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

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 phosphoprot...

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Autores principales: Haas, Kelsey M., McGregor, Michael J., Bouhaddou, Mehdi, Polacco, Benjamin J., Kim, Eun-Young, Nguyen, Thong T., Newton, Billy W., Urbanowski, Matthew, Kim, Heejin, Williams, Michael A. P., Rezelj, Veronica V., Hardy, Alexandra, Fossati, Andrea, Stevenson, Erica J., Sukerman, Ellie, Kim, Tiffany, Penugonda, Sudhir, Moreno, Elena, Braberg, Hannes, Zhou, Yuan, Metreveli, Giorgi, Harjai, Bhavya, Tummino, Tia A., Melnyk, James E., Soucheray, Margaret, Batra, Jyoti, Pache, Lars, Martin-Sancho, Laura, Carlson-Stevermer, Jared, Jureka, Alexander S., Basler, Christopher F., Shokat, Kevan M., Shoichet, Brian K., Shriver, Leah P., Johnson, Jeffrey R., Shaw, Megan L., Chanda, Sumit K., Roden, Dan M., Carter, Tonia C., Kottyan, Leah C., Chisholm, Rex L., Pacheco, Jennifer A., Smith, Maureen E., Schrodi, Steven J., Albrecht, Randy A., Vignuzzi, Marco, Zuliani-Alvarez, Lorena, Swaney, Danielle L., Eckhardt, Manon, Wolinsky, Steven M., White, Kris M., Hultquist, Judd F., Kaake, Robyn M., García-Sastre, Adolfo, Krogan, Nevan J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10533562/
https://www.ncbi.nlm.nih.gov/pubmed/37758692
http://dx.doi.org/10.1038/s41467-023-41442-z
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author Haas, Kelsey M.
McGregor, Michael J.
Bouhaddou, Mehdi
Polacco, Benjamin J.
Kim, Eun-Young
Nguyen, Thong T.
Newton, Billy W.
Urbanowski, Matthew
Kim, Heejin
Williams, Michael A. P.
Rezelj, Veronica V.
Hardy, Alexandra
Fossati, Andrea
Stevenson, Erica J.
Sukerman, Ellie
Kim, Tiffany
Penugonda, Sudhir
Moreno, Elena
Braberg, Hannes
Zhou, Yuan
Metreveli, Giorgi
Harjai, Bhavya
Tummino, Tia A.
Melnyk, James E.
Soucheray, Margaret
Batra, Jyoti
Pache, Lars
Martin-Sancho, Laura
Carlson-Stevermer, Jared
Jureka, Alexander S.
Basler, Christopher F.
Shokat, Kevan M.
Shoichet, Brian K.
Shriver, Leah P.
Johnson, Jeffrey R.
Shaw, Megan L.
Chanda, Sumit K.
Roden, Dan M.
Carter, Tonia C.
Kottyan, Leah C.
Chisholm, Rex L.
Pacheco, Jennifer A.
Smith, Maureen E.
Schrodi, Steven J.
Albrecht, Randy A.
Vignuzzi, Marco
Zuliani-Alvarez, Lorena
Swaney, Danielle L.
Eckhardt, Manon
Wolinsky, Steven M.
White, Kris M.
Hultquist, Judd F.
Kaake, Robyn M.
García-Sastre, Adolfo
Krogan, Nevan J.
author_facet Haas, Kelsey M.
McGregor, Michael J.
Bouhaddou, Mehdi
Polacco, Benjamin J.
Kim, Eun-Young
Nguyen, Thong T.
Newton, Billy W.
Urbanowski, Matthew
Kim, Heejin
Williams, Michael A. P.
Rezelj, Veronica V.
Hardy, Alexandra
Fossati, Andrea
Stevenson, Erica J.
Sukerman, Ellie
Kim, Tiffany
Penugonda, Sudhir
Moreno, Elena
Braberg, Hannes
Zhou, Yuan
Metreveli, Giorgi
Harjai, Bhavya
Tummino, Tia A.
Melnyk, James E.
Soucheray, Margaret
Batra, Jyoti
Pache, Lars
Martin-Sancho, Laura
Carlson-Stevermer, Jared
Jureka, Alexander S.
Basler, Christopher F.
Shokat, Kevan M.
Shoichet, Brian K.
Shriver, Leah P.
Johnson, Jeffrey R.
Shaw, Megan L.
Chanda, Sumit K.
Roden, Dan M.
Carter, Tonia C.
Kottyan, Leah C.
Chisholm, Rex L.
Pacheco, Jennifer A.
Smith, Maureen E.
Schrodi, Steven J.
Albrecht, Randy A.
Vignuzzi, Marco
Zuliani-Alvarez, Lorena
Swaney, Danielle L.
Eckhardt, Manon
Wolinsky, Steven M.
White, Kris M.
Hultquist, Judd F.
Kaake, Robyn M.
García-Sastre, Adolfo
Krogan, Nevan J.
author_sort Haas, Kelsey M.
collection PubMed
description 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.
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spelling pubmed-105335622023-09-29 Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets Haas, Kelsey M. McGregor, Michael J. Bouhaddou, Mehdi Polacco, Benjamin J. Kim, Eun-Young Nguyen, Thong T. Newton, Billy W. Urbanowski, Matthew Kim, Heejin Williams, Michael A. P. Rezelj, Veronica V. Hardy, Alexandra Fossati, Andrea Stevenson, Erica J. Sukerman, Ellie Kim, Tiffany Penugonda, Sudhir Moreno, Elena Braberg, Hannes Zhou, Yuan Metreveli, Giorgi Harjai, Bhavya Tummino, Tia A. Melnyk, James E. Soucheray, Margaret Batra, Jyoti Pache, Lars Martin-Sancho, Laura Carlson-Stevermer, Jared Jureka, Alexander S. Basler, Christopher F. Shokat, Kevan M. Shoichet, Brian K. Shriver, Leah P. Johnson, Jeffrey R. Shaw, Megan L. Chanda, Sumit K. Roden, Dan M. Carter, Tonia C. Kottyan, Leah C. Chisholm, Rex L. Pacheco, Jennifer A. Smith, Maureen E. Schrodi, Steven J. Albrecht, Randy A. Vignuzzi, Marco Zuliani-Alvarez, Lorena Swaney, Danielle L. Eckhardt, Manon Wolinsky, Steven M. White, Kris M. Hultquist, Judd F. Kaake, Robyn M. García-Sastre, Adolfo Krogan, Nevan J. Nat Commun Article 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. Nature Publishing Group UK 2023-09-27 /pmc/articles/PMC10533562/ /pubmed/37758692 http://dx.doi.org/10.1038/s41467-023-41442-z Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Haas, Kelsey M.
McGregor, Michael J.
Bouhaddou, Mehdi
Polacco, Benjamin J.
Kim, Eun-Young
Nguyen, Thong T.
Newton, Billy W.
Urbanowski, Matthew
Kim, Heejin
Williams, Michael A. P.
Rezelj, Veronica V.
Hardy, Alexandra
Fossati, Andrea
Stevenson, Erica J.
Sukerman, Ellie
Kim, Tiffany
Penugonda, Sudhir
Moreno, Elena
Braberg, Hannes
Zhou, Yuan
Metreveli, Giorgi
Harjai, Bhavya
Tummino, Tia A.
Melnyk, James E.
Soucheray, Margaret
Batra, Jyoti
Pache, Lars
Martin-Sancho, Laura
Carlson-Stevermer, Jared
Jureka, Alexander S.
Basler, Christopher F.
Shokat, Kevan M.
Shoichet, Brian K.
Shriver, Leah P.
Johnson, Jeffrey R.
Shaw, Megan L.
Chanda, Sumit K.
Roden, Dan M.
Carter, Tonia C.
Kottyan, Leah C.
Chisholm, Rex L.
Pacheco, Jennifer A.
Smith, Maureen E.
Schrodi, Steven J.
Albrecht, Randy A.
Vignuzzi, Marco
Zuliani-Alvarez, Lorena
Swaney, Danielle L.
Eckhardt, Manon
Wolinsky, Steven M.
White, Kris M.
Hultquist, Judd F.
Kaake, Robyn M.
García-Sastre, Adolfo
Krogan, Nevan J.
Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets
title Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets
title_full Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets
title_fullStr Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets
title_full_unstemmed Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets
title_short Proteomic and genetic analyses of influenza A viruses identify pan-viral host targets
title_sort proteomic and genetic analyses of influenza a viruses identify pan-viral host targets
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10533562/
https://www.ncbi.nlm.nih.gov/pubmed/37758692
http://dx.doi.org/10.1038/s41467-023-41442-z
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