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The IFN Response in Bats Displays Distinctive IFN-Stimulated Gene Expression Kinetics with Atypical RNASEL Induction

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The IFN Response in Bats Displays Distinctive IFN-Stimulated Gene Expression Kinetics with Atypical RNASEL Induction The IFN Response in Bats Displays Distinctive IFN-Stimulated Gene Expression Kinetics with Atypical RNASEL Induction This information is current as Pamela C. De La Cruz-Rivera, Mohammed Kanchwala, of September 25, 2021. Hanquan Liang, Ashwani Kumar, Lin-Fa Wang, Chao Xing and John W. Schoggins J Immunol published online 27 November 2017 http://www.jimmunol.org/content/early/2017/11/23/jimmun ol.1701214 Downloaded from Supplementary http://www.jimmunol.org/content/suppl/2017/11/23/jimmunol.170121 Material 4.DCSupplemental 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 25, 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 © 2017 by The American Association of Immunologists, Inc. All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. Published November 27, 2017, doi:10.4049/jimmunol.1701214 The Journal of Immunology The IFN Response in Bats Displays Distinctive IFN-Stimulated Gene Expression Kinetics with Atypical RNASEL Induction Pamela C. De La Cruz-Rivera,* Mohammed Kanchwala,† Hanquan Liang,† Ashwani Kumar,† Lin-Fa Wang,‡ Chao Xing,†,x,{ and John W. Schoggins* Bats host a large number of zoonotic viruses, including several viruses that are highly pathogenic to other mammals. The mechanisms underlying this rich viral diversity are unknown, but they may be linked to unique immunological features that allow bats to act as asymptomatic viral reservoirs. Vertebrates respond to viral infection by inducing IFNs, which trigger antiviral defenses through IFN- stimulated gene (ISG) expression. Although the IFN system of several bats is characterized at the genomic level, less is known about bat IFN-mediated transcriptional responses. In this article, we show that IFN signaling in bat cells from the black flying fox (Pteropus Downloaded from alecto) consists of conserved and unique ISG expression profiles. In IFN-stimulated cells, bat ISGs comprise two unique temporal subclusters with similar early induction kinetics but distinct late-phase declines. In contrast, human ISGs lack this decline phase and remained elevated for longer periods. Notably, in unstimulated cells, bat ISGs were expressed more highly than their human counterparts. We also found that the antiviral effector 2-5A–dependent endoribonuclease, which is not an ISG in humans, is highly IFN inducible in black flying fox cells and contributes to cell-intrinsic control of viral infection. These studies reveal distinctive innate immune features that may underlie a unique virus–host relationship in bats. The Journal of Immunology, 2018, 200: 000–000. http://www.jimmunol.org/ ats are recognized as important viral reservoirs, and viruses than all other mammalian orders tested, with the highest viral many highly pathogenic viruses, including Nipah virus richness found in flaviviruses, bunyaviruses, and rhabdoviruses (10). B (1), Hendra virus (2), Marburg virus (3), severe acute Although the mechanisms underlying disease resistance are not known, respiratory syndrome–like coronaviruses (4), and Ebola virus (5), it has been speculated that bats possess unique immune features that have been detected in various bat species. In experimental infec- confer innate antiviral protection (9, 11). In vertebrates, one of the first tion studies, certain bats can be productively infected with path- lines of defense against viral pathogens is the IFN response. Upon viral ogenic viruses without obvious disease symptoms (6–9). A recent infection, pattern-recognition receptors sense viral components and by guest on September 25, 2021 study identified bats as hosts for a greater proportion of zoonotic initiate a signaling cascade that results in the secretion of IFNs. These IFNs bind their cognate receptors to activate the JAK–STAT signaling *Department of Microbiology, University of Texas Southwestern Medical Center, pathway, leading to the transcriptional induction of hundreds of IFN- Dallas, TX 75390; †McDermott Center Bioinformatics Core, University of Texas stimulated genes (ISGs), many of which have antiviral activity (12). ‡ Southwestern Medical Center, Dallas, TX 75390; Programme in Emerging Infec- The black flying fox (Pteropus alecto) is an asymptomatic natural tious Diseases, Duke-National University of Singapore Medical School, Singapore 169857, Singapore; xDepartment of Bioinformatics, University of Texas Southwest- reservoir for the highly lethal Hendra virus (2, 13, 14). Studies of the ern Medical Center, Dallas, TX 75390; and {Department of Clinical Sciences, Uni- recently sequenced black flying fox genome revealed that genes for versity of Texas Southwestern Medical Center, Dallas, TX 75390 key components of antiviral immunity are conserved in bats, such as ORCIDs: 0000-0002-8806-8688 (P.C.D.L.C.-R.); 0000-0001-6035-2970 (M.K.); pathogen sensors, including TLRs (15), RIG-I–like helicases, and 0000-0003-2752-0535 (L.-F.W.); 0000-0002-1838-0502 (C.X.); 0000-0002-7944- 6800 (J.W.S.). NOD-like receptors, IFNs and their receptors, and ISGs (11, 16). Received for publication August 24, 2017. Accepted for publication October 25, Previous efforts to study bat–virus interactions have mainly focused 2017. on the host response to viral infection (17–20), and global tran- This work was supported in part by National Institutes of Health Grant AI117922 (to J.W.S.), scriptional responses to type I IFN remain uncharacterized. the University of Texas Southwestern Endowed Scholars Program (to J.W.S.), the Univer- Because the black flying fox harbors pathogenic human viruses and sity of Texas Southwestern High Impact/High Risk Grant Program (to J.W.S.), the William F. and Grace H. Kirkpatrick Award (to P.C.D.L.C.-R.), and National Research Foundation- has an annotated genome, we sought to characterize the IFN-induced Competitive Research Programme Grant NRF2012NRF-CRP001–056 (to L.-F.W.). C.X. was transcriptional response in this species. Gene-expression analyses partially supported by National Institutes of Health Grant UL1TR001105. revealed that bat cells induce a pool of common ISGs. However, they The sequences presented in this article have been submitted to the Gene Expression also induced a small number of apparent novel ISGs, including 2-5A– Omnibus (https://www.ncbi.nlm.nih.gov/geo/) under accession number GSE102296. dependent endoribonuclease (RNASEL). Kinetic analyses revealed Address correspondence and reprint requests to John W. Schoggins, University of that bat ISGs can be categorized into distinct groups, depending on Texas Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9048. E-mail address: [email protected] their temporal gene-expression patterns. Additionally, maintenance The online version of this article contains supplemental material. of ISG expression over time differed between bat and human cells, Abbreviations used in this article: CRISPR, clustered regularly interspaced short suggesting distinct mechanisms of gene regulation. palindromic repeats; FC, fold change; FDR, false discovery rate; ISG, IFN- stimulated gene; KO, knockout; NEAA, nonessential amino acids; OAS, oligoade- nylate synthase; poly(I:C), polyinosinic-polycytidylic acid; RNASEL, 2-5A– Materials and Methods dependent endoribonuclease; RNA-Seq, RNA sequencing; SC, subcluster; VSV, ve- Cell lines sicular stomatitis virus; WT, wild-type; YFV, yellow fever virus. Black flying fox–derived PaBr (brain), PaLu (lung), and PaKi (kidney) im- Copyright Ó 2017 by The American Association of Immunologists, Inc. 0022-1767/17/$35.00 mortalized cell lines (21) were grown at 37˚C and 5% CO2 and passaged in www.jimmunol.org/cgi/doi/10.4049/jimmunol.1701214 2 IFN RESPONSE OF A BAT VIRAL RESERVOIR DMEM/F-12 (catalog number 11320033; Life Technologies) supplemented Data were deposited in the Gene Expression Omnibus database (https:// with 10% FBS. Human A549 lung adenocarcinoma and HEK293 cells were www.ncbi.nlm.nih.gov/geo/) under accession number GSE102296. grown at 37˚C and 5% CO2 and passaged in DMEM (catalog number 11995065) supplemented with 10% FBS and 13 nonessential amino acids Heat maps (NEAA) (catalog number 11140076; both from Life Technologies). Heat maps were constructed using Morpheus (https://software.broadinstitute. Viruses org/morpheus/). Yellow fever virus (YFV)-Venus (derived from YF17D-5C25Venus2AUbi) NanoString analysis stocks were generated by electroporation of in vitro–transcribed RNA into 2 2 A customized panel targeting black flying fox and human genes (Schog- STAT1 / fibroblasts, as previously described (12). Vesicular stomatitis virus gins_1_C4066; NanoString Technologies, Seattle, WA) was used to mea- (VSV) encoding GFP, Indiana serotype (provided by J. Rose) was generated sure the expression of 50 genes per species. Probes were designed to target by passage in BHK-J cells. For both viruses, virus-containing supernatant 2 as many known transcript variants as possible (see Supplemental
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