The phosphorylation of Smad3 by CaMKIIγ leads to the hepatocyte pyroptosis under perfluorooctane sulfonate exposure

Perfluorooctane sulfonate (PFOS) is a persistent organic pollutant and accumulated in the liver of mammals. PFOS exposure is closely associated with the development of pyroptosis. Nevertheless, the underlying mechanism is unclear. We found here that PFOS induced pyroptosis in the mice liver and L-02...

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Main Authors: Siyu Ren, Peiyao Liang, Ruzhen Feng, Wei Yang, Tianming Qiu, Jingyuan Zhang, Qiujuan Li, Guang Yang, Xiance Sun, Xiaofeng Yao
Format: Article
Language:English
Published: Elsevier 2024-10-01
Series:Ecotoxicology and Environmental Safety
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Online Access:http://www.sciencedirect.com/science/article/pii/S0147651324010005
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author Siyu Ren
Peiyao Liang
Ruzhen Feng
Wei Yang
Tianming Qiu
Jingyuan Zhang
Qiujuan Li
Guang Yang
Xiance Sun
Xiaofeng Yao
author_facet Siyu Ren
Peiyao Liang
Ruzhen Feng
Wei Yang
Tianming Qiu
Jingyuan Zhang
Qiujuan Li
Guang Yang
Xiance Sun
Xiaofeng Yao
author_sort Siyu Ren
collection DOAJ
description Perfluorooctane sulfonate (PFOS) is a persistent organic pollutant and accumulated in the liver of mammals. PFOS exposure is closely associated with the development of pyroptosis. Nevertheless, the underlying mechanism is unclear. We found here that PFOS induced pyroptosis in the mice liver and L-02 cells as demonstrated by activation of the NOD-like receptor protein 3 inflammasome, gasdermin D cleavage and increased release of interleukin-1β and interleukin-18. The level of cytoplasmic calcium was accelerated in hepatocytes upon exposure to PFOS. The phosphorylated/activated form of calcium/calmodulin-dependent protein kinase II (CaMKII) was augmented by PFOS in vivo and in vitro. PFOS-induced pyroptosis was relieved by CaMKII inhibitor. Among various CaMKII subtypes, we identified that CaMKIIγ was activated specifically by PFOS. CaMKIIγ interacted with Smad family member 3 (Smad3) under PFOS exposure. PFOS increased the phosphorylation of Smad3, and CaMKII inhibitor or CaMKIIγ siRNA alleviated PFOS-caused phosphorylation of Smad3. Inhibiting Smad3 activity was found to alleviate PFOS-induced hepatocyte pyroptosis. This study puts forward that CaMKIIγ-Smad3 is the linkage between calcium homeostasis disturbance and pyroptosis, providing a mechanistic explanation for PFOS-induced pyroptosis.
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spelling doaj-art-6beb476e515d46ad9be020f718fd2f022025-08-20T01:54:44ZengElsevierEcotoxicology and Environmental Safety0147-65132024-10-0128411692410.1016/j.ecoenv.2024.116924The phosphorylation of Smad3 by CaMKIIγ leads to the hepatocyte pyroptosis under perfluorooctane sulfonate exposureSiyu Ren0Peiyao Liang1Ruzhen Feng2Wei Yang3Tianming Qiu4Jingyuan Zhang5Qiujuan Li6Guang Yang7Xiance Sun8Xiaofeng Yao9Department of Occupation and Environment Health, Dalian Medical University, 9 Lvshun South Road, Dalian, ChinaDepartment of Occupation and Environment Health, Dalian Medical University, 9 Lvshun South Road, Dalian, ChinaDepartment of Occupation and Environment Health, Dalian Medical University, 9 Lvshun South Road, Dalian, ChinaDepartment of Occupation and Environment Health, Dalian Medical University, 9 Lvshun South Road, Dalian, ChinaDepartment of Occupation and Environment Health, Dalian Medical University, 9 Lvshun South Road, Dalian, China; Corresponding authors.Department of Occupation and Environment Health, Dalian Medical University, 9 Lvshun South Road, Dalian, ChinaDepartment of Nutrition, Dalian Medical University, 9 Lvshun South Road, Dalian, ChinaDepartment of Nutrition, Dalian Medical University, 9 Lvshun South Road, Dalian, ChinaDepartment of Occupation and Environment Health, Dalian Medical University, 9 Lvshun South Road, Dalian, ChinaDepartment of Occupation and Environment Health, Dalian Medical University, 9 Lvshun South Road, Dalian, China; Corresponding authors.Perfluorooctane sulfonate (PFOS) is a persistent organic pollutant and accumulated in the liver of mammals. PFOS exposure is closely associated with the development of pyroptosis. Nevertheless, the underlying mechanism is unclear. We found here that PFOS induced pyroptosis in the mice liver and L-02 cells as demonstrated by activation of the NOD-like receptor protein 3 inflammasome, gasdermin D cleavage and increased release of interleukin-1β and interleukin-18. The level of cytoplasmic calcium was accelerated in hepatocytes upon exposure to PFOS. The phosphorylated/activated form of calcium/calmodulin-dependent protein kinase II (CaMKII) was augmented by PFOS in vivo and in vitro. PFOS-induced pyroptosis was relieved by CaMKII inhibitor. Among various CaMKII subtypes, we identified that CaMKIIγ was activated specifically by PFOS. CaMKIIγ interacted with Smad family member 3 (Smad3) under PFOS exposure. PFOS increased the phosphorylation of Smad3, and CaMKII inhibitor or CaMKIIγ siRNA alleviated PFOS-caused phosphorylation of Smad3. Inhibiting Smad3 activity was found to alleviate PFOS-induced hepatocyte pyroptosis. This study puts forward that CaMKIIγ-Smad3 is the linkage between calcium homeostasis disturbance and pyroptosis, providing a mechanistic explanation for PFOS-induced pyroptosis.http://www.sciencedirect.com/science/article/pii/S0147651324010005Perfluorooctane sulfonatePyroptosisCytoplasmic calciumCalcium/calmodulin-dependent protein kinase II γSmad family member 3
spellingShingle Siyu Ren
Peiyao Liang
Ruzhen Feng
Wei Yang
Tianming Qiu
Jingyuan Zhang
Qiujuan Li
Guang Yang
Xiance Sun
Xiaofeng Yao
The phosphorylation of Smad3 by CaMKIIγ leads to the hepatocyte pyroptosis under perfluorooctane sulfonate exposure
Ecotoxicology and Environmental Safety
Perfluorooctane sulfonate
Pyroptosis
Cytoplasmic calcium
Calcium/calmodulin-dependent protein kinase II γ
Smad family member 3
title The phosphorylation of Smad3 by CaMKIIγ leads to the hepatocyte pyroptosis under perfluorooctane sulfonate exposure
title_full The phosphorylation of Smad3 by CaMKIIγ leads to the hepatocyte pyroptosis under perfluorooctane sulfonate exposure
title_fullStr The phosphorylation of Smad3 by CaMKIIγ leads to the hepatocyte pyroptosis under perfluorooctane sulfonate exposure
title_full_unstemmed The phosphorylation of Smad3 by CaMKIIγ leads to the hepatocyte pyroptosis under perfluorooctane sulfonate exposure
title_short The phosphorylation of Smad3 by CaMKIIγ leads to the hepatocyte pyroptosis under perfluorooctane sulfonate exposure
title_sort phosphorylation of smad3 by camkiiγ leads to the hepatocyte pyroptosis under perfluorooctane sulfonate exposure
topic Perfluorooctane sulfonate
Pyroptosis
Cytoplasmic calcium
Calcium/calmodulin-dependent protein kinase II γ
Smad family member 3
url http://www.sciencedirect.com/science/article/pii/S0147651324010005
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