ArticleCell2020
Hybrid Gene Origination Creates Human-Virus Chimeric Proteins during Infection.
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Article in Cell, 2020. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 32 papers.
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32citing papers in PubMed
5.0field-weighted citation impact, top 4% of its field
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Who cites it
32 citing papers in PubMed, 45 citations in OpenAlex.
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- Cryptic proteins translated from deletion-containing viral genomes dramatically expand the influenza virus proteome.bioRxiv : the preprint server for biology · 2024Article
- Avian ANP32A incorporated in avian influenza A virions promotes interspecies transmission by priming early viral replication in mammals.Science advances · 2024Article
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- Viral RNA Is a Hub for Critical Host-Virus Interactions.Sub-cellular biochemistry · 2023Article
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- Hijacking Self-Assembly to Establish Intracellular Functional Nanoparticles.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2022Article
- Proximity interactome analysis of Lassa polymerase reveals eRF3a/GSPT1 as a druggable target for host-directed antivirals.Proceedings of the National Academy of Sciences of the United States of America · 2022Article
- Upstream open reading frames regulate translation of cancer-associated transcripts and encode HLA-presented immunogenic tumor antigens.Cellular and molecular life sciences : CMLS · 2022Article
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Authors and funding
54 authors at 13 institutions in 4 countries.
Jessica Sook Yuin HoDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Matthew AngelLaboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA.
Yixuan MaDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Elizabeth SloanMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UK.
Guojun WangDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Carles Martinez-RomeroDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Division of Infectious Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Marta AlenquerInstituto Gulbenkian de Ciência, 2780-156 Oeiras, Portugal.
Vladimir RoudkoTisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Medicine, Hematology and Medical Oncology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Pathology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Liliane ChungThe Roslin Institute, University of Edinburgh, Edinburgh EH25 9PS, UK.
Simin ZhengDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Max ChangDepartment of Medicine, School of Medicine, University of California San Diego, La Jolla, CA 92037, USA.
Yesai FstkchyanDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Sara ClohiseyThe Roslin Institute, University of Edinburgh, Edinburgh EH25 9PS, UK.
Adam M DinanDivision of Virology, Department of Pathology, University of Cambridge, Cambridge CB2 0SP, UK.
James GibbsLaboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA.
Robert GiffordMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UK.
Rong ShenDivision of Structural Biology, The Institute of Cancer Research, London SW7 3RP, UK.
Quan GuMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UK.
Nerea IrigoyenDivision of Virology, Department of Pathology, University of Cambridge, Cambridge CB2 0SP, UK.
Laura CampisiDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Cheng HuangDepartment of Pathology, the University of Texas Medical Branch, Galveston, TX 77555, USA.
Nan ZhaoDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Joshua D JonesDivision of Virology, Department of Pathology, University of Cambridge, Cambridge CB2 0SP, UK.
Ingeborg van KnippenbergMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UK.
Zeyu ZhuDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Natasha MoshkinaDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Léa MeyerMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UK.
Justine NoelDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Zuleyma PeraltaDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Veronica RezeljMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UK.
Robyn KaakeDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA.
Brad RosenbergDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Bo WangThe Roslin Institute, University of Edinburgh, Edinburgh EH25 9PS, UK.
Jiajie WeiLaboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA.
Slobodan PaesslerDepartment of Pathology, the University of Texas Medical Branch, Galveston, TX 77555, USA.
Helen M WiseThe Roslin Institute, University of Edinburgh, Edinburgh EH25 9PS, UK.
Jeffrey JohnsonDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA.
Alessandro VanniniDivision of Structural Biology, The Institute of Cancer Research, London SW7 3RP, UK; Fondazione Human Technopole, Structural Biology Research Centre, 20157 Milan, Italy.
Maria João AmorimInstituto Gulbenkian de Ciência, 2780-156 Oeiras, Portugal.
J Kenneth BaillieThe Roslin Institute, University of Edinburgh, Edinburgh EH25 9PS, UK.
Emily R MiraldiDivisions of Immunobiology and Biomedical Informatics, Cincinnati Children's Hospital, Cincinnati, OH 45229, USA; Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, OH 45257, USA.
Christopher BennerDepartment of Medicine, School of Medicine, University of California San Diego, La Jolla, CA 92037, USA.
Ian BrierleyDivision of Virology, Department of Pathology, University of Cambridge, Cambridge CB2 0SP, UK.
Paul DigardThe Roslin Institute, University of Edinburgh, Edinburgh EH25 9PS, UK.
Marta ŁukszaDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Andrew E FirthDivision of Virology, Department of Pathology, University of Cambridge, Cambridge CB2 0SP, UK.
Nevan KroganDepartment of Cellular and Molecular Pharmacology, University of California, San Francisco, San Francisco, CA 94158, USA.
Benjamin D GreenbaumTisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Medicine, Hematology and Medical Oncology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Oncological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Pathology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Megan K MacLeodCentre for Immunobiology, Institute of Infection, Immunity and Inflammation, University of Glasgow, Glasgow G12 8QQ, UK.
Harm van BakelDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Adolfo Garcìa-SastreDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Division of Infectious Diseases, Department of Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Jonathan W YewdellLaboratory of Viral Diseases, National Institute of Allergy and Infectious Diseases, NIH, Bethesda, MD 20892, USA.
Edward HutchinsonMRC-University of Glasgow Centre for Virus Research, Glasgow G61 1QH, UK. Electronic address: edward.hutchinson@glasgow.ac.uk.
Ivan MarazziDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA. Electronic address: ivan.marazzi@mssm.edu.
Icahn School of Medicine at Mount Sinai · USMRC University of Glasgow Centre for Virus Research · GBUniversity of Cambridge · GBNational Institute of Allergy and Infectious Diseases · USRoslin Institute · GBUniversity of California, San Francisco · USInstitute of Cancer Research · GBInstituto Gulbenkian de Ciência · PTThe University of Texas Medical Branch at Galveston · USUniversity of California, San Diego · USUniversity of Edinburgh · GBUniversity of Cincinnati Medical Center · USUniversity of Glasgow · GB
Funding
SARS-CoV adaptations through a Systems Biology Lens (SYBIL)U19AI135972 · NIAID · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI Adolfo Garcia-Sastre · 2018 to 2026
$27.2MTranslation in ImmunityZIAAI001210 · NIAID · NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES · PI YEWDELL, JONATHAN W · 2016 to 2025
$12.5MMulti-level analysis of influenza virus polymerase and its role in pathogenesisR01AI113186 · NIAID · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI MARAZZI, IVAN, VAN BAKEL, HARM · 2015 to 2019
$3.0MA host-dependent mechanism controlling influenza virus infection by suppressing viral RNA synthesisR01AI143840 · NIAID · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI MARAZZI, IVAN · 2019 to 2023
$2.1MBiotechnology and Biological Sciences Research Council BB/J004324/1Biotechnology and Biological Sciences Research Council BB/P013740/1European Research Council 646891Medical Research Council MC_UU_12014/12Medical Research Council MC_UU_12014/9Medical Research Council MR/K000241/1Medical Research Council MR/M011747/1Medical Research Council MR/N008618/1Medical Research Council MR/N02995X/1Medical Research Council MR/R009945/1NIAID NIH HHS R01 AI113186NIAID NIH HHS R01 AI143840NIAID NIH HHS U19 AI135972Wellcome Trust 099220/Z/12/ZWellcome Trust 103258/Z/13/ZWellcome Trust 106207Wellcome Trust 210703/Z/18/Z
Abstract
RNA viruses are a major human health threat. The life cycles of many highly pathogenic RNA viruses like influenza A virus (IAV) and Lassa virus depends on host mRNA, because viral polymerases cleave 5'-m7G-capped host transcripts to prime viral mRNA synthesis ("cap-snatching"). We hypothesized that start codons within cap-snatched host transcripts could generate chimeric human-viral mRNAs with coding potential. We report the existence of this mechanism of gene origination, which we named "start-snatching." Depending on the reading frame, start-snatching allows the translation of host and viral "untranslated regions" (UTRs) to create N-terminally extended viral proteins or entirely novel polypeptides by genetic overprinting. We show that both types of chimeric proteins are made in IAV-infected cells, generate T cell responses, and contribute to virulence. Our results indicate that during infection with IAV, and likely a multitude of other human, animal and plant viruses, a host-dependent mechanism allows the genesis of hybrid genes.
Indexed as
5' Untranslated RegionsAnimalsCattleCell LineCricetinaeDogsHumansInfluenza A virusMiceMutant Chimeric ProteinsOpen Reading FramesRecombinant Fusion ProteinsRNA CapsRNA-Dependent RNA PolymeraseRNA, MessengerRNA, Viral5' Untranslated RegionsMutant Chimeric ProteinsRecombinant Fusion ProteinsRNA CapsRNA-Dependent RNA PolymeraseRNA, MessengerRNA, ViralViral Proteinscap-snatchingchimeric proteinsgene originationinfluenzaRNA hybridsegmented negative-strand RNA virusesuORFsupstream AUGviral evolutionviral RNA
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