Nrf2-induced miR-23a-27a-24-2 cluster modulates damage repair of intestinal mucosa by targeting the Bach1/HO-1 axis in inflammatory bowel diseases
IBD is an idiopathic, chronic autoimmune disease associated with intense oxidative stress. As a master modulator of oxidative stress, Nrf2 has an important anti-inflammatory role in colitis by activating HO-1 transcription. Meanwhile, HO-1 expression is transcriptionally suppressed by Bach1. The Nrf...
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| Published in | Free radical biology & medicine Vol. 163; pp. 1 - 9 |
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| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Elsevier Inc
01.02.2021
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| Abstract | IBD is an idiopathic, chronic autoimmune disease associated with intense oxidative stress. As a master modulator of oxidative stress, Nrf2 has an important anti-inflammatory role in colitis by activating HO-1 transcription. Meanwhile, HO-1 expression is transcriptionally suppressed by Bach1. The Nrf2-activated HO-1 transcription depends on the inactivation of Bach1. However, how Bach1 is inactivated and how Nrf2, Bach1 and HO-1 participate in IBD remains elusive. We found that in response to inflammatory stimuli, Nrf2-induced transcription of miR-23a-27a-24-2 cluster directly inhibits Bach1 expression by binding to the 3′UTR and thereby relieved the Bach1-mediated suppression of HO-1. Besides, elevated miR-23a, miR-27a and miR-24-2 promotes the proliferation and wound healing through regulating Bach1/HO-1 expression in SW480 cell. Additionally, miR-23a, miR-27a and miR-24-2 exert a protective effect on the intestinal mucosa in DSS-induced colitis mouse model. In conclusion, our study revealed that the Nrf2/miR-23a-27a-24-2/Bach1/HO-1 regulatory axis promotes the damage repair of intestinal mucosa during the development of inflammatory bowel diseases.
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•The expression of Nrf2, Bach1 and HO-1 in the inflammatory tissues of IBD colitis.•Nrf2 promotes the transcription of miR-23a-27a-24-2 cluster by targeting the promoter.•miR-23a-27a-24-2 cluster inhibits Bach1 protein by binding to the 3′UTR.•The cluster of miR-23a-27a-24-2 promotes the proliferation and wound healing in LPS-induced SW480 in vitro.•The cluster of miR-23a-27a-24-2 conduces to the intestinal damage repair in vivo. |
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| AbstractList | IBD is an idiopathic, chronic autoimmune disease associated with intense oxidative stress. As a master modulator of oxidative stress, Nrf2 has an important anti-inflammatory role in colitis by activating HO-1 transcription. Meanwhile, HO-1 expression is transcriptionally suppressed by Bach1. The Nrf2-activated HO-1 transcription depends on the inactivation of Bach1. However, how Bach1 is inactivated and how Nrf2, Bach1 and HO-1 participate in IBD remains elusive. We found that in response to inflammatory stimuli, Nrf2-induced transcription of miR-23a-27a-24-2 cluster directly inhibits Bach1 expression by binding to the 3'UTR and thereby relieved the Bach1-mediated suppression of HO-1. Besides, elevated miR-23a, miR-27a and miR-24-2 promotes the proliferation and wound healing through regulating Bach1/HO-1 expression in SW480 cell. Additionally, miR-23a, miR-27a and miR-24-2 exert a protective effect on the intestinal mucosa in DSS-induced colitis mouse model. In conclusion, our study revealed that the Nrf2/miR-23a-27a-24-2/Bach1/HO-1 regulatory axis promotes the damage repair of intestinal mucosa during the development of inflammatory bowel diseases.IBD is an idiopathic, chronic autoimmune disease associated with intense oxidative stress. As a master modulator of oxidative stress, Nrf2 has an important anti-inflammatory role in colitis by activating HO-1 transcription. Meanwhile, HO-1 expression is transcriptionally suppressed by Bach1. The Nrf2-activated HO-1 transcription depends on the inactivation of Bach1. However, how Bach1 is inactivated and how Nrf2, Bach1 and HO-1 participate in IBD remains elusive. We found that in response to inflammatory stimuli, Nrf2-induced transcription of miR-23a-27a-24-2 cluster directly inhibits Bach1 expression by binding to the 3'UTR and thereby relieved the Bach1-mediated suppression of HO-1. Besides, elevated miR-23a, miR-27a and miR-24-2 promotes the proliferation and wound healing through regulating Bach1/HO-1 expression in SW480 cell. Additionally, miR-23a, miR-27a and miR-24-2 exert a protective effect on the intestinal mucosa in DSS-induced colitis mouse model. In conclusion, our study revealed that the Nrf2/miR-23a-27a-24-2/Bach1/HO-1 regulatory axis promotes the damage repair of intestinal mucosa during the development of inflammatory bowel diseases. IBD is an idiopathic, chronic autoimmune disease associated with intense oxidative stress. As a master modulator of oxidative stress, Nrf2 has an important anti-inflammatory role in colitis by activating HO-1 transcription. Meanwhile, HO-1 expression is transcriptionally suppressed by Bach1. The Nrf2-activated HO-1 transcription depends on the inactivation of Bach1. However, how Bach1 is inactivated and how Nrf2, Bach1 and HO-1 participate in IBD remains elusive. We found that in response to inflammatory stimuli, Nrf2-induced transcription of miR-23a-27a-24-2 cluster directly inhibits Bach1 expression by binding to the 3'UTR and thereby relieved the Bach1-mediated suppression of HO-1. Besides, elevated miR-23a, miR-27a and miR-24-2 promotes the proliferation and wound healing through regulating Bach1/HO-1 expression in SW480 cell. Additionally, miR-23a, miR-27a and miR-24-2 exert a protective effect on the intestinal mucosa in DSS-induced colitis mouse model. In conclusion, our study revealed that the Nrf2/miR-23a-27a-24-2/Bach1/HO-1 regulatory axis promotes the damage repair of intestinal mucosa during the development of inflammatory bowel diseases. IBD is an idiopathic, chronic autoimmune disease associated with intense oxidative stress. As a master modulator of oxidative stress, Nrf2 has an important anti-inflammatory role in colitis by activating HO-1 transcription. Meanwhile, HO-1 expression is transcriptionally suppressed by Bach1. The Nrf2-activated HO-1 transcription depends on the inactivation of Bach1. However, how Bach1 is inactivated and how Nrf2, Bach1 and HO-1 participate in IBD remains elusive. We found that in response to inflammatory stimuli, Nrf2-induced transcription of miR-23a-27a-24-2 cluster directly inhibits Bach1 expression by binding to the 3′UTR and thereby relieved the Bach1-mediated suppression of HO-1. Besides, elevated miR-23a, miR-27a and miR-24-2 promotes the proliferation and wound healing through regulating Bach1/HO-1 expression in SW480 cell. Additionally, miR-23a, miR-27a and miR-24-2 exert a protective effect on the intestinal mucosa in DSS-induced colitis mouse model. In conclusion, our study revealed that the Nrf2/miR-23a-27a-24-2/Bach1/HO-1 regulatory axis promotes the damage repair of intestinal mucosa during the development of inflammatory bowel diseases. [Display omitted] •The expression of Nrf2, Bach1 and HO-1 in the inflammatory tissues of IBD colitis.•Nrf2 promotes the transcription of miR-23a-27a-24-2 cluster by targeting the promoter.•miR-23a-27a-24-2 cluster inhibits Bach1 protein by binding to the 3′UTR.•The cluster of miR-23a-27a-24-2 promotes the proliferation and wound healing in LPS-induced SW480 in vitro.•The cluster of miR-23a-27a-24-2 conduces to the intestinal damage repair in vivo. |
| Author | Jinshen Wang Yulin Liu Hao, Jinghua Zhang, Li Dun Su Yongqu Lu Xingfang Wang Wang, Xingwen Ma, Yan |
| Author_xml | – sequence: 1 surname: Dun Su fullname: Dun Su email: sudun19950212@163.com organization: Department of Gastrointestinal Surgery, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China – sequence: 2 givenname: Xingwen surname: Wang fullname: Wang, Xingwen email: 15168886581@163.com organization: Department of Oncology, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China – sequence: 3 givenname: Yan surname: Ma fullname: Ma, Yan organization: Department of Gastrointestinal Surgery, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China – sequence: 4 givenname: Jinghua surname: Hao fullname: Hao, Jinghua organization: Department of Digestive System, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China – sequence: 5 surname: Jinshen Wang fullname: Jinshen Wang organization: Department of Gastrointestinal Surgery, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China – sequence: 6 surname: Yongqu Lu fullname: Yongqu Lu organization: Department of General Surgery, Peking University Third Hospital, Beijing, 100000, China – sequence: 7 surname: Yulin Liu fullname: Yulin Liu organization: Department of Gastrointestinal Surgery, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China – sequence: 8 surname: Xingfang Wang fullname: Xingfang Wang organization: Department of Emergency, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China – sequence: 9 givenname: Li surname: Zhang fullname: Zhang, Li email: Pzzl710318@163.com organization: Department of Gastrointestinal Surgery, Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China |
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| Keywords | TNFα ORF miRNAs IHC CTLs HO-1 IBD WB UC CHIP Nrf2 RT-PCR MAREs IC β-gal AGE CD Bach1 DSS 3′UTR qRT-PCR CT ARE miR-23a-27a-24-2 cluster NK HE |
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| Title | Nrf2-induced miR-23a-27a-24-2 cluster modulates damage repair of intestinal mucosa by targeting the Bach1/HO-1 axis in inflammatory bowel diseases |
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