Gut microbiota mediates SREBP-1c-driven hepatic lipogenesis and steatosis in response to zero-fat high-sucrose diet

Objectives: Sucrose-rich diets promote hepatic de novo lipogenesis (DNL) and steatosis through interactions with the gut microbiota. However, the role of sugar-microbiota dynamics in the absence of dietary fat remains unclear. This study aimed to investigate the effects of a high-sucrose, zero-fat d...

Full description

Saved in:
Bibliographic Details
Main Authors: Mattias Bergentall, Valentina Tremaroli, Chuqing Sun, Marcus Henricsson, Muhammad Tanweer Khan, Louise Mannerås Holm, Lisa Olsson, Per-Olof Bergh, Antonio Molinaro, Adil Mardinoglu, Robert Caesar, Max Nieuwdorp, Fredrik Bäckhed
Format: Article
Language:English
Published: Elsevier 2025-07-01
Series:Molecular Metabolism
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2212877825000699
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849725228475744256
author Mattias Bergentall
Valentina Tremaroli
Chuqing Sun
Marcus Henricsson
Muhammad Tanweer Khan
Louise Mannerås Holm
Lisa Olsson
Per-Olof Bergh
Antonio Molinaro
Adil Mardinoglu
Robert Caesar
Max Nieuwdorp
Fredrik Bäckhed
author_facet Mattias Bergentall
Valentina Tremaroli
Chuqing Sun
Marcus Henricsson
Muhammad Tanweer Khan
Louise Mannerås Holm
Lisa Olsson
Per-Olof Bergh
Antonio Molinaro
Adil Mardinoglu
Robert Caesar
Max Nieuwdorp
Fredrik Bäckhed
author_sort Mattias Bergentall
collection DOAJ
description Objectives: Sucrose-rich diets promote hepatic de novo lipogenesis (DNL) and steatosis through interactions with the gut microbiota. However, the role of sugar-microbiota dynamics in the absence of dietary fat remains unclear. This study aimed to investigate the effects of a high-sucrose, zero-fat diet (ZFD) on hepatic steatosis and host metabolism in conventionally raised (CONVR) and germ-free (GF) mice. Methods: CONVR and GF mice were fed a ZFD, and hepatic lipid accumulation, gene expression, and metabolite levels were analyzed. DNL activity was assessed by measuring malonyl-CoA levels, expression of key DNL enzymes, and activation of the transcription factor SREBP-1c. Metabolomic analyses of portal vein plasma identified microbiota-derived metabolites linked to hepatic steatosis. To further examine the role of SREBP-1c, its hepatic expression was knocked down using antisense oligonucleotides in CONVR ZFD-fed mice. Results: The gut microbiota was essential for sucrose-induced DNL and hepatic steatosis. In CONVR ZFD-fed mice, hepatic fat accumulation increased alongside elevated expression of genes encoding DNL enzymes, higher malonyl-CoA levels, and upregulation of SREBP-1c. Regardless of microbiota status, ZFD induced fatty acid elongase and desaturase gene expression and increased hepatic monounsaturated fatty acids. Metabolomic analyses identified microbiota-derived metabolites associated with hepatic steatosis. SREBP-1c knockdown in CONVR ZFD-fed mice reduced hepatic steatosis and suppressed fatty acid synthase expression. Conclusions: Sucrose-microbiota interactions and SREBP-1c are required for DNL and hepatic steatosis in the absence of dietary fat. These findings provide new insights into the complex interplay between diet, gut microbiota, and metabolic regulation.
format Article
id doaj-art-de9f5e1747ce4b86a73821fff4aeb83f
institution DOAJ
issn 2212-8778
language English
publishDate 2025-07-01
publisher Elsevier
record_format Article
series Molecular Metabolism
spelling doaj-art-de9f5e1747ce4b86a73821fff4aeb83f2025-08-20T03:10:31ZengElsevierMolecular Metabolism2212-87782025-07-019710216210.1016/j.molmet.2025.102162Gut microbiota mediates SREBP-1c-driven hepatic lipogenesis and steatosis in response to zero-fat high-sucrose dietMattias Bergentall0Valentina Tremaroli1Chuqing Sun2Marcus Henricsson3Muhammad Tanweer Khan4Louise Mannerås Holm5Lisa Olsson6Per-Olof Bergh7Antonio Molinaro8Adil Mardinoglu9Robert Caesar10Max Nieuwdorp11Fredrik Bäckhed12Wallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, SwedenWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, SwedenWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, SwedenWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, SwedenWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, SwedenWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, SwedenWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, SwedenWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, SwedenWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, SwedenScience for Life Laboratory, KTH - Royal Institute of Technology, Stockholm, Sweden; Centre for Host-Microbiome Interactions, Faculty of Dentistry, Oral & Craniofacial Sciences, King's College London, London, SE1 9RT, UKWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, Sweden; Corresponding author.Department of (Experimental) Vascular Medicine, Amsterdam University Medical Centers, University of Amsterdam, Amsterdam, the NetherlandsWallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, Sweden; Department of Clinical Physiology Region Västra Götaland, Sahlgrenska University Hospital Gothenburg Sweden, Sweden; Corresponding author. Wallenberg Laboratory, Department of Molecular and Clinical Medicine and Sahlgrenska Center for Cardiovascular and Metabolic Research, University of Gothenburg, Gothenburg, SE-413 45, Sweden.Objectives: Sucrose-rich diets promote hepatic de novo lipogenesis (DNL) and steatosis through interactions with the gut microbiota. However, the role of sugar-microbiota dynamics in the absence of dietary fat remains unclear. This study aimed to investigate the effects of a high-sucrose, zero-fat diet (ZFD) on hepatic steatosis and host metabolism in conventionally raised (CONVR) and germ-free (GF) mice. Methods: CONVR and GF mice were fed a ZFD, and hepatic lipid accumulation, gene expression, and metabolite levels were analyzed. DNL activity was assessed by measuring malonyl-CoA levels, expression of key DNL enzymes, and activation of the transcription factor SREBP-1c. Metabolomic analyses of portal vein plasma identified microbiota-derived metabolites linked to hepatic steatosis. To further examine the role of SREBP-1c, its hepatic expression was knocked down using antisense oligonucleotides in CONVR ZFD-fed mice. Results: The gut microbiota was essential for sucrose-induced DNL and hepatic steatosis. In CONVR ZFD-fed mice, hepatic fat accumulation increased alongside elevated expression of genes encoding DNL enzymes, higher malonyl-CoA levels, and upregulation of SREBP-1c. Regardless of microbiota status, ZFD induced fatty acid elongase and desaturase gene expression and increased hepatic monounsaturated fatty acids. Metabolomic analyses identified microbiota-derived metabolites associated with hepatic steatosis. SREBP-1c knockdown in CONVR ZFD-fed mice reduced hepatic steatosis and suppressed fatty acid synthase expression. Conclusions: Sucrose-microbiota interactions and SREBP-1c are required for DNL and hepatic steatosis in the absence of dietary fat. These findings provide new insights into the complex interplay between diet, gut microbiota, and metabolic regulation.http://www.sciencedirect.com/science/article/pii/S2212877825000699de novo lipogenesisGut microbiotaHepatic steatosisHigh-sucrose dietMetabolomicsSREBP-1c
spellingShingle Mattias Bergentall
Valentina Tremaroli
Chuqing Sun
Marcus Henricsson
Muhammad Tanweer Khan
Louise Mannerås Holm
Lisa Olsson
Per-Olof Bergh
Antonio Molinaro
Adil Mardinoglu
Robert Caesar
Max Nieuwdorp
Fredrik Bäckhed
Gut microbiota mediates SREBP-1c-driven hepatic lipogenesis and steatosis in response to zero-fat high-sucrose diet
Molecular Metabolism
de novo lipogenesis
Gut microbiota
Hepatic steatosis
High-sucrose diet
Metabolomics
SREBP-1c
title Gut microbiota mediates SREBP-1c-driven hepatic lipogenesis and steatosis in response to zero-fat high-sucrose diet
title_full Gut microbiota mediates SREBP-1c-driven hepatic lipogenesis and steatosis in response to zero-fat high-sucrose diet
title_fullStr Gut microbiota mediates SREBP-1c-driven hepatic lipogenesis and steatosis in response to zero-fat high-sucrose diet
title_full_unstemmed Gut microbiota mediates SREBP-1c-driven hepatic lipogenesis and steatosis in response to zero-fat high-sucrose diet
title_short Gut microbiota mediates SREBP-1c-driven hepatic lipogenesis and steatosis in response to zero-fat high-sucrose diet
title_sort gut microbiota mediates srebp 1c driven hepatic lipogenesis and steatosis in response to zero fat high sucrose diet
topic de novo lipogenesis
Gut microbiota
Hepatic steatosis
High-sucrose diet
Metabolomics
SREBP-1c
url http://www.sciencedirect.com/science/article/pii/S2212877825000699
work_keys_str_mv AT mattiasbergentall gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT valentinatremaroli gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT chuqingsun gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT marcushenricsson gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT muhammadtanweerkhan gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT louisemannerasholm gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT lisaolsson gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT perolofbergh gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT antoniomolinaro gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT adilmardinoglu gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT robertcaesar gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT maxnieuwdorp gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet
AT fredrikbackhed gutmicrobiotamediatessrebp1cdrivenhepaticlipogenesisandsteatosisinresponsetozerofathighsucrosediet