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Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets

Author

Listed:
  • Kelsey M. Haas

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Michael J. McGregor

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Mehdi Bouhaddou

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Benjamin J. Polacco

    (University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Eun-Young Kim

    (Northwestern University Feinberg School of Medicine)

  • Thong T. Nguyen

    (J. David Gladstone Institutes)

  • Billy W. Newton

    (University of California San Francisco
    University of California San Francisco)

  • Matthew Urbanowski

    (Icahn School of Medicine at Mount Sinai)

  • Heejin Kim

    (Northwestern University Feinberg School of Medicine)

  • Michael A. P. Williams

    (Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG)
    Icahn School of Medicine at Mount Sinai
    Icahn School of Medicine at Mount Sinai)

  • Veronica V. Rezelj

    (Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG)
    Viral Populations and Pathogenesis Unit)

  • Alexandra Hardy

    (Viral Populations and Pathogenesis Unit)

  • Andrea Fossati

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Erica J. Stevenson

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Ellie Sukerman

    (Oregon Health & Science University)

  • Tiffany Kim

    (Northwestern University Feinberg School of Medicine)

  • Sudhir Penugonda

    (Northwestern University Feinberg School of Medicine)

  • Elena Moreno

    (Icahn School of Medicine at Mount Sinai
    Icahn School of Medicine at Mount Sinai
    Hospital Universitario Ramón y Cajal and IRYCIS
    Instituto de Salud Carlos III)

  • Hannes Braberg

    (University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Yuan Zhou

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Giorgi Metreveli

    (Icahn School of Medicine at Mount Sinai)

  • Bhavya Harjai

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Tia A. Tummino

    (University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG)
    University of California San Francisco
    University of California San Francisco)

  • James E. Melnyk

    (University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Margaret Soucheray

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Jyoti Batra

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Lars Pache

    (Sanford Burnham Prebys Medical Discovery Institute)

  • Laura Martin-Sancho

    (The Scripps Research Institute
    Imperial College London)

  • Jared Carlson-Stevermer

    (Synthego Corporation
    Serotiny Inc.)

  • Alexander S. Jureka

    (Centers for Disease Control & Prevention
    Federal Civilian Division)

  • Christopher F. Basler

    (Icahn School of Medicine at Mount Sinai)

  • Kevan M. Shokat

    (University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG)
    Howard Hughes Medical Institute)

  • Brian K. Shoichet

    (University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG)
    University of California San Francisco)

  • Leah P. Shriver

    (Washington University in St. Louis
    Center for Metabolomics and Isotope Tracing, Washington University in St. Louis)

  • Jeffrey R. Johnson

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Icahn School of Medicine at Mount Sinai)

  • Megan L. Shaw

    (Icahn School of Medicine at Mount Sinai
    University of the Western Cape)

  • Sumit K. Chanda

    (The Scripps Research Institute)

  • Dan M. Roden

    (Vanderbilt University Medical Center
    Vanderbilt University Medical Center
    Vanderbilt University Medical Center)

  • Tonia C. Carter

    (Marshfield Clinic Research Institute)

  • Leah C. Kottyan

    (Cincinnati Children’s Hospital Medical Center
    Cincinnati Children’s Hospital Medical Center
    University of Cincinnati College of Medicine)

  • Rex L. Chisholm

    (Northwestern University)

  • Jennifer A. Pacheco

    (Northwestern University)

  • Maureen E. Smith

    (Northwestern University)

  • Steven J. Schrodi

    (University of Wisconsin Madison)

  • Randy A. Albrecht

    (Icahn School of Medicine at Mount Sinai
    Icahn School of Medicine at Mount Sinai)

  • Marco Vignuzzi

    (Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG)
    Viral Populations and Pathogenesis Unit)

  • Lorena Zuliani-Alvarez

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Danielle L. Swaney

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Manon Eckhardt

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Steven M. Wolinsky

    (Northwestern University Feinberg School of Medicine)

  • Kris M. White

    (Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG)
    Icahn School of Medicine at Mount Sinai
    Icahn School of Medicine at Mount Sinai)

  • Judd F. Hultquist

    (Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG)
    Northwestern University Feinberg School of Medicine
    Northwestern University Havey Institute for Global Health)

  • Robyn M. Kaake

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

  • Adolfo García-Sastre

    (Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG)
    Icahn School of Medicine at Mount Sinai
    Icahn School of Medicine at Mount Sinai
    Icahn School of Medicine at Mount Sinai)

  • Nevan J. Krogan

    (J. David Gladstone Institutes
    University of California San Francisco
    University of California San Francisco
    Quantitative Biosciences Institute (QBI) Coronavirus Research Group (QCRG))

Abstract

Influenza A Virus (IAV) is a recurring respiratory virus with limited availability of antiviral therapies. Understanding host proteins essential for IAV infection can identify targets for alternative host-directed therapies (HDTs). Using affinity purification-mass spectrometry and global phosphoproteomic and protein abundance analyses using three IAV strains (pH1N1, H3N2, H5N1) in three human cell types (A549, NHBE, THP-1), we map 332 IAV-human protein-protein interactions and identify 13 IAV-modulated kinases. Whole exome sequencing of patients who experienced severe influenza reveals several genes, including scaffold protein AHNAK, with predicted loss-of-function variants that are also identified in our proteomic analyses. Of our identified host factors, 54 significantly alter IAV infection upon siRNA knockdown, and two factors, AHNAK and coatomer subunit COPB1, are also essential for productive infection by SARS-CoV-2. Finally, 16 compounds targeting our identified host factors suppress IAV replication, with two targeting CDK2 and FLT3 showing pan-antiviral activity across influenza and coronavirus families. This study provides a comprehensive network model of IAV infection in human cells, identifying functional host targets for pan-viral HDT.

Suggested Citation

  • Kelsey M. Haas & Michael J. McGregor & Mehdi Bouhaddou & Benjamin J. Polacco & Eun-Young Kim & Thong T. Nguyen & Billy W. Newton & Matthew Urbanowski & Heejin Kim & Michael A. P. Williams & Veronica V, 2023. "Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets," Nature Communications, Nature, vol. 14(1), pages 1-27, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41442-z
    DOI: 10.1038/s41467-023-41442-z
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    as
    1. Lucy G. Thorne & Mehdi Bouhaddou & Ann-Kathrin Reuschl & Lorena Zuliani-Alvarez & Ben Polacco & Adrian Pelin & Jyoti Batra & Matthew V. X. Whelan & Myra Hosmillo & Andrea Fossati & Roberta Ragazzini &, 2022. "Evolution of enhanced innate immune evasion by SARS-CoV-2," Nature, Nature, vol. 602(7897), pages 487-495, February.
    2. David E. Gordon & Gwendolyn M. Jang & Mehdi Bouhaddou & Jiewei Xu & Kirsten Obernier & Kris M. White & Matthew J. O’Meara & Veronica V. Rezelj & Jeffrey Z. Guo & Danielle L. Swaney & Tia A. Tummino & , 2020. "A SARS-CoV-2 protein interaction map reveals targets for drug repurposing," Nature, Nature, vol. 583(7816), pages 459-468, July.
    3. Petra Mlcochova & Steven A. Kemp & Mahesh Shanker Dhar & Guido Papa & Bo Meng & Isabella A. T. M. Ferreira & Rawlings Datir & Dami A. Collier & Anna Albecka & Sujeet Singh & Rajesh Pandey & Jonathan B, 2021. "SARS-CoV-2 B.1.617.2 Delta variant replication and immune evasion," Nature, Nature, vol. 599(7883), pages 114-119, November.
    4. Houriiyah Tegally & Eduan Wilkinson & Marta Giovanetti & Arash Iranzadeh & Vagner Fonseca & Jennifer Giandhari & Deelan Doolabh & Sureshnee Pillay & Emmanuel James San & Nokukhanya Msomi & Koleka Mlis, 2021. "Detection of a SARS-CoV-2 variant of concern in South Africa," Nature, Nature, vol. 592(7854), pages 438-443, April.
    5. Joseph Hiatt & Judd F. Hultquist & Michael J. McGregor & Mehdi Bouhaddou & Ryan T. Leenay & Lacy M. Simons & Janet M. Young & Paige Haas & Theodore L. Roth & Victoria Tobin & Jason A. Wojcechowskyj & , 2022. "A functional map of HIV-host interactions in primary human T cells," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    6. Denisa Bojkova & Kevin Klann & Benjamin Koch & Marek Widera & David Krause & Sandra Ciesek & Jindrich Cinatl & Christian Münch, 2020. "Proteomics of SARS-CoV-2-infected host cells reveals therapy targets," Nature, Nature, vol. 583(7816), pages 469-472, July.
    7. Nicky Phillips, 2021. "The coronavirus is here to stay — here’s what that means," Nature, Nature, vol. 590(7846), pages 382-384, February.
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