Serum transferrin as a biomarker of hepatocyte nuclear factor 4 alpha activity and hepatocyte function in liver diseases.


Journal

BMC medicine
ISSN: 1741-7015
Titre abrégé: BMC Med
Pays: England
ID NLM: 101190723

Informations de publication

Date de publication:
17 02 2021
Historique:
received: 30 06 2020
accepted: 18 01 2021
entrez: 17 2 2021
pubmed: 18 2 2021
medline: 22 6 2021
Statut: epublish

Résumé

Serum transferrin levels represent an independent predictor of mortality in patients with liver failure. Hepatocyte nuclear factor 4 alpha (HNF4α) is a master regulator of hepatocyte functions. The aim of this study was to explore whether serum transferrin reflects HNF4α activity. Factors regulating transferrin expression in alcoholic hepatitis (AH) were assessed via transcriptomic/methylomic analysis as well as chromatin immunoprecipitation coupled to DNA sequencing. The findings were corroborated in primary hepatocytes. Serum and liver samples from 40 patients with advanced liver disease of multiple etiologies were also studied. In patients with advanced liver disease, serum transferrin levels correlated with hepatic transferrin expression (r = 0.51, p = 0.01). Immunohistochemical and biochemical tests confirmed reduced HNF4α and transferrin protein levels in individuals with cirrhosis. In AH, hepatic gene-gene correlation analysis in liver transcriptome revealed an enrichment of HNF4α signature in transferrin-correlated transcriptome while transforming growth factor beta 1 (TGFβ1), tumor necrosis factor α (TNFα), interleukin 1 beta (IL-1β), and interleukin 6 (IL-6) negatively associated with transferrin signature. A key regulatory region in transferrin promoter was hypermethylated in patients with AH. In primary hepatocytes, treatment with TGFβ1 or the HNF4α inhibitor BI6015 suppressed transferrin production, while exposure to TNFα, IL-1β, and IL-6 had no effect. The correlation between hepatic HNF4A and transferrin mRNA levels was also seen in advanced liver disease. Serum transferrin levels constitute a prognostic and mechanistic biomarker. Consequently, they may serve as a surrogate of impaired hepatic HNF4α signaling and liver failure.

Sections du résumé

BACKGROUND
Serum transferrin levels represent an independent predictor of mortality in patients with liver failure. Hepatocyte nuclear factor 4 alpha (HNF4α) is a master regulator of hepatocyte functions. The aim of this study was to explore whether serum transferrin reflects HNF4α activity.
METHODS
Factors regulating transferrin expression in alcoholic hepatitis (AH) were assessed via transcriptomic/methylomic analysis as well as chromatin immunoprecipitation coupled to DNA sequencing. The findings were corroborated in primary hepatocytes. Serum and liver samples from 40 patients with advanced liver disease of multiple etiologies were also studied.
RESULTS
In patients with advanced liver disease, serum transferrin levels correlated with hepatic transferrin expression (r = 0.51, p = 0.01). Immunohistochemical and biochemical tests confirmed reduced HNF4α and transferrin protein levels in individuals with cirrhosis. In AH, hepatic gene-gene correlation analysis in liver transcriptome revealed an enrichment of HNF4α signature in transferrin-correlated transcriptome while transforming growth factor beta 1 (TGFβ1), tumor necrosis factor α (TNFα), interleukin 1 beta (IL-1β), and interleukin 6 (IL-6) negatively associated with transferrin signature. A key regulatory region in transferrin promoter was hypermethylated in patients with AH. In primary hepatocytes, treatment with TGFβ1 or the HNF4α inhibitor BI6015 suppressed transferrin production, while exposure to TNFα, IL-1β, and IL-6 had no effect. The correlation between hepatic HNF4A and transferrin mRNA levels was also seen in advanced liver disease.
CONCLUSIONS
Serum transferrin levels constitute a prognostic and mechanistic biomarker. Consequently, they may serve as a surrogate of impaired hepatic HNF4α signaling and liver failure.

Identifiants

pubmed: 33593348
doi: 10.1186/s12916-021-01917-6
pii: 10.1186/s12916-021-01917-6
pmc: PMC7887823
doi:

Substances chimiques

Hepatocyte Nuclear Factors 0
RNA, Messenger 0
TGFB1 protein, human 0
Transforming Growth Factor beta1 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

39

Subventions

Organisme : Medical Research Council
ID : MR/R014019/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/R023026/1
Pays : United Kingdom
Organisme : NIAAA NIH HHS
ID : U01 AA026978
Pays : United States
Organisme : NIAAA NIH HHS
ID : U01 AA026972
Pays : United States

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Auteurs

Nurdan Guldiken (N)

Department of Internal Medicine III, University Hospital RWTH Aachen, Pauwelsstraße 30, 52074, Aachen, Germany.

Josepmaria Argemi (J)

Pittsburgh Liver Research Center, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.
Liver Unit, Clinica Universidad de Navarra, Hepatology Program, Center for Applied Medical Research, Pamplona, Spain.

Berivan Gurbuz (B)

Department of Internal Medicine III, University Hospital RWTH Aachen, Pauwelsstraße 30, 52074, Aachen, Germany.

Stephen R Atkinson (SR)

Department of Hepatology, Imperial College London, London, UK.

Martin Oliverius (M)

Center of Cardiovascular Surgery and Transplantation Brno, Brno, Czech Republic.

Petr Fila (P)

Center of Cardiovascular Surgery and Transplantation Brno, Brno, Czech Republic.

Karim Hamesch (K)

Department of Internal Medicine III, University Hospital RWTH Aachen, Pauwelsstraße 30, 52074, Aachen, Germany.

Tony Bruns (T)

Department of Internal Medicine III, University Hospital RWTH Aachen, Pauwelsstraße 30, 52074, Aachen, Germany.

Joaquín Cabezas (J)

Research Institute Valdecilla (Instituto de Investigación Sanitaria Valdecilla), Santander, Spain.
Gastroenterology and Hepatology Unit, University Hospital Marqués de Valdecilla, Santander, Spain.

Juan J Lozano (JJ)

Centro de Investigacion Biomedica en Red, Enfermedades Hepáticas y Digestivas (CIBERehd), Barcelona, Spain.

Jelena Mann (J)

Newcastle Fibrosis Research Group, Biosciences Institute, Faculty of Medical Sciences, Newcastle University, Newcastle, UK.

Sheng Cao (S)

Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, MN, USA.

Philippe Mathurin (P)

Hôpital Claude Huriez, Services des Maladies de l'Appareil Digestif, CHRU Lille, and Unité INSERM 995, Lille, France.

Vijay H Shah (VH)

Division of Gastroenterology and Hepatology, Mayo Clinic, Rochester, MN, USA.

Christian Trautwein (C)

Department of Internal Medicine III, University Hospital RWTH Aachen, Pauwelsstraße 30, 52074, Aachen, Germany.

Mark R Thursz (MR)

Department of Hepatology, Imperial College London, London, UK.

Ramon Bataller (R)

Pittsburgh Liver Research Center, University of Pittsburgh Medical Center, Pittsburgh, PA, USA.

Pavel Strnad (P)

Department of Internal Medicine III, University Hospital RWTH Aachen, Pauwelsstraße 30, 52074, Aachen, Germany. pstrnad@ukaachen.de.

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