ACSS2‐Mediated Histone H4 Lysine 12 Crotonylation (H4K12cr) Alleviates Colitis via Enhancing Transcription of CLDN7

Abstract Histone lysine crotonylation (Kcr), a highly conserved posttranslational modification, plays critical roles in various biological processes. Nevertheless, the dynamic alterations and functions of histone Kcr in inflammatory bowel disease (IBD) remain poorly explored. Herein, a notable decre...

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Main Authors: Ming Yuan, Shaopeng Chen, Zhensen Lin, Runfeng Yu, Kang Chao, Shubiao Ye, Qing Li, Haoxian Ke, Chi Zhang, Junfeng Huang, Guanzhan Liang, Tuo Hu, Xiang Gao, Ping Lan, Xianrui Wu
Format: Article
Language:English
Published: Wiley 2025-08-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202500461
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author Ming Yuan
Shaopeng Chen
Zhensen Lin
Runfeng Yu
Kang Chao
Shubiao Ye
Qing Li
Haoxian Ke
Chi Zhang
Junfeng Huang
Guanzhan Liang
Tuo Hu
Xiang Gao
Ping Lan
Xianrui Wu
author_facet Ming Yuan
Shaopeng Chen
Zhensen Lin
Runfeng Yu
Kang Chao
Shubiao Ye
Qing Li
Haoxian Ke
Chi Zhang
Junfeng Huang
Guanzhan Liang
Tuo Hu
Xiang Gao
Ping Lan
Xianrui Wu
author_sort Ming Yuan
collection DOAJ
description Abstract Histone lysine crotonylation (Kcr), a highly conserved posttranslational modification, plays critical roles in various biological processes. Nevertheless, the dynamic alterations and functions of histone Kcr in inflammatory bowel disease (IBD) remain poorly explored. Herein, a notable decrease of both Pan‐Kcr and ACSS2 (acyl‐CoA synthetase short‐chain family member 2), the key enzyme for crotonyl‐CoA generation, is revealed in inflamed intestinal epithelial cells. Genetic or pharmacological inhibition of ACSS2 dramatically impairs mouse intestinal barrier integrity and exacerbates colitis. Mechanistically, ACSS2‐mediated histone H4 lysine 12 crotonylation (H4K12cr) upregulates CLDN7 expression to fortify intestinal epithelial barrier, which can be augmented by crotonate supplementation. Furthermore, tumor necrosis factor‐α (TNF‐α) is revealed to enhance the m6A modification of ACSS2 mRNA, consequently destabilizing and downregulating ACSS2. Combinational therapy involving anti‐TNF‐α and crotonate can significantly ameliorate colitis. Overall, ACSS2‐mediated H4K12cr emerges as a pivotal modulator governing intestinal barrier function during IBD progression.
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institution Kabale University
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spelling doaj-art-d6f7cbf88aed437e9e886963d9376a1a2025-08-20T11:56:11ZengWileyAdvanced Science2198-38442025-08-011230n/an/a10.1002/advs.202500461ACSS2‐Mediated Histone H4 Lysine 12 Crotonylation (H4K12cr) Alleviates Colitis via Enhancing Transcription of CLDN7Ming Yuan0Shaopeng Chen1Zhensen Lin2Runfeng Yu3Kang Chao4Shubiao Ye5Qing Li6Haoxian Ke7Chi Zhang8Junfeng Huang9Guanzhan Liang10Tuo Hu11Xiang Gao12Ping Lan13Xianrui Wu14Department of General Surgery (Colorectal Surgery) The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaDepartment of General Surgery (Colorectal Surgery) The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaDepartment of General Surgery (Colorectal Surgery) The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaDepartment of General Surgery (Colorectal Surgery) The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaGuangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaDepartment of General Surgery (Colorectal Surgery) The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaGuangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaDepartment of Gastrointestinal Surgery Sun Yat‐sen Memorial Hospital Sun Yat‐sen University Guangzhou Guangdong 510288 ChinaDepartment of General Surgery (Colorectal Surgery) The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaDepartment of Gastrointestinal Surgery Sun Yat‐sen Memorial Hospital Sun Yat‐sen University Guangzhou Guangdong 510288 ChinaDepartment of General Surgery (Colorectal Surgery) The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaDepartment of General Surgery (Colorectal Surgery) The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaGuangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaDepartment of General Surgery (Colorectal Surgery) The Sixth Affiliated Hospital Sun Yat‐sen University Guangzhou Guangdong 510655 ChinaDepartment of Gastrointestinal Surgery Sun Yat‐sen Memorial Hospital Sun Yat‐sen University Guangzhou Guangdong 510288 ChinaAbstract Histone lysine crotonylation (Kcr), a highly conserved posttranslational modification, plays critical roles in various biological processes. Nevertheless, the dynamic alterations and functions of histone Kcr in inflammatory bowel disease (IBD) remain poorly explored. Herein, a notable decrease of both Pan‐Kcr and ACSS2 (acyl‐CoA synthetase short‐chain family member 2), the key enzyme for crotonyl‐CoA generation, is revealed in inflamed intestinal epithelial cells. Genetic or pharmacological inhibition of ACSS2 dramatically impairs mouse intestinal barrier integrity and exacerbates colitis. Mechanistically, ACSS2‐mediated histone H4 lysine 12 crotonylation (H4K12cr) upregulates CLDN7 expression to fortify intestinal epithelial barrier, which can be augmented by crotonate supplementation. Furthermore, tumor necrosis factor‐α (TNF‐α) is revealed to enhance the m6A modification of ACSS2 mRNA, consequently destabilizing and downregulating ACSS2. Combinational therapy involving anti‐TNF‐α and crotonate can significantly ameliorate colitis. Overall, ACSS2‐mediated H4K12cr emerges as a pivotal modulator governing intestinal barrier function during IBD progression.https://doi.org/10.1002/advs.202500461ACSS2inflammatory bowel diseaseintestinal barrierhistone lysine crotonylation
spellingShingle Ming Yuan
Shaopeng Chen
Zhensen Lin
Runfeng Yu
Kang Chao
Shubiao Ye
Qing Li
Haoxian Ke
Chi Zhang
Junfeng Huang
Guanzhan Liang
Tuo Hu
Xiang Gao
Ping Lan
Xianrui Wu
ACSS2‐Mediated Histone H4 Lysine 12 Crotonylation (H4K12cr) Alleviates Colitis via Enhancing Transcription of CLDN7
Advanced Science
ACSS2
inflammatory bowel disease
intestinal barrier
histone lysine crotonylation
title ACSS2‐Mediated Histone H4 Lysine 12 Crotonylation (H4K12cr) Alleviates Colitis via Enhancing Transcription of CLDN7
title_full ACSS2‐Mediated Histone H4 Lysine 12 Crotonylation (H4K12cr) Alleviates Colitis via Enhancing Transcription of CLDN7
title_fullStr ACSS2‐Mediated Histone H4 Lysine 12 Crotonylation (H4K12cr) Alleviates Colitis via Enhancing Transcription of CLDN7
title_full_unstemmed ACSS2‐Mediated Histone H4 Lysine 12 Crotonylation (H4K12cr) Alleviates Colitis via Enhancing Transcription of CLDN7
title_short ACSS2‐Mediated Histone H4 Lysine 12 Crotonylation (H4K12cr) Alleviates Colitis via Enhancing Transcription of CLDN7
title_sort acss2 mediated histone h4 lysine 12 crotonylation h4k12cr alleviates colitis via enhancing transcription of cldn7
topic ACSS2
inflammatory bowel disease
intestinal barrier
histone lysine crotonylation
url https://doi.org/10.1002/advs.202500461
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