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Mechanisms of Mitochondrial Toxicity and Cytotoxicity Caused by Pseudomonas aeruginosa Pyocyanin in Human Nasal Epithelial Cells.

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International forum of allergy & rhinology 2025
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Thompson JC, Park A, Kouakou YI, Miller ZA, Darwich NF, Adappa ND, Palmer JN, Carey RM, Lee RJ

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[BACKGROUND] Pseudomonas aeruginosa is an opportunistic pathogen in cystic fibrosis-related chronic rhinosinusitis (CF-CRS) that produces phenazine metabolites pyocyanin and 1-hydroxyphenazine (1-HP),

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APA Thompson JC, Park A, et al. (2025). Mechanisms of Mitochondrial Toxicity and Cytotoxicity Caused by Pseudomonas aeruginosa Pyocyanin in Human Nasal Epithelial Cells.. International forum of allergy & rhinology. https://doi.org/10.1002/alr.70084
MLA Thompson JC, et al.. "Mechanisms of Mitochondrial Toxicity and Cytotoxicity Caused by Pseudomonas aeruginosa Pyocyanin in Human Nasal Epithelial Cells.." International forum of allergy & rhinology, 2025.
PMID 41416815
DOI 10.1002/alr.70084

Abstract

[BACKGROUND] Pseudomonas aeruginosa is an opportunistic pathogen in cystic fibrosis-related chronic rhinosinusitis (CF-CRS) that produces phenazine metabolites pyocyanin and 1-hydroxyphenazine (1-HP), which may have detrimental effects on mitochondria, reactive oxygen species (ROS), Ca signaling, and apoptosis. However, prior studies utilized lung cancer cells or dissociated animal cells. We sought to better define human nasal epithelial responses to phenazines, including the role of Ca.

[METHODS] Live cell imaging was used to measure Ca and mitochondrial function in RPMI2650 nasal carcinoma cells and primary human nasal epithelial cells (HNECs) cultured in submersion and at air-liquid interface (ALI). Gene expression was measured by quantitative PCR. Ciliary beat frequency (CBF) was quantified by high-speed imaging.

[RESULTS] Pyocyanin, but not 1-HP, increased mitochondrial Ca dependent on phospholipase C and endoplasmic reticulum (ER) Ca release, correlating with protein kinase C activation. Mitochondrial membrane potential decreased and mitochondrial ROS increased with both pyocyanin and 1-HP in a Ca-independent manner. Both pyocyanin and 1-HP decreased viability of RPMI2650s and other squamous carcinoma cell lines over 24 h, whereas HNECs survived, possibly due to differential regulation of protein homeostasis genes, including activating transcription factor 6 (ATF6). Mitochondrial ROS was enhanced in CF-CRS ALIs, which may explain why pyocyanin reduced CBF in CF but not non-CF ALIs.

[CONCLUSIONS] Ca signaling is not required for phenazine mitochondrial toxicity. The greater sensitivity of cancer cells to phenazine cytotoxicity necessitates use of primary cells when studying host responses to bacterial phenazines. Enhanced ROS production and ciliotoxicity in CF-CRS may contribute to susceptibility to P. aeruginosa infection.