and 8 are members of the TLR9 subfamily that sequences within synthetic RNAs (12, 18), and among different sense pathogen-derived RNA (TLR 7/8) and DNA (TLR9) moi- sources of cellular RNA (13). The natural ligands for TLR7 acti- eties intracellularly, and signal through the adaptor MyD88 (9). vation, and particularly TLR7-type I IFN signaling, are ssRNA viruses that gain access to TLR7-containing endocytic organelles (4, 16, 17, 19). Unique aspects of ssRNA viruses can be used as *Department of Medicine and †Center for Infectious Disease and Vaccine Research, University of Massachusetts Medical School, Worcester, MA 01655 tools to elucidate regulation of TLR7 signaling beyond spatial recognition. Received for publication February 8, 2006. Accepted for publication August 25, 2006. We examined viral RNA (vRNA)-TLR7 recognition and signal- The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance ing using two ssRNA viruses, dengue-2 virus (D2V) and influenza with 18 U.S.C. Section 1734 solely to indicate this fact. A X31 virus (flu X31). D2V is an enveloped flavivirus containing 1 This work was supported by the National Institutes of Health (NIH U19 AI57319, a single 11 kb, positive-strand, ssRNA genome. The vRNA has a R21 AI060791, and K08AI053542). The contents of this publication are solely the capped 5Ј-triphosphate end. Virus fusion and uncoating from en- responsibility of the authors and do not necessarily represent the official views of the National Institutes of Health. docytic vacuoles is pH dependent and occurs in early endosomes 2 Address correspondence and reprint requests to Dr. Jennifer P. Wang, Department through a type II fusion process (20, 21). Influenza A viruses are of Medicine, University of Massachusetts Medical School, LRB 219, 55 Lake Avenue enveloped orthomyxoviruses containing a segmented, negative- North, Worcester, MA 01655. E-mail address: [email protected] strand, ssRNA genome totaling 13.5 kb. The vRNA segments have 3 Abbreviations used in this paper: DC, dendritic cell; pDC, plasmacytoid DC; mDC, uncapped, 5Ј-triphosphate ends. Virus fusion and uncoating from myeloid DC; vRNA, viral RNA; D2V, dengue-2 virus; siRNA, short-interfering RNA; ODN, oligodeoxyribonucleotide; MOI, multiplicity of infection; ER, endoplas- endocytic vacuoles is pH dependent and occurs in late endosomes mic reticulum; SNV, Sin Nombre virus. through a type I fusion process (21, 22). Flu X31 is a reassortment Copyright © 2006 by The American Association of Immunologists, Inc. 0022-1767/06/$02.00 The Journal of Immunology 7115 of A/PR/8/34 (H1N1) (PR8) virus with A/Aichi/68 (H3N2). By resulted in a Ͼ104 PFU/ml decrease in the titers of both viruses, as con- using these RNA viruses, synthetic ssRNAs, and R-848 to stimu- firmed by limiting dilution plaque assays. Stably transfected HEK/hTLR7/ ␬ ␬ late pDCs and a TLR7-transfected cell line, we were able to de- NF- B cells and HEK/NF- B control cells were continuously passaged and maintained in DMEM (Invitrogen Life Technologies) supplemented lineate key elements affecting TLR7 activation. TLR7 recognition with 10% FCS. of enveloped ssRNA virus genomes appeared linked to the virus fusion or uncoating process from endosomal compartments. The RNA isolation and transfection signaling threshold required to activate TLR7-type I IFN produc- Viral genomic RNAs from influenza virus and D2V were isolated from tion was greater than that required to activate TLR7-NF-␬B-IL-8 virus stocks using the QIAamp Viral RNA kit (Qiagen). Sin Nombre virus production, but the specialized nature of pDCs allowed them to (SNV) G2 RNA was obtained by T7 polymerase-driven in vitro transcrip- produce IFN-␣ in response to low potency TLR7 agonists. Finally, tion of a pcDNA 3.1/SNV G2 plasmid (a gift from C. Schmaljohn, U.S. the higher order structure of viral genomic RNAs was an important Army Medical Research Institute for Infectious Diseases, Fort Detrick, MD) using the Riboprobe In Vitro Transcription kit (Promega) followed by determinant of TLR7-signaling potency. RNA extraction and isolation using phenol/chloroform and isopropanol. Isolated vRNAs were treated with RNase-free DNase I for 30 min at 37°C. Materials and Methods DNase was removed by phenol/chloroform extraction and isopropanol pre- Viruses, reagents, and cells cipitation of the RNA. In some experiments, influenza vRNA was then treated with proteinase K (Promega) or Triton X-100 (Sigma-Aldrich), and Influenza A virus X31 strain was purchased from Charles River Interna- the vRNA was re-extracted as noted above. Or, the 5Ј-␤ and -␥ phosphates tional and titered by limiting dilution plaque assay on Madin-Darby canine were removed from influenza vRNA using tobacco acid pyrophosphatase kidney cells in the presence of trypsin (0.2 ␮g/ml).
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