Inhibition of PU.1 ameliorates metabolic dysfunction and non-alcoholic steatohepatitis.


Journal

Journal of hepatology
ISSN: 1600-0641
Titre abrégé: J Hepatol
Pays: Netherlands
ID NLM: 8503886

Informations de publication

Date de publication:
08 2020
Historique:
received: 19 09 2019
revised: 14 02 2020
accepted: 17 02 2020
pubmed: 7 3 2020
medline: 4 11 2021
entrez: 6 3 2020
Statut: ppublish

Résumé

Obesity is a well-established risk factor for type 2 diabetes (T2D) and non-alcoholic steatohepatitis (NASH), but the underlying mechanisms remain incompletely understood. Herein, we aimed to identify novel pathogenic factors (and possible therapeutic targets) underlying metabolic dysfunction in the liver. We applied a tandem quantitative proteomics strategy to enrich and identify transcription factors (TFs) induced in the obese liver. We used flow cytometry of liver cells to analyze the source of the induced TFs. We employed conditional knockout mice, shRNA, and small-molecule inhibitors to test the metabolic consequences of the induction of identified TFs. Finally, we validated mouse data in patient liver biopsies. We identified PU.1/SPI1, the master hematopoietic regulator, as one of the most upregulated TFs in livers from diet-induced obese (DIO) and genetically obese (db/db) mice. Targeting PU.1 in the whole liver, but not hepatocytes alone, significantly improved glucose homeostasis and suppressed liver inflammation. Consistently, treatment with the PU.1 inhibitor DB1976 markedly reduced inflammation and improved glucose homeostasis and dyslipidemia in DIO mice, and strongly suppressed glucose intolerance, liver steatosis, inflammation, and fibrosis in a dietary NASH mouse model. Furthermore, hepatic PU.1 expression was positively correlated with insulin resistance and inflammation in liver biopsies from patients. These data suggest that the elevated hematopoietic factor PU.1 promotes liver metabolic dysfunction, and may be a useful therapeutic target for obesity, insulin resistance/T2D, and NASH. Expression of the immune regulator PU.1 is increased in livers of obese mice and people. Blocking PU.1 improved glucose homeostasis, and reduced liver steatosis, inflammation and fibrosis in mouse models of non-alcoholic steatohepatitis. Inhibition of PU.1 is thus a potential therapeutic strategy for treating obesity-associated liver dysfunction and metabolic diseases.

Sections du résumé

BACKGROUND & AIMS
Obesity is a well-established risk factor for type 2 diabetes (T2D) and non-alcoholic steatohepatitis (NASH), but the underlying mechanisms remain incompletely understood. Herein, we aimed to identify novel pathogenic factors (and possible therapeutic targets) underlying metabolic dysfunction in the liver.
METHODS
We applied a tandem quantitative proteomics strategy to enrich and identify transcription factors (TFs) induced in the obese liver. We used flow cytometry of liver cells to analyze the source of the induced TFs. We employed conditional knockout mice, shRNA, and small-molecule inhibitors to test the metabolic consequences of the induction of identified TFs. Finally, we validated mouse data in patient liver biopsies.
RESULTS
We identified PU.1/SPI1, the master hematopoietic regulator, as one of the most upregulated TFs in livers from diet-induced obese (DIO) and genetically obese (db/db) mice. Targeting PU.1 in the whole liver, but not hepatocytes alone, significantly improved glucose homeostasis and suppressed liver inflammation. Consistently, treatment with the PU.1 inhibitor DB1976 markedly reduced inflammation and improved glucose homeostasis and dyslipidemia in DIO mice, and strongly suppressed glucose intolerance, liver steatosis, inflammation, and fibrosis in a dietary NASH mouse model. Furthermore, hepatic PU.1 expression was positively correlated with insulin resistance and inflammation in liver biopsies from patients.
CONCLUSIONS
These data suggest that the elevated hematopoietic factor PU.1 promotes liver metabolic dysfunction, and may be a useful therapeutic target for obesity, insulin resistance/T2D, and NASH.
LAY SUMMARY
Expression of the immune regulator PU.1 is increased in livers of obese mice and people. Blocking PU.1 improved glucose homeostasis, and reduced liver steatosis, inflammation and fibrosis in mouse models of non-alcoholic steatohepatitis. Inhibition of PU.1 is thus a potential therapeutic strategy for treating obesity-associated liver dysfunction and metabolic diseases.

Identifiants

pubmed: 32135178
pii: S0168-8278(20)30124-0
doi: 10.1016/j.jhep.2020.02.025
pii:
doi:

Substances chimiques

Proto-Oncogene Proteins 0
RNA, Small Interfering 0
Trans-Activators 0
Transcription Factors 0
proto-oncogene protein Spi-1 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

361-370

Informations de copyright

Copyright © 2020 European Association for the Study of the Liver. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Conflict of interest The authors declare no conflicts of interest that pertain to this work. Please refer to the accompanying ICMJE disclosure forms for further details.

Auteurs

Qiongming Liu (Q)

Naomi Berrie Diabetes Center, Department of Pathology and Cell Biology, College of Physicians and Surgeons, Columbia University, New York, 10032, USA; State Key Laboratory of Proteomics, Beijing Proteome Research Center, Beijing Institute of Lifeomics, National Center for Protein Sciences (The PHOENIX Center at Beijing), Beijing 102206, China.

Junjie Yu (J)

Naomi Berrie Diabetes Center, Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, New York, 10032, USA.

Liheng Wang (L)

Naomi Berrie Diabetes Center, Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, New York, 10032, USA.

Yuliang Tang (Y)

Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, Department of Chemical Biology, College of Chemistry and Molecular Engineering, Synthetic and Functional Biomolecules Center, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871, China.

Quan Zhou (Q)

State Key Laboratory of Proteomics, Beijing Proteome Research Center, Beijing Institute of Lifeomics, National Center for Protein Sciences (The PHOENIX Center at Beijing), Beijing 102206, China.

Shuhui Ji (S)

State Key Laboratory of Proteomics, Beijing Proteome Research Center, Beijing Institute of Lifeomics, National Center for Protein Sciences (The PHOENIX Center at Beijing), Beijing 102206, China.

Yi Wang (Y)

Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas, 77030, USA.

Luis Santos (L)

Diabetes, Obesity, and Metabolism Institute, Icahn School of Medicine at Mount Sinai, New York, United States.

Rebecca A Haeusler (RA)

Naomi Berrie Diabetes Center, Department of Pathology and Cell Biology, College of Physicians and Surgeons, Columbia University, New York, 10032, USA.

Jianwen Que (J)

Columbia Center for Human Development and Department of Medicine, Columbia University, New York, NY 10032.

Prashant Rajbhandari (P)

Diabetes, Obesity, and Metabolism Institute, Icahn School of Medicine at Mount Sinai, New York, United States.

Xiaoguang Lei (X)

Beijing National Laboratory for Molecular Sciences, Key Laboratory of Bioorganic Chemistry and Molecular Engineering of Ministry of Education, Department of Chemical Biology, College of Chemistry and Molecular Engineering, Synthetic and Functional Biomolecules Center, Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871, China.

Luca Valenti (L)

Department of Pathophysiology and Transplantation, Università degli Studi Milano, and Internal Medicine and Metabolic Diseases, Fondazione IRCCS Ca' Granda Ospedale Policlinico, Milan, Italy.

Utpal B Pajvani (UB)

Naomi Berrie Diabetes Center, Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, New York, 10032, USA. Electronic address: up2104@cumc.columbia.edu.

Jun Qin (J)

State Key Laboratory of Proteomics, Beijing Proteome Research Center, Beijing Institute of Lifeomics, National Center for Protein Sciences (The PHOENIX Center at Beijing), Beijing 102206, China; Department of Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas, 77030, USA. Electronic address: jqin@bcm.edu.

Li Qiang (L)

Naomi Berrie Diabetes Center, Department of Pathology and Cell Biology, College of Physicians and Surgeons, Columbia University, New York, 10032, USA. Electronic address: LQ2123@cumc.columbia.edu.

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