Modulation of TNF‐α mRNA stability by human antigen R and miR181s in sepsis‐induced immunoparalysis

Abstract Immunoparalysis is an important pathological mechanism in sepsis. However, an effective small molecule therapy is lacking. Here, we show that ouabain, a Na+,K+‐ATPase ligand, can reverse immunoparalysis in vitro, in vivo, and in clinical samples. Notably, the effect of ouabain was criticall...

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Main Authors: Cao Dan, Bian Jinjun, Hua Zi‐Chun, Ma Lin, Chen Wei, Zhang Xu, Zhou Ri, Cheng Shun, Sun Wen‐Zhu, Jiao Qing‐Cai, Yin Wu
Format: Article
Language:English
Published: Springer Nature 2014-12-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.201404797
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author Cao Dan
Bian Jinjun
Hua Zi‐Chun
Ma Lin
Chen Wei
Zhang Xu
Zhou Ri
Cheng Shun
Sun Wen‐Zhu
Jiao Qing‐Cai
Yin Wu
author_facet Cao Dan
Bian Jinjun
Hua Zi‐Chun
Ma Lin
Chen Wei
Zhang Xu
Zhou Ri
Cheng Shun
Sun Wen‐Zhu
Jiao Qing‐Cai
Yin Wu
author_sort Cao Dan
collection DOAJ
description Abstract Immunoparalysis is an important pathological mechanism in sepsis. However, an effective small molecule therapy is lacking. Here, we show that ouabain, a Na+,K+‐ATPase ligand, can reverse immunoparalysis in vitro, in vivo, and in clinical samples. Notably, the effect of ouabain was critically dependent on TNF‐α expression. However, ouabain had opposing effects on the stability of TNF‐α mRNA: Ouabain triggered miR‐181 transcription, which promoted TNF‐α mRNA degradation and induced immunoparalysis, and ouabain triggered the nuclear export of human antigen R (HuR), which stabilized TNF‐α mRNA and suppressed immuno‐paralysis. Interestingly, because the miR‐181 binding site is located within the HuR binding site in the 3′‐untranslated region of TNF‐α, in ouabain‐treated cells, HuR competed with miR‐181 for binding to TNF‐α mRNA and recruited TNF‐α mRNA to stress granules, thereby stabilizing TNF‐α mRNA and reversing immunoparalysis. Ouabain also induced GM‐CSF and interferon‐γ expression in a HuR‐dependent manner. Hence, the fine‐tuning of TNF‐α mRNA stability by HuR and miR181 plays a crucial role in immunoparalysis, and Na+,K+‐ATPase ligands are promising agents for immunoparalysis therapy.
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spelling doaj-art-cbc0c8aff9524431ae27ac1e86b40f972025-08-20T03:06:01ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842014-12-017214015710.15252/emmm.201404797Modulation of TNF‐α mRNA stability by human antigen R and miR181s in sepsis‐induced immunoparalysisCao Dan0Bian Jinjun1Hua Zi‐Chun2Ma Lin3Chen Wei4Zhang Xu5Zhou Ri6Cheng Shun7Sun Wen‐Zhu8Jiao Qing‐Cai9Yin Wu10The State Key Lab of Pharmaceutical Biotechnology, College of life Sciences, Nanjing UniversityDepartment of Anesthesiology and Intensive Care Unit, Changhai Hospital, Affiliated Hospital of the Second Military Medical UniversityThe State Key Lab of Pharmaceutical Biotechnology, College of life Sciences, Nanjing UniversityThe State Key Lab of Pharmaceutical Biotechnology, College of life Sciences, Nanjing UniversityThe State Key Lab of Pharmaceutical Biotechnology, College of life Sciences, Nanjing UniversityDepartment of Anesthesiology and Intensive Care Unit, Changhai Hospital, Affiliated Hospital of the Second Military Medical UniversityThe State Key Lab of Pharmaceutical Biotechnology, College of life Sciences, Nanjing UniversityThe State Key Lab of Pharmaceutical Biotechnology, College of life Sciences, Nanjing UniversityThe State Key Lab of Pharmaceutical Biotechnology, College of life Sciences, Nanjing UniversityThe State Key Lab of Pharmaceutical Biotechnology, College of life Sciences, Nanjing UniversityThe State Key Lab of Pharmaceutical Biotechnology, College of life Sciences, Nanjing UniversityAbstract Immunoparalysis is an important pathological mechanism in sepsis. However, an effective small molecule therapy is lacking. Here, we show that ouabain, a Na+,K+‐ATPase ligand, can reverse immunoparalysis in vitro, in vivo, and in clinical samples. Notably, the effect of ouabain was critically dependent on TNF‐α expression. However, ouabain had opposing effects on the stability of TNF‐α mRNA: Ouabain triggered miR‐181 transcription, which promoted TNF‐α mRNA degradation and induced immunoparalysis, and ouabain triggered the nuclear export of human antigen R (HuR), which stabilized TNF‐α mRNA and suppressed immuno‐paralysis. Interestingly, because the miR‐181 binding site is located within the HuR binding site in the 3′‐untranslated region of TNF‐α, in ouabain‐treated cells, HuR competed with miR‐181 for binding to TNF‐α mRNA and recruited TNF‐α mRNA to stress granules, thereby stabilizing TNF‐α mRNA and reversing immunoparalysis. Ouabain also induced GM‐CSF and interferon‐γ expression in a HuR‐dependent manner. Hence, the fine‐tuning of TNF‐α mRNA stability by HuR and miR181 plays a crucial role in immunoparalysis, and Na+,K+‐ATPase ligands are promising agents for immunoparalysis therapy.https://doi.org/10.15252/emmm.201404797human antigen RimmunoparalysismicroRNA181ouabaintumor necrosis factor α
spellingShingle Cao Dan
Bian Jinjun
Hua Zi‐Chun
Ma Lin
Chen Wei
Zhang Xu
Zhou Ri
Cheng Shun
Sun Wen‐Zhu
Jiao Qing‐Cai
Yin Wu
Modulation of TNF‐α mRNA stability by human antigen R and miR181s in sepsis‐induced immunoparalysis
EMBO Molecular Medicine
human antigen R
immunoparalysis
microRNA181
ouabain
tumor necrosis factor α
title Modulation of TNF‐α mRNA stability by human antigen R and miR181s in sepsis‐induced immunoparalysis
title_full Modulation of TNF‐α mRNA stability by human antigen R and miR181s in sepsis‐induced immunoparalysis
title_fullStr Modulation of TNF‐α mRNA stability by human antigen R and miR181s in sepsis‐induced immunoparalysis
title_full_unstemmed Modulation of TNF‐α mRNA stability by human antigen R and miR181s in sepsis‐induced immunoparalysis
title_short Modulation of TNF‐α mRNA stability by human antigen R and miR181s in sepsis‐induced immunoparalysis
title_sort modulation of tnf α mrna stability by human antigen r and mir181s in sepsis induced immunoparalysis
topic human antigen R
immunoparalysis
microRNA181
ouabain
tumor necrosis factor α
url https://doi.org/10.15252/emmm.201404797
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