Exploring secretory proteome and cytokine kinetic of human peripheral blood mononuclear cells exposed to methicillin-resistant Staphylococcus aureus biofilms and planktonic bacteria
Staphylococcus aureus is a highly successful pathogen infecting various body parts and forming biofilms on natural and artificial surfaces resulting in difficult-to-treat and chronic infections. We investigated the secreted cytokines and proteomes of isolated peripheral blood mononuclear cells (PBMC...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2024-03-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1334616/full |
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| author | Reza Gheitasi Daniela Röll Mario M. Müller Mario M. Müller Mohadeseh Naseri Rainer König Rainer König Hortense Slevogt Hortense Slevogt Mathias W. Pletz Mathias W. Pletz Mathias W. Pletz Oliwia Makarewicz Oliwia Makarewicz |
| author_facet | Reza Gheitasi Daniela Röll Mario M. Müller Mario M. Müller Mohadeseh Naseri Rainer König Rainer König Hortense Slevogt Hortense Slevogt Mathias W. Pletz Mathias W. Pletz Mathias W. Pletz Oliwia Makarewicz Oliwia Makarewicz |
| author_sort | Reza Gheitasi |
| collection | DOAJ |
| description | Staphylococcus aureus is a highly successful pathogen infecting various body parts and forming biofilms on natural and artificial surfaces resulting in difficult-to-treat and chronic infections. We investigated the secreted cytokines and proteomes of isolated peripheral blood mononuclear cells (PBMCs) from healthy volunteers exposed to methicillin-resistant S. aureus (MRSA) biofilms or planktonic bacteria. Additionally, the cytokine profiles in sera from patients with community-acquired pneumonia (CAP) caused by S. aureus were investigated. The aim was to gain insights into the immune response involved and differentiate between the planktonic and sessile MRSA forms. We identified 321 and 298 targets that were significantly differently expressed in PBMCs when exposed to planktonic or biofilm-embedded bacteria, respectively. PBMCs exposed to planktonic MRSA cells secreted increased levels of TNF-α, while IL-18 was elevated when exposed to the biofilm. The machine-learning analyses of the cytokine profiles obtained for the in vitro PBMCs and CAP sera distinguished between the two types of bacteria forms based on cytokines IL-18, IL12, and IL-17, and with a lower importance IL-6. Particularly, IL-18 which has not been correlated with S. aureus biofilms so far might represent a suitable marker for monitoring chronification during MRSA infection to individualize the therapy, but this hypothesis must be proved in clinical trials. |
| first_indexed | 2024-04-24T21:49:44Z |
| format | Article |
| id | doaj.art-1caaf566d8ca4884aa0204e4d29d5610 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-24T21:49:44Z |
| publishDate | 2024-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-1caaf566d8ca4884aa0204e4d29d56102024-03-20T14:41:50ZengFrontiers Media S.A.Frontiers in Immunology1664-32242024-03-011510.3389/fimmu.2024.13346161334616Exploring secretory proteome and cytokine kinetic of human peripheral blood mononuclear cells exposed to methicillin-resistant Staphylococcus aureus biofilms and planktonic bacteriaReza Gheitasi0Daniela Röll1Mario M. Müller2Mario M. Müller3Mohadeseh Naseri4Rainer König5Rainer König6Hortense Slevogt7Hortense Slevogt8Mathias W. Pletz9Mathias W. Pletz10Mathias W. Pletz11Oliwia Makarewicz12Oliwia Makarewicz13Institute of Infectious Diseases and Infection Control, Jena University Hospital/Friedrich Schiller University, Jena, GermanyInstitute of Infectious Diseases and Infection Control, Jena University Hospital/Friedrich Schiller University, Jena, GermanySeptomics Research Center, Jena University Hospital, Jena, GermanyIntegrated Research and Treatment Center - Center for Sepsis Control and Care (CSCC), Jena University Hospital, Jena, GermanyInstitute of Infectious Diseases and Infection Control, Jena University Hospital/Friedrich Schiller University, Jena, GermanyInstitute of Infectious Diseases and Infection Control, Jena University Hospital/Friedrich Schiller University, Jena, GermanyIntegrated Research and Treatment Center - Center for Sepsis Control and Care (CSCC), Jena University Hospital, Jena, GermanyRespiratory Infection Dynamics, Helmholtz Centre for Infection Research-HZI Braunschweig, Braunschweig, GermanyDepartment of Respiratory Medicine and Infectious Diseases, Hannover Medical School, German Center for Lung Research (DZL), Biomedical Research in Endstage & Obstructive Lung Disease (BREATH), Hannover, GermanyInstitute of Infectious Diseases and Infection Control, Jena University Hospital/Friedrich Schiller University, Jena, GermanyIntegrated Research and Treatment Center - Center for Sepsis Control and Care (CSCC), Jena University Hospital, Jena, GermanyCAPNETZ STIFTUNG, Hannover, GermanyInstitute of Infectious Diseases and Infection Control, Jena University Hospital/Friedrich Schiller University, Jena, GermanyIntegrated Research and Treatment Center - Center for Sepsis Control and Care (CSCC), Jena University Hospital, Jena, GermanyStaphylococcus aureus is a highly successful pathogen infecting various body parts and forming biofilms on natural and artificial surfaces resulting in difficult-to-treat and chronic infections. We investigated the secreted cytokines and proteomes of isolated peripheral blood mononuclear cells (PBMCs) from healthy volunteers exposed to methicillin-resistant S. aureus (MRSA) biofilms or planktonic bacteria. Additionally, the cytokine profiles in sera from patients with community-acquired pneumonia (CAP) caused by S. aureus were investigated. The aim was to gain insights into the immune response involved and differentiate between the planktonic and sessile MRSA forms. We identified 321 and 298 targets that were significantly differently expressed in PBMCs when exposed to planktonic or biofilm-embedded bacteria, respectively. PBMCs exposed to planktonic MRSA cells secreted increased levels of TNF-α, while IL-18 was elevated when exposed to the biofilm. The machine-learning analyses of the cytokine profiles obtained for the in vitro PBMCs and CAP sera distinguished between the two types of bacteria forms based on cytokines IL-18, IL12, and IL-17, and with a lower importance IL-6. Particularly, IL-18 which has not been correlated with S. aureus biofilms so far might represent a suitable marker for monitoring chronification during MRSA infection to individualize the therapy, but this hypothesis must be proved in clinical trials.https://www.frontiersin.org/articles/10.3389/fimmu.2024.1334616/fullbiomarkersmachine learningchronic infectionsproteomicsartificial neural networkscytokine profiling |
| spellingShingle | Reza Gheitasi Daniela Röll Mario M. Müller Mario M. Müller Mohadeseh Naseri Rainer König Rainer König Hortense Slevogt Hortense Slevogt Mathias W. Pletz Mathias W. Pletz Mathias W. Pletz Oliwia Makarewicz Oliwia Makarewicz Exploring secretory proteome and cytokine kinetic of human peripheral blood mononuclear cells exposed to methicillin-resistant Staphylococcus aureus biofilms and planktonic bacteria Frontiers in Immunology biomarkers machine learning chronic infections proteomics artificial neural networks cytokine profiling |
| title | Exploring secretory proteome and cytokine kinetic of human peripheral blood mononuclear cells exposed to methicillin-resistant Staphylococcus aureus biofilms and planktonic bacteria |
| title_full | Exploring secretory proteome and cytokine kinetic of human peripheral blood mononuclear cells exposed to methicillin-resistant Staphylococcus aureus biofilms and planktonic bacteria |
| title_fullStr | Exploring secretory proteome and cytokine kinetic of human peripheral blood mononuclear cells exposed to methicillin-resistant Staphylococcus aureus biofilms and planktonic bacteria |
| title_full_unstemmed | Exploring secretory proteome and cytokine kinetic of human peripheral blood mononuclear cells exposed to methicillin-resistant Staphylococcus aureus biofilms and planktonic bacteria |
| title_short | Exploring secretory proteome and cytokine kinetic of human peripheral blood mononuclear cells exposed to methicillin-resistant Staphylococcus aureus biofilms and planktonic bacteria |
| title_sort | exploring secretory proteome and cytokine kinetic of human peripheral blood mononuclear cells exposed to methicillin resistant staphylococcus aureus biofilms and planktonic bacteria |
| topic | biomarkers machine learning chronic infections proteomics artificial neural networks cytokine profiling |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2024.1334616/full |
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