The Transcriptome Landscape of the In Vitro Human Airway Epithelium Response to SARS-CoV-2
Airway-liquid interface cultures of primary epithelial cells and of induced pluripotent stem-cell-derived airway epithelial cells (ALI and iALI, respectively) are physiologically relevant models for respiratory virus infection studies because they can mimic the in vivo human bronchial epithelium. He...
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| Veröffentlicht in: | International journal of molecular sciences 2023-07, Vol.24 (15), p.12017 |
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| creator | Assou, Said Ahmed, Engi Morichon, Lisa Nasri, Amel Foisset, Florent Bourdais, Carine Gros, Nathalie Tieo, Sonia Petit, Aurelie Vachier, Isabelle Muriaux, Delphine Bourdin, Arnaud De Vos, John |
| description | Airway-liquid interface cultures of primary epithelial cells and of induced pluripotent stem-cell-derived airway epithelial cells (ALI and iALI, respectively) are physiologically relevant models for respiratory virus infection studies because they can mimic the in vivo human bronchial epithelium. Here, we investigated gene expression profiles in human airway cultures (ALI and iALI models), infected or not with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), using our own and publicly available bulk and single-cell transcriptome datasets. SARS-CoV-2 infection significantly increased the expression of interferon-stimulated genes (
,
,
,
,
,
,
,
and
) and inflammatory genes (
,
,
,
and
) by day 4 post-infection, indicating activation of the interferon and immune responses to the virus. Extracellular matrix genes (
,
and
) were also altered in infected cells. Single-cell RNA sequencing data revealed that SARS-CoV-2 infection damaged the respiratory epithelium, particularly mature ciliated cells. The expression of genes encoding intercellular communication and adhesion proteins was also deregulated, suggesting a mechanism to promote shedding of infected epithelial cells. These data demonstrate that ALI/iALI models help to explain the airway epithelium response to SARS-CoV-2 infection and are a key tool for developing COVID-19 treatments. |
| doi_str_mv | 10.3390/ijms241512017 |
| format | Article |
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,
,
,
,
,
,
,
and
) and inflammatory genes (
,
,
,
and
) by day 4 post-infection, indicating activation of the interferon and immune responses to the virus. Extracellular matrix genes (
,
and
) were also altered in infected cells. Single-cell RNA sequencing data revealed that SARS-CoV-2 infection damaged the respiratory epithelium, particularly mature ciliated cells. The expression of genes encoding intercellular communication and adhesion proteins was also deregulated, suggesting a mechanism to promote shedding of infected epithelial cells. These data demonstrate that ALI/iALI models help to explain the airway epithelium response to SARS-CoV-2 infection and are a key tool for developing COVID-19 treatments.</description><identifier>ISSN: 1422-0067</identifier><identifier>ISSN: 1661-6596</identifier><identifier>EISSN: 1422-0067</identifier><identifier>DOI: 10.3390/ijms241512017</identifier><identifier>PMID: 37569398</identifier><language>eng</language><publisher>Switzerland: MDPI AG</publisher><subject>Biochemistry, Molecular Biology ; Biological response modifiers ; Biopsy ; Cells ; Coronaviruses ; COVID-19 ; Development and progression ; Disease transmission ; Emerging diseases ; Epithelium ; Gene expression ; Genes ; Genomics ; Health aspects ; Human health and pathology ; Infections ; Infectious diseases ; Interferon ; Jones, S.A ; Life Sciences ; Medical research ; Medicine, Experimental ; MicroRNAs ; Pulmonology and respiratory tract ; Respiratory diseases ; RNA ; RNA sequencing ; Severe acute respiratory syndrome ; Severe acute respiratory syndrome coronavirus 2 ; Stem cells ; Viral infections ; Virus diseases ; Viruses</subject><ispartof>International journal of molecular sciences, 2023-07, Vol.24 (15), p.12017</ispartof><rights>COPYRIGHT 2023 MDPI AG</rights><rights>2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2023 by the authors. 2023</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c517t-c9d065e35ad9d4418a4bbecdd1c37f3f1d5e38c033c1436b5cf784b75dddf06d3</citedby><cites>FETCH-LOGICAL-c517t-c9d065e35ad9d4418a4bbecdd1c37f3f1d5e38c033c1436b5cf784b75dddf06d3</cites><orcidid>0000-0003-2146-1837 ; 0000-0001-6448-7995 ; 0000-0001-9498-8985 ; 0009-0007-4639-2459 ; 0000-0002-9069-9868 ; 0009-0004-3375-2409 ; 0009-0001-4577-5155 ; 0000-0003-2730-5165 ; 0000-0003-1880-4130</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10418806/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10418806/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,27915,27916,53782,53784</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37569398$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-04180636$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Assou, Said</creatorcontrib><creatorcontrib>Ahmed, Engi</creatorcontrib><creatorcontrib>Morichon, Lisa</creatorcontrib><creatorcontrib>Nasri, Amel</creatorcontrib><creatorcontrib>Foisset, Florent</creatorcontrib><creatorcontrib>Bourdais, Carine</creatorcontrib><creatorcontrib>Gros, Nathalie</creatorcontrib><creatorcontrib>Tieo, Sonia</creatorcontrib><creatorcontrib>Petit, Aurelie</creatorcontrib><creatorcontrib>Vachier, Isabelle</creatorcontrib><creatorcontrib>Muriaux, Delphine</creatorcontrib><creatorcontrib>Bourdin, Arnaud</creatorcontrib><creatorcontrib>De Vos, John</creatorcontrib><title>The Transcriptome Landscape of the In Vitro Human Airway Epithelium Response to SARS-CoV-2</title><title>International journal of molecular sciences</title><addtitle>Int J Mol Sci</addtitle><description>Airway-liquid interface cultures of primary epithelial cells and of induced pluripotent stem-cell-derived airway epithelial cells (ALI and iALI, respectively) are physiologically relevant models for respiratory virus infection studies because they can mimic the in vivo human bronchial epithelium. Here, we investigated gene expression profiles in human airway cultures (ALI and iALI models), infected or not with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), using our own and publicly available bulk and single-cell transcriptome datasets. SARS-CoV-2 infection significantly increased the expression of interferon-stimulated genes (
,
,
,
,
,
,
,
and
) and inflammatory genes (
,
,
,
and
) by day 4 post-infection, indicating activation of the interferon and immune responses to the virus. Extracellular matrix genes (
,
and
) were also altered in infected cells. Single-cell RNA sequencing data revealed that SARS-CoV-2 infection damaged the respiratory epithelium, particularly mature ciliated cells. The expression of genes encoding intercellular communication and adhesion proteins was also deregulated, suggesting a mechanism to promote shedding of infected epithelial cells. These data demonstrate that ALI/iALI models help to explain the airway epithelium response to SARS-CoV-2 infection and are a key tool for developing COVID-19 treatments.</description><subject>Biochemistry, Molecular Biology</subject><subject>Biological response modifiers</subject><subject>Biopsy</subject><subject>Cells</subject><subject>Coronaviruses</subject><subject>COVID-19</subject><subject>Development and progression</subject><subject>Disease transmission</subject><subject>Emerging diseases</subject><subject>Epithelium</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genomics</subject><subject>Health aspects</subject><subject>Human health and pathology</subject><subject>Infections</subject><subject>Infectious diseases</subject><subject>Interferon</subject><subject>Jones, S.A</subject><subject>Life Sciences</subject><subject>Medical research</subject><subject>Medicine, Experimental</subject><subject>MicroRNAs</subject><subject>Pulmonology and respiratory tract</subject><subject>Respiratory diseases</subject><subject>RNA</subject><subject>RNA sequencing</subject><subject>Severe acute respiratory syndrome</subject><subject>Severe acute respiratory syndrome coronavirus 2</subject><subject>Stem cells</subject><subject>Viral infections</subject><subject>Virus 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Said</creator><creator>Ahmed, Engi</creator><creator>Morichon, Lisa</creator><creator>Nasri, Amel</creator><creator>Foisset, Florent</creator><creator>Bourdais, Carine</creator><creator>Gros, Nathalie</creator><creator>Tieo, Sonia</creator><creator>Petit, Aurelie</creator><creator>Vachier, Isabelle</creator><creator>Muriaux, Delphine</creator><creator>Bourdin, Arnaud</creator><creator>De Vos, John</creator><general>MDPI 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Transcriptome Landscape of the In Vitro Human Airway Epithelium Response to SARS-CoV-2</title><author>Assou, Said ; Ahmed, Engi ; Morichon, Lisa ; Nasri, Amel ; Foisset, Florent ; Bourdais, Carine ; Gros, Nathalie ; Tieo, Sonia ; Petit, Aurelie ; Vachier, Isabelle ; Muriaux, Delphine ; Bourdin, Arnaud ; De Vos, John</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c517t-c9d065e35ad9d4418a4bbecdd1c37f3f1d5e38c033c1436b5cf784b75dddf06d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Biochemistry, Molecular Biology</topic><topic>Biological response modifiers</topic><topic>Biopsy</topic><topic>Cells</topic><topic>Coronaviruses</topic><topic>COVID-19</topic><topic>Development and progression</topic><topic>Disease transmission</topic><topic>Emerging diseases</topic><topic>Epithelium</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genomics</topic><topic>Health aspects</topic><topic>Human health and pathology</topic><topic>Infections</topic><topic>Infectious diseases</topic><topic>Interferon</topic><topic>Jones, S.A</topic><topic>Life Sciences</topic><topic>Medical research</topic><topic>Medicine, Experimental</topic><topic>MicroRNAs</topic><topic>Pulmonology and respiratory tract</topic><topic>Respiratory diseases</topic><topic>RNA</topic><topic>RNA sequencing</topic><topic>Severe acute respiratory syndrome</topic><topic>Severe acute respiratory syndrome coronavirus 2</topic><topic>Stem cells</topic><topic>Viral infections</topic><topic>Virus diseases</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Assou, Said</creatorcontrib><creatorcontrib>Ahmed, Engi</creatorcontrib><creatorcontrib>Morichon, Lisa</creatorcontrib><creatorcontrib>Nasri, Amel</creatorcontrib><creatorcontrib>Foisset, Florent</creatorcontrib><creatorcontrib>Bourdais, Carine</creatorcontrib><creatorcontrib>Gros, Nathalie</creatorcontrib><creatorcontrib>Tieo, Sonia</creatorcontrib><creatorcontrib>Petit, Aurelie</creatorcontrib><creatorcontrib>Vachier, Isabelle</creatorcontrib><creatorcontrib>Muriaux, Delphine</creatorcontrib><creatorcontrib>Bourdin, Arnaud</creatorcontrib><creatorcontrib>De Vos, John</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central 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sciences</jtitle><addtitle>Int J Mol Sci</addtitle><date>2023-07-27</date><risdate>2023</risdate><volume>24</volume><issue>15</issue><spage>12017</spage><pages>12017-</pages><issn>1422-0067</issn><issn>1661-6596</issn><eissn>1422-0067</eissn><abstract>Airway-liquid interface cultures of primary epithelial cells and of induced pluripotent stem-cell-derived airway epithelial cells (ALI and iALI, respectively) are physiologically relevant models for respiratory virus infection studies because they can mimic the in vivo human bronchial epithelium. Here, we investigated gene expression profiles in human airway cultures (ALI and iALI models), infected or not with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), using our own and publicly available bulk and single-cell transcriptome datasets. SARS-CoV-2 infection significantly increased the expression of interferon-stimulated genes (
,
,
,
,
,
,
,
and
) and inflammatory genes (
,
,
,
and
) by day 4 post-infection, indicating activation of the interferon and immune responses to the virus. Extracellular matrix genes (
,
and
) were also altered in infected cells. Single-cell RNA sequencing data revealed that SARS-CoV-2 infection damaged the respiratory epithelium, particularly mature ciliated cells. The expression of genes encoding intercellular communication and adhesion proteins was also deregulated, suggesting a mechanism to promote shedding of infected epithelial cells. These data demonstrate that ALI/iALI models help to explain the airway epithelium response to SARS-CoV-2 infection and are a key tool for developing COVID-19 treatments.</abstract><cop>Switzerland</cop><pub>MDPI AG</pub><pmid>37569398</pmid><doi>10.3390/ijms241512017</doi><orcidid>https://orcid.org/0000-0003-2146-1837</orcidid><orcidid>https://orcid.org/0000-0001-6448-7995</orcidid><orcidid>https://orcid.org/0000-0001-9498-8985</orcidid><orcidid>https://orcid.org/0009-0007-4639-2459</orcidid><orcidid>https://orcid.org/0000-0002-9069-9868</orcidid><orcidid>https://orcid.org/0009-0004-3375-2409</orcidid><orcidid>https://orcid.org/0009-0001-4577-5155</orcidid><orcidid>https://orcid.org/0000-0003-2730-5165</orcidid><orcidid>https://orcid.org/0000-0003-1880-4130</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | International journal of molecular sciences, 2023-07, Vol.24 (15), p.12017 |
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| source | Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; MDPI - Multidisciplinary Digital Publishing Institute; PubMed Central |
| subjects | Biochemistry, Molecular Biology Biological response modifiers Biopsy Cells Coronaviruses COVID-19 Development and progression Disease transmission Emerging diseases Epithelium Gene expression Genes Genomics Health aspects Human health and pathology Infections Infectious diseases Interferon Jones, S.A Life Sciences Medical research Medicine, Experimental MicroRNAs Pulmonology and respiratory tract Respiratory diseases RNA RNA sequencing Severe acute respiratory syndrome Severe acute respiratory syndrome coronavirus 2 Stem cells Viral infections Virus diseases Viruses |
| title | The Transcriptome Landscape of the In Vitro Human Airway Epithelium Response to SARS-CoV-2 |
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