Increased intracellular survival of Salmonella Typhimurium ST313 in HIV‐1‐infected primary human macrophages is not associated with Salmonella hijacking the HIV compartment

Background Non‐typhoidal Salmonella (NTS) causes a severe invasive syndrome (iNTS disease) described in HIV‐positive adults. The impact of HIV‐1 on Salmonella pathogenesis and the molecular basis for the differences between these bacteria and classical diarrhoeal S. Typhimurium remains unclear. Resu...

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Veröffentlicht in:Biology of the cell 2020-03, Vol.112 (3), p.92-101
Hauptverfasser: Lê‐Bury, G., Deschamps, C., Kizilyaprak, C., Blanchard, W., Daraspe, J., Dumas, A., Gordon, M.A., Hinton, J.C.D., Humbel, B.M., Niedergang, F.
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container_end_page 101
container_issue 3
container_start_page 92
container_title Biology of the cell
container_volume 112
creator Lê‐Bury, G.
Deschamps, C.
Kizilyaprak, C.
Blanchard, W.
Daraspe, J.
Dumas, A.
Gordon, M.A.
Hinton, J.C.D.
Humbel, B.M.
Niedergang, F.
description Background Non‐typhoidal Salmonella (NTS) causes a severe invasive syndrome (iNTS disease) described in HIV‐positive adults. The impact of HIV‐1 on Salmonella pathogenesis and the molecular basis for the differences between these bacteria and classical diarrhoeal S. Typhimurium remains unclear. Results Here, we show that iNTS‐associated S. Typhimurium Sequence Type 313 (ST313) bacteria show greater intracellular survival in primary human macrophages, compared with a ‘classical’ diarrhoeal S. Typhimurium ST19 isolate. The increased intracellular survival phenotype of ST313 is more pronounced in HIV‐infected macrophages. We explored the possibility that the bacteria take advantage of the HIV‐associated viral‐containing compartments created in human macrophages that have low pH. Confocal fluorescence microscopy and focussed ion beam‐scanning electron microscopy tomography showed that Salmonella did not co‐localise extensively with HIV‐positive compartments. Conclusion The capacity of ST313 bacteria to survive better than ST19 bacteria within primary human macrophages is enhanced in cells pre‐infected with HIV‐1. Our results indicate that the ST313 bacteria do not directly benefit from the niche created by the virus in HIV‐1‐infected macrophages, and that they might take advantage from a more globally modified host cell. Significance A better understanding of the interplay between HIV‐1 and Salmonella is important not only for these bacteria but also for other opportunistic pathogens. Research article: HIV infection of human macrophages leads to defective clearance activities of these cells, allowing the development of opportunistic bacteria. We found that Salmonella Typhimurium Sequence Type 313 (ST313) survives better in HIV‐infected macrophages than the gastroenteritis‐associated S. Typhimurium ST19 pathovariant. Confocal and electron microscopy showed that the bacteria do not directly hijack the viral compartment but might benefit from a globally modified macrophage.
doi_str_mv 10.1111/boc.201900055
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The impact of HIV‐1 on Salmonella pathogenesis and the molecular basis for the differences between these bacteria and classical diarrhoeal S. Typhimurium remains unclear. Results Here, we show that iNTS‐associated S. Typhimurium Sequence Type 313 (ST313) bacteria show greater intracellular survival in primary human macrophages, compared with a ‘classical’ diarrhoeal S. Typhimurium ST19 isolate. The increased intracellular survival phenotype of ST313 is more pronounced in HIV‐infected macrophages. We explored the possibility that the bacteria take advantage of the HIV‐associated viral‐containing compartments created in human macrophages that have low pH. Confocal fluorescence microscopy and focussed ion beam‐scanning electron microscopy tomography showed that Salmonella did not co‐localise extensively with HIV‐positive compartments. Conclusion The capacity of ST313 bacteria to survive better than ST19 bacteria within primary human macrophages is enhanced in cells pre‐infected with HIV‐1. Our results indicate that the ST313 bacteria do not directly benefit from the niche created by the virus in HIV‐1‐infected macrophages, and that they might take advantage from a more globally modified host cell. Significance A better understanding of the interplay between HIV‐1 and Salmonella is important not only for these bacteria but also for other opportunistic pathogens. Research article: HIV infection of human macrophages leads to defective clearance activities of these cells, allowing the development of opportunistic bacteria. We found that Salmonella Typhimurium Sequence Type 313 (ST313) survives better in HIV‐infected macrophages than the gastroenteritis‐associated S. Typhimurium ST19 pathovariant. Confocal and electron microscopy showed that the bacteria do not directly hijack the viral compartment but might benefit from a globally modified macrophage.</description><identifier>ISSN: 0248-4900</identifier><identifier>EISSN: 1768-322X</identifier><identifier>DOI: 10.1111/boc.201900055</identifier><identifier>PMID: 31922615</identifier><language>eng</language><publisher>England: Wiley</publisher><subject>Coinfection - microbiology ; Cytoplasm - microbiology ; Cytoplasm - virology ; Electron Microscope Tomography - methods ; FIB‐SEM ; HIV Infections - complications ; HIV-1 - growth &amp; development ; HIV‐1 ; Host Microbial Interactions - physiology ; Humans ; invasive Salmonella enterica Typhimurium ST313 ; Life Sciences ; macrophages ; Macrophages - microbiology ; Macrophages - physiology ; Macrophages - virology ; Microbial Interactions - physiology ; Microscopy, Confocal ; Primary Cell Culture ; Salmonella Infections - etiology ; Salmonella typhimurium - growth &amp; development</subject><ispartof>Biology of the cell, 2020-03, Vol.112 (3), p.92-101</ispartof><rights>2020 Société Française des Microscopies and Société de Biologie Cellulaire de France. Published by John Wiley &amp; Sons Ltd</rights><rights>2020 Société Française des Microscopies and Société de Biologie Cellulaire de France. 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The impact of HIV‐1 on Salmonella pathogenesis and the molecular basis for the differences between these bacteria and classical diarrhoeal S. Typhimurium remains unclear. Results Here, we show that iNTS‐associated S. Typhimurium Sequence Type 313 (ST313) bacteria show greater intracellular survival in primary human macrophages, compared with a ‘classical’ diarrhoeal S. Typhimurium ST19 isolate. The increased intracellular survival phenotype of ST313 is more pronounced in HIV‐infected macrophages. We explored the possibility that the bacteria take advantage of the HIV‐associated viral‐containing compartments created in human macrophages that have low pH. Confocal fluorescence microscopy and focussed ion beam‐scanning electron microscopy tomography showed that Salmonella did not co‐localise extensively with HIV‐positive compartments. Conclusion The capacity of ST313 bacteria to survive better than ST19 bacteria within primary human macrophages is enhanced in cells pre‐infected with HIV‐1. Our results indicate that the ST313 bacteria do not directly benefit from the niche created by the virus in HIV‐1‐infected macrophages, and that they might take advantage from a more globally modified host cell. Significance A better understanding of the interplay between HIV‐1 and Salmonella is important not only for these bacteria but also for other opportunistic pathogens. Research article: HIV infection of human macrophages leads to defective clearance activities of these cells, allowing the development of opportunistic bacteria. We found that Salmonella Typhimurium Sequence Type 313 (ST313) survives better in HIV‐infected macrophages than the gastroenteritis‐associated S. Typhimurium ST19 pathovariant. Confocal and electron microscopy showed that the bacteria do not directly hijack the viral compartment but might benefit from a globally modified macrophage.</description><subject>Coinfection - microbiology</subject><subject>Cytoplasm - microbiology</subject><subject>Cytoplasm - virology</subject><subject>Electron Microscope Tomography - methods</subject><subject>FIB‐SEM</subject><subject>HIV Infections - complications</subject><subject>HIV-1 - growth &amp; development</subject><subject>HIV‐1</subject><subject>Host Microbial Interactions - physiology</subject><subject>Humans</subject><subject>invasive Salmonella enterica Typhimurium ST313</subject><subject>Life Sciences</subject><subject>macrophages</subject><subject>Macrophages - microbiology</subject><subject>Macrophages - physiology</subject><subject>Macrophages - virology</subject><subject>Microbial Interactions - physiology</subject><subject>Microscopy, Confocal</subject><subject>Primary Cell Culture</subject><subject>Salmonella Infections - etiology</subject><subject>Salmonella typhimurium - growth &amp; 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development</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lê‐Bury, G.</creatorcontrib><creatorcontrib>Deschamps, C.</creatorcontrib><creatorcontrib>Kizilyaprak, C.</creatorcontrib><creatorcontrib>Blanchard, W.</creatorcontrib><creatorcontrib>Daraspe, J.</creatorcontrib><creatorcontrib>Dumas, A.</creatorcontrib><creatorcontrib>Gordon, M.A.</creatorcontrib><creatorcontrib>Hinton, J.C.D.</creatorcontrib><creatorcontrib>Humbel, B.M.</creatorcontrib><creatorcontrib>Niedergang, F.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Biology of the cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lê‐Bury, G.</au><au>Deschamps, C.</au><au>Kizilyaprak, C.</au><au>Blanchard, W.</au><au>Daraspe, J.</au><au>Dumas, A.</au><au>Gordon, M.A.</au><au>Hinton, J.C.D.</au><au>Humbel, B.M.</au><au>Niedergang, F.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Increased intracellular survival of Salmonella Typhimurium ST313 in HIV‐1‐infected primary human macrophages is not associated with Salmonella hijacking the HIV compartment</atitle><jtitle>Biology of the cell</jtitle><addtitle>Biol Cell</addtitle><date>2020-03</date><risdate>2020</risdate><volume>112</volume><issue>3</issue><spage>92</spage><epage>101</epage><pages>92-101</pages><issn>0248-4900</issn><eissn>1768-322X</eissn><abstract>Background Non‐typhoidal Salmonella (NTS) causes a severe invasive syndrome (iNTS disease) described in HIV‐positive adults. The impact of HIV‐1 on Salmonella pathogenesis and the molecular basis for the differences between these bacteria and classical diarrhoeal S. Typhimurium remains unclear. Results Here, we show that iNTS‐associated S. Typhimurium Sequence Type 313 (ST313) bacteria show greater intracellular survival in primary human macrophages, compared with a ‘classical’ diarrhoeal S. Typhimurium ST19 isolate. The increased intracellular survival phenotype of ST313 is more pronounced in HIV‐infected macrophages. We explored the possibility that the bacteria take advantage of the HIV‐associated viral‐containing compartments created in human macrophages that have low pH. Confocal fluorescence microscopy and focussed ion beam‐scanning electron microscopy tomography showed that Salmonella did not co‐localise extensively with HIV‐positive compartments. Conclusion The capacity of ST313 bacteria to survive better than ST19 bacteria within primary human macrophages is enhanced in cells pre‐infected with HIV‐1. Our results indicate that the ST313 bacteria do not directly benefit from the niche created by the virus in HIV‐1‐infected macrophages, and that they might take advantage from a more globally modified host cell. Significance A better understanding of the interplay between HIV‐1 and Salmonella is important not only for these bacteria but also for other opportunistic pathogens. Research article: HIV infection of human macrophages leads to defective clearance activities of these cells, allowing the development of opportunistic bacteria. We found that Salmonella Typhimurium Sequence Type 313 (ST313) survives better in HIV‐infected macrophages than the gastroenteritis‐associated S. Typhimurium ST19 pathovariant. Confocal and electron microscopy showed that the bacteria do not directly hijack the viral compartment but might benefit from a globally modified macrophage.</abstract><cop>England</cop><pub>Wiley</pub><pmid>31922615</pmid><doi>10.1111/boc.201900055</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-7064-830X</orcidid><oa>free_for_read</oa></addata></record>
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subjects Coinfection - microbiology
Cytoplasm - microbiology
Cytoplasm - virology
Electron Microscope Tomography - methods
FIB‐SEM
HIV Infections - complications
HIV-1 - growth & development
HIV‐1
Host Microbial Interactions - physiology
Humans
invasive Salmonella enterica Typhimurium ST313
Life Sciences
macrophages
Macrophages - microbiology
Macrophages - physiology
Macrophages - virology
Microbial Interactions - physiology
Microscopy, Confocal
Primary Cell Culture
Salmonella Infections - etiology
Salmonella typhimurium - growth & development
title Increased intracellular survival of Salmonella Typhimurium ST313 in HIV‐1‐infected primary human macrophages is not associated with Salmonella hijacking the HIV compartment
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