Inhibition of RACK1‐Mediated NLRP3 Oligomerization (Active Conformation) Ameliorates Acute Respiratory Distress Syndrome

Abstract Aberrant activation of the NACHT, LRR, and PYD domain‐containing protein 3 (NLRP3) inflammasome contributes to the pathogenesis of fatal and perplexing pulmonary diseases. Although pharmacological inhibition of the NLRP3 inflammasome brings potent therapeutic effects in clinical trials and...

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Main Authors: Jian Cui, Meng Yang, Chengli Yu, Haidong Zhang, Yuan Gong, Yang Hu, Yue Wang, Qingxin Yuan, An Pan, Jiepin Li, Yaowen Hu, Zecheng Jin, Xuemei Peng, Anyuan Wu, Junwei Wang, Qian Wang, Yinan Zhang, Lihong Hu
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202411355
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author Jian Cui
Meng Yang
Chengli Yu
Haidong Zhang
Yuan Gong
Yang Hu
Yue Wang
Qingxin Yuan
An Pan
Jiepin Li
Yaowen Hu
Zecheng Jin
Xuemei Peng
Anyuan Wu
Junwei Wang
Qian Wang
Yinan Zhang
Lihong Hu
author_facet Jian Cui
Meng Yang
Chengli Yu
Haidong Zhang
Yuan Gong
Yang Hu
Yue Wang
Qingxin Yuan
An Pan
Jiepin Li
Yaowen Hu
Zecheng Jin
Xuemei Peng
Anyuan Wu
Junwei Wang
Qian Wang
Yinan Zhang
Lihong Hu
author_sort Jian Cui
collection DOAJ
description Abstract Aberrant activation of the NACHT, LRR, and PYD domain‐containing protein 3 (NLRP3) inflammasome contributes to the pathogenesis of fatal and perplexing pulmonary diseases. Although pharmacological inhibition of the NLRP3 inflammasome brings potent therapeutic effects in clinical trials and preclinical models, the molecular chaperones and transition governing its transformation from an auto‐suppressed state to an active oligomer remain controversial. Here, this work shows that sesquiterpene bigelovin inhibited NLRP3 inflammasome activation and downstream pro‐inflammatory cytokines release via canonical, noncanonical, and alternative pathways at nanomolar ranges. Chemoproteomic target identification discloses that bigelovin covalently bound to Cys168 of RACK1, disrupting the interaction between RACK1 and NLRP3 monomer and thereby suppressing NLRP3 inflammasome oligomerization in vitro and in vivo. Bigelovin treatment significantly alleviates the severity of NLRP3‐related pulmonary disorders in murine models, such as LPS‐induced ARDS and silicosis. These results consolidated the intricate role of RACK1 in transiting the NLRP3 state and provided a new anti‐inflammatory lead and therapy for NLRP3‐driven diseases.
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spelling doaj-art-817c72cb997e44e29db4c5241ea88bcd2025-08-20T03:50:58ZengWileyAdvanced Science2198-38442025-07-011227n/an/a10.1002/advs.202411355Inhibition of RACK1‐Mediated NLRP3 Oligomerization (Active Conformation) Ameliorates Acute Respiratory Distress SyndromeJian Cui0Meng Yang1Chengli Yu2Haidong Zhang3Yuan Gong4Yang Hu5Yue Wang6Qingxin Yuan7An Pan8Jiepin Li9Yaowen Hu10Zecheng Jin11Xuemei Peng12Anyuan Wu13Junwei Wang14Qian Wang15Yinan Zhang16Lihong Hu17Jiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaDepartment of Respiratory Medicine Affiliated Hospital of Nanjing University of Chinese Medicine Jiangsu Province Hospital of Chinese Medicine Nanjing Jiangsu 210029 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaDepartment of Respiratory Medicine Affiliated Hospital of Nanjing University of Chinese Medicine Jiangsu Province Hospital of Chinese Medicine Nanjing Jiangsu 210029 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaDepartment of Respiratory Medicine Affiliated Hospital of Nanjing University of Chinese Medicine Jiangsu Province Hospital of Chinese Medicine Nanjing Jiangsu 210029 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaJiangsu Key Laboratory for Functional Substance of Chinese Medicine Stake Key Laboratory Cultivation Base for TCM Quality and Efficacy School of Pharmacy Nanjing University of Chinese Medicine Nanjing 210023 ChinaAbstract Aberrant activation of the NACHT, LRR, and PYD domain‐containing protein 3 (NLRP3) inflammasome contributes to the pathogenesis of fatal and perplexing pulmonary diseases. Although pharmacological inhibition of the NLRP3 inflammasome brings potent therapeutic effects in clinical trials and preclinical models, the molecular chaperones and transition governing its transformation from an auto‐suppressed state to an active oligomer remain controversial. Here, this work shows that sesquiterpene bigelovin inhibited NLRP3 inflammasome activation and downstream pro‐inflammatory cytokines release via canonical, noncanonical, and alternative pathways at nanomolar ranges. Chemoproteomic target identification discloses that bigelovin covalently bound to Cys168 of RACK1, disrupting the interaction between RACK1 and NLRP3 monomer and thereby suppressing NLRP3 inflammasome oligomerization in vitro and in vivo. Bigelovin treatment significantly alleviates the severity of NLRP3‐related pulmonary disorders in murine models, such as LPS‐induced ARDS and silicosis. These results consolidated the intricate role of RACK1 in transiting the NLRP3 state and provided a new anti‐inflammatory lead and therapy for NLRP3‐driven diseases.https://doi.org/10.1002/advs.202411355ARDSbigelovinNLRP3 inflammasomeRACK1
spellingShingle Jian Cui
Meng Yang
Chengli Yu
Haidong Zhang
Yuan Gong
Yang Hu
Yue Wang
Qingxin Yuan
An Pan
Jiepin Li
Yaowen Hu
Zecheng Jin
Xuemei Peng
Anyuan Wu
Junwei Wang
Qian Wang
Yinan Zhang
Lihong Hu
Inhibition of RACK1‐Mediated NLRP3 Oligomerization (Active Conformation) Ameliorates Acute Respiratory Distress Syndrome
Advanced Science
ARDS
bigelovin
NLRP3 inflammasome
RACK1
title Inhibition of RACK1‐Mediated NLRP3 Oligomerization (Active Conformation) Ameliorates Acute Respiratory Distress Syndrome
title_full Inhibition of RACK1‐Mediated NLRP3 Oligomerization (Active Conformation) Ameliorates Acute Respiratory Distress Syndrome
title_fullStr Inhibition of RACK1‐Mediated NLRP3 Oligomerization (Active Conformation) Ameliorates Acute Respiratory Distress Syndrome
title_full_unstemmed Inhibition of RACK1‐Mediated NLRP3 Oligomerization (Active Conformation) Ameliorates Acute Respiratory Distress Syndrome
title_short Inhibition of RACK1‐Mediated NLRP3 Oligomerization (Active Conformation) Ameliorates Acute Respiratory Distress Syndrome
title_sort inhibition of rack1 mediated nlrp3 oligomerization active conformation ameliorates acute respiratory distress syndrome
topic ARDS
bigelovin
NLRP3 inflammasome
RACK1
url https://doi.org/10.1002/advs.202411355
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