Modulation of Staphylococcus aureus gene expression during proliferation in platelet concentrates with focus on virulence and platelet functionality
Staphylococcus aureus is a well-documented bacterial contaminant in platelet concentrates (PCs), a blood component used to treat patients with platelet deficiencies. This bacterium can evade routine PC culture screening and cause septic transfusion reactions. Here, we investigated the gene expressio...
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| description | Staphylococcus aureus is a well-documented bacterial contaminant in platelet concentrates (PCs), a blood component used to treat patients with platelet deficiencies. This bacterium can evade routine PC culture screening and cause septic transfusion reactions. Here, we investigated the gene expression modulation within the PC niche versus trypticase soy media (TSB) of S. aureus CBS2016-05, a strain isolated from a septic reaction, in comparison to PS/BAC/317/16/W, a strain identified during PC screening. RNA-seq analysis revealed upregulation of the capsule biosynthesis operon (capA-H), surface adhesion factors (sasADF), clumping factor A (clfA), protein A (spa), and anaerobic metabolism genes (pflAB, nrdDG) in CBS2016-05 when grown in PCs versus TSB, implying its enhanced pathogenicity in this milieu, in contrast to the PS/BAC/317/16/W strain. Furthermore, we investigated the impact of S. aureus CBS2016-05 on platelet functionality in spiked PCs versus non-spiked PC units. Flow cytometry analyses revealed a significant decrease in glycoprotein (GP) IIb (CD41) and GPIbα (CD42b) expression, alongside increased P-selectin (CD62P) and phosphatidylserine (annexin V) expression in spiked PCs compared to non-spiked PCs (p = 0.01). Moreover, spiked PCs exhibited a drastic reduction in MitoTrack Red FM and Calcein AM positive platelets (87.3% vs. 29.4%, p = 0.0001 and 95.4% vs. 24.7%, p = 0.0001) in a bacterial cell density manner. These results indicated that S. aureus CBS2016-05 triggers platelet activation and apoptosis, and compromises mitochondrial functionality and platelet viability, in contaminated PCs. Furthermore, this study enhanced our understanding of the effects of platelet-bacteria interactions in the unique PC niche, highlighting S. aureus increased pathogenicity and deleterious effect on platelet functionality in a strain specific manner. Our novel insights serve as a platform to improve PC transfusion safety. |
| doi_str_mv | 10.1371/journal.pone.0307920 |
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This bacterium can evade routine PC culture screening and cause septic transfusion reactions. Here, we investigated the gene expression modulation within the PC niche versus trypticase soy media (TSB) of S. aureus CBS2016-05, a strain isolated from a septic reaction, in comparison to PS/BAC/317/16/W, a strain identified during PC screening. RNA-seq analysis revealed upregulation of the capsule biosynthesis operon (capA-H), surface adhesion factors (sasADF), clumping factor A (clfA), protein A (spa), and anaerobic metabolism genes (pflAB, nrdDG) in CBS2016-05 when grown in PCs versus TSB, implying its enhanced pathogenicity in this milieu, in contrast to the PS/BAC/317/16/W strain. Furthermore, we investigated the impact of S. aureus CBS2016-05 on platelet functionality in spiked PCs versus non-spiked PC units. Flow cytometry analyses revealed a significant decrease in glycoprotein (GP) IIb (CD41) and GPIbα (CD42b) expression, alongside increased P-selectin (CD62P) and phosphatidylserine (annexin V) expression in spiked PCs compared to non-spiked PCs (p = 0.01). Moreover, spiked PCs exhibited a drastic reduction in MitoTrack Red FM and Calcein AM positive platelets (87.3% vs. 29.4%, p = 0.0001 and 95.4% vs. 24.7%, p = 0.0001) in a bacterial cell density manner. These results indicated that S. aureus CBS2016-05 triggers platelet activation and apoptosis, and compromises mitochondrial functionality and platelet viability, in contaminated PCs. Furthermore, this study enhanced our understanding of the effects of platelet-bacteria interactions in the unique PC niche, highlighting S. aureus increased pathogenicity and deleterious effect on platelet functionality in a strain specific manner. Our novel insights serve as a platform to improve PC transfusion safety.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0307920</identifier><identifier>PMID: 39052660</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino acids ; Analysis ; Annexin V ; Antibiotics ; Apoptosis ; Automation ; Bacteria ; Bacterial artificial chromosomes ; Bacterial genetics ; Bacterial Proteins - genetics ; Bacterial Proteins - metabolism ; Biofilms ; Biology and Life Sciences ; Biosynthesis ; Blood & organ donations ; Blood platelets ; Blood Platelets - metabolism ; Blood Platelets - microbiology ; Blood transfusion ; Calcein ; Cell activation ; Cell culture ; Cell density ; Chromosomes ; Contaminants ; Culture media ; Flow cytometry ; Gene expression ; Gene Expression Regulation, Bacterial ; Genetic aspects ; Genomes ; Glycoproteins ; Humans ; Medicine and Health Sciences ; Modulation ; P-selectin ; Pathogenicity ; Pathogens ; Peptides ; Phosphatidylserine ; Platelets ; Protein A ; Protein turnover ; Proteins ; RNA ; Staphylococcal Infections - microbiology ; Staphylococcus aureus ; Staphylococcus aureus - genetics ; Staphylococcus aureus - pathogenicity ; Strain analysis ; Transfusion ; Virulence ; Virulence - genetics</subject><ispartof>PloS one, 2024-07, Vol.19 (7), p.e0307920</ispartof><rights>Copyright: © 2024 Yousuf et al. 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This bacterium can evade routine PC culture screening and cause septic transfusion reactions. Here, we investigated the gene expression modulation within the PC niche versus trypticase soy media (TSB) of S. aureus CBS2016-05, a strain isolated from a septic reaction, in comparison to PS/BAC/317/16/W, a strain identified during PC screening. RNA-seq analysis revealed upregulation of the capsule biosynthesis operon (capA-H), surface adhesion factors (sasADF), clumping factor A (clfA), protein A (spa), and anaerobic metabolism genes (pflAB, nrdDG) in CBS2016-05 when grown in PCs versus TSB, implying its enhanced pathogenicity in this milieu, in contrast to the PS/BAC/317/16/W strain. Furthermore, we investigated the impact of S. aureus CBS2016-05 on platelet functionality in spiked PCs versus non-spiked PC units. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yousuf, Basit</au><au>Pasha, Roya</au><au>Pineault, Nicolas</au><au>Ramirez-Arcos, Sandra</au><au>Seo, Keun Seok</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Modulation of Staphylococcus aureus gene expression during proliferation in platelet concentrates with focus on virulence and platelet functionality</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2024-07-25</date><risdate>2024</risdate><volume>19</volume><issue>7</issue><spage>e0307920</spage><pages>e0307920-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Staphylococcus aureus is a well-documented bacterial contaminant in platelet concentrates (PCs), a blood component used to treat patients with platelet deficiencies. This bacterium can evade routine PC culture screening and cause septic transfusion reactions. Here, we investigated the gene expression modulation within the PC niche versus trypticase soy media (TSB) of S. aureus CBS2016-05, a strain isolated from a septic reaction, in comparison to PS/BAC/317/16/W, a strain identified during PC screening. RNA-seq analysis revealed upregulation of the capsule biosynthesis operon (capA-H), surface adhesion factors (sasADF), clumping factor A (clfA), protein A (spa), and anaerobic metabolism genes (pflAB, nrdDG) in CBS2016-05 when grown in PCs versus TSB, implying its enhanced pathogenicity in this milieu, in contrast to the PS/BAC/317/16/W strain. Furthermore, we investigated the impact of S. aureus CBS2016-05 on platelet functionality in spiked PCs versus non-spiked PC units. Flow cytometry analyses revealed a significant decrease in glycoprotein (GP) IIb (CD41) and GPIbα (CD42b) expression, alongside increased P-selectin (CD62P) and phosphatidylserine (annexin V) expression in spiked PCs compared to non-spiked PCs (p = 0.01). Moreover, spiked PCs exhibited a drastic reduction in MitoTrack Red FM and Calcein AM positive platelets (87.3% vs. 29.4%, p = 0.0001 and 95.4% vs. 24.7%, p = 0.0001) in a bacterial cell density manner. These results indicated that S. aureus CBS2016-05 triggers platelet activation and apoptosis, and compromises mitochondrial functionality and platelet viability, in contaminated PCs. Furthermore, this study enhanced our understanding of the effects of platelet-bacteria interactions in the unique PC niche, highlighting S. aureus increased pathogenicity and deleterious effect on platelet functionality in a strain specific manner. Our novel insights serve as a platform to improve PC transfusion safety.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39052660</pmid><doi>10.1371/journal.pone.0307920</doi><tpages>e0307920</tpages><orcidid>https://orcid.org/0000-0002-3452-8749</orcidid><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_3084712060 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Amino acids Analysis Annexin V Antibiotics Apoptosis Automation Bacteria Bacterial artificial chromosomes Bacterial genetics Bacterial Proteins - genetics Bacterial Proteins - metabolism Biofilms Biology and Life Sciences Biosynthesis Blood & organ donations Blood platelets Blood Platelets - metabolism Blood Platelets - microbiology Blood transfusion Calcein Cell activation Cell culture Cell density Chromosomes Contaminants Culture media Flow cytometry Gene expression Gene Expression Regulation, Bacterial Genetic aspects Genomes Glycoproteins Humans Medicine and Health Sciences Modulation P-selectin Pathogenicity Pathogens Peptides Phosphatidylserine Platelets Protein A Protein turnover Proteins RNA Staphylococcal Infections - microbiology Staphylococcus aureus Staphylococcus aureus - genetics Staphylococcus aureus - pathogenicity Strain analysis Transfusion Virulence Virulence - genetics |
| title | Modulation of Staphylococcus aureus gene expression during proliferation in platelet concentrates with focus on virulence and platelet functionality |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-23T02%3A38%3A23IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Modulation%20of%20Staphylococcus%20aureus%20gene%20expression%20during%20proliferation%20in%20platelet%20concentrates%20with%20focus%20on%20virulence%20and%20platelet%20functionality&rft.jtitle=PloS%20one&rft.au=Yousuf,%20Basit&rft.date=2024-07-25&rft.volume=19&rft.issue=7&rft.spage=e0307920&rft.pages=e0307920-&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0307920&rft_dat=%3Cgale_plos_%3EA802596885%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3084712060&rft_id=info:pmid/39052660&rft_galeid=A802596885&rft_doaj_id=oai_doaj_org_article_d27d47d5fdcb4adba61a0d0fee6ffe68&rfr_iscdi=true |