ArticleCell host & microbe2026
Coronavirus protein interaction mapping in bat and human cells reveals network rewiring governing immune evasion and zoonotic potential.
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64 authors.
Jyoti BatraJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Magdalena RutkowskaDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Yuan ZhouJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Chengjin YeTexas Biomedical Research Institute, San Antonio, TX 78227, USA.
Rithika AdavikolanuJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Janet M YoungDivision of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA.
Durga AnandJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Sooraj VermaJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Haripriya ParthasarathyJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Martin GordonJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Shivali MalpotraJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Anastasija CupicDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Graduate School of Biomedical Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Thomas KehrerDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Melanie Dos SantosInteractomics, RNA and Immunity Laboratory, Institut Pasteur, Université Paris Cité, Paris 75015, France.
Ronald BenjaminJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Jack M MoenJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Declan M WintersDepartment of Microbiology, Immunology, and Molecular Genetics (MIMG), University of California, Los Angeles, Los Angeles, CA 90024, USA; Institute for Quantitative and Computational Biosciences (QCBio), University of California, Los Angeles, Los Angeles, CA 90024, USA.
Vincent CavalInstitut Pasteur, Université Paris Cité, CNRS UMR 3569, Virus sensing and signaling Unit, Paris 75015, France.
Ajda RojcJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Ignacio MenaDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Global Health Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; The Scripps Research Institute, Immunology and Microbiology Department, La Jolla, CA 92037, USA.
Sadaf AslamDepartment of Microbiology, 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 Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Memorial Sloan Kettering Cancer Center, New York, NY 10065, USA.
Isabela Conde ViñasDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Global Health Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Zain KhalilDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Keith FarrugiaDepartment of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Fernando Villalón-LetelierDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Atoshi BanerjeeJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Dafna Tussia-CohenShmunis School of Biomedicine and Cancer Research, George S Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 6997801, Israel.
Amy DialloQuantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA.
Sourobh MajiQuantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA.
Monita MuralidharanJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Helene FoussardJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Irene P ChenJ. David Gladstone Institutes, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Medicine, University of California, San Francisco, San Francisco, CA 94158, USA.
Rotem FuchsShmunis School of Biomedicine and Cancer Research, George S Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 6997801, Israel.
C J San FelipeQuantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA.
Lorena Zuliani-AlvarezJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Promisree ChoudhuryJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Kirsten ObernierJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Ségolène GraciasInstitut Pasteur, Université Paris Cité, CNRS UMR 3569, Virus sensing and signaling Unit, Paris 75015, France.
Rahul K SuryawanshiJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Laboratory of Neurological Infections and Immunity, Division of Intramural Research, National Institute of Allergy and Infectious Diseases, Rocky Mountain Laboratories, Hamilton, MT 59840, USA.
Boris BonaventureDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Carlos IbáñezEstación Biológica de Doñana (CSIC), Avda. Américo Vespucio 26, 41092 Seville, Spain.
Jeffrey R JohnsonDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Global Health Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Javier JusteEstación Biológica de Doñana (CSIC), Avda. Américo Vespucio 26, 41092 Seville, Spain; CIBER Epidemiology and Public Health, CIBERESP, 28029 Madrid, Spain.
Lars PacheNCI Designated Cancer Center, Sanford Burnham Prebys Medical Discovery Institute, La Jolla, CA 92037, USA.
Robert M StroudQuantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA.
Kliment A VerbaQuantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA.
James S FraserQuantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA.
Harm van BakelDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Icahn Genomics Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Artificial Intelligence and Human Health, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA.
Taha Y TahaJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Melanie OttJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Medicine, University of California, San Francisco, San Francisco, CA 94158, USA; Biohub, San Francisco, CA 94158, USA.
Tzachi HagaiShmunis School of Biomedicine and Cancer Research, George S Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv 6997801, Israel.
Nolwenn JouvenetInstitut Pasteur, Université Paris Cité, CNRS UMR 3569, Virus sensing and signaling Unit, Paris 75015, France.
Caroline DemeretInteractomics, RNA and Immunity Laboratory, Institut Pasteur, Université Paris Cité, Paris 75015, France.
Benjamin J PolaccoJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Danielle L SwaneyJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Ignacia EcheverriaQuantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Mehdi BouhaddouDepartment of Microbiology, Immunology, and Molecular Genetics (MIMG), University of California, Los Angeles, Los Angeles, CA 90024, USA; Institute for Quantitative and Computational Biosciences (QCBio), University of California, Los Angeles, Los Angeles, CA 90024, USA.
Manon EckhardtJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA.
Harmit S MalikDivision of Basic Sciences, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA; Howard Hughes Medical Institute, Fred Hutchinson Cancer Center, Seattle, WA 98109, USA.
Luis Martinez-SobridoTexas Biomedical Research Institute, San Antonio, TX 78227, USA.
Lisa MiorinDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Global Health Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA. Electronic address: lisa.miorin@mssm.edu.
Adolfo García-SastreDepartment of Microbiology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Global Health Emerging Pathogens Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Medicine, Division of Infectious Diseases, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; The Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; The Icahn Genomics Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA; Department of Pathology, Molecular and Cell-Based Medicine, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA. Electronic address: adolfo.garcia-sastre@mssm.edu.
Nevan J KroganJ. David Gladstone Institutes, San Francisco, CA 94158, USA; Quantitative Biosciences Institute (QBI), University of California, San Francisco, San Francisco, CA 94158, USA; QBI Coronavirus Research Group (QCRG), University of California, San Francisco, San Francisco, CA 94158, USA; Department of Bioengineering and Therapeutic Sciences, University of California, San Francisco, San Francisco, CA 94158, USA. Electronic address: nevan.krogan@ucsf.edu.
Funding
X-RAY CRYSTALLOGRAPHYP30CA008748 · NCI · SLOAN-KETTERING INSTITUTE FOR CANCER RES · PI SELWYN M VICKERS · 1985 to 2026
$347.4MSARS-CoV adaptations through a Systems Biology Lens (SYBIL)U19AI135972 · NIAID · ICAHN SCHOOL OF MEDICINE AT MOUNT SINAI · PI Adolfo Garcia-Sastre · 2018 to 2026
$27.2MRESEARCH PROJECT 2U19AI135990 · NIAID · UNIVERSITY OF CALIFORNIA, SAN FRANCISCO · PI Melanie Maria Ott · 2018 to 2026
$21.4MNCI NIH HHS P30 CA008748NIAID NIH HHS U19 AI135972NIAID NIH HHS U19 AI135990
Abstract
Coronaviruses, including severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), can cause severe disease in humans, whereas reservoir hosts such as horseshoe bats remain asymptomatic. To investigate how host-specific protein-protein interactions (PPIs) influence infection, we generated comparative PPI maps for SARS-CoV-2 and its bat progenitor RaTG13, using affinity purification mass spectrometry (AP-MS) in human and greater horseshoe bat cells. We identify both conserved and virus- and host-specific interactions that regulate infection dynamics. Notably, SARS-CoV-2 requires a nonsynonymous mutation in the nucleocapsid to replicate in bat cells expressing human ACE2 and TMPRSS2. Strikingly, a single amino acid difference in Orf9b between viruses acts as a molecular switch that reprograms mitochondrial targeting: in human cells, enhanced translocase of outer mitochondrial membrane 70 (Tom70) binding promotes immune evasion, whereas in bat cells, strengthened interaction with the bat-enriched restriction factor mitochondrial amidoxime reducing component 2 (MTARC2) limits infection. These findings establish a general principle by which minimal sequence variation can reshape virus-host interactions and contribute to immune antagonism, host adaptation, and species barriers.
Indexed as
COVID-19Immune EvasionSARS-CoV-2Viral ProteinsAngiotensin-Converting Enzyme 2AnimalsCell LineChiropteraHost-Pathogen InteractionsHumansMitochondrial Membrane Transport ProteinsMitochondrial Precursor Protein Import Complex ProteinsProtein Interaction MappingProtein Interaction MapsVirus ReplicationZoonosesAngiotensin-Converting Enzyme 2Mitochondrial Membrane Transport ProteinsMitochondrial Precursor Protein Import Complex ProteinsTOMM70 protein, humanViral Proteinsbatscoronaviruseshost-pathogen interactionMTARC2proteomicsRaTG13SARS-CoV-2Tom70viral reservoirsvirus-host tropism
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