A Small-Scale shRNA Screen in Primary Mouse Macrophages Identifies a Role for the Rab GTPase Rab1b in Controlling Salmonella Typhi Growth
Typhi is a human-restricted bacterial pathogen that causes typhoid fever, a life-threatening systemic infection. A fundamental aspect of . Typhi pathogenesis is its ability to survive in human macrophages but not in macrophages from other animals (i.e. mice). Despite the importance of macrophages in...
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Published in | Frontiers in cellular and infection microbiology Vol. 11; p. 660689 |
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Main Authors | , , , , |
Format | Journal Article |
Language | English |
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Abstract | Typhi is a human-restricted bacterial pathogen that causes typhoid fever, a life-threatening systemic infection. A fundamental aspect of
. Typhi pathogenesis is its ability to survive in human macrophages but not in macrophages from other animals (i.e. mice). Despite the importance of macrophages in establishing systemic
. Typhi infection, the mechanisms that macrophages use to control the growth of
. Typhi and the role of these mechanisms in the bacterium's adaptation to the human host are mostly unknown. To facilitate unbiased identification of genes involved in controlling the growth of
. Typhi in macrophages, we report optimized experimental conditions required to perform loss-of function pooled shRNA screens in primary mouse bone-marrow derived macrophages. Following infection with a fluorescent-labeled
. Typhi, infected cells are sorted based on the intensity of fluorescence (i.e. number of intracellular fluorescent bacteria). shRNAs enriched in the fluorescent population are identified by next-generation sequencing. A proof-of-concept screen targeting the mouse Rab GTPases confirmed Rab32 as important to restrict
. Typhi in mouse macrophages. Interestingly and rather unexpectedly, this screen also revealed that Rab1b controls
. Typhi growth in mouse macrophages. This constitutes the first report of a Rab GTPase other than Rab32 involved in
. Typhi host-restriction. The methodology described here should allow genome-wide screening to identify mechanisms controlling the growth of
. Typhi and other intracellular pathogens in primary immune cells. |
---|---|
AbstractList | Salmonella
Typhi is a human-restricted bacterial pathogen that causes typhoid fever, a life-threatening systemic infection. A fundamental aspect of
S
. Typhi pathogenesis is its ability to survive in human macrophages but not in macrophages from other animals (i.e. mice). Despite the importance of macrophages in establishing systemic
S
. Typhi infection, the mechanisms that macrophages use to control the growth of
S
. Typhi and the role of these mechanisms in the bacterium’s adaptation to the human host are mostly unknown. To facilitate unbiased identification of genes involved in controlling the growth of
S
. Typhi in macrophages, we report optimized experimental conditions required to perform loss-of function pooled shRNA screens in primary mouse bone-marrow derived macrophages. Following infection with a fluorescent-labeled
S
. Typhi, infected cells are sorted based on the intensity of fluorescence (i.e. number of intracellular fluorescent bacteria). shRNAs enriched in the fluorescent population are identified by next-generation sequencing. A proof-of-concept screen targeting the mouse Rab GTPases confirmed Rab32 as important to restrict
S
. Typhi in mouse macrophages. Interestingly and rather unexpectedly, this screen also revealed that Rab1b controls
S
. Typhi growth in mouse macrophages. This constitutes the first report of a Rab GTPase other than Rab32 involved in
S
. Typhi host-restriction. The methodology described here should allow genome-wide screening to identify mechanisms controlling the growth of
S
. Typhi and other intracellular pathogens in primary immune cells. Typhi is a human-restricted bacterial pathogen that causes typhoid fever, a life-threatening systemic infection. A fundamental aspect of . Typhi pathogenesis is its ability to survive in human macrophages but not in macrophages from other animals (i.e. mice). Despite the importance of macrophages in establishing systemic . Typhi infection, the mechanisms that macrophages use to control the growth of . Typhi and the role of these mechanisms in the bacterium's adaptation to the human host are mostly unknown. To facilitate unbiased identification of genes involved in controlling the growth of . Typhi in macrophages, we report optimized experimental conditions required to perform loss-of function pooled shRNA screens in primary mouse bone-marrow derived macrophages. Following infection with a fluorescent-labeled . Typhi, infected cells are sorted based on the intensity of fluorescence (i.e. number of intracellular fluorescent bacteria). shRNAs enriched in the fluorescent population are identified by next-generation sequencing. A proof-of-concept screen targeting the mouse Rab GTPases confirmed Rab32 as important to restrict . Typhi in mouse macrophages. Interestingly and rather unexpectedly, this screen also revealed that Rab1b controls . Typhi growth in mouse macrophages. This constitutes the first report of a Rab GTPase other than Rab32 involved in . Typhi host-restriction. The methodology described here should allow genome-wide screening to identify mechanisms controlling the growth of . Typhi and other intracellular pathogens in primary immune cells. Salmonella Typhi is a human-restricted bacterial pathogen that causes typhoid fever, a life-threatening systemic infection. A fundamental aspect of S. Typhi pathogenesis is its ability to survive in human macrophages but not in macrophages from other animals (i.e. mice). Despite the importance of macrophages in establishing systemic S. Typhi infection, the mechanisms that macrophages use to control the growth of S. Typhi and the role of these mechanisms in the bacterium's adaptation to the human host are mostly unknown. To facilitate unbiased identification of genes involved in controlling the growth of S. Typhi in macrophages, we report optimized experimental conditions required to perform loss-of function pooled shRNA screens in primary mouse bone-marrow derived macrophages. Following infection with a fluorescent-labeled S. Typhi, infected cells are sorted based on the intensity of fluorescence (i.e. number of intracellular fluorescent bacteria). shRNAs enriched in the fluorescent population are identified by next-generation sequencing. A proof-of-concept screen targeting the mouse Rab GTPases confirmed Rab32 as important to restrict S. Typhi in mouse macrophages. Interestingly and rather unexpectedly, this screen also revealed that Rab1b controls S. Typhi growth in mouse macrophages. This constitutes the first report of a Rab GTPase other than Rab32 involved in S. Typhi host-restriction. The methodology described here should allow genome-wide screening to identify mechanisms controlling the growth of S. Typhi and other intracellular pathogens in primary immune cells. Salmonella Typhi is a human-restricted bacterial pathogen that causes typhoid fever, a life-threatening systemic infection. A fundamental aspect of S. Typhi pathogenesis is its ability to survive in human macrophages but not in macrophages from other animals (i.e. mice). Despite the importance of macrophages in establishing systemic S. Typhi infection, the mechanisms that macrophages use to control the growth of S. Typhi and the role of these mechanisms in the bacterium’s adaptation to the human host are mostly unknown. To facilitate unbiased identification of genes involved in controlling the growth of S. Typhi in macrophages, we report optimized experimental conditions required to perform loss-of function pooled shRNA screens in primary mouse bone-marrow derived macrophages. Following infection with a fluorescent-labeled S. Typhi, infected cells are sorted based on the intensity of fluorescence (i.e. number of intracellular fluorescent bacteria). shRNAs enriched in the fluorescent population are identified by next-generation sequencing. A proof-of-concept screen targeting the mouse Rab GTPases confirmed Rab32 as important to restrict S. Typhi in mouse macrophages. Interestingly and rather unexpectedly, this screen also revealed that Rab1b controls S. Typhi growth in mouse macrophages. This constitutes the first report of a Rab GTPase other than Rab32 involved in S. Typhi host-restriction. The methodology described here should allow genome-wide screening to identify mechanisms controlling the growth of S. Typhi and other intracellular pathogens in primary immune cells. |
Author | Solano-Collado, Virtu Baldassarre, Massimiliano Colamarino, Rosa Angela Spanò, Stefania Calderwood, David A |
AuthorAffiliation | 2 Department of Pharmacology, Yale University School of Medicine , New Haven, CT , United States 3 Department of Cell Biology, Yale University School of Medicine , New Haven, CT , United States 1 Institute of Medical Sciences, University of Aberdeen , Aberdeen , United Kingdom |
AuthorAffiliation_xml | – name: 2 Department of Pharmacology, Yale University School of Medicine , New Haven, CT , United States – name: 3 Department of Cell Biology, Yale University School of Medicine , New Haven, CT , United States – name: 1 Institute of Medical Sciences, University of Aberdeen , Aberdeen , United Kingdom |
Author_xml | – sequence: 1 givenname: Virtu surname: Solano-Collado fullname: Solano-Collado, Virtu organization: Institute of Medical Sciences, University of Aberdeen, Aberdeen, United Kingdom – sequence: 2 givenname: Rosa Angela surname: Colamarino fullname: Colamarino, Rosa Angela organization: Institute of Medical Sciences, University of Aberdeen, Aberdeen, United Kingdom – sequence: 3 givenname: David A surname: Calderwood fullname: Calderwood, David A organization: Department of Cell Biology, Yale University School of Medicine, New Haven, CT, United States – sequence: 4 givenname: Massimiliano surname: Baldassarre fullname: Baldassarre, Massimiliano organization: Institute of Medical Sciences, University of Aberdeen, Aberdeen, United Kingdom – sequence: 5 givenname: Stefania surname: Spanò fullname: Spanò, Stefania organization: Institute of Medical Sciences, University of Aberdeen, Aberdeen, United Kingdom |
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Copyright | Copyright © 2021 Solano-Collado, Colamarino, Calderwood, Baldassarre and Spanò. Copyright © 2021 Solano-Collado, Colamarino, Calderwood, Baldassarre and Spanò 2021 Solano-Collado, Colamarino, Calderwood, Baldassarre and Spanò |
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Keywords | macrophages shRNA screen host-defense Rab GTPases Rab1b Salmonella Typhi |
Language | English |
License | Copyright © 2021 Solano-Collado, Colamarino, Calderwood, Baldassarre and Spanò. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Xiaoyun Liu, Peking University, China; V. K. Viswanathan, University of Arizona, United States This article was submitted to Bacteria and Host, a section of the journal Frontiers in Cellular and Infection Microbiology Edited by: Stephanie M. Seveau, The Ohio State University, United States Deceased |
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Snippet | Typhi is a human-restricted bacterial pathogen that causes typhoid fever, a life-threatening systemic infection. A fundamental aspect of
. Typhi pathogenesis... Salmonella Typhi is a human-restricted bacterial pathogen that causes typhoid fever, a life-threatening systemic infection. A fundamental aspect of S . Typhi... Salmonella Typhi is a human-restricted bacterial pathogen that causes typhoid fever, a life-threatening systemic infection. A fundamental aspect of S. Typhi... |
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SubjectTerms | Animals Cellular and Infection Microbiology host-defense macrophages Macrophages - metabolism Mice rab GTP-Binding Proteins - metabolism Rab GTPases Rab1b RNA, Small Interfering Salmonella Typhi Salmonella typhi - genetics shRNA screen Typhoid Fever |
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Title | A Small-Scale shRNA Screen in Primary Mouse Macrophages Identifies a Role for the Rab GTPase Rab1b in Controlling Salmonella Typhi Growth |
URI | https://www.ncbi.nlm.nih.gov/pubmed/33898333 https://search.proquest.com/docview/2518738680 https://pubmed.ncbi.nlm.nih.gov/PMC8059790 https://doaj.org/article/72a538667f73415bb587daec80cd7ab1 |
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