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Single-Stranded Oligonucleotide-Mediated Inhibition of Respiratory Syncytial Virus Infection

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Single-Stranded Oligonucleotide-Mediated Inhibition of Respiratory Syncytial Virus Infection Single-Stranded Oligonucleotide-mediated Inhibition of Respiratory Syncytial Virus Infection Axberg Palsson, S., Dondalska, A., Bergenstrahle, J. A., Rolfes, C., Bjork, A., Sedano, L., Power, U., Remeix- Welti, M-A., Mastrangelo, P., Eleouet, J-F., Le Goffic, R., Galloux, M., & Spetz, A-L. (2020). Single-Stranded Oligonucleotide-mediated Inhibition of Respiratory Syncytial Virus Infection. Frontiers in immunology, 11, [580547]. https://doi.org/10.3389/fimmu.2020.580547 Published in: Frontiers in immunology Document Version: Publisher's PDF, also known as Version of record Queen's University Belfast - Research Portal: Link to publication record in Queen's University Belfast Research Portal Publisher rights Copyright 2020 the authors. This is an open access article published under a Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited. General rights Copyright for the publications made accessible via the Queen's University Belfast Research Portal is retained by the author(s) and / or other copyright owners and it is a condition of accessing these publications that users recognise and abide by the legal requirements associated with these rights. Take down policy The Research Portal is Queen's institutional repository that provides access to Queen's research output. Every effort has been made to ensure that content in the Research Portal does not infringe any person's rights, or applicable UK laws. If you discover content in the Research Portal that you believe breaches copyright or violates any law, please contact [email protected]. Download date:05. Oct. 2021 ORIGINAL RESEARCH published: 08 December 2020 doi: 10.3389/fimmu.2020.580547 Single-Stranded Oligonucleotide- Mediated Inhibition of Respiratory Syncytial Virus Infection Sandra Axberg Pålsson 1*, Aleksandra Dondalska 1, Joseph Bergenstråhle 2, Caroline Rolfes 1, Albin Björk 3, Laura Sedano 4, Ultan F. Power 5, Marie-Anne Rameix-Welti 6, Joakim Lundeberg 2, Marie Wahren-Herlenius 3, 7 4 4 4 Edited by: Peter Mastrangelo , Jean-Francois Eleouet , Ronan Le Goffic , Marie Galloux 1 Aurelio Cafaro, and Anna-Lena Spetz * National Institute of Health (ISS), Italy 1 Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, Sweden, 2 Science for Reviewed by: Life Laboratory, Department of Gene Technology, Royal Institute of Technology, Stockholm, Sweden, 3 Division of Michael Teng, Rheumatology, Department of Medicine, Karolinska Institutet, Karolinska University Hospital, Stockholm, Sweden, 4 UR0892 University of South Florida, Unite´ VIM, INRAE, Universite´ Paris-Saclay, Jouy-en-Josas, France, 5 Wellcome-Wolfson Institute for Experimental Medicine, United States School of Medicine, Dentistry and Biomedical Sciences, Queen’s University Belfast, Belfast, Northern Ireland, 6 UMR INSERM Nicolas Cuburu, U1173 I2, UFR des Sciences de la Sante´ Simone Veil—UVSQ, Montigny-Le-Bretonneux, France, 7 Department of Laboratory National Cancer Institute (NCI), Medicine and Pathobiology, University of Toronto, Toronto, Canada United States *Correspondence: Sandra Axberg Pålsson Respiratory syncytial virus (RSV) is the leading cause of acute lower respiratory tract [email protected] infections in young children. Currently, there is no RSV vaccine or universally accessible Anna-Lena Spetz [email protected] antiviral treatment available. Addressing the urgent need for new antiviral agents, we have investigated the capacity of a non-coding single-stranded oligonucleotide (ssON) to inhibit Specialty section: RSV infection. By utilizing a GFP-expressing RSV, we demonstrate that the ssON This article was submitted to significantly reduced the proportion of RSV infected A549 cells (lung epithelial cells). Viral Immunology, a section of the journal Furthermore, we show that ssON’s antiviral activity was length dependent and that both Frontiers in Immunology RNA and DNA of this class of oligonucleotides have antiviral activity. We reveal that ssON Received: 06 July 2020 inhibited RSV infection by competing with the virus for binding to the cellular receptor Accepted: 09 November 2020 Published: 08 December 2020 nucleolin in vitro. Additionally, using a recombinant RSV that expresses luciferase we Citation: show that ssON effectively blocked RSV infection in mice. Treatment with ssON in vivo Pålsson SA, Dondalska A, resulted in the upregulation of RSV-induced interferon stimulated genes (ISGs) such as Bergenstråhle J, Rolfes C, Björk A, Stat1, Stat2, Cxcl10,andCcl2. This study highlights the possibility of using Sedano L, Power UF, Rameix-Welti M-A, Lundeberg J, Wahren-Herlenius M, oligonucleotides as therapeutic agents against RSV infection. We demonstrate that the Mastrangelo P, Eleouet J-F, mechanism of action of ssON is the inhibition of viral entry in vitro, likely through the Le GofficR,Galloux M and Spetz A-L (2020) Single-Stranded binding of the receptor, nucleolin and that ssON treatment against RSV infection in vivo Oligonucleotide-Mediated Inhibition of additionally results in the upregulation of ISGs. Respiratory Syncytial Virus Infection. Front. Immunol. 11:580547. Keywords: respiratory syncytial virus (RSV), oligonucleotides, single-stranded oligonucleotides, ssON, antiviral, doi: 10.3389/fimmu.2020.580547 nucleolin, ISGs Frontiers in Immunology | www.frontiersin.org 1 December 2020 | Volume 11 | Article 580547 Pålsson et al. Oligonucleotide-Mediated Inhibition of RSV infection INTRODUCTION shown to inhibit clathrin- and caveolin-mediated endocytosis (11), could inhibit RSV infection. We evaluated anti-RSV activity Human respiratory syncytial virus (RSV) is a negative sense single- against a RSV-A virus expressing GFP (RSV-GFP) by assessing stranded RNA virus of the Pneumoviridae family. It causes acute the proportion of A549 infected cells using flow cytometry severe infections in the lower respiratory tract of children, the elderly (Supplementary Figure 1, gating strategy). Pre-treatment with and immunocompromised individuals (1). Annually, 64 million cases ssON or concomitant addition of ssON and RSV to A549 cells of RSV infection are reported globally and of these, approximately resulted in a significantly reduced proportion of GFP positive 160,000 cases result in death (National Institute of Allergy and RSV-infected cells (~10%) (Figure 1A) as compared to the RSV- Infectious Diseases; https://www.niaid.nih.gov). Furthermore, reports infected untreated controls (~60%). indicate that 90% of children are infected with RSV within their first We next evaluated ssON´s anti-RSV activity using MOIs two years of life (2). In addition, the development of wheezing and ranging from 0.01 to 1 (Figure 1B). We found that ssON asthma have been associated with early-life RSV infection (3). effectively blocked RSV infection for all MOIs assessed There is currently no RSV-specific antiviral treatment or vaccine regardless of whether ssON was added before infection or against RSV, except for an immunoprophylactic anti-RSV monoclonal simultaneously with the virus (Figure 1B). The antiviral antibody (Palivizumab) or intravenous immunoglobulin (IVIG) activity persisted for up to 96h after a single ssON exposure. treatment. Unfortunately, due to high cost, use of Palivizumab is We also monitored cell viability and found that the highest RSV restricted to children at a high risk of developing severe RSV-induced infection dose (MOI 1) resulted in increased cell death overtime disease, such as premature infants, immunocompromised newborn (~10-30%). Notably, neither pre-incubation nor concomitant babies, or children with congenital heart or lung disease, in high addition of ssON and RSV negatively affected the viability of income countries (4, 5). Although several ongoing clinical studies are A549 cells. Instead, there was a clear trend that ssON treatment exploring potential RSV vaccines and new anti-RSV monoclonal reduced the cell death by up to 25% in the cell cultures exposed to antibodies, successful progress has been slow. In parallel, many the highest MOI 1 (Figure 1C). recent studies are focusing on the development of alternative RSV We have previously reported that the capability of ssONs to inhibitors and the pipeline of new anti-RSV therapeutics was recently interfere with endocytosis is dependent on the length of the reviewed (6). Examples of new antiviral compounds are the fusion oligonucleotide. Oligonucleotides with the same lengths as inhibitors Presatovir (GS-5806), TMC353121 and JNJ-678, and miRNAs do not possess this feature. However, somewhat replication inhibitors such as Lumicitabine (ALS-8176) (7). longer oligonucleotides of at least 25 bases may exert such RSV was shown to enter ciliated epithelial cells via receptor- activity (11). The endocytosis inhibitory capacity is not based mediated endocytosis, utilizing nucleolin as a possible cellular receptor on complementary binding to another oligonucleotide but for viral entry (8). However, emerging studies indicate that RSV is requires certain structural features to have this activity (11). In taken up via macropinocytosis rather than endocytosis (9, 10). Hence, addition, there is extensive data in the literature that the chemical a detailed route of RSV infection remains to be further elucidated and phosphorothioate (PS) modification of the backbone prolongs entry is likely to involve a multimeric protein complex. Here, we the half-life of the oligonucleotides
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