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A Novel Model of Staphylococcus aureus-Induced Lymphoplasmacytic Rhinosinusitis in Rats
 
 
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Volume 25
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Article

Staphylococcus aureus Biofilm-Secreted Factors Cause Mucosal Damage, Mast Cell Infiltration, and Goblet Cell Hyperplasia in a Rat Rhinosinusitis Model

by
Ghais Houtak
1,2,
Roshan Nepal
1,2,
George Bouras
1,2,
Gohar Shaghayegh
1,2,
Catherine Bennett
3,
John Finnie
1,
Kevin Fenix
1,2,
Alkis James Psaltis
1,2,
Peter-John Wormald
1,2 and
Sarah Vreugde
1,2,*
1
Adelaide Medical School, Faculty of Health and Medical Sciences, The University of Adelaide, Adelaide, SA 5005, Australia
2
The Department of Surgery—Otolaryngology-Head and Neck Surgery, The University of Adelaide and the Basil Hetzel Institute for Translational Health Research, Central Adelaide Local Health Network, Adelaide, SA 5000, Australia
3
Jones Radiology, Eastwood, SA 5063, Australia
*
Author to whom correspondence should be addressed.
Int. J. Mol. Sci. 2024, 25(6), 3402; https://doi.org/10.3390/ijms25063402
Submission received: 11 January 2024 / Revised: 29 February 2024 / Accepted: 11 March 2024 / Published: 17 March 2024
(This article belongs to the Special Issue Chronic Rhinosinusitis: Aetiology, Immunology and Treatment 2.0)
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Abstract

Chronic rhinosinusitis (CRS) is an inflammatory condition of the sinonasal mucosa. Despite being a common health issue, the exact cause of CRS is yet to be understood. However, research suggests that Staphylococcus aureus, particularly in its biofilm form, is associated with the disease. This study aimed to investigate the impact of long-term exposure to secreted factors of Staphylococcus aureus biofilm (SABSFs), harvested from clinical isolates of non-CRS carrier and CRS patients, on the nasal mucosa in a rat model. Animals were randomised (n = 5/group) to receive daily intranasal instillations of 40 μL (200 μg/μL) SABSFs for 28 days or vehicle control. The sinonasal samples were analysed through histopathology and transcriptome profiling. The results showed that all three intervention groups displayed significant lymphocytic infiltration (p ≤ 0.05). However, only the SABSFs collected from the CRSwNP patient caused significant mucosal damage, mast cell infiltration, and goblet cell hyperplasia compared to the control. The transcriptomics results indicated that SABSFs significantly enriched multiple inflammatory pathways and showed distinct transcriptional expression differences between the control group and the SABSFs collected from CRS patients (p ≤ 0.05). Additionally, the SABSF challenges induced the expression of IgA and IgG but not IgE. This in vivo study indicates that long-term exposure to SABSFs leads to an inflammatory response in the nasal mucosa with increased severity for S. aureus isolated from a CRSwNP patient. Moreover, exposure to SABSFs does not induce local production of IgE.
Keywords: Chronic rhinosinusitis; Staphylococcus aureus; biofilm; eosinophilic; IgE Chronic rhinosinusitis; Staphylococcus aureus; biofilm; eosinophilic; IgE

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MDPI and ACS Style

Houtak, G.; Nepal, R.; Bouras, G.; Shaghayegh, G.; Bennett, C.; Finnie, J.; Fenix, K.; Psaltis, A.J.; Wormald, P.-J.; Vreugde, S. Staphylococcus aureus Biofilm-Secreted Factors Cause Mucosal Damage, Mast Cell Infiltration, and Goblet Cell Hyperplasia in a Rat Rhinosinusitis Model. Int. J. Mol. Sci. 2024, 25, 3402. https://doi.org/10.3390/ijms25063402

AMA Style

Houtak G, Nepal R, Bouras G, Shaghayegh G, Bennett C, Finnie J, Fenix K, Psaltis AJ, Wormald P-J, Vreugde S. Staphylococcus aureus Biofilm-Secreted Factors Cause Mucosal Damage, Mast Cell Infiltration, and Goblet Cell Hyperplasia in a Rat Rhinosinusitis Model. International Journal of Molecular Sciences. 2024; 25(6):3402. https://doi.org/10.3390/ijms25063402

Chicago/Turabian Style

Houtak, Ghais, Roshan Nepal, George Bouras, Gohar Shaghayegh, Catherine Bennett, John Finnie, Kevin Fenix, Alkis James Psaltis, Peter-John Wormald, and Sarah Vreugde. 2024. "Staphylococcus aureus Biofilm-Secreted Factors Cause Mucosal Damage, Mast Cell Infiltration, and Goblet Cell Hyperplasia in a Rat Rhinosinusitis Model" International Journal of Molecular Sciences 25, no. 6: 3402. https://doi.org/10.3390/ijms25063402

APA Style

Houtak, G., Nepal, R., Bouras, G., Shaghayegh, G., Bennett, C., Finnie, J., Fenix, K., Psaltis, A. J., Wormald, P.-J., & Vreugde, S. (2024). Staphylococcus aureus Biofilm-Secreted Factors Cause Mucosal Damage, Mast Cell Infiltration, and Goblet Cell Hyperplasia in a Rat Rhinosinusitis Model. International Journal of Molecular Sciences, 25(6), 3402. https://doi.org/10.3390/ijms25063402

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