Lung Cancer Models Reveal Severe Acute Respiratory Syndrome Coronavirus 2–Induced Epithelial-to-Mesenchymal Transition Contributes to Coronavirus Disease 2019 Pathophysiology

Coronavirus disease 2019 is an infectious disease caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which enters host cells through the cell surface proteins ACE2 and TMPRSS2. Using a variety of normal and malignant models and tissues from the aerodigestive and respiratory trac...

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Published inJournal of thoracic oncology Vol. 16; no. 11; pp. 1821 - 1839
Main Authors Stewart, C. Allison, Gay, Carl M., Ramkumar, Kavya, Cargill, Kasey R., Cardnell, Robert J., Nilsson, Monique B., Heeke, Simon, Park, Elizabeth M., Kundu, Samrat T., Diao, Lixia, Wang, Qi, Shen, Li, Xi, Yuanxin, Zhang, Bingnan, Della Corte, Carminia Maria, Fan, Youhong, Kundu, Kiran, Gao, Boning, Avila, Kimberley, Pickering, Curtis R., Johnson, Faye M., Zhang, Jianjun, Kadara, Humam, Minna, John D., Gibbons, Don L., Wang, Jing, Heymach, John V., Byers, Lauren Averett
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 01.11.2021
International Association for the Study of Lung Cancer. Published by Elsevier Inc
Subjects
ACE2
AXL
Bronchi
COVID-19
EMT
Humans
Lung
Lung Neoplasms
NSCLC
Original
Peptidyl-Dipeptidase A
SARS-CoV-2
ZEB1
ACE2
SARS-CoV-2
ZEB1
NSCLC
AXL
EMT
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Abstract Coronavirus disease 2019 is an infectious disease caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which enters host cells through the cell surface proteins ACE2 and TMPRSS2. Using a variety of normal and malignant models and tissues from the aerodigestive and respiratory tracts, we investigated the expression and regulation of ACE2 and TMPRSS2. We find that ACE2 expression is restricted to a select population of epithelial cells. Notably, infection with SARS-CoV-2 in cancer cell lines, bronchial organoids, and patient nasal epithelium induces metabolic and transcriptional changes consistent with epithelial-to-mesenchymal transition (EMT), including up-regulation of ZEB1 and AXL, resulting in an increased EMT score. In addition, a transcriptional loss of genes associated with tight junction function occurs with SARS-CoV-2 infection. The SARS-CoV-2 receptor, ACE2, is repressed by EMT through the transforming growth factor-β, ZEB1 overexpression, and onset of EGFR tyrosine kinase inhibitor resistance. This suggests a novel model of SARS-CoV-2 pathogenesis in which infected cells shift toward an increasingly mesenchymal state, associated with a loss of tight junction components with acute respiratory distress syndrome-protective effects. AXL inhibition and ZEB1 reduction, as with bemcentinib, offer a potential strategy to reverse this effect. These observations highlight the use of aerodigestive and, especially, lung cancer model systems in exploring the pathogenesis of SARS-CoV-2 and other respiratory viruses and offer important insights into the potential mechanisms underlying the morbidity and mortality of coronavirus disease 2019 in healthy patients and patients with cancer alike.
AbstractList Coronavirus disease 2019 is an infectious disease caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which enters host cells through the cell surface proteins ACE2 and TMPRSS2. Using a variety of normal and malignant models and tissues from the aerodigestive and respiratory tracts, we investigated the expression and regulation of ACE2 and TMPRSS2. We find that ACE2 expression is restricted to a select population of epithelial cells. Notably, infection with SARS-CoV-2 in cancer cell lines, bronchial organoids, and patient nasal epithelium induces metabolic and transcriptional changes consistent with epithelial-to-mesenchymal transition (EMT), including up-regulation of ZEB1 and AXL, resulting in an increased EMT score. In addition, a transcriptional loss of genes associated with tight junction function occurs with SARS-CoV-2 infection. The SARS-CoV-2 receptor, ACE2, is repressed by EMT through the transforming growth factor-β, ZEB1 overexpression, and onset of EGFR tyrosine kinase inhibitor resistance. This suggests a novel model of SARS-CoV-2 pathogenesis in which infected cells shift toward an increasingly mesenchymal state, associated with a loss of tight junction components with acute respiratory distress syndrome-protective effects. AXL inhibition and ZEB1 reduction, as with bemcentinib, offer a potential strategy to reverse this effect. These observations highlight the use of aerodigestive and, especially, lung cancer model systems in exploring the pathogenesis of SARS-CoV-2 and other respiratory viruses and offer important insights into the potential mechanisms underlying the morbidity and mortality of coronavirus disease 2019 in healthy patients and patients with cancer alike.
Coronavirus disease 2019 is an infectious disease caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which enters host cells through the cell surface proteins ACE2 and TMPRSS2.INTRODUCTIONCoronavirus disease 2019 is an infectious disease caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which enters host cells through the cell surface proteins ACE2 and TMPRSS2.Using a variety of normal and malignant models and tissues from the aerodigestive and respiratory tracts, we investigated the expression and regulation of ACE2 and TMPRSS2.METHODSUsing a variety of normal and malignant models and tissues from the aerodigestive and respiratory tracts, we investigated the expression and regulation of ACE2 and TMPRSS2.We find that ACE2 expression is restricted to a select population of epithelial cells. Notably, infection with SARS-CoV-2 in cancer cell lines, bronchial organoids, and patient nasal epithelium induces metabolic and transcriptional changes consistent with epithelial-to-mesenchymal transition (EMT), including up-regulation of ZEB1 and AXL, resulting in an increased EMT score. In addition, a transcriptional loss of genes associated with tight junction function occurs with SARS-CoV-2 infection. The SARS-CoV-2 receptor, ACE2, is repressed by EMT through the transforming growth factor-β, ZEB1 overexpression, and onset of EGFR tyrosine kinase inhibitor resistance. This suggests a novel model of SARS-CoV-2 pathogenesis in which infected cells shift toward an increasingly mesenchymal state, associated with a loss of tight junction components with acute respiratory distress syndrome-protective effects. AXL inhibition and ZEB1 reduction, as with bemcentinib, offer a potential strategy to reverse this effect.RESULTSWe find that ACE2 expression is restricted to a select population of epithelial cells. Notably, infection with SARS-CoV-2 in cancer cell lines, bronchial organoids, and patient nasal epithelium induces metabolic and transcriptional changes consistent with epithelial-to-mesenchymal transition (EMT), including up-regulation of ZEB1 and AXL, resulting in an increased EMT score. In addition, a transcriptional loss of genes associated with tight junction function occurs with SARS-CoV-2 infection. The SARS-CoV-2 receptor, ACE2, is repressed by EMT through the transforming growth factor-β, ZEB1 overexpression, and onset of EGFR tyrosine kinase inhibitor resistance. This suggests a novel model of SARS-CoV-2 pathogenesis in which infected cells shift toward an increasingly mesenchymal state, associated with a loss of tight junction components with acute respiratory distress syndrome-protective effects. AXL inhibition and ZEB1 reduction, as with bemcentinib, offer a potential strategy to reverse this effect.These observations highlight the use of aerodigestive and, especially, lung cancer model systems in exploring the pathogenesis of SARS-CoV-2 and other respiratory viruses and offer important insights into the potential mechanisms underlying the morbidity and mortality of coronavirus disease 2019 in healthy patients and patients with cancer alike.CONCLUSIONSThese observations highlight the use of aerodigestive and, especially, lung cancer model systems in exploring the pathogenesis of SARS-CoV-2 and other respiratory viruses and offer important insights into the potential mechanisms underlying the morbidity and mortality of coronavirus disease 2019 in healthy patients and patients with cancer alike.
Author Avila, Kimberley
Ramkumar, Kavya
Cargill, Kasey R.
Johnson, Faye M.
Xi, Yuanxin
Diao, Lixia
Gao, Boning
Kundu, Kiran
Gay, Carl M.
Gibbons, Don L.
Kundu, Samrat T.
Della Corte, Carminia Maria
Stewart, C. Allison
Cardnell, Robert J.
Park, Elizabeth M.
Shen, Li
Minna, John D.
Heeke, Simon
Wang, Jing
Byers, Lauren Averett
Nilsson, Monique B.
Fan, Youhong
Heymach, John V.
Kadara, Humam
Pickering, Curtis R.
Zhang, Jianjun
Wang, Qi
Zhang, Bingnan
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  organization: Department of Thoracic/Head & Neck Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, Texas
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ContentType Journal Article
Copyright 2021 International Association for the Study of Lung Cancer
Copyright © 2021 International Association for the Study of Lung Cancer. Published by Elsevier Inc. All rights reserved.
2021 International Association for the Study of Lung Cancer. Published by Elsevier Inc. 2021 International Association for the Study of Lung Cancer
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– notice: 2021 International Association for the Study of Lung Cancer. Published by Elsevier Inc. 2021 International Association for the Study of Lung Cancer
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Keywords ACE2
SARS-CoV-2
ZEB1
NSCLC
AXL
EMT
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32577652 - bioRxiv. 2021 Jan 28:2020.05.28.122291. doi: 10.1101/2020.05.28.122291
34716001 - J Thorac Oncol. 2021 Nov;16(11):1785-1787. doi: 10.1016/j.jtho.2021.08.014
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Snippet Coronavirus disease 2019 is an infectious disease caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which enters host cells through the...
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SubjectTerms ACE2
AXL
Bronchi
COVID-19
EMT
Humans
Lung
Lung Neoplasms
NSCLC
Original
Peptidyl-Dipeptidase A
SARS-CoV-2
ZEB1
Title Lung Cancer Models Reveal Severe Acute Respiratory Syndrome Coronavirus 2–Induced Epithelial-to-Mesenchymal Transition Contributes to Coronavirus Disease 2019 Pathophysiology
URI https://dx.doi.org/10.1016/j.jtho.2021.07.002
https://www.ncbi.nlm.nih.gov/pubmed/34274504
https://www.proquest.com/docview/2553242438
https://pubmed.ncbi.nlm.nih.gov/PMC8282443
Volume 16
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