SARS-CoV-2 infection of airway organoids reveals conserved use of Tetraspanin-8 by Ancestral, Delta, and Omicron variants
Ancestral SARS coronavirus-2 (SARS-CoV-2) and variants of concern (VOC) caused a global pandemic with a spectrum of disease severity. The mechanistic explaining variations related to airway epithelium are relatively understudied. Here, we biobanked airway organoids (AO) by preserving stem cell funct...
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| Published in | Stem cell reports Vol. 18; no. 3; pp. 636 - 653 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier Inc
14.03.2023
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| Abstract | Ancestral SARS coronavirus-2 (SARS-CoV-2) and variants of concern (VOC) caused a global pandemic with a spectrum of disease severity. The mechanistic explaining variations related to airway epithelium are relatively understudied. Here, we biobanked airway organoids (AO) by preserving stem cell function. We optimized viral infection with H1N1/PR8 and comprehensively characterized epithelial responses to SARS-CoV-2 infection in phenotypically stable AO from 20 different subjects. We discovered Tetraspanin-8 (TSPAN8) as a facilitator of SARS-CoV-2 infection. TSPAN8 facilitates SARS-CoV-2 infection rates independently of ACE2-Spike interaction. In head-to-head comparisons with Ancestral SARS-CoV-2, Delta and Omicron VOC displayed lower overall infection rates of AO but triggered changes in epithelial response. All variants shared highest tropism for ciliated and goblet cells. TSPAN8-blocking antibodies diminish SARS-CoV-2 infection and may spur novel avenues for COVID-19 therapy.
•Airway organoids from different donors display distinct compositions of cell types•Organoid biobank models the spectrum of the epithelium response to pathogens•TSPAN8 is a conserved mediator of infection for SARS-CoV-2 variants
Roose and colleagues generated a biobank of 20 airway organoids for modeling variations of airway epithelium response to SARS-CoV-2. They discovered Tetraspanin-8 (TSPAN8) as a facilitator of SARS-CoV-2 infection independently of ACE2-Spike interaction. Pre-treatment of airway organoids with a blocking TSPAN8 antibody decreased SARS-CoV-2 infection levels in airway organoids, suggesting TSPAN8 as a therapeutic target for COVID-19. |
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| AbstractList | Ancestral SARS coronavirus-2 (SARS-CoV-2) and variants of concern (VOC) caused a global pandemic with a spectrum of disease severity. The mechanistic explaining variations related to airway epithelium are relatively understudied. Here, we biobanked airway organoids (AO) by preserving stem cell function. We optimized viral infection with H1N1/PR8 and comprehensively characterized epithelial responses to SARS-CoV-2 infection in phenotypically stable AO from 20 different subjects. We discovered Tetraspanin-8 (TSPAN8) as a facilitator of SARS-CoV-2 infection. TSPAN8 facilitates SARS-CoV-2 infection rates independently of ACE2-Spike interaction. In head-to-head comparisons with Ancestral SARS-CoV-2, Delta and Omicron VOC displayed lower overall infection rates of AO but triggered changes in epithelial response. All variants shared highest tropism for ciliated and goblet cells. TSPAN8-blocking antibodies diminish SARS-CoV-2 infection and may spur novel avenues for COVID-19 therapy.Ancestral SARS coronavirus-2 (SARS-CoV-2) and variants of concern (VOC) caused a global pandemic with a spectrum of disease severity. The mechanistic explaining variations related to airway epithelium are relatively understudied. Here, we biobanked airway organoids (AO) by preserving stem cell function. We optimized viral infection with H1N1/PR8 and comprehensively characterized epithelial responses to SARS-CoV-2 infection in phenotypically stable AO from 20 different subjects. We discovered Tetraspanin-8 (TSPAN8) as a facilitator of SARS-CoV-2 infection. TSPAN8 facilitates SARS-CoV-2 infection rates independently of ACE2-Spike interaction. In head-to-head comparisons with Ancestral SARS-CoV-2, Delta and Omicron VOC displayed lower overall infection rates of AO but triggered changes in epithelial response. All variants shared highest tropism for ciliated and goblet cells. TSPAN8-blocking antibodies diminish SARS-CoV-2 infection and may spur novel avenues for COVID-19 therapy. Ancestral SARS coronavirus-2 (SARS-CoV-2) and variants of concern (VOC) caused a global pandemic with a spectrum of disease severity. The mechanistic explaining variations related to airway epithelium are relatively understudied. Here, we biobanked airway organoids (AO) by preserving stem cell function. We optimized viral infection with H1N1/PR8 and comprehensively characterized epithelial responses to SARS-CoV-2 infection in phenotypically stable AO from 20 different subjects. We discovered Tetraspanin-8 (TSPAN8) as a facilitator of SARS-CoV-2 infection. TSPAN8 facilitates SARS-CoV-2 infection rates independently of ACE2-Spike interaction. In head-to-head comparisons with Ancestral SARS-CoV-2, Delta and Omicron VOC displayed lower overall infection rates of AO but triggered changes in epithelial response. All variants shared highest tropism for ciliated and goblet cells. TSPAN8-blocking antibodies diminish SARS-CoV-2 infection and may spur novel avenues for COVID-19 therapy. Roose and colleagues generated a biobank of 20 airway organoids for modeling variations of airway epithelium response to SARS-CoV-2. They discovered Tetraspanin-8 (TSPAN8) as a facilitator of SARS-CoV-2 infection independently of ACE2-Spike interaction. Pre-treatment of airway organoids with a blocking TSPAN8 antibody decreased SARS-CoV-2 infection levels in airway organoids, suggesting TSPAN8 as a therapeutic target for COVID-19. Ancestral SARS coronavirus-2 (SARS-CoV-2) and variants of concern (VOC) caused a global pandemic with a spectrum of disease severity. The mechanistic explaining variations related to airway epithelium are relatively understudied. Here, we biobanked airway organoids (AO) by preserving stem cell function. We optimized viral infection with H1N1/PR8 and comprehensively characterized epithelial responses to SARS-CoV-2 infection in phenotypically stable AO from 20 different subjects. We discovered Tetraspanin-8 (TSPAN8) as a facilitator of SARS-CoV-2 infection. TSPAN8 facilitates SARS-CoV-2 infection rates independently of ACE2-Spike interaction. In head-to-head comparisons with Ancestral SARS-CoV-2, Delta and Omicron VOC displayed lower overall infection rates of AO but triggered changes in epithelial response. All variants shared highest tropism for ciliated and goblet cells. TSPAN8-blocking antibodies diminish SARS-CoV-2 infection and may spur novel avenues for COVID-19 therapy. Ancestral SARS coronavirus-2 (SARS-CoV-2) and variants of concern (VOC) caused a global pandemic with a spectrum of disease severity. The mechanistic explaining variations related to airway epithelium are relatively understudied. Here, we biobanked airway organoids (AO) by preserving stem cell function. We optimized viral infection with H1N1/PR8 and comprehensively characterized epithelial responses to SARS-CoV-2 infection in phenotypically stable AO from 20 different subjects. We discovered Tetraspanin-8 (TSPAN8) as a facilitator of SARS-CoV-2 infection. TSPAN8 facilitates SARS-CoV-2 infection rates independently of ACE2-Spike interaction. In head-to-head comparisons with Ancestral SARS-CoV-2, Delta and Omicron VOC displayed lower overall infection rates of AO but triggered changes in epithelial response. All variants shared highest tropism for ciliated and goblet cells. TSPAN8-blocking antibodies diminish SARS-CoV-2 infection and may spur novel avenues for COVID-19 therapy. •Airway organoids from different donors display distinct compositions of cell types•Organoid biobank models the spectrum of the epithelium response to pathogens•TSPAN8 is a conserved mediator of infection for SARS-CoV-2 variants Roose and colleagues generated a biobank of 20 airway organoids for modeling variations of airway epithelium response to SARS-CoV-2. They discovered Tetraspanin-8 (TSPAN8) as a facilitator of SARS-CoV-2 infection independently of ACE2-Spike interaction. Pre-treatment of airway organoids with a blocking TSPAN8 antibody decreased SARS-CoV-2 infection levels in airway organoids, suggesting TSPAN8 as a therapeutic target for COVID-19. |
| Author | Li, Jack Z. Combes, Alexis J. Ott, Melanie Khan, Khajida Lupin-Jimenez, Leonard C. Matthay, Michael Krummel, Matthew Kratz, Johannes R. Little, Samantha von Gottberg, Anne Simoneau, Camille Looney, Mark R. Shen, Alan Prinz, Morgan Maishan, Mazharul Fragiadakis, Gabriela K. Khalid, Mir M. Kumar, Renuka Matsumoto, Shotaro Langelier, Charles R. Bahl, Kriti Andersen, Christopher Lone, Jean-Christophe Mick, Eran Ding, Vivianne W. Roose, Jeroen P. Bonser, Luke R. Sil, Anita Kulhanek, Kayla Nazarenko, Irina Jablons, David M. Magnen, Melia Gbenedio, Oghenekevwe M. Hysenaj, Lisiena Rao, Arjun Arkal Serwas, Nina K. Sigal, Alex Tomlinson, Michael G. Erle, David J. Rodriguez, Lauren Sreekumar, Bharath Taha, Taha Y. |
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givenname: Alan surname: Shen fullname: Shen, Alan organization: UCSF CoLabs, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 12 givenname: Jean-Christophe surname: Lone fullname: Lone, Jean-Christophe organization: School of Life Science, University of Essex, C04 3SQ Colchester, UK – sequence: 13 givenname: Leonard C. surname: Lupin-Jimenez fullname: Lupin-Jimenez, Leonard C. organization: UCSF CoLabs, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 14 givenname: Luke R. surname: Bonser fullname: Bonser, Luke R. organization: Lung Biology Center, Department of Medicine, University of California, San Francisco, San Francisco, CA, USA – sequence: 15 givenname: Nina K. surname: Serwas fullname: Serwas, Nina K. organization: Department of Pathology, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 16 givenname: Eran surname: Mick fullname: Mick, Eran organization: Division of Infectious Diseases, University of California, San Francisco, San Francisco, CA, USA – sequence: 17 givenname: Mir M. surname: Khalid fullname: Khalid, Mir M. organization: Gladstone Institute of Virology, Department of Medicine, University of California, San Francisco, San Francisco, CA, USA – sequence: 18 givenname: Taha Y. surname: Taha fullname: Taha, Taha Y. organization: Gladstone Institute of Virology, Department of Medicine, University of California, San Francisco, San Francisco, CA, USA – sequence: 19 givenname: Renuka surname: Kumar fullname: Kumar, Renuka organization: Gladstone Institute of Virology, Department of Medicine, University of California, San Francisco, San Francisco, CA, USA – sequence: 20 givenname: Jack Z. surname: Li fullname: Li, Jack Z. organization: Department of Surgery, Division of Cardiothoracic Surgery, University of California, San Francisco, San Francisco, CA, USA – sequence: 21 givenname: Vivianne W. surname: Ding fullname: Ding, Vivianne W. organization: Department of Surgery, Division of Cardiothoracic Surgery, University of California, San Francisco, San Francisco, CA, USA – sequence: 22 givenname: Shotaro surname: Matsumoto fullname: Matsumoto, Shotaro organization: Cardiovascular Research Institute, Departments of Medicine and Anesthesia, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 23 givenname: Mazharul surname: Maishan fullname: Maishan, Mazharul organization: Cardiovascular Research Institute, Departments of Medicine and Anesthesia, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 24 givenname: Bharath surname: Sreekumar fullname: Sreekumar, Bharath organization: Gladstone Institute of Virology, Department of Medicine, University of California, San Francisco, San Francisco, CA, USA – sequence: 25 givenname: Camille surname: Simoneau fullname: Simoneau, Camille organization: Gladstone Institute of Virology, Department of Medicine, University of California, San 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University of California, San Francisco, San Francisco, CA, USA – sequence: 32 givenname: Gabriela K. surname: Fragiadakis fullname: Fragiadakis, Gabriela K. organization: UCSF CoLabs, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 33 givenname: David M. surname: Jablons fullname: Jablons, David M. organization: Division of Pulmonary and Critical Care, San Francisco, San Francisco, CA, USA – sequence: 34 givenname: Charles R. surname: Langelier fullname: Langelier, Charles R. organization: Division of Infectious Diseases, University of California, San Francisco, San Francisco, CA, USA – sequence: 35 givenname: Michael surname: Matthay fullname: Matthay, Michael organization: Division of Pulmonary and Critical Care, San Francisco, San Francisco, CA, USA – sequence: 36 givenname: Matthew surname: Krummel fullname: Krummel, Matthew organization: Department of Anatomy, University of California, San Francisco, 513 Parnassus Avenue, San Francisco, CA 94143, 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| Keywords | spectral flow SARS-CoV-2 therapeutics TSPAN8 single cell RNAseq cell composition variants H1N1 virus airway organoids |
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| SubjectTerms | airway organoids cell composition COVID-19 H1N1 Humans Influenza A Virus, H1N1 Subtype Organoids SARS-CoV-2 single cell RNAseq spectral flow Tetraspanins - genetics therapeutics TSPAN8 variants virus |
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| Title | SARS-CoV-2 infection of airway organoids reveals conserved use of Tetraspanin-8 by Ancestral, Delta, and Omicron variants |
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