Nature

, volume 583 , issue 7816 , pages 459-468

A SARS-CoV-2 Protein Interaction Map Reveals Targets for Drug-Repurposing

Iouli E Gordon ^{1, 2, 3, 4}

Gwendolyn M Jang ^{1, 2, 3, 4}

Mehdi Bouhaddou ^{1, 2, 3, 4}

Jiewei Xu ^{1, 2, 3, 4}

Kirsten Obernier ^{1, 2, 3, 4}

Kris M White ^{5, 6}

Matthew J Omeara ⁷

Veronica V Rezelj ⁸

Jeffrey Z Guo ^{1, 2, 3, 4}

Danielle Swaney ^{1, 2, 3, 4}

Tia A Tummino ^{1, 2, 9}

Ruth Hüttenhain ^{1, 2, 3, 4}

Robyn M Kaake ^{1, 2, 3, 4}

Alicia C. Richards ^{1, 2, 3, 4}

Beril Tutuncuoglu ^{1, 2, 3, 4}

Hélène Foussard ^{1, 2, 3, 4}

Jyoti Batra ^{1, 2, 3, 4}

Kelsey Haas ^{1, 2, 3, 4}

Maya Modak ^{1, 2, 3, 4}

Min-Kyu Kim ^{1, 2, 3, 4}

P Haas ^{1, 2, 3, 4}

Ben Polacco ^{1, 2, 3, 4}

Hannes Braberg ^{1, 2, 3, 4}

Jacqueline M Fabius ^{1, 2, 3, 4}

Manon Eckhardt ^{1, 2, 3, 4}

Margaret Soucheray ^{1, 2, 3, 4}

Melanie J Bennett ^{1, 2, 3, 4}

Merve Cakir ^{1, 2, 3, 4}

Michael J Mcgregor ^{1, 2, 3, 4}

QIONGYU LI ^{1, 2, 3, 4}

Bjoern Meyer ⁸

Ferdinand Roesch ⁸

Thomas Vallet ⁸

Alice Mac Kain ⁸

Lisa Miorin ^{5, 6}

E. Moreno ^{5, 6}

Zun Zar Chi Naing ^{1, 2, 3, 4}

Yuan Zhou ^{1, 2, 3, 4}

Shiming Peng ^{1, 2, 9}

Ying Shi ^{1, 2, 4, 10}

Ziyang Zhang ^{1, 2, 4, 10}

Wenqi Shen ^{1, 2, 4, 10}

Ilsa T Kirby ^{1, 2, 4, 10}

James E Melnyk ^{1, 2, 4, 10}

John S. Chorba ^{1, 2, 4, 10}

Kevin Lou ^{1, 2, 4, 10}

Shizhong A Dai ^{1, 2, 4, 10}

Inigo Barrio-Hernandez ¹¹

Danish Memon ¹¹

Claudia I. Hernández-Armenta ¹¹

Jiankun Lyu ^{1, 2, 9}

Christopher J P Mathy ^{1, 2, 12, 13}

Tina Perica ^{1, 2, 12}

Kala Bharath Pilla ^{1, 2, 12}

Sai J. Ganesan ^{1, 2, 12}

Daniel J Saltzberg ^{1, 2, 12}

Ramachandran Rakesh ^{1, 2, 12}

Xi Liu ^{1, 2, 9}

Sara B. Rosenthal ¹⁴

Lorenzo Calviello ^{1, 15}

Srivats Venkataramanan ^{1, 15}

Jose Liboy Lugo ^{1, 15}

Yizhu Lin ^{1, 15}

Xi-Ping Huang ¹⁶

Yongfeng Liu ¹⁶

Stephanie A.M. Wankowicz ^{1, 2, 12, 17}

Markus Bohn ^{1, 2, 9}

Maliheh Safari ^{1, 2, 18}

Fatima S. Ugur ^{1, 2, 4, 9}

Cassandra Koh ⁸

Nastaran Sadat Savar ⁸

Quang Dinh Tran ⁸

Djoshkun Shengjuler ⁸

Sabrina J Fletcher ⁸

Michael C Oneal ¹⁹

Yiming Cai ¹⁹

Jason C J Chang ¹⁹

David J Broadhurst ¹⁹

Saker Klippsten ¹⁹

Phillip P Sharp ⁴

Nicole A Wenzell ^{1, 2, 4}

Duygu Kuzuoglu Ozturk ^{1, 20, 21}

Haoyuan Wang ^{1, 2, 4}

R Trenker ^{1, 2, 22}

JANET E. YOUNG ²³

Devin A Cavero ^{1, 3, 24}

Joseph Hiatt ^{1, 3, 25}

Theodore L. Roth ^{1, 3, 24, 25}

Ujjwal Rathore ^{1, 3, 24}

Advait Subramanian ^{1, 2, 24}

J Noack ^{1, 2, 24}

Mathieu Hubert ²⁶

Robert M. Stroud ^{1, 2, 18}

Alan D Frankel ^{1, 2, 18}

Oren S. Rosenberg ^{1, 2, 18, 27}

Kliment A. Verba ^{1, 2, 9}

David A. Agard ^{1, 2, 18}

Melanie Ott ^{1, 2, 3, 27}

Michael Emerman ²⁸

Natalia Jura ^{1, 2, 4, 22}

M. von Zastrow ^{1, 2, 4, 29}

Eric Verdin ^{1, 27, 30}

Alan Ashworth ^{1, 2, 20}

Olivier Schwartz ²⁶

Christophe d’Enfert ³¹

Shaeri Mukherjee ^{1, 2, 24}

Matthew P. Jacobson ^{1, 2, 9}

Harmit S Malik ²³

Danica G Fujimori ^{1, 2, 4, 9}

Trey Ideker ^{1, 32}

Charles Craik ^{1, 2, 9, 20}

Stephen N Floor ^{1, 15, 20}

James M. Fraser ^{1, 2, 12}

John Gross ^{1, 2, 9}

Andrej Sali ^{1, 2, 9, 12}

Bryan L. Roth ¹⁶

Davide Ruggero ^{1, 2, 4, 20, 21}

Jack Taunton ^{1, 2, 4}

Tanja Kortemme ^{1, 2, 12, 13}

Pedro Beltrao ^{1, 11}

Marco Vignuzzi ⁸

Adolfo García-Sastre ^{5, 6, 33, 34}

Kevan M. Shokat ^{1, 2, 4, 10}

Brian K. Shoichet ^{1, 2, 9}

Nevan J. Krogan ^{1, 2, 3, 4, 5}

Hide authors affiliations Show authors affiliations: 34 affiliations

QBI COVID-19 Research Group (QCRG), San Francisco, USA |

Quantitative Biosciences Institute (QBI), University of California San Francisco, San Francisco, USA |

J. David Gladstone Institutes, San Francisco, USA |

⁴

Department of Cellular and Molecular Pharmacology, University of California San Francisco, San Francisco, USA |

⁵

Department of Microbiology, Icahn School of Medicine At Mount Sinai, New York, USA |

⁶

Global Health and Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, USA |

⁷

Department of Computational Medicine and Bioinformatics, University of Michigan, Ann Arbor, USA |

⁸

Viral Populations and Pathogenesis Unit, CNRS UMR 3569, Institut Pasteur, Paris, France |

⁹

Department of Pharmaceutical Chemistry, University of California San Francisco, San Francisco, USA |

¹⁰

Howard Hughes Medical Institute, University of California San Francisco, San Francisco, USA

University of California, San Francisco

Howard Hughes Medical Institute

¹¹

European Molecular Biology Laboratory (EMBL), European Bioinformatics Institute, Wellcome Genome Campus, Cambridge, UK |

¹²

Department of Bioengineering and Therapeutic Sciences, University of California San Francisco, San Francisco, USA |

¹³

The UC Berkeley-UCSF Graduate Program in Bioengineering, University of California San Francisco, San Francisco, USA

University of California, Berkeley

University of California, San Francisco

¹⁴

Center for Computational Biology and Bioinformatics, Department of Medicine, University of California San Diego, San Diego, USA |

¹⁵

Department of Cell and Tissue Biology, University of California San Francisco, San Francisco, USA |

¹⁶

Department of Pharmacology, University of North Carolina at Chapel Hill School of Medicine, Chapel Hill, USA |

¹⁷

Biophysics Graduate Program, University of California San Francisco, San Francisco, USA |

¹⁸

Department of Biochemistry and Biophysics, University of California San Francisco, San Francisco, USA |

¹⁹

Zoic Labs, Culver City, USA |

²⁰

Helen Diller Family Comprehensive Cancer Center, University of California San Francisco, San Francisco, USA |

²¹

Department of Urology, University of California San Francisco, San Francisco, USA |

²²

Cardiovascular Research Institute, University of California San Francisco, San Francisco, USA |

²³

Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, USA |

²⁴

George William Hooper Foundation, Department of Microbiology and Immunology, University of California San Francisco, San Francisco, USA |

²⁵

Medical Scientist Training Program, University of California San Francisco, San Francisco, USA |

²⁶

Virus and Immunity Unit, Institut Pasteur, Paris, France |

²⁷

Department of Medicine, University of California San Francisco, San Francisco, USA |

²⁸

Division of Human Biology, Fred Hutchinson Cancer Research Center, Seattle, USA |

²⁹

Department of Psychiatry, University of California San Francisco, San Francisco, USA |

³⁰

Buck Institute for Research On Aging, Novato, USA |

³¹

Direction Scientifique, Institut Pasteur, Paris, France |

³²

Division of Genetics, Department of Medicine, University of California San Diego, San Diego, USA |

³³

Department of Medicine, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, USA |

³⁴

The Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, USA |

Publication type: Journal Article

Publication date: 2020-04-30

Springer Nature

Nature

scimago Q1

wos Q1

SJR: 18.288

CiteScore: 78.1

Impact factor: 48.5

ISSN: 00280836, 14764687

DOI: 10.1038/s41586-020-2286-9

Copy DOI

PubMed ID: 32353859

Multidisciplinary

Abstract

A newly described coronavirus named severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which is the causative agent of coronavirus disease 2019 (COVID-19), has infected over 2.3 million people, led to the death of more than 160,000 individuals and caused worldwide social and economic disruption 1 , 2 . There are no antiviral drugs with proven clinical efficacy for the treatment of COVID-19, nor are there any vaccines that prevent infection with SARS-CoV-2, and efforts to develop drugs and vaccines are hampered by the limited knowledge of the molecular details of how SARS-CoV-2 infects cells. Here we cloned, tagged and expressed 26 of the 29 SARS-CoV-2 proteins in human cells and identified the human proteins that physically associated with each of the SARS-CoV-2 proteins using affinity-purification mass spectrometry, identifying 332 high-confidence protein–protein interactions between SARS-CoV-2 and human proteins. Among these, we identify 66 druggable human proteins or host factors targeted by 69 compounds (of which, 29 drugs are approved by the US Food and Drug Administration, 12 are in clinical trials and 28 are preclinical compounds). We screened a subset of these in multiple viral assays and found two sets of pharmacological agents that displayed antiviral activity: inhibitors of mRNA translation and predicted regulators of the sigma-1 and sigma-2 receptors. Further studies of these host-factor-targeting agents, including their combination with drugs that directly target viral enzymes, could lead to a therapeutic regimen to treat COVID-19. A human–SARS-CoV-2 protein interaction map highlights cellular processes that are hijacked by the virus and that can be targeted by existing drugs, including inhibitors of mRNA translation and predicted regulators of the sigma receptors.

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Kazan State Medical University

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Casiraghi Maurizio

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Roviello Giovanni

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Institute of Biostructure and Bioimaging

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Autonomous University of Barcelona

Hospital Universitari Germans Trias i Pujol

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Ruđer Bošković Institute

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Gordon I. E. et al. A SARS-CoV-2 Protein Interaction Map Reveals Targets for Drug-Repurposing // Nature. 2020. Vol. 583. No. 7816. pp. 459-468.

GOST all authors (up to 50) Copy

Gordon I. E. et al. A SARS-CoV-2 Protein Interaction Map Reveals Targets for Drug-Repurposing // Nature. 2020. Vol. 583. No. 7816. pp. 459-468.

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BibTex (up to 50 authors) Copy

@article{2020_Gordon,

author = {Iouli E Gordon and Gwendolyn M Jang and Mehdi Bouhaddou and Jiewei Xu and Kirsten Obernier and Kris M White and Matthew J Omeara and Veronica V Rezelj and Jeffrey Z Guo and Danielle Swaney and Tia A Tummino and Ruth Hüttenhain and Robyn M Kaake and Alicia C. Richards and Beril Tutuncuoglu and Hélène Foussard and Jyoti Batra and Kelsey Haas and Maya Modak and Min-Kyu Kim and P Haas and Ben Polacco and Hannes Braberg and Jacqueline M Fabius and Manon Eckhardt and Margaret Soucheray and Melanie J Bennett and Merve Cakir and Michael J Mcgregor and QIONGYU LI and Bjoern Meyer and Ferdinand Roesch and Thomas Vallet and Alice Mac Kain and Lisa Miorin and E. Moreno and Zun Zar Chi Naing and Yuan Zhou and Shiming Peng and Ying Shi and Ziyang Zhang and Wenqi Shen and Ilsa T Kirby and James E Melnyk and John S. Chorba and Kevin Lou and Shizhong A Dai and Inigo Barrio-Hernandez and Danish Memon and Claudia I. Hernández-Armenta and others},

title = {A SARS-CoV-2 Protein Interaction Map Reveals Targets for Drug-Repurposing},

journal = {Nature},

year = {2020},

volume = {583},

publisher = {Springer Nature},

month = {apr},

url = {https://doi.org/10.1038/s41586-020-2286-9},

number = {7816},

pages = {459--468},

doi = {10.1038/s41586-020-2286-9}

}

MLA

Cite this

MLA Copy

Gordon, Iouli E., et al. “A SARS-CoV-2 Protein Interaction Map Reveals Targets for Drug-Repurposing.” Nature, vol. 583, no. 7816, Apr. 2020, pp. 459-468. https://doi.org/10.1038/s41586-020-2286-9.

Publisher

Springer Nature

Journal

Nature

scimago Q1

wos Q1

SJR

18.288

CiteScore

78.1

Impact factor

48.5

ISSN

00280836 (Print)

14764687 (Electronic)