Interferon gamma induced-ACSL5 shapes the lipidome of kidney tubular cells

Summary: Acyl-CoA synthetase long-chain family (ACSL) enzymes are critical in the activation of long-chain fatty acid. To determine the regulatory mechanisms of ACSL5 and its biological functions within the kidney tubule, we generated transcriptomic, metabolomic, and lipidomic data from experimental...

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Main Authors: Virginie Poindessous, Julio L. Sampaio, Lydia Bouidghaghen, Ivan Nemazanyy, Alexandre Pallet, Maarten Naesens, Thibaut Vaulet, Dany Anglicheau, Nicolas Pallet
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:iScience
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Online Access:http://www.sciencedirect.com/science/article/pii/S258900422501003X
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author Virginie Poindessous
Julio L. Sampaio
Lydia Bouidghaghen
Ivan Nemazanyy
Alexandre Pallet
Maarten Naesens
Thibaut Vaulet
Dany Anglicheau
Nicolas Pallet
author_facet Virginie Poindessous
Julio L. Sampaio
Lydia Bouidghaghen
Ivan Nemazanyy
Alexandre Pallet
Maarten Naesens
Thibaut Vaulet
Dany Anglicheau
Nicolas Pallet
author_sort Virginie Poindessous
collection DOAJ
description Summary: Acyl-CoA synthetase long-chain family (ACSL) enzymes are critical in the activation of long-chain fatty acid. To determine the regulatory mechanisms of ACSL5 and its biological functions within the kidney tubule, we generated transcriptomic, metabolomic, and lipidomic data from experimental models and patient cohorts. We show that ACSL5 is a constituent of a gamma interferon-related gene signature linked to rejection in kidney transplant recipients and the urinary metabolome of kidney transplant recipients who experienced rejection exhibited a deficiency in ACSL5 substrates. We demonstrate that ACSL5 expression is induced in kidney tubular cells in response to IRF-1 signaling, and that it is involved in maintaining ATP production and cell viability and influences their lipid composition, reducing the accumulation of ceramides and the contents in glycerolipids. Thus, modulation of the activity of ACSL5 could impact tubular cell energy metabolism and lipid composition, with a clinical impact in response to kidney allograft injury.
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spelling doaj-art-e7174a9f286245fba5ed634c76b58d762025-08-20T02:05:36ZengElsevieriScience2589-00422025-06-0128611274210.1016/j.isci.2025.112742Interferon gamma induced-ACSL5 shapes the lipidome of kidney tubular cellsVirginie Poindessous0Julio L. Sampaio1Lydia Bouidghaghen2Ivan Nemazanyy3Alexandre Pallet4Maarten Naesens5Thibaut Vaulet6Dany Anglicheau7Nicolas Pallet8Centre de Recherche des Cordeliers, INSERM UMRS1138, Université Paris Cité, Paris, FranceCurieCoreTech Metabolomics and Lipidomics Technology Platform, Institut Curie, Paris, FranceCurieCoreTech Metabolomics and Lipidomics Technology Platform, Institut Curie, Paris, FrancePlatform for Metabolic Analyses, Structure Fédérative de Recherche Necker, INSERM US24/CNRS UMS 3633, Paris, FranceCentre de Recherche des Cordeliers, INSERM UMRS1138, Université Paris Cité, Paris, FranceDepartment of Microbiology, Immunology and Transplantation, Nephrology and Kidney Transplantation Research Group, KU Leuven, Leuven, BelgiumDepartment of Microbiology, Immunology and Transplantation, Nephrology and Kidney Transplantation Research Group, KU Leuven, Leuven, BelgiumDepartment of Kidney and Metabolic Diseases, Transplantation and Clinical Immunology, Necker Hospital, Assistance Publique - Hôpitaux de Paris Université Paris Cité, Paris, FranceCentre de Recherche des Cordeliers, INSERM UMRS1138, Université Paris Cité, Paris, France; Department of Nephrology, Georges Pompidou European Hospital, Assistance Publique Hôpitaux de Paris, Université Paris Cité, Paris, France; Department of Clinical Chemistry, Georges Pompidou European Hospital, Assistance Publique Hôpitaux de Paris, Université Paris Cité, Paris, France; Corresponding authorSummary: Acyl-CoA synthetase long-chain family (ACSL) enzymes are critical in the activation of long-chain fatty acid. To determine the regulatory mechanisms of ACSL5 and its biological functions within the kidney tubule, we generated transcriptomic, metabolomic, and lipidomic data from experimental models and patient cohorts. We show that ACSL5 is a constituent of a gamma interferon-related gene signature linked to rejection in kidney transplant recipients and the urinary metabolome of kidney transplant recipients who experienced rejection exhibited a deficiency in ACSL5 substrates. We demonstrate that ACSL5 expression is induced in kidney tubular cells in response to IRF-1 signaling, and that it is involved in maintaining ATP production and cell viability and influences their lipid composition, reducing the accumulation of ceramides and the contents in glycerolipids. Thus, modulation of the activity of ACSL5 could impact tubular cell energy metabolism and lipid composition, with a clinical impact in response to kidney allograft injury.http://www.sciencedirect.com/science/article/pii/S258900422501003XIntegrative aspects of cell biologyLipidomicsMetabolomicsTranscriptomics
spellingShingle Virginie Poindessous
Julio L. Sampaio
Lydia Bouidghaghen
Ivan Nemazanyy
Alexandre Pallet
Maarten Naesens
Thibaut Vaulet
Dany Anglicheau
Nicolas Pallet
Interferon gamma induced-ACSL5 shapes the lipidome of kidney tubular cells
iScience
Integrative aspects of cell biology
Lipidomics
Metabolomics
Transcriptomics
title Interferon gamma induced-ACSL5 shapes the lipidome of kidney tubular cells
title_full Interferon gamma induced-ACSL5 shapes the lipidome of kidney tubular cells
title_fullStr Interferon gamma induced-ACSL5 shapes the lipidome of kidney tubular cells
title_full_unstemmed Interferon gamma induced-ACSL5 shapes the lipidome of kidney tubular cells
title_short Interferon gamma induced-ACSL5 shapes the lipidome of kidney tubular cells
title_sort interferon gamma induced acsl5 shapes the lipidome of kidney tubular cells
topic Integrative aspects of cell biology
Lipidomics
Metabolomics
Transcriptomics
url http://www.sciencedirect.com/science/article/pii/S258900422501003X
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