Natural Antimicrobials Promote the Anti-Oxidative Inhibition of COX-2 Mediated Inflammatory Response in Primary Oral Cells Infected with <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i>
<i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> can colonize the tooth root canals, adhere to dentin walls, and frequently cause periodontitis in dogs. Bacterial periodontal diseases are common in domesticated pets, cau...
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| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2023-04-01
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| Series: | Antioxidants |
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| Online Access: | https://www.mdpi.com/2076-3921/12/5/1017 |
| _version_ | 1797601368206213120 |
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| author | Eugenia Butucel Igori Balta Iulia Adelina Bundurus Cosmin Alin Popescu Tiberiu Iancu Adelina Venig Ioan Pet Ducu Stef David McCleery Lavinia Stef Nicolae Corcionivoschi |
| author_facet | Eugenia Butucel Igori Balta Iulia Adelina Bundurus Cosmin Alin Popescu Tiberiu Iancu Adelina Venig Ioan Pet Ducu Stef David McCleery Lavinia Stef Nicolae Corcionivoschi |
| author_sort | Eugenia Butucel |
| collection | DOAJ |
| description | <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> can colonize the tooth root canals, adhere to dentin walls, and frequently cause periodontitis in dogs. Bacterial periodontal diseases are common in domesticated pets, causing severe oral cavity inflammation and a strong immune response. This study investigates the antioxidant effect of a natural antimicrobial mixture (Auraguard—Ag) on the ability of <i>S. aureus</i>, <i>S. pyogenes</i> and <i>E. faecalis</i> to infect primary canine oral epithelial cells as well as its impact on their virulence factors. Our data show that a concentration of 0.25% Ag is sufficient to inhibit the growth of all three pathogens, whereas a concentration of 0.5% will become bactericidal. The sub-inhibitory concentration of 0.125% Ag reveals that the antimicrobial mixture can significantly reduce biofilm formation and exopolysaccharide production. The impact on these virulence factors was further translated into a significantly reduced ability to infect primary canine oral epithelial cells and restore epithelial tight junctions, with no impact on the epithelial cell viability. The post-infection inflammatory cytokines (IL-1β and IL-8) and the COX-2 mediator were also reduced both in mRNA and protein expression levels. The oxidative burst, detected upon infection, was also decreased in the presence of Ag, as our results show a significant decrease in H<sub>2</sub>O<sub>2</sub> released by the infected cells. We show that inhibition of either NADPH or ERK activity will result in a downregulation of COX-2 expression and lower levels of H<sub>2</sub>O<sub>2</sub> in infected cells. Conclusively, our study shows that natural antimicrobials reduce pro-inflammatory events, post infection, through an antioxidative mechanism that involves the downregulation of the COX-2 mediator via the inactivation of ERK in the absence of H<sub>2</sub>O<sub>2</sub>. As a result, they significantly reduce the risk of secondary bacterial infections and host oxidative stress caused by <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> accumulation in biofilms in an in vitro canine oral infection model. |
| first_indexed | 2024-03-11T03:59:59Z |
| format | Article |
| id | doaj.art-e5f9106f4e844e099660e7b5cc2f2d06 |
| institution | Directory Open Access Journal |
| issn | 2076-3921 |
| language | English |
| last_indexed | 2024-03-11T03:59:59Z |
| publishDate | 2023-04-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Antioxidants |
| spelling | doaj.art-e5f9106f4e844e099660e7b5cc2f2d062023-11-18T00:14:14ZengMDPI AGAntioxidants2076-39212023-04-01125101710.3390/antiox12051017Natural Antimicrobials Promote the Anti-Oxidative Inhibition of COX-2 Mediated Inflammatory Response in Primary Oral Cells Infected with <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i>Eugenia Butucel0Igori Balta1Iulia Adelina Bundurus2Cosmin Alin Popescu3Tiberiu Iancu4Adelina Venig5Ioan Pet6Ducu Stef7David McCleery8Lavinia Stef9Nicolae Corcionivoschi10Bacteriology Branch, Veterinary Sciences Division, Agri-Food and Biosciences Institute, Belfast BT4 3SD, UKFaculty of Bioengineering of Animal Resources, University of Life Sciences King Mihai I from Timisoara, 300645 Timisoara, RomaniaFaculty of Bioengineering of Animal Resources, University of Life Sciences King Mihai I from Timisoara, 300645 Timisoara, RomaniaFaculty of Agriculture, University of Life Sciences King Mihai I from Timisoara, 300645 Timisoara, RomaniaFaculty of Management and Rural Tourism, University of Life Sciences King Mihai I from Timisoara, 300645 Timisoara, RomaniaFaculty of Environmental Protection, University of Oradea, 410087 Oradea, RomaniaFaculty of Bioengineering of Animal Resources, University of Life Sciences King Mihai I from Timisoara, 300645 Timisoara, RomaniaFaculty of Food Engineering, University of Life Sciences King Mihai I from Timisoara, 300645 Timisoara, RomaniaBacteriology Branch, Veterinary Sciences Division, Agri-Food and Biosciences Institute, Belfast BT4 3SD, UKFaculty of Bioengineering of Animal Resources, University of Life Sciences King Mihai I from Timisoara, 300645 Timisoara, RomaniaBacteriology Branch, Veterinary Sciences Division, Agri-Food and Biosciences Institute, Belfast BT4 3SD, UK<i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> can colonize the tooth root canals, adhere to dentin walls, and frequently cause periodontitis in dogs. Bacterial periodontal diseases are common in domesticated pets, causing severe oral cavity inflammation and a strong immune response. This study investigates the antioxidant effect of a natural antimicrobial mixture (Auraguard—Ag) on the ability of <i>S. aureus</i>, <i>S. pyogenes</i> and <i>E. faecalis</i> to infect primary canine oral epithelial cells as well as its impact on their virulence factors. Our data show that a concentration of 0.25% Ag is sufficient to inhibit the growth of all three pathogens, whereas a concentration of 0.5% will become bactericidal. The sub-inhibitory concentration of 0.125% Ag reveals that the antimicrobial mixture can significantly reduce biofilm formation and exopolysaccharide production. The impact on these virulence factors was further translated into a significantly reduced ability to infect primary canine oral epithelial cells and restore epithelial tight junctions, with no impact on the epithelial cell viability. The post-infection inflammatory cytokines (IL-1β and IL-8) and the COX-2 mediator were also reduced both in mRNA and protein expression levels. The oxidative burst, detected upon infection, was also decreased in the presence of Ag, as our results show a significant decrease in H<sub>2</sub>O<sub>2</sub> released by the infected cells. We show that inhibition of either NADPH or ERK activity will result in a downregulation of COX-2 expression and lower levels of H<sub>2</sub>O<sub>2</sub> in infected cells. Conclusively, our study shows that natural antimicrobials reduce pro-inflammatory events, post infection, through an antioxidative mechanism that involves the downregulation of the COX-2 mediator via the inactivation of ERK in the absence of H<sub>2</sub>O<sub>2</sub>. As a result, they significantly reduce the risk of secondary bacterial infections and host oxidative stress caused by <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> accumulation in biofilms in an in vitro canine oral infection model.https://www.mdpi.com/2076-3921/12/5/1017<i>Staphylococcus aureus</i><i>Streptococcus pyogenes</i><i>Enterococcus faecalis</i>oral infectionnatural antimicrobialscanine primary oral epithelial cells |
| spellingShingle | Eugenia Butucel Igori Balta Iulia Adelina Bundurus Cosmin Alin Popescu Tiberiu Iancu Adelina Venig Ioan Pet Ducu Stef David McCleery Lavinia Stef Nicolae Corcionivoschi Natural Antimicrobials Promote the Anti-Oxidative Inhibition of COX-2 Mediated Inflammatory Response in Primary Oral Cells Infected with <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> Antioxidants <i>Staphylococcus aureus</i> <i>Streptococcus pyogenes</i> <i>Enterococcus faecalis</i> oral infection natural antimicrobials canine primary oral epithelial cells |
| title | Natural Antimicrobials Promote the Anti-Oxidative Inhibition of COX-2 Mediated Inflammatory Response in Primary Oral Cells Infected with <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> |
| title_full | Natural Antimicrobials Promote the Anti-Oxidative Inhibition of COX-2 Mediated Inflammatory Response in Primary Oral Cells Infected with <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> |
| title_fullStr | Natural Antimicrobials Promote the Anti-Oxidative Inhibition of COX-2 Mediated Inflammatory Response in Primary Oral Cells Infected with <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> |
| title_full_unstemmed | Natural Antimicrobials Promote the Anti-Oxidative Inhibition of COX-2 Mediated Inflammatory Response in Primary Oral Cells Infected with <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> |
| title_short | Natural Antimicrobials Promote the Anti-Oxidative Inhibition of COX-2 Mediated Inflammatory Response in Primary Oral Cells Infected with <i>Staphylococcus aureus</i>, <i>Streptococcus pyogenes</i> and <i>Enterococcus faecalis</i> |
| title_sort | natural antimicrobials promote the anti oxidative inhibition of cox 2 mediated inflammatory response in primary oral cells infected with i staphylococcus aureus i i streptococcus pyogenes i and i enterococcus faecalis i |
| topic | <i>Staphylococcus aureus</i> <i>Streptococcus pyogenes</i> <i>Enterococcus faecalis</i> oral infection natural antimicrobials canine primary oral epithelial cells |
| url | https://www.mdpi.com/2076-3921/12/5/1017 |
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