Endoplasmic Reticulum Stress and Unfolded Protein Response Sensor ERN1 Regulates Organic Dust Induction of Lung Inflammation

ABSTRACT Inhalation of organic dust increases the risk for respiratory symptoms and respiratory diseases, with chronic inflammation playing a major role in their development. Previously, we reported that organic dust induction of inflammatory mediators in bronchial epithelial cells is mediated throu...

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Main Authors: Shilpa Kusampudi, Velmurugan Meganathan, Vijay Boggaram
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:FASEB BioAdvances
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Online Access:https://doi.org/10.1096/fba.2025-00069
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author Shilpa Kusampudi
Velmurugan Meganathan
Vijay Boggaram
author_facet Shilpa Kusampudi
Velmurugan Meganathan
Vijay Boggaram
author_sort Shilpa Kusampudi
collection DOAJ
description ABSTRACT Inhalation of organic dust increases the risk for respiratory symptoms and respiratory diseases, with chronic inflammation playing a major role in their development. Previously, we reported that organic dust induction of inflammatory mediators in bronchial epithelial cells is mediated through increase of intracellular reactive oxygen species (ROS) and activation of NFκB and Stat3. Oxidative stress caused by increased ROS has been linked to the activation of endoplasmic reticulum (ER) stress and unfolded protein response (UPR). UPR modulates immune responses and plays key roles in the development of acute and chronic diseases. Herein, we hypothesized that organic dust‐induced ER stress‐UPR regulates airway epithelial cell inflammatory responses. We found that poultry organic dust extract (referred to as dust extract) increased the expression of ER stress/UPR sensor ERN1 in Beas2B bronchial epithelial cells. Dust extract was also found to increase ERN1 protein levels in mouse lungs with ERN1 immunostaining detected predominantly in the bronchial epithelium. Additionally, dust extract increased Ser724 ERN1 phosphorylation in the mouse bronchial epithelium indicating activation. Chemical inhibition and mRNA knockdown studies revealed that TLR2/TLR4‐Myd88‐ROS‐NFκB/Stat3 pathway mediates ERN1 induction. ERN1 chemical inhibitors, KIRA6 and APY29, and ERN1 mRNA knockdown reduced the induction of IL6, CXCL8, and pro IL1β. KIRA6 inhibited dust extract stimulation of NFκB‐p65, Stat3, Jun and MAPK 8/9 phosphorylation. Our studies have shown that ER stress and ERN1 are new players in the control of organic dust induced lung inflammation. Cross‐regulation between members of cell signaling cascade, TLR2‐TLR4/MyD88/ROS/ERN1/NFκB/Stat3 may fine tune immune and inflammatory responses elicited by organic dust.
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spelling doaj-art-98b1cc31d0fc4ee0953b6102c74e893c2025-08-20T03:35:32ZengWileyFASEB BioAdvances2573-98322025-07-0177n/an/a10.1096/fba.2025-00069Endoplasmic Reticulum Stress and Unfolded Protein Response Sensor ERN1 Regulates Organic Dust Induction of Lung InflammationShilpa Kusampudi0Velmurugan Meganathan1Vijay Boggaram2Department of Cellular and Molecular Biology, Health Science Center University of Texas at Tyler Tyler Texas USADepartment of Cellular and Molecular Biology, Health Science Center University of Texas at Tyler Tyler Texas USADepartment of Cellular and Molecular Biology, Health Science Center University of Texas at Tyler Tyler Texas USAABSTRACT Inhalation of organic dust increases the risk for respiratory symptoms and respiratory diseases, with chronic inflammation playing a major role in their development. Previously, we reported that organic dust induction of inflammatory mediators in bronchial epithelial cells is mediated through increase of intracellular reactive oxygen species (ROS) and activation of NFκB and Stat3. Oxidative stress caused by increased ROS has been linked to the activation of endoplasmic reticulum (ER) stress and unfolded protein response (UPR). UPR modulates immune responses and plays key roles in the development of acute and chronic diseases. Herein, we hypothesized that organic dust‐induced ER stress‐UPR regulates airway epithelial cell inflammatory responses. We found that poultry organic dust extract (referred to as dust extract) increased the expression of ER stress/UPR sensor ERN1 in Beas2B bronchial epithelial cells. Dust extract was also found to increase ERN1 protein levels in mouse lungs with ERN1 immunostaining detected predominantly in the bronchial epithelium. Additionally, dust extract increased Ser724 ERN1 phosphorylation in the mouse bronchial epithelium indicating activation. Chemical inhibition and mRNA knockdown studies revealed that TLR2/TLR4‐Myd88‐ROS‐NFκB/Stat3 pathway mediates ERN1 induction. ERN1 chemical inhibitors, KIRA6 and APY29, and ERN1 mRNA knockdown reduced the induction of IL6, CXCL8, and pro IL1β. KIRA6 inhibited dust extract stimulation of NFκB‐p65, Stat3, Jun and MAPK 8/9 phosphorylation. Our studies have shown that ER stress and ERN1 are new players in the control of organic dust induced lung inflammation. Cross‐regulation between members of cell signaling cascade, TLR2‐TLR4/MyD88/ROS/ERN1/NFκB/Stat3 may fine tune immune and inflammatory responses elicited by organic dust.https://doi.org/10.1096/fba.2025-00069endoplasmic reticulum stressinflammationlungoxidative stressunfolded protein response
spellingShingle Shilpa Kusampudi
Velmurugan Meganathan
Vijay Boggaram
Endoplasmic Reticulum Stress and Unfolded Protein Response Sensor ERN1 Regulates Organic Dust Induction of Lung Inflammation
FASEB BioAdvances
endoplasmic reticulum stress
inflammation
lung
oxidative stress
unfolded protein response
title Endoplasmic Reticulum Stress and Unfolded Protein Response Sensor ERN1 Regulates Organic Dust Induction of Lung Inflammation
title_full Endoplasmic Reticulum Stress and Unfolded Protein Response Sensor ERN1 Regulates Organic Dust Induction of Lung Inflammation
title_fullStr Endoplasmic Reticulum Stress and Unfolded Protein Response Sensor ERN1 Regulates Organic Dust Induction of Lung Inflammation
title_full_unstemmed Endoplasmic Reticulum Stress and Unfolded Protein Response Sensor ERN1 Regulates Organic Dust Induction of Lung Inflammation
title_short Endoplasmic Reticulum Stress and Unfolded Protein Response Sensor ERN1 Regulates Organic Dust Induction of Lung Inflammation
title_sort endoplasmic reticulum stress and unfolded protein response sensor ern1 regulates organic dust induction of lung inflammation
topic endoplasmic reticulum stress
inflammation
lung
oxidative stress
unfolded protein response
url https://doi.org/10.1096/fba.2025-00069
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AT vijayboggaram endoplasmicreticulumstressandunfoldedproteinresponsesensorern1regulatesorganicdustinductionoflunginflammation