Cigarette Smoke Exposure and Inflammatory Signaling Increase the Expression of the SARS-CoV-2 Receptor ACE2 in the Respiratory Tract

The factors mediating fatal SARS-CoV-2 infections are poorly understood. Here, we show that cigarette smoke causes a dose-dependent upregulation of angiotensin converting enzyme 2 (ACE2), the SARS-CoV-2 receptor, in rodent and human lungs. Using single-cell sequencing data, we demonstrate that ACE2...

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Published inDevelopmental cell Vol. 53; no. 5; pp. 514 - 529.e3
Main Authors Smith, Joan C., Sausville, Erin L., Girish, Vishruth, Yuan, Monet Lou, Vasudevan, Anand, John, Kristen M., Sheltzer, Jason M.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 08.06.2020
Subjects
ACE2
Adult
Aged
Alveolar Epithelial Cells - metabolism
Angiotensin-Converting Enzyme 2
Animals
Caco-2 Cells
Cells, Cultured
Coronavirus
Coronavirus Infections - epidemiology
COVID-19
Female
HCT116 Cells
Humans
inflammation
interferon
Interferons - genetics
Interferons - metabolism
lung development
Male
Mice
Middle Aged
Pandemics
Peptidyl-Dipeptidase A - genetics
Peptidyl-Dipeptidase A - metabolism
Pneumonia, Viral - epidemiology
Rats
Respiratory Mucosa - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
RNA-Seq
SARS-CoV-2
Signal Transduction
Single-Cell Analysis
smoking
Tobacco Smoke Pollution - adverse effects
Tobacco Smoking - epidemiology
Tobacco Smoking - genetics
Tobacco Smoking - metabolism
Up-Regulation
COVID-19
ACE2
SARS-CoV-2
Coronavirus
inflammation
smoking
interferon
lung development
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Abstract The factors mediating fatal SARS-CoV-2 infections are poorly understood. Here, we show that cigarette smoke causes a dose-dependent upregulation of angiotensin converting enzyme 2 (ACE2), the SARS-CoV-2 receptor, in rodent and human lungs. Using single-cell sequencing data, we demonstrate that ACE2 is expressed in a subset of secretory cells in the respiratory tract. Chronic smoke exposure triggers the expansion of this cell population and a concomitant increase in ACE2 expression. In contrast, quitting smoking decreases the abundance of these secretory cells and reduces ACE2 levels. Finally, we demonstrate that ACE2 expression is responsive to inflammatory signaling and can be upregulated by viral infections or interferon treatment. Taken together, these results may partially explain why smokers are particularly susceptible to severe SARS-CoV-2 infections. Furthermore, our work identifies ACE2 as an interferon-stimulated gene in lung cells, suggesting that SARS-CoV-2 infections could create positive feedback loops that increase ACE2 levels and facilitate viral dissemination. [Display omitted] •Lung ACE2 levels do not vary by age or sex, but smokers exhibit upregulated ACE2•ACE2 is expressed in several lung cell types, including the secretory lineage•Chronic smoking triggers the expansion of ACE2+ secretory cells•ACE2 is also upregulated by viral infections and interferon exposure Smith et al. report that smokers’ lungs harbor higher levels of the coronavirus receptor ACE2. They further demonstrate that ACE2 is expressed in a subpopulation of secretory cells that expand in response to smoke exposure. Finally, they establish that ACE2 is an interferon-stimulated gene that is upregulated by viral infections.
AbstractList The factors mediating fatal SARS-CoV-2 infections are poorly understood. Here, we show that cigarette smoke causes a dose-dependent upregulation of angiotensin converting enzyme 2 (ACE2), the SARS-CoV-2 receptor, in rodent and human lungs. Using single-cell sequencing data, we demonstrate that ACE2 is expressed in a subset of secretory cells in the respiratory tract. Chronic smoke exposure triggers the expansion of this cell population and a concomitant increase in ACE2 expression. In contrast, quitting smoking decreases the abundance of these secretory cells and reduces ACE2 levels. Finally, we demonstrate that ACE2 expression is responsive to inflammatory signaling and can be upregulated by viral infections or interferon treatment. Taken together, these results may partially explain why smokers are particularly susceptible to severe SARS-CoV-2 infections. Furthermore, our work identifies ACE2 as an interferon-stimulated gene in lung cells, suggesting that SARS-CoV-2 infections could create positive feedback loops that increase ACE2 levels and facilitate viral dissemination.
The factors mediating fatal SARS-CoV-2 infections are poorly understood. Here, we show that cigarette smoke causes a dose-dependent upregulation of angiotensin converting enzyme 2 (ACE2), the SARS-CoV-2 receptor, in rodent and human lungs. Using single-cell sequencing data, we demonstrate that ACE2 is expressed in a subset of secretory cells in the respiratory tract. Chronic smoke exposure triggers the expansion of this cell population and a concomitant increase in ACE2 expression. In contrast, quitting smoking decreases the abundance of these secretory cells and reduces ACE2 levels. Finally, we demonstrate that ACE2 expression is responsive to inflammatory signaling and can be upregulated by viral infections or interferon treatment. Taken together, these results may partially explain why smokers are particularly susceptible to severe SARS-CoV-2 infections. Furthermore, our work identifies ACE2 as an interferon-stimulated gene in lung cells, suggesting that SARS-CoV-2 infections could create positive feedback loops that increase ACE2 levels and facilitate viral dissemination. • Lung ACE2 levels do not vary by age or sex, but smokers exhibit upregulated ACE2 • ACE2 is expressed in several lung cell types, including the secretory lineage • Chronic smoking triggers the expansion of ACE2 + secretory cells • ACE2 is also upregulated by viral infections and interferon exposure Smith et al. report that smokers’ lungs harbor higher levels of the coronavirus receptor ACE2. They further demonstrate that ACE2 is expressed in a subpopulation of secretory cells that expand in response to smoke exposure. Finally, they establish that ACE2 is an interferon-stimulated gene that is upregulated by viral infections.
The factors mediating fatal SARS-CoV-2 infections are poorly understood. Here, we show that cigarette smoke causes a dose-dependent upregulation of angiotensin converting enzyme 2 (ACE2), the SARS-CoV-2 receptor, in rodent and human lungs. Using single-cell sequencing data, we demonstrate that ACE2 is expressed in a subset of secretory cells in the respiratory tract. Chronic smoke exposure triggers the expansion of this cell population and a concomitant increase in ACE2 expression. In contrast, quitting smoking decreases the abundance of these secretory cells and reduces ACE2 levels. Finally, we demonstrate that ACE2 expression is responsive to inflammatory signaling and can be upregulated by viral infections or interferon treatment. Taken together, these results may partially explain why smokers are particularly susceptible to severe SARS-CoV-2 infections. Furthermore, our work identifies ACE2 as an interferon-stimulated gene in lung cells, suggesting that SARS-CoV-2 infections could create positive feedback loops that increase ACE2 levels and facilitate viral dissemination.The factors mediating fatal SARS-CoV-2 infections are poorly understood. Here, we show that cigarette smoke causes a dose-dependent upregulation of angiotensin converting enzyme 2 (ACE2), the SARS-CoV-2 receptor, in rodent and human lungs. Using single-cell sequencing data, we demonstrate that ACE2 is expressed in a subset of secretory cells in the respiratory tract. Chronic smoke exposure triggers the expansion of this cell population and a concomitant increase in ACE2 expression. In contrast, quitting smoking decreases the abundance of these secretory cells and reduces ACE2 levels. Finally, we demonstrate that ACE2 expression is responsive to inflammatory signaling and can be upregulated by viral infections or interferon treatment. Taken together, these results may partially explain why smokers are particularly susceptible to severe SARS-CoV-2 infections. Furthermore, our work identifies ACE2 as an interferon-stimulated gene in lung cells, suggesting that SARS-CoV-2 infections could create positive feedback loops that increase ACE2 levels and facilitate viral dissemination.
The factors mediating fatal SARS-CoV-2 infections are poorly understood. Here, we show that cigarette smoke causes a dose-dependent upregulation of angiotensin converting enzyme 2 (ACE2), the SARS-CoV-2 receptor, in rodent and human lungs. Using single-cell sequencing data, we demonstrate that ACE2 is expressed in a subset of secretory cells in the respiratory tract. Chronic smoke exposure triggers the expansion of this cell population and a concomitant increase in ACE2 expression. In contrast, quitting smoking decreases the abundance of these secretory cells and reduces ACE2 levels. Finally, we demonstrate that ACE2 expression is responsive to inflammatory signaling and can be upregulated by viral infections or interferon treatment. Taken together, these results may partially explain why smokers are particularly susceptible to severe SARS-CoV-2 infections. Furthermore, our work identifies ACE2 as an interferon-stimulated gene in lung cells, suggesting that SARS-CoV-2 infections could create positive feedback loops that increase ACE2 levels and facilitate viral dissemination. [Display omitted] •Lung ACE2 levels do not vary by age or sex, but smokers exhibit upregulated ACE2•ACE2 is expressed in several lung cell types, including the secretory lineage•Chronic smoking triggers the expansion of ACE2+ secretory cells•ACE2 is also upregulated by viral infections and interferon exposure Smith et al. report that smokers’ lungs harbor higher levels of the coronavirus receptor ACE2. They further demonstrate that ACE2 is expressed in a subpopulation of secretory cells that expand in response to smoke exposure. Finally, they establish that ACE2 is an interferon-stimulated gene that is upregulated by viral infections.
Author Vasudevan, Anand
Girish, Vishruth
John, Kristen M.
Sausville, Erin L.
Smith, Joan C.
Yuan, Monet Lou
Sheltzer, Jason M.
Author_xml – sequence: 1
  givenname: Joan C.
  surname: Smith
  fullname: Smith, Joan C.
  organization: Google, Inc., New York City, NY 10011, USA
– sequence: 2
  givenname: Erin L.
  surname: Sausville
  fullname: Sausville, Erin L.
  organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
– sequence: 3
  givenname: Vishruth
  surname: Girish
  fullname: Girish, Vishruth
  organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
– sequence: 4
  givenname: Monet Lou
  surname: Yuan
  fullname: Yuan, Monet Lou
  organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
– sequence: 5
  givenname: Anand
  surname: Vasudevan
  fullname: Vasudevan, Anand
  organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
– sequence: 6
  givenname: Kristen M.
  surname: John
  fullname: John, Kristen M.
  organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
– sequence: 7
  givenname: Jason M.
  surname: Sheltzer
  fullname: Sheltzer, Jason M.
  email: sheltzer@cshl.edu
  organization: Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32425701$$D View this record in MEDLINE/PubMed
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Snippet The factors mediating fatal SARS-CoV-2 infections are poorly understood. Here, we show that cigarette smoke causes a dose-dependent upregulation of angiotensin...
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SubjectTerms ACE2
Adult
Aged
Alveolar Epithelial Cells - metabolism
Angiotensin-Converting Enzyme 2
Animals
Caco-2 Cells
Cells, Cultured
Coronavirus
Coronavirus Infections - epidemiology
COVID-19
Female
HCT116 Cells
Humans
inflammation
interferon
Interferons - genetics
Interferons - metabolism
lung development
Male
Mice
Middle Aged
Pandemics
Peptidyl-Dipeptidase A - genetics
Peptidyl-Dipeptidase A - metabolism
Pneumonia, Viral - epidemiology
Rats
Respiratory Mucosa - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
RNA-Seq
SARS-CoV-2
Signal Transduction
Single-Cell Analysis
smoking
Tobacco Smoke Pollution - adverse effects
Tobacco Smoking - epidemiology
Tobacco Smoking - genetics
Tobacco Smoking - metabolism
Up-Regulation
Title Cigarette Smoke Exposure and Inflammatory Signaling Increase the Expression of the SARS-CoV-2 Receptor ACE2 in the Respiratory Tract
URI https://dx.doi.org/10.1016/j.devcel.2020.05.012
https://www.ncbi.nlm.nih.gov/pubmed/32425701
https://www.proquest.com/docview/2404641772
https://pubmed.ncbi.nlm.nih.gov/PMC7229915
Volume 53
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