STING expression in monocyte-derived macrophages is associated with the progression of liver inflammation and fibrosis in patients with nonalcoholic fatty liver disease

The stimulator of interferon genes (STING) in macrophages plays a crucial role in nonalcoholic fatty liver disease (NAFLD) progression. However, there is a lack of evidence from large samples of patients to validate a deleterious role for STING in NAFLD. Moreover, sources of STING-expressing cells t...

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Bibliographic Details
Published inLaboratory investigation Vol. 100; no. 4; pp. 542 - 552
Main Authors Wang, Xiaoxiao, Rao, Huiying, Zhao, Jingmin, Wee, Aileen, Li, Xiaohe, Fei, Ran, Huang, Rui, Wu, Chaodong, Liu, Feng, Wei, Lai
Format Journal Article
LanguageEnglish
Published New York Elsevier Inc 01.04.2020
Nature Publishing Group US
Nature Publishing Group
Subjects
13
13/51
14
14/63
692/699/1503/1607/2750
692/699/1503/1607/2751
Adult
Aged
CCR2 protein
CD163 antigen
Cell activation
Collagen (type I)
Correlation analysis
Disease Progression
Fatty liver
Female
Fibrosis
Gene expression
Genes
Hepatitis - metabolism
Hepatocytes
Humans
Inflammation
Interferon
Interleukin 1
Interleukin 6
Kupffer cells
Laboratory Medicine
Liver
Liver - metabolism
Liver - pathology
Liver Cirrhosis - metabolism
Liver diseases
Macrophages
Macrophages - metabolism
Male
Medicine
Medicine & Public Health
Membrane Proteins - analysis
Membrane Proteins - metabolism
Middle Aged
Monocyte chemoattractant protein 1
Monocytes
Non-alcoholic Fatty Liver Disease - metabolism
Non-alcoholic Fatty Liver Disease - pathology
Pathology
Signal transduction
Stimulators
Transforming growth factor-b1
Young Adult
Online AccessGet full text
ISSN0023-6837
1530-0307
1530-0307
DOI10.1038/s41374-019-0342-6

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Abstract The stimulator of interferon genes (STING) in macrophages plays a crucial role in nonalcoholic fatty liver disease (NAFLD) progression. However, there is a lack of evidence from large samples of patients to validate a deleterious role for STING in NAFLD. Moreover, sources of STING-expressing cells that are related to NAFLD remain to be definitively characterized. To investigate STING expression and explore its correlation with NAFLD progression in human subjects, our study involved liver samples from 98 NAFLD subjects and 8 controls. STING and p-TBK1 expression in nonparenchymal liver cells was analyzed and correlated with NAFLD pathological features. Numbers of STING+ cells were increased in livers from nonalcoholic steatohepatitis (NASH) patients compared with controls, especially in the liver portal tract of NASH patients with fibrosis (p < 0.05). Moreover, numbers of STING+ cells in livers of NASH patients were increased with aggravation of inflammation grade and fibrosis stage (p < 0.05). STING was mainly expressed in macrophages, including monocyte-derived macrophages (CCR2+, S100A9+), Kupffer cells (CD68+) and CD163+ macrophages. Compared with controls, numbers of STING+/CCR2+ and STING+/S100A9+ cells were significantly increased in livers from NASH patients with fibrosis and positively correlated with liver inflammation grade and fibrosis stage (p < 0.05). However, numbers of STING+/CD68+ and STING+/CD163+ cells were significantly increased in livers from NASH patients with advanced fibrosis and correlated only with aggravation of fibrosis stage (p < 0.05). Furthermore, compared with controls, NASH patients exhibited significantly increased STING+/p-TBK1+ cell numbers. In a coculture system, the amount of p-TBK1 and the mRNAs of IL1β and IL6 in THP1 macrophages, as well as the amount of α-SMA and the mRNAs of Col1a1, Fn and TGFβ1 in LX2 cells were significantly increased upon STING activation in macrophages (p < 0.05). Therefore, increased STING expression in MoMFs appears to be indicative of NAFLD progression, and STING could be a new target for NAFLD therapy.
AbstractList The stimulator of interferon genes (STING) in macrophages plays a crucial role in nonalcoholic fatty liver disease (NAFLD) progression. However, there is a lack of evidence from large samples of patients to validate a deleterious role for STING in NAFLD. Moreover, sources of STING-expressing cells that are related to NAFLD remain to be definitively characterized. To investigate STING expression and explore its correlation with NAFLD progression in human subjects, our study involved liver samples from 98 NAFLD subjects and 8 controls. STING and p-TBK1 expression in nonparenchymal liver cells was analyzed and correlated with NAFLD pathological features. Numbers of STING+ cells were increased in livers from nonalcoholic steatohepatitis (NASH) patients compared with controls, especially in the liver portal tract of NASH patients with fibrosis (p < 0.05). Moreover, numbers of STING+ cells in livers of NASH patients were increased with aggravation of inflammation grade and fibrosis stage (p < 0.05). STING was mainly expressed in macrophages, including monocyte-derived macrophages (CCR2+, S100A9+), Kupffer cells (CD68+) and CD163+ macrophages. Compared with controls, numbers of STING+/CCR2+ and STING+/S100A9+ cells were significantly increased in livers from NASH patients with fibrosis and positively correlated with liver inflammation grade and fibrosis stage (p < 0.05). However, numbers of STING+/CD68+ and STING+/CD163+ cells were significantly increased in livers from NASH patients with advanced fibrosis and correlated only with aggravation of fibrosis stage (p < 0.05). Furthermore, compared with controls, NASH patients exhibited significantly increased STING+/p-TBK1+ cell numbers. In a coculture system, the amount of p-TBK1 and the mRNAs of IL1β and IL6 in THP1 macrophages, as well as the amount of α-SMA and the mRNAs of Col1a1, Fn and TGFβ1 in LX2 cells were significantly increased upon STING activation in macrophages (p < 0.05). Therefore, increased STING expression in MoMFs appears to be indicative of NAFLD progression, and STING could be a new target for NAFLD therapy.The expression of the stimulator of interferon genes (STING) in liver tissues is associated with the progression of human nonalcoholic fatty liver disease. Specifically, STING-expressing macrophages, in particular, monocyte-derived macrophages, are positively correlated with the degree of liver inflammation and/or fibrosis progression, which appeared to be mediated by the activation of the STING-TBK1 signaling pathway in macrophage.
The stimulator of interferon genes (STING) in macrophages plays a crucial role in nonalcoholic fatty liver disease (NAFLD) progression. However, there is a lack of evidence from large samples of patients to validate a deleterious role for STING in NAFLD. Moreover, sources of STING-expressing cells that are related to NAFLD remain to be definitively characterized. To investigate STING expression and explore its correlation with NAFLD progression in human subjects, our study involved liver samples from 98 NAFLD subjects and 8 controls. STING and p-TBK1 expression in nonparenchymal liver cells was analyzed and correlated with NAFLD pathological features. Numbers of STING + cells were increased in livers from nonalcoholic steatohepatitis (NASH) patients compared with controls, especially in the liver portal tract of NASH patients with fibrosis ( p  < 0.05). Moreover, numbers of STING + cells in livers of NASH patients were increased with aggravation of inflammation grade and fibrosis stage ( p  < 0.05). STING was mainly expressed in macrophages, including monocyte-derived macrophages (CCR2 + , S100A9 + ), Kupffer cells (CD68 + ) and CD163 + macrophages. Compared with controls, numbers of STING + /CCR2 + and STING + /S100A9 + cells were significantly increased in livers from NASH patients with fibrosis and positively correlated with liver inflammation grade and fibrosis stage ( p  < 0.05). However, numbers of STING + /CD68 + and STING + /CD163 + cells were significantly increased in livers from NASH patients with advanced fibrosis and correlated only with aggravation of fibrosis stage ( p  < 0.05). Furthermore, compared with controls, NASH patients exhibited significantly increased STING + /p-TBK1 + cell numbers. In a coculture system, the amount of p-TBK1 and the mRNAs of IL1β and IL6 in THP1 macrophages, as well as the amount of α-SMA and the mRNAs of Col1a1, Fn and TGFβ1 in LX2 cells were significantly increased upon STING activation in macrophages ( p  < 0.05). Therefore, increased STING expression in MoMFs appears to be indicative of NAFLD progression, and STING could be a new target for NAFLD therapy. The expression of the stimulator of interferon genes (STING) in liver tissues is associated with the progression of human nonalcoholic fatty liver disease. Specifically, STING-expressing macrophages, in particular, monocyte-derived macrophages, are positively correlated with the degree of liver inflammation and/or fibrosis progression, which appeared to be mediated by the activation of the STING-TBK1 signaling pathway in macrophage.
The stimulator of interferon genes (STING) in macrophages plays a crucial role in nonalcoholic fatty liver disease (NAFLD) progression. However, there is a lack of evidence from large samples of patients to validate a deleterious role for STING in NAFLD. Moreover, sources of STING-expressing cells that are related to NAFLD remain to be definitively characterized. To investigate STING expression and explore its correlation with NAFLD progression in human subjects, our study involved liver samples from 98 NAFLD subjects and 8 controls. STING and p-TBK1 expression in nonparenchymal liver cells was analyzed and correlated with NAFLD pathological features. Numbers of STING cells were increased in livers from nonalcoholic steatohepatitis (NASH) patients compared with controls, especially in the liver portal tract of NASH patients with fibrosis (p < 0.05). Moreover, numbers of STING cells in livers of NASH patients were increased with aggravation of inflammation grade and fibrosis stage (p < 0.05). STING was mainly expressed in macrophages, including monocyte-derived macrophages (CCR2 , S100A9 ), Kupffer cells (CD68 ) and CD163 macrophages. Compared with controls, numbers of STING /CCR2 and STING /S100A9 cells were significantly increased in livers from NASH patients with fibrosis and positively correlated with liver inflammation grade and fibrosis stage (p < 0.05). However, numbers of STING /CD68 and STING /CD163 cells were significantly increased in livers from NASH patients with advanced fibrosis and correlated only with aggravation of fibrosis stage (p < 0.05). Furthermore, compared with controls, NASH patients exhibited significantly increased STING /p-TBK1 cell numbers. In a coculture system, the amount of p-TBK1 and the mRNAs of IL1β and IL6 in THP1 macrophages, as well as the amount of α-SMA and the mRNAs of Col1a1, Fn and TGFβ1 in LX2 cells were significantly increased upon STING activation in macrophages (p < 0.05). Therefore, increased STING expression in MoMFs appears to be indicative of NAFLD progression, and STING could be a new target for NAFLD therapy.
The stimulator of interferon genes (STING) in macrophages plays a crucial role in nonalcoholic fatty liver disease (NAFLD) progression. However, there is a lack of evidence from large samples of patients to validate a deleterious role for STING in NAFLD. Moreover, sources of STING-expressing cells that are related to NAFLD remain to be definitively characterized. To investigate STING expression and explore its correlation with NAFLD progression in human subjects, our study involved liver samples from 98 NAFLD subjects and 8 controls. STING and p-TBK1 expression in nonparenchymal liver cells was analyzed and correlated with NAFLD pathological features. Numbers of STING+ cells were increased in livers from nonalcoholic steatohepatitis (NASH) patients compared with controls, especially in the liver portal tract of NASH patients with fibrosis (p < 0.05). Moreover, numbers of STING+ cells in livers of NASH patients were increased with aggravation of inflammation grade and fibrosis stage (p < 0.05). STING was mainly expressed in macrophages, including monocyte-derived macrophages (CCR2+, S100A9+), Kupffer cells (CD68+) and CD163+ macrophages. Compared with controls, numbers of STING+/CCR2+ and STING+/S100A9+ cells were significantly increased in livers from NASH patients with fibrosis and positively correlated with liver inflammation grade and fibrosis stage (p < 0.05). However, numbers of STING+/CD68+ and STING+/CD163+ cells were significantly increased in livers from NASH patients with advanced fibrosis and correlated only with aggravation of fibrosis stage (p < 0.05). Furthermore, compared with controls, NASH patients exhibited significantly increased STING+/p-TBK1+ cell numbers. In a coculture system, the amount of p-TBK1 and the mRNAs of IL1β and IL6 in THP1 macrophages, as well as the amount of α-SMA and the mRNAs of Col1a1, Fn and TGFβ1 in LX2 cells were significantly increased upon STING activation in macrophages (p < 0.05). Therefore, increased STING expression in MoMFs appears to be indicative of NAFLD progression, and STING could be a new target for NAFLD therapy.
The stimulator of interferon genes (STING) in macrophages plays a crucial role in nonalcoholic fatty liver disease (NAFLD) progression. However, there is a lack of evidence from large samples of patients to validate a deleterious role for STING in NAFLD. Moreover, sources of STING-expressing cells that are related to NAFLD remain to be definitively characterized. To investigate STING expression and explore its correlation with NAFLD progression in human subjects, our study involved liver samples from 98 NAFLD subjects and 8 controls. STING and p-TBK1 expression in nonparenchymal liver cells was analyzed and correlated with NAFLD pathological features. Numbers of STING+ cells were increased in livers from nonalcoholic steatohepatitis (NASH) patients compared with controls, especially in the liver portal tract of NASH patients with fibrosis (p < 0.05). Moreover, numbers of STING+ cells in livers of NASH patients were increased with aggravation of inflammation grade and fibrosis stage (p < 0.05). STING was mainly expressed in macrophages, including monocyte-derived macrophages (CCR2+, S100A9+), Kupffer cells (CD68+) and CD163+ macrophages. Compared with controls, numbers of STING+/CCR2+ and STING+/S100A9+ cells were significantly increased in livers from NASH patients with fibrosis and positively correlated with liver inflammation grade and fibrosis stage (p < 0.05). However, numbers of STING+/CD68+ and STING+/CD163+ cells were significantly increased in livers from NASH patients with advanced fibrosis and correlated only with aggravation of fibrosis stage (p < 0.05). Furthermore, compared with controls, NASH patients exhibited significantly increased STING+/p-TBK1+ cell numbers. In a coculture system, the amount of p-TBK1 and the mRNAs of IL1β and IL6 in THP1 macrophages, as well as the amount of α-SMA and the mRNAs of Col1a1, Fn and TGFβ1 in LX2 cells were significantly increased upon STING activation in macrophages (p < 0.05). Therefore, increased STING expression in MoMFs appears to be indicative of NAFLD progression, and STING could be a new target for NAFLD therapy.The stimulator of interferon genes (STING) in macrophages plays a crucial role in nonalcoholic fatty liver disease (NAFLD) progression. However, there is a lack of evidence from large samples of patients to validate a deleterious role for STING in NAFLD. Moreover, sources of STING-expressing cells that are related to NAFLD remain to be definitively characterized. To investigate STING expression and explore its correlation with NAFLD progression in human subjects, our study involved liver samples from 98 NAFLD subjects and 8 controls. STING and p-TBK1 expression in nonparenchymal liver cells was analyzed and correlated with NAFLD pathological features. Numbers of STING+ cells were increased in livers from nonalcoholic steatohepatitis (NASH) patients compared with controls, especially in the liver portal tract of NASH patients with fibrosis (p < 0.05). Moreover, numbers of STING+ cells in livers of NASH patients were increased with aggravation of inflammation grade and fibrosis stage (p < 0.05). STING was mainly expressed in macrophages, including monocyte-derived macrophages (CCR2+, S100A9+), Kupffer cells (CD68+) and CD163+ macrophages. Compared with controls, numbers of STING+/CCR2+ and STING+/S100A9+ cells were significantly increased in livers from NASH patients with fibrosis and positively correlated with liver inflammation grade and fibrosis stage (p < 0.05). However, numbers of STING+/CD68+ and STING+/CD163+ cells were significantly increased in livers from NASH patients with advanced fibrosis and correlated only with aggravation of fibrosis stage (p < 0.05). Furthermore, compared with controls, NASH patients exhibited significantly increased STING+/p-TBK1+ cell numbers. In a coculture system, the amount of p-TBK1 and the mRNAs of IL1β and IL6 in THP1 macrophages, as well as the amount of α-SMA and the mRNAs of Col1a1, Fn and TGFβ1 in LX2 cells were significantly increased upon STING activation in macrophages (p < 0.05). Therefore, increased STING expression in MoMFs appears to be indicative of NAFLD progression, and STING could be a new target for NAFLD therapy.
Author Fei, Ran
Wei, Lai
Wu, Chaodong
Rao, Huiying
Zhao, Jingmin
Wee, Aileen
Li, Xiaohe
Huang, Rui
Liu, Feng
Wang, Xiaoxiao
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  surname: Wang
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  organization: Peking University People's Hospital, Peking University Hepatology Institute, Beijing Key Laboratory of Hepatitis C and Immunotherapy for Liver Diseases, 100044, Beijing, China
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  givenname: Huiying
  surname: Rao
  fullname: Rao, Huiying
  organization: Peking University People's Hospital, Peking University Hepatology Institute, Beijing Key Laboratory of Hepatitis C and Immunotherapy for Liver Diseases, 100044, Beijing, China
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  givenname: Jingmin
  surname: Zhao
  fullname: Zhao, Jingmin
  organization: Department of Pathology, The Fifth Medical Center of PLA General Hospital, 100039, Beijing, China
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  surname: Wee
  fullname: Wee, Aileen
  organization: Department of Pathology, Yong Loo Lin School of Medicine, National University of Singapore, National University Hospital, 5 Lower Kent Ridge Road, 119074, Singapore, Singapore
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  givenname: Ran
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  organization: Peking University People's Hospital, Peking University Hepatology Institute, Beijing Key Laboratory of Hepatitis C and Immunotherapy for Liver Diseases, 100044, Beijing, China
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  givenname: Rui
  surname: Huang
  fullname: Huang, Rui
  organization: Peking University People's Hospital, Peking University Hepatology Institute, Beijing Key Laboratory of Hepatitis C and Immunotherapy for Liver Diseases, 100044, Beijing, China
– sequence: 8
  givenname: Chaodong
  surname: Wu
  fullname: Wu, Chaodong
  organization: Department of Nutrition and Food Science, Texas A&M University, 77843, College Station, TX, USA
– sequence: 9
  givenname: Feng
  surname: Liu
  fullname: Liu, Feng
  email: liu1116m@sina.com
  organization: Peking University People's Hospital, Peking University Hepatology Institute, Beijing Key Laboratory of Hepatitis C and Immunotherapy for Liver Diseases, 100044, Beijing, China
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  givenname: Lai
  surname: Wei
  fullname: Wei, Lai
  email: weilai@pkuph.edu.cn
  organization: Peking University People's Hospital, Peking University Hepatology Institute, Beijing Key Laboratory of Hepatitis C and Immunotherapy for Liver Diseases, 100044, Beijing, China
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31745210$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 2019 United States & Canadian Academy of Pathology
The Author(s), under exclusive licence to United States and Canadian Academy of Pathology 2019
2019© The Author(s), under exclusive licence to United States and Canadian Academy of Pathology 2019
The Author(s), under exclusive licence to United States and Canadian Academy of Pathology 2019.
Copyright_xml – notice: 2019 United States & Canadian Academy of Pathology
– notice: The Author(s), under exclusive licence to United States and Canadian Academy of Pathology 2019
– notice: 2019© The Author(s), under exclusive licence to United States and Canadian Academy of Pathology 2019
– notice: The Author(s), under exclusive licence to United States and Canadian Academy of Pathology 2019.
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Snippet The stimulator of interferon genes (STING) in macrophages plays a crucial role in nonalcoholic fatty liver disease (NAFLD) progression. However, there is a...
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SubjectTerms 13
13/51
14
14/63
692/699/1503/1607/2750
692/699/1503/1607/2751
Adult
Aged
CCR2 protein
CD163 antigen
Cell activation
Collagen (type I)
Correlation analysis
Disease Progression
Fatty liver
Female
Fibrosis
Gene expression
Genes
Hepatitis - metabolism
Hepatocytes
Humans
Inflammation
Interferon
Interleukin 1
Interleukin 6
Kupffer cells
Laboratory Medicine
Liver
Liver - metabolism
Liver - pathology
Liver Cirrhosis - metabolism
Liver diseases
Macrophages
Macrophages - metabolism
Male
Medicine
Medicine & Public Health
Membrane Proteins - analysis
Membrane Proteins - metabolism
Middle Aged
Monocyte chemoattractant protein 1
Monocytes
Non-alcoholic Fatty Liver Disease - metabolism
Non-alcoholic Fatty Liver Disease - pathology
Pathology
Signal transduction
Stimulators
Transforming growth factor-b1
Young Adult
Title STING expression in monocyte-derived macrophages is associated with the progression of liver inflammation and fibrosis in patients with nonalcoholic fatty liver disease
URI https://dx.doi.org/10.1038/s41374-019-0342-6
https://link.springer.com/article/10.1038/s41374-019-0342-6
https://www.ncbi.nlm.nih.gov/pubmed/31745210
https://www.proquest.com/docview/2382998233
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Volume 100
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