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An In Vitro Model to Assess Early Immune Markers Following Co-Exposure of Epithelial Cells to Carbon Black (Nano)Particles in the Presence of S. aureus: A Role for Stressed Cells in Toxicological Testing

Scott Brown, Stephen Evans Orcid Logo, Michael J. Burgum Orcid Logo, Kirsty Meldrum Orcid Logo, Jack Herridge, Blessing Akinbola, Llinos Harris Orcid Logo, Rowena Jenkins Orcid Logo, Shareen Doak Orcid Logo, Martin Clift Orcid Logo, Thomas Wilkinson Orcid Logo

Biomedicines, Volume: 12, Issue: 1, Start page: 128

Swansea University Authors: Stephen Evans Orcid Logo, Michael J. Burgum Orcid Logo, Llinos Harris Orcid Logo, Rowena Jenkins Orcid Logo, Shareen Doak Orcid Logo, Martin Clift Orcid Logo, Thomas Wilkinson Orcid Logo

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DOI (Published version): 10.3390/biomedicines12010128

Abstract

The exposure of human lung and skin to carbon black (CB) is continuous due to its widespread applications. Current toxicological testing uses ‘healthy’ cellular systems; however, questions remain whether this mimics the everyday stresses that human cells are exposed to, including infection. Staphylo...

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Published in: Biomedicines
ISSN: 2227-9059
Published: MDPI AG 2024
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Burgum</name><active>true</active><ethesisStudent>true</ethesisStudent></author><author><sid>dc70f9d4badbbdb5d467fd321986d173</sid><ORCID>0000-0002-0295-3038</ORCID><firstname>Llinos</firstname><surname>Harris</surname><name>Llinos Harris</name><active>true</active><ethesisStudent>false</ethesisStudent></author><author><sid>caf58cd775a27bf8b9ee340079a29cc0</sid><ORCID>0000-0001-6664-6099</ORCID><firstname>Rowena</firstname><surname>Jenkins</surname><name>Rowena Jenkins</name><active>true</active><ethesisStudent>false</ethesisStudent></author><author><sid>8f70286908f67238a527a98cbf66d387</sid><ORCID>0000-0002-6753-1987</ORCID><firstname>Shareen</firstname><surname>Doak</surname><name>Shareen Doak</name><active>true</active><ethesisStudent>false</ethesisStudent></author><author><sid>71bf49b157691e541950f5c3f49c9169</sid><ORCID>0000-0001-6133-3368</ORCID><firstname>Martin</firstname><surname>Clift</surname><name>Martin Clift</name><active>true</active><ethesisStudent>false</ethesisStudent></author><author><sid>86cca6bf31bfe8572de27c1b441420d8</sid><ORCID>0000-0003-0397-6079</ORCID><firstname>Thomas</firstname><surname>Wilkinson</surname><name>Thomas Wilkinson</name><active>true</active><ethesisStudent>false</ethesisStudent></author></swanseaauthors><date>2024-01-09</date><deptcode>BMS</deptcode><abstract>The exposure of human lung and skin to carbon black (CB) is continuous due to its widespread applications. Current toxicological testing uses ‘healthy’ cellular systems; however, questions remain whether this mimics the everyday stresses that human cells are exposed to, including infection. Staphylococcus aureus lung and skin infections remain prevalent in society, and include pneumonia and atopic dermatitis, respectively, but current in vitro toxicological testing does not consider infection stress. Therefore, investigating the effects of CB co-exposure in ‘stressed’ infected epithelial cells in vitro may better approximate true toxicity. This work aims to study the impact of CB exposure during Staphylococcus aureus infection stress in A549 (lung) and HaCaT (skin) epithelial cells. Physicochemical characterisation of CB confirmed its dramatic polydispersity and potential to aggregate. CB significantly inhibited S. aureus growth in cell culture media. CB did not induce cytokines or antimicrobial peptides from lung and skin epithelial cells, when given alone, but did reduce HaCaT and A549 cell viability to 55% and 77%, respectively. In contrast, S. aureus induced a robust interleukin (IL)-8 response in both lung and skin epithelial cells. IL-6 and human beta defensin (hβD)-2 could only be detected when cells were stimulated with S. aureus with no decreases in cell viability. However, co-exposure to CB (100 µg/mL) and S. aureus resulted in significant inhibition of IL-8 (compared to S. aureus alone) without further reduction in cell viability. Furthermore, the same co-exposure induced significantly more hβD-2 (compared to S. aureus alone). This work confirms that toxicological testing in healthy versus stressed cells gives significantly different responses. This has significant implications for toxicological testing and suggests that cell stresses (including infection) should be included in current models to better represent the diversity of cell viabilities found in lung and skin within a general population. This model will have significant application when estimating CB exposure in at-risk groups, such as factory workers, the elderly, and the immunocompromised.</abstract><type>Journal Article</type><journal>Biomedicines</journal><volume>12</volume><journalNumber>1</journalNumber><paginationStart>128</paginationStart><paginationEnd/><publisher>MDPI AG</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint/><issnElectronic>2227-9059</issnElectronic><keywords>epithelial cells; A549; HaCaT; carbon black (nano)particles; cytokines; Staphylococcus aureus; infection; particle exposure; in vitro co-exposure models</keywords><publishedDay>8</publishedDay><publishedMonth>1</publishedMonth><publishedYear>2024</publishedYear><publishedDate>2024-01-08</publishedDate><doi>10.3390/biomedicines12010128</doi><url/><notes>Data Availability Statement:The data presented in this study are available on request from the corresponding author.</notes><college>COLLEGE NANME</college><department>Biomedical Sciences</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>BMS</DepartmentCode><institution>Swansea University</institution><apcterm>Other</apcterm><funders>he work was partly funded by a studentship from SUMS to T.S.W. In addition, M.J.D.C. and K.M. acknowledge the financial support from the SPF Clean Air Challenge Funded (UKRI NERC) project, RESPIRE (NE/W002264/1).</funders><projectreference/><lastEdited>2024-03-21T12:08:26.2749357</lastEdited><Created>2024-01-09T14:02:50.3757795</Created><path><level id="1">Faculty of Medicine, Health and Life Sciences</level><level id="2">Swansea University Medical School - Biomedical Science</level></path><authors><author><firstname>Scott</firstname><surname>Brown</surname><order>1</order></author><author><firstname>Stephen</firstname><surname>Evans</surname><orcid>0000-0002-5352-9800</orcid><order>2</order></author><author><firstname>Michael J.</firstname><surname>Burgum</surname><orcid>NULL</orcid><order>3</order></author><author><firstname>Kirsty</firstname><surname>Meldrum</surname><orcid>0000-0002-2658-6850</orcid><order>4</order></author><author><firstname>Jack</firstname><surname>Herridge</surname><order>5</order></author><author><firstname>Blessing</firstname><surname>Akinbola</surname><order>6</order></author><author><firstname>Llinos</firstname><surname>Harris</surname><orcid>0000-0002-0295-3038</orcid><order>7</order></author><author><firstname>Rowena</firstname><surname>Jenkins</surname><orcid>0000-0001-6664-6099</orcid><order>8</order></author><author><firstname>Shareen</firstname><surname>Doak</surname><orcid>0000-0002-6753-1987</orcid><order>9</order></author><author><firstname>Martin</firstname><surname>Clift</surname><orcid>0000-0001-6133-3368</orcid><order>10</order></author><author><firstname>Thomas</firstname><surname>Wilkinson</surname><orcid>0000-0003-0397-6079</orcid><order>11</order></author></authors><documents><document><filename>65427__29422__8ba2e4b9dd2f4d8a9b9d2b25f7bb0ab1.pdf</filename><originalFilename>biomedicines-12-00128 Copy.pdf</originalFilename><uploaded>2024-01-09T14:11:02.0623395</uploaded><type>Output</type><contentLength>3379148</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><documentNotes>© 2024 by the authors. 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spelling v2 65427 2024-01-09 An In Vitro Model to Assess Early Immune Markers Following Co-Exposure of Epithelial Cells to Carbon Black (Nano)Particles in the Presence of S. aureus: A Role for Stressed Cells in Toxicological Testing cfca981bdfb8492873a48cc1629def9a 0000-0002-5352-9800 Stephen Evans Stephen Evans true false 9a3ab85e1f89e7664b83f1016d4a9a93 NULL Michael J. Burgum Michael J. Burgum true true dc70f9d4badbbdb5d467fd321986d173 0000-0002-0295-3038 Llinos Harris Llinos Harris true false caf58cd775a27bf8b9ee340079a29cc0 0000-0001-6664-6099 Rowena Jenkins Rowena Jenkins true false 8f70286908f67238a527a98cbf66d387 0000-0002-6753-1987 Shareen Doak Shareen Doak true false 71bf49b157691e541950f5c3f49c9169 0000-0001-6133-3368 Martin Clift Martin Clift true false 86cca6bf31bfe8572de27c1b441420d8 0000-0003-0397-6079 Thomas Wilkinson Thomas Wilkinson true false 2024-01-09 BMS The exposure of human lung and skin to carbon black (CB) is continuous due to its widespread applications. Current toxicological testing uses ‘healthy’ cellular systems; however, questions remain whether this mimics the everyday stresses that human cells are exposed to, including infection. Staphylococcus aureus lung and skin infections remain prevalent in society, and include pneumonia and atopic dermatitis, respectively, but current in vitro toxicological testing does not consider infection stress. Therefore, investigating the effects of CB co-exposure in ‘stressed’ infected epithelial cells in vitro may better approximate true toxicity. This work aims to study the impact of CB exposure during Staphylococcus aureus infection stress in A549 (lung) and HaCaT (skin) epithelial cells. Physicochemical characterisation of CB confirmed its dramatic polydispersity and potential to aggregate. CB significantly inhibited S. aureus growth in cell culture media. CB did not induce cytokines or antimicrobial peptides from lung and skin epithelial cells, when given alone, but did reduce HaCaT and A549 cell viability to 55% and 77%, respectively. In contrast, S. aureus induced a robust interleukin (IL)-8 response in both lung and skin epithelial cells. IL-6 and human beta defensin (hβD)-2 could only be detected when cells were stimulated with S. aureus with no decreases in cell viability. However, co-exposure to CB (100 µg/mL) and S. aureus resulted in significant inhibition of IL-8 (compared to S. aureus alone) without further reduction in cell viability. Furthermore, the same co-exposure induced significantly more hβD-2 (compared to S. aureus alone). This work confirms that toxicological testing in healthy versus stressed cells gives significantly different responses. This has significant implications for toxicological testing and suggests that cell stresses (including infection) should be included in current models to better represent the diversity of cell viabilities found in lung and skin within a general population. This model will have significant application when estimating CB exposure in at-risk groups, such as factory workers, the elderly, and the immunocompromised. Journal Article Biomedicines 12 1 128 MDPI AG 2227-9059 epithelial cells; A549; HaCaT; carbon black (nano)particles; cytokines; Staphylococcus aureus; infection; particle exposure; in vitro co-exposure models 8 1 2024 2024-01-08 10.3390/biomedicines12010128 Data Availability Statement:The data presented in this study are available on request from the corresponding author. COLLEGE NANME Biomedical Sciences COLLEGE CODE BMS Swansea University Other he work was partly funded by a studentship from SUMS to T.S.W. In addition, M.J.D.C. and K.M. acknowledge the financial support from the SPF Clean Air Challenge Funded (UKRI NERC) project, RESPIRE (NE/W002264/1). 2024-03-21T12:08:26.2749357 2024-01-09T14:02:50.3757795 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Biomedical Science Scott Brown 1 Stephen Evans 0000-0002-5352-9800 2 Michael J. Burgum NULL 3 Kirsty Meldrum 0000-0002-2658-6850 4 Jack Herridge 5 Blessing Akinbola 6 Llinos Harris 0000-0002-0295-3038 7 Rowena Jenkins 0000-0001-6664-6099 8 Shareen Doak 0000-0002-6753-1987 9 Martin Clift 0000-0001-6133-3368 10 Thomas Wilkinson 0000-0003-0397-6079 11 65427__29422__8ba2e4b9dd2f4d8a9b9d2b25f7bb0ab1.pdf biomedicines-12-00128 Copy.pdf 2024-01-09T14:11:02.0623395 Output 3379148 application/pdf Version of Record true © 2024 by the authors. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license. true eng https://creativecommons.org/licenses/by/4.0/
title An In Vitro Model to Assess Early Immune Markers Following Co-Exposure of Epithelial Cells to Carbon Black (Nano)Particles in the Presence of S. aureus: A Role for Stressed Cells in Toxicological Testing
spellingShingle An In Vitro Model to Assess Early Immune Markers Following Co-Exposure of Epithelial Cells to Carbon Black (Nano)Particles in the Presence of S. aureus: A Role for Stressed Cells in Toxicological Testing
Stephen Evans
Michael J. Burgum
Llinos Harris
Rowena Jenkins
Shareen Doak
Martin Clift
Thomas Wilkinson
title_short An In Vitro Model to Assess Early Immune Markers Following Co-Exposure of Epithelial Cells to Carbon Black (Nano)Particles in the Presence of S. aureus: A Role for Stressed Cells in Toxicological Testing
title_full An In Vitro Model to Assess Early Immune Markers Following Co-Exposure of Epithelial Cells to Carbon Black (Nano)Particles in the Presence of S. aureus: A Role for Stressed Cells in Toxicological Testing
title_fullStr An In Vitro Model to Assess Early Immune Markers Following Co-Exposure of Epithelial Cells to Carbon Black (Nano)Particles in the Presence of S. aureus: A Role for Stressed Cells in Toxicological Testing
title_full_unstemmed An In Vitro Model to Assess Early Immune Markers Following Co-Exposure of Epithelial Cells to Carbon Black (Nano)Particles in the Presence of S. aureus: A Role for Stressed Cells in Toxicological Testing
title_sort An In Vitro Model to Assess Early Immune Markers Following Co-Exposure of Epithelial Cells to Carbon Black (Nano)Particles in the Presence of S. aureus: A Role for Stressed Cells in Toxicological Testing
author_id_str_mv cfca981bdfb8492873a48cc1629def9a
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author_id_fullname_str_mv cfca981bdfb8492873a48cc1629def9a_***_Stephen Evans
9a3ab85e1f89e7664b83f1016d4a9a93_***_Michael J. Burgum
dc70f9d4badbbdb5d467fd321986d173_***_Llinos Harris
caf58cd775a27bf8b9ee340079a29cc0_***_Rowena Jenkins
8f70286908f67238a527a98cbf66d387_***_Shareen Doak
71bf49b157691e541950f5c3f49c9169_***_Martin Clift
86cca6bf31bfe8572de27c1b441420d8_***_Thomas Wilkinson
author Stephen Evans
Michael J. Burgum
Llinos Harris
Rowena Jenkins
Shareen Doak
Martin Clift
Thomas Wilkinson
author2 Scott Brown
Stephen Evans
Michael J. Burgum
Kirsty Meldrum
Jack Herridge
Blessing Akinbola
Llinos Harris
Rowena Jenkins
Shareen Doak
Martin Clift
Thomas Wilkinson
format Journal article
container_title Biomedicines
container_volume 12
container_issue 1
container_start_page 128
publishDate 2024
institution Swansea University
issn 2227-9059
doi_str_mv 10.3390/biomedicines12010128
publisher MDPI AG
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Biomedical Science{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Biomedical Science
document_store_str 1
active_str 0
description The exposure of human lung and skin to carbon black (CB) is continuous due to its widespread applications. Current toxicological testing uses ‘healthy’ cellular systems; however, questions remain whether this mimics the everyday stresses that human cells are exposed to, including infection. Staphylococcus aureus lung and skin infections remain prevalent in society, and include pneumonia and atopic dermatitis, respectively, but current in vitro toxicological testing does not consider infection stress. Therefore, investigating the effects of CB co-exposure in ‘stressed’ infected epithelial cells in vitro may better approximate true toxicity. This work aims to study the impact of CB exposure during Staphylococcus aureus infection stress in A549 (lung) and HaCaT (skin) epithelial cells. Physicochemical characterisation of CB confirmed its dramatic polydispersity and potential to aggregate. CB significantly inhibited S. aureus growth in cell culture media. CB did not induce cytokines or antimicrobial peptides from lung and skin epithelial cells, when given alone, but did reduce HaCaT and A549 cell viability to 55% and 77%, respectively. In contrast, S. aureus induced a robust interleukin (IL)-8 response in both lung and skin epithelial cells. IL-6 and human beta defensin (hβD)-2 could only be detected when cells were stimulated with S. aureus with no decreases in cell viability. However, co-exposure to CB (100 µg/mL) and S. aureus resulted in significant inhibition of IL-8 (compared to S. aureus alone) without further reduction in cell viability. Furthermore, the same co-exposure induced significantly more hβD-2 (compared to S. aureus alone). This work confirms that toxicological testing in healthy versus stressed cells gives significantly different responses. This has significant implications for toxicological testing and suggests that cell stresses (including infection) should be included in current models to better represent the diversity of cell viabilities found in lung and skin within a general population. This model will have significant application when estimating CB exposure in at-risk groups, such as factory workers, the elderly, and the immunocompromised.
published_date 2024-01-08T12:08:23Z
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