Reprogramming of liver metabolism during West Nile virus infection unveils novel aspects of disease pathophysiology

Abstract Background West Nile virus (WNV) is a neurotropic mosquito-borne flavivirus responsible for outbreaks of encephalitis and meningitis worldwide. About 20% of infected patients exhibit abnormal liver function tests, although the participation of this organ in the pathophysiology of the diseas...

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Main Authors: Patricia Mingo-Casas, Ana-Belén Blázquez, Josefina Casas, Ana Esteban, Estela Escribano-Romero, Pedro J. Sánchez-Cordón, Nereida Jiménez de Oya, Juan-Carlos Saiz, Miguel A. Martín-Acebes
Format: Article
Language:English
Published: BMC 2025-07-01
Series:Molecular Medicine
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Online Access:https://doi.org/10.1186/s10020-025-01300-8
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author Patricia Mingo-Casas
Ana-Belén Blázquez
Josefina Casas
Ana Esteban
Estela Escribano-Romero
Pedro J. Sánchez-Cordón
Nereida Jiménez de Oya
Juan-Carlos Saiz
Miguel A. Martín-Acebes
author_facet Patricia Mingo-Casas
Ana-Belén Blázquez
Josefina Casas
Ana Esteban
Estela Escribano-Romero
Pedro J. Sánchez-Cordón
Nereida Jiménez de Oya
Juan-Carlos Saiz
Miguel A. Martín-Acebes
author_sort Patricia Mingo-Casas
collection DOAJ
description Abstract Background West Nile virus (WNV) is a neurotropic mosquito-borne flavivirus responsible for outbreaks of encephalitis and meningitis worldwide. About 20% of infected patients exhibit abnormal liver function tests, although the participation of this organ in the pathophysiology of the disease remains unclear. To fill this gap, this study explores changes in liver metabolism during WNV infection. Methods Given the relevance of the liver as a major immune and metabolic organ, the changes in response to WNV infection were analyzed in the mouse model combining transcriptomics, lipidomics and histopathological analyses. Results Despite the absence of detectable viral replication in the liver, infection resulted in hepatic transcriptomic reprogramming that affected inflammation, immunity, biological oxidation and lipid metabolisms. Changes in the expression of genes related to glutathione metabolism, detoxification reactions, fatty acid metabolism (fatty acid oxidation and fatty acyl-CoA biosynthesis), phospholipid synthesis (phosphatidylcholine and phosphatidylethanolamine), sphingolipid synthesis, sterol metabolism and lipid droplet organization were identified. The reduction in glutathione in the liver of infected animals was confirmed and lipidomic analyses showed an increase in the content of sphingolipids, triacylglycerols and cholesteryl esters. A decrease in the cholesterol, phosphatidylcholine and phosphatidylethanolamine levels was also observed. Moreover, histopathological findings supported the development of steatosis in one-third of WNV-infected animals. Conclusions The discovery of these underestimated metabolic aspects of the infection repurposes the impact of WNV on liver function. These results will contribute to a better understanding of the physiopathology of the disease and warrant special attention to liver function during WNV infection.
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spelling doaj-art-ae252706077d4b52b50883f67fafceb22025-08-20T03:38:18ZengBMCMolecular Medicine1528-36582025-07-0131111810.1186/s10020-025-01300-8Reprogramming of liver metabolism during West Nile virus infection unveils novel aspects of disease pathophysiologyPatricia Mingo-Casas0Ana-Belén Blázquez1Josefina Casas2Ana Esteban3Estela Escribano-Romero4Pedro J. Sánchez-Cordón5Nereida Jiménez de Oya6Juan-Carlos Saiz7Miguel A. Martín-Acebes8Department of Biotechnology, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Consejo Superior de Investigaciones Científicas (INIA-CSIC)Department of Biotechnology, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Consejo Superior de Investigaciones Científicas (INIA-CSIC)Department of Biological Chemistry, Institute for Advanced Chemistry of Catalonia (IQAC-CSIC)Department of Biotechnology, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Consejo Superior de Investigaciones Científicas (INIA-CSIC)Department of Biotechnology, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Consejo Superior de Investigaciones Científicas (INIA-CSIC)Centro de Investigación en Sanidad Animal (CISA, INIA-CSIC)Department of Biotechnology, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Consejo Superior de Investigaciones Científicas (INIA-CSIC)Department of Biotechnology, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Consejo Superior de Investigaciones Científicas (INIA-CSIC)Department of Biotechnology, Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria, Consejo Superior de Investigaciones Científicas (INIA-CSIC)Abstract Background West Nile virus (WNV) is a neurotropic mosquito-borne flavivirus responsible for outbreaks of encephalitis and meningitis worldwide. About 20% of infected patients exhibit abnormal liver function tests, although the participation of this organ in the pathophysiology of the disease remains unclear. To fill this gap, this study explores changes in liver metabolism during WNV infection. Methods Given the relevance of the liver as a major immune and metabolic organ, the changes in response to WNV infection were analyzed in the mouse model combining transcriptomics, lipidomics and histopathological analyses. Results Despite the absence of detectable viral replication in the liver, infection resulted in hepatic transcriptomic reprogramming that affected inflammation, immunity, biological oxidation and lipid metabolisms. Changes in the expression of genes related to glutathione metabolism, detoxification reactions, fatty acid metabolism (fatty acid oxidation and fatty acyl-CoA biosynthesis), phospholipid synthesis (phosphatidylcholine and phosphatidylethanolamine), sphingolipid synthesis, sterol metabolism and lipid droplet organization were identified. The reduction in glutathione in the liver of infected animals was confirmed and lipidomic analyses showed an increase in the content of sphingolipids, triacylglycerols and cholesteryl esters. A decrease in the cholesterol, phosphatidylcholine and phosphatidylethanolamine levels was also observed. Moreover, histopathological findings supported the development of steatosis in one-third of WNV-infected animals. Conclusions The discovery of these underestimated metabolic aspects of the infection repurposes the impact of WNV on liver function. These results will contribute to a better understanding of the physiopathology of the disease and warrant special attention to liver function during WNV infection.https://doi.org/10.1186/s10020-025-01300-8West Nile virusInfectionMetabolismGlutathioneLipidLipid droplet
spellingShingle Patricia Mingo-Casas
Ana-Belén Blázquez
Josefina Casas
Ana Esteban
Estela Escribano-Romero
Pedro J. Sánchez-Cordón
Nereida Jiménez de Oya
Juan-Carlos Saiz
Miguel A. Martín-Acebes
Reprogramming of liver metabolism during West Nile virus infection unveils novel aspects of disease pathophysiology
Molecular Medicine
West Nile virus
Infection
Metabolism
Glutathione
Lipid
Lipid droplet
title Reprogramming of liver metabolism during West Nile virus infection unveils novel aspects of disease pathophysiology
title_full Reprogramming of liver metabolism during West Nile virus infection unveils novel aspects of disease pathophysiology
title_fullStr Reprogramming of liver metabolism during West Nile virus infection unveils novel aspects of disease pathophysiology
title_full_unstemmed Reprogramming of liver metabolism during West Nile virus infection unveils novel aspects of disease pathophysiology
title_short Reprogramming of liver metabolism during West Nile virus infection unveils novel aspects of disease pathophysiology
title_sort reprogramming of liver metabolism during west nile virus infection unveils novel aspects of disease pathophysiology
topic West Nile virus
Infection
Metabolism
Glutathione
Lipid
Lipid droplet
url https://doi.org/10.1186/s10020-025-01300-8
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