ACE2-lentiviral transduction enables mouse SARS-CoV-2 infection and mapping of receptor interactions
SARS-CoV-2 uses the human ACE2 (hACE2) receptor for cell attachment and entry, with mouse ACE2 (mACE2) unable to support infection. Herein we describe an ACE2-lentivirus system and illustrate its utility for in vitro and in vivo SARS-CoV-2 infection models. Transduction of non-permissive cell lines...
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| Veröffentlicht in: | PLoS pathogens 2021-07, Vol.17 (7), p.e1009723 |
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| creator | Rawle, Daniel J Le, Thuy T Dumenil, Troy Yan, Kexin Tang, Bing Nguyen, Wilson Watterson, Daniel Modhiran, Naphak Hobson-Peters, Jody Bishop, Cameron Suhrbier, Andreas |
| description | SARS-CoV-2 uses the human ACE2 (hACE2) receptor for cell attachment and entry, with mouse ACE2 (mACE2) unable to support infection. Herein we describe an ACE2-lentivirus system and illustrate its utility for
in vitro
and
in vivo
SARS-CoV-2 infection models. Transduction of non-permissive cell lines with hACE2 imparted replication competence, and transduction with mACE2 containing N30D, N31K, F83Y and H353K substitutions, to match hACE2, rescued SARS-CoV-2 replication. Intrapulmonary hACE2-lentivirus transduction of C57BL/6J mice permitted significant virus replication in lung epithelium. RNA-Seq and histological analyses illustrated that this model involved an acute inflammatory disease followed by resolution and tissue repair, with a transcriptomic profile similar to that seen in COVID-19 patients. hACE2-lentivirus transduction of IFNAR
-/-
and IL-28RA
-/-
mouse lungs was used to illustrate that loss of type I or III interferon responses have no significant effect on virus replication. However, their importance in driving inflammatory responses was illustrated by RNA-Seq analyses. We also demonstrate the utility of the hACE2-lentivirus transduction system for vaccine evaluation in C57BL/6J mice. The ACE2-lentivirus system thus has broad application in SARS-CoV-2 research, providing a tool for both mutagenesis studies and mouse model development. |
| doi_str_mv | 10.1371/journal.ppat.1009723 |
| format | Article |
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in vitro
and
in vivo
SARS-CoV-2 infection models. Transduction of non-permissive cell lines with hACE2 imparted replication competence, and transduction with mACE2 containing N30D, N31K, F83Y and H353K substitutions, to match hACE2, rescued SARS-CoV-2 replication. Intrapulmonary hACE2-lentivirus transduction of C57BL/6J mice permitted significant virus replication in lung epithelium. RNA-Seq and histological analyses illustrated that this model involved an acute inflammatory disease followed by resolution and tissue repair, with a transcriptomic profile similar to that seen in COVID-19 patients. hACE2-lentivirus transduction of IFNAR
-/-
and IL-28RA
-/-
mouse lungs was used to illustrate that loss of type I or III interferon responses have no significant effect on virus replication. However, their importance in driving inflammatory responses was illustrated by RNA-Seq analyses. We also demonstrate the utility of the hACE2-lentivirus transduction system for vaccine evaluation in C57BL/6J mice. The ACE2-lentivirus system thus has broad application in SARS-CoV-2 research, providing a tool for both mutagenesis studies and mouse model development.</description><identifier>ISSN: 1553-7374</identifier><identifier>ISSN: 1553-7366</identifier><identifier>EISSN: 1553-7374</identifier><identifier>DOI: 10.1371/journal.ppat.1009723</identifier><identifier>PMID: 34214142</identifier><language>eng</language><publisher>San Francisco: Public Library of Science</publisher><subject>ACE2 ; Amino acids ; Angiotensin-converting enzyme 2 ; Animal models ; Biology and life sciences ; Cell adhesion ; Cell culture ; Cell lines ; Cell receptors ; Coronaviruses ; COVID-19 ; COVID-19 vaccines ; Cystic fibrosis ; Epithelium ; Flow cytometry ; Gene expression ; Health aspects ; Host-virus relationships ; Infections ; Inflammatory diseases ; Interferon ; Kinases ; Lungs ; Medical research ; Medicine and health sciences ; Mutagenesis ; Pandemics ; Receptors ; Replication ; Research and Analysis Methods ; Severe acute respiratory syndrome ; Severe acute respiratory syndrome coronavirus 2 ; Transcriptomics ; Transduction ; Vaccines ; Viral diseases ; Viruses</subject><ispartof>PLoS pathogens, 2021-07, Vol.17 (7), p.e1009723</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Rawle et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Rawle et al 2021 Rawle et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c755t-593b7708ce1ce709f614979d71476d335d5f8585a61b6f5148b2f549047ea67b3</citedby><cites>FETCH-LOGICAL-c755t-593b7708ce1ce709f614979d71476d335d5f8585a61b6f5148b2f549047ea67b3</cites><orcidid>0000-0003-3205-4970 ; 0000-0002-5710-9942 ; 0000-0001-7248-0101 ; 0000-0002-5789-4928 ; 0000-0001-8986-9025 ; 0000-0001-5957-2853 ; 0000-0001-9134-0104</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/PMC8282004/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8282004/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids></links><search><contributor>Lee, Benhur</contributor><creatorcontrib>Rawle, Daniel J</creatorcontrib><creatorcontrib>Le, Thuy T</creatorcontrib><creatorcontrib>Dumenil, Troy</creatorcontrib><creatorcontrib>Yan, Kexin</creatorcontrib><creatorcontrib>Tang, Bing</creatorcontrib><creatorcontrib>Nguyen, Wilson</creatorcontrib><creatorcontrib>Watterson, Daniel</creatorcontrib><creatorcontrib>Modhiran, Naphak</creatorcontrib><creatorcontrib>Hobson-Peters, Jody</creatorcontrib><creatorcontrib>Bishop, Cameron</creatorcontrib><creatorcontrib>Suhrbier, Andreas</creatorcontrib><title>ACE2-lentiviral transduction enables mouse SARS-CoV-2 infection and mapping of receptor interactions</title><title>PLoS pathogens</title><description>SARS-CoV-2 uses the human ACE2 (hACE2) receptor for cell attachment and entry, with mouse ACE2 (mACE2) unable to support infection. Herein we describe an ACE2-lentivirus system and illustrate its utility for
in vitro
and
in vivo
SARS-CoV-2 infection models. Transduction of non-permissive cell lines with hACE2 imparted replication competence, and transduction with mACE2 containing N30D, N31K, F83Y and H353K substitutions, to match hACE2, rescued SARS-CoV-2 replication. Intrapulmonary hACE2-lentivirus transduction of C57BL/6J mice permitted significant virus replication in lung epithelium. RNA-Seq and histological analyses illustrated that this model involved an acute inflammatory disease followed by resolution and tissue repair, with a transcriptomic profile similar to that seen in COVID-19 patients. hACE2-lentivirus transduction of IFNAR
-/-
and IL-28RA
-/-
mouse lungs was used to illustrate that loss of type I or III interferon responses have no significant effect on virus replication. However, their importance in driving inflammatory responses was illustrated by RNA-Seq analyses. We also demonstrate the utility of the hACE2-lentivirus transduction system for vaccine evaluation in C57BL/6J mice. The ACE2-lentivirus system thus has broad application in SARS-CoV-2 research, providing a tool for both mutagenesis studies and mouse model development.</description><subject>ACE2</subject><subject>Amino acids</subject><subject>Angiotensin-converting enzyme 2</subject><subject>Animal models</subject><subject>Biology and life sciences</subject><subject>Cell adhesion</subject><subject>Cell culture</subject><subject>Cell lines</subject><subject>Cell receptors</subject><subject>Coronaviruses</subject><subject>COVID-19</subject><subject>COVID-19 vaccines</subject><subject>Cystic fibrosis</subject><subject>Epithelium</subject><subject>Flow cytometry</subject><subject>Gene expression</subject><subject>Health aspects</subject><subject>Host-virus relationships</subject><subject>Infections</subject><subject>Inflammatory diseases</subject><subject>Interferon</subject><subject>Kinases</subject><subject>Lungs</subject><subject>Medical research</subject><subject>Medicine and health sciences</subject><subject>Mutagenesis</subject><subject>Pandemics</subject><subject>Receptors</subject><subject>Replication</subject><subject>Research and Analysis Methods</subject><subject>Severe acute respiratory syndrome</subject><subject>Severe acute respiratory syndrome coronavirus 2</subject><subject>Transcriptomics</subject><subject>Transduction</subject><subject>Vaccines</subject><subject>Viral 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transduction enables mouse SARS-CoV-2 infection and mapping of receptor interactions</title><author>Rawle, Daniel J ; Le, Thuy T ; Dumenil, Troy ; Yan, Kexin ; Tang, Bing ; Nguyen, Wilson ; Watterson, Daniel ; Modhiran, Naphak ; Hobson-Peters, Jody ; Bishop, Cameron ; Suhrbier, Andreas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c755t-593b7708ce1ce709f614979d71476d335d5f8585a61b6f5148b2f549047ea67b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>ACE2</topic><topic>Amino acids</topic><topic>Angiotensin-converting enzyme 2</topic><topic>Animal models</topic><topic>Biology and life sciences</topic><topic>Cell adhesion</topic><topic>Cell culture</topic><topic>Cell lines</topic><topic>Cell receptors</topic><topic>Coronaviruses</topic><topic>COVID-19</topic><topic>COVID-19 vaccines</topic><topic>Cystic fibrosis</topic><topic>Epithelium</topic><topic>Flow cytometry</topic><topic>Gene expression</topic><topic>Health aspects</topic><topic>Host-virus relationships</topic><topic>Infections</topic><topic>Inflammatory diseases</topic><topic>Interferon</topic><topic>Kinases</topic><topic>Lungs</topic><topic>Medical research</topic><topic>Medicine and health sciences</topic><topic>Mutagenesis</topic><topic>Pandemics</topic><topic>Receptors</topic><topic>Replication</topic><topic>Research and Analysis Methods</topic><topic>Severe acute respiratory syndrome</topic><topic>Severe acute respiratory syndrome coronavirus 2</topic><topic>Transcriptomics</topic><topic>Transduction</topic><topic>Vaccines</topic><topic>Viral diseases</topic><topic>Viruses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Rawle, Daniel J</creatorcontrib><creatorcontrib>Le, Thuy T</creatorcontrib><creatorcontrib>Dumenil, Troy</creatorcontrib><creatorcontrib>Yan, Kexin</creatorcontrib><creatorcontrib>Tang, 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Naphak</au><au>Hobson-Peters, Jody</au><au>Bishop, Cameron</au><au>Suhrbier, Andreas</au><au>Lee, Benhur</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>ACE2-lentiviral transduction enables mouse SARS-CoV-2 infection and mapping of receptor interactions</atitle><jtitle>PLoS pathogens</jtitle><date>2021-07-02</date><risdate>2021</risdate><volume>17</volume><issue>7</issue><spage>e1009723</spage><pages>e1009723-</pages><issn>1553-7374</issn><issn>1553-7366</issn><eissn>1553-7374</eissn><abstract>SARS-CoV-2 uses the human ACE2 (hACE2) receptor for cell attachment and entry, with mouse ACE2 (mACE2) unable to support infection. Herein we describe an ACE2-lentivirus system and illustrate its utility for
in vitro
and
in vivo
SARS-CoV-2 infection models. Transduction of non-permissive cell lines with hACE2 imparted replication competence, and transduction with mACE2 containing N30D, N31K, F83Y and H353K substitutions, to match hACE2, rescued SARS-CoV-2 replication. Intrapulmonary hACE2-lentivirus transduction of C57BL/6J mice permitted significant virus replication in lung epithelium. RNA-Seq and histological analyses illustrated that this model involved an acute inflammatory disease followed by resolution and tissue repair, with a transcriptomic profile similar to that seen in COVID-19 patients. hACE2-lentivirus transduction of IFNAR
-/-
and IL-28RA
-/-
mouse lungs was used to illustrate that loss of type I or III interferon responses have no significant effect on virus replication. However, their importance in driving inflammatory responses was illustrated by RNA-Seq analyses. We also demonstrate the utility of the hACE2-lentivirus transduction system for vaccine evaluation in C57BL/6J mice. The ACE2-lentivirus system thus has broad application in SARS-CoV-2 research, providing a tool for both mutagenesis studies and mouse model development.</abstract><cop>San Francisco</cop><pub>Public Library of Science</pub><pmid>34214142</pmid><doi>10.1371/journal.ppat.1009723</doi><orcidid>https://orcid.org/0000-0003-3205-4970</orcidid><orcidid>https://orcid.org/0000-0002-5710-9942</orcidid><orcidid>https://orcid.org/0000-0001-7248-0101</orcidid><orcidid>https://orcid.org/0000-0002-5789-4928</orcidid><orcidid>https://orcid.org/0000-0001-8986-9025</orcidid><orcidid>https://orcid.org/0000-0001-5957-2853</orcidid><orcidid>https://orcid.org/0000-0001-9134-0104</orcidid><oa>free_for_read</oa></addata></record> |
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| source | DOAJ Directory of Open Access Journals; PubMed Central Open Access; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central |
| subjects | ACE2 Amino acids Angiotensin-converting enzyme 2 Animal models Biology and life sciences Cell adhesion Cell culture Cell lines Cell receptors Coronaviruses COVID-19 COVID-19 vaccines Cystic fibrosis Epithelium Flow cytometry Gene expression Health aspects Host-virus relationships Infections Inflammatory diseases Interferon Kinases Lungs Medical research Medicine and health sciences Mutagenesis Pandemics Receptors Replication Research and Analysis Methods Severe acute respiratory syndrome Severe acute respiratory syndrome coronavirus 2 Transcriptomics Transduction Vaccines Viral diseases Viruses |
| title | ACE2-lentiviral transduction enables mouse SARS-CoV-2 infection and mapping of receptor interactions |
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