Intragastric administration of short chain fatty acids greatly reduces voluntary ethanol intake in rats

Abstract Alcohol use disorder (AUD) represents a public health crisis with few FDA-approved medications for its treatment. Growing evidence supports the key role of the bidirectional communication between the gut microbiota and the central nervous system (CNS) during the initiation and progression o...

Full description

Saved in:
Bibliographic Details
Main Authors: María Elena Quintanilla, Daniela Santapau, Eugenio Diaz, Ignacio Valenzuela Martinez, Nicolas Medina, Glauben Landskron, Antonia Dominguez, Paola Morales, David Ramírez, Marcela Hermoso, Belén Olivares, Pablo Berríos-Cárcamo, Marcelo Ezquer, Mario Herrera-Marschitz, Yedy Israel, Fernando Ezquer
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-024-80228-1
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1846147929246531584
author María Elena Quintanilla
Daniela Santapau
Eugenio Diaz
Ignacio Valenzuela Martinez
Nicolas Medina
Glauben Landskron
Antonia Dominguez
Paola Morales
David Ramírez
Marcela Hermoso
Belén Olivares
Pablo Berríos-Cárcamo
Marcelo Ezquer
Mario Herrera-Marschitz
Yedy Israel
Fernando Ezquer
author_facet María Elena Quintanilla
Daniela Santapau
Eugenio Diaz
Ignacio Valenzuela Martinez
Nicolas Medina
Glauben Landskron
Antonia Dominguez
Paola Morales
David Ramírez
Marcela Hermoso
Belén Olivares
Pablo Berríos-Cárcamo
Marcelo Ezquer
Mario Herrera-Marschitz
Yedy Israel
Fernando Ezquer
author_sort María Elena Quintanilla
collection DOAJ
description Abstract Alcohol use disorder (AUD) represents a public health crisis with few FDA-approved medications for its treatment. Growing evidence supports the key role of the bidirectional communication between the gut microbiota and the central nervous system (CNS) during the initiation and progression of alcohol use disorder. Among the different protective molecules that could mediate this communication, short chain fatty acids (SCFAs) have emerged as attractive candidates, since these gut microbiota-derived molecules have multi-target effects that could normalize several of the functional and structural parameters altered by chronic alcohol abuse. The present study, conducted in male alcohol-preferring UChB rats, shows that the initiation of voluntary ethanol intake was inhibited in 85% by the intragastric administration of a combination of SCFAs (acetate, propionate and butyrate) given before ethanol exposure, while SCFAs administration after two months of ethanol intake induced a 90% reduction in its consumption. These SCFAs therapeutic effects were associated with (1) a significant reduction of ethanol-induced intestinal inflammation and damage; (2) reduction of plasma lipopolysaccharide levels and hepatic inflammation; (3) reduction of ethanol-induced astrocyte and microglia activation; and (4) attenuation of the ethanol-induced gene expression changes within the nucleus accumbens. Finally, we determined that among the different SCFAs evaluated, butyrate was the most potent, reducing chronic ethanol intake in a dose–response manner. These findings support a key role of SCFAs, and especially butyrate, in regulating AUD, providing a simple, inexpensive, and safe approach as a preventive and intervention-based strategy to address this devastating disease.
format Article
id doaj-art-f6ed752d118c41c4a83889d462d6c5e7
institution Kabale University
issn 2045-2322
language English
publishDate 2024-11-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-f6ed752d118c41c4a83889d462d6c5e72024-12-01T12:20:21ZengNature PortfolioScientific Reports2045-23222024-11-0114111610.1038/s41598-024-80228-1Intragastric administration of short chain fatty acids greatly reduces voluntary ethanol intake in ratsMaría Elena Quintanilla0Daniela Santapau1Eugenio Diaz2Ignacio Valenzuela Martinez3Nicolas Medina4Glauben Landskron5Antonia Dominguez6Paola Morales7David Ramírez8Marcela Hermoso9Belén Olivares10Pablo Berríos-Cárcamo11Marcelo Ezquer12Mario Herrera-Marschitz13Yedy Israel14Fernando Ezquer15Molecular and Clinical Pharmacology Program, Institute of Biomedical Sciences, Faculty of Medicine, Universidad de ChileCenter for Regenerative Medicine, Faculty of Medicine Clínica Alemana-Universidad del DesarrolloDepartment of Neuroscience, Faculty of Medicine, Universidad de ChileDepartamento de Farmacología, Facultad de Ciencias Biológicas, Universidad de ConcepciónDepartamento de Farmacología, Facultad de Ciencias Biológicas, Universidad de ConcepciónCenter for Biomedical Research, CIBMED, Faculty of Medicine, Universidad Finis TerraeCenter for Biomedical Research, CIBMED, Faculty of Medicine, Universidad Finis TerraeMolecular and Clinical Pharmacology Program, Institute of Biomedical Sciences, Faculty of Medicine, Universidad de ChileDepartamento de Farmacología, Facultad de Ciencias Biológicas, Universidad de ConcepciónDepartment of Gastroenterology and Hepatology, University Medical CenterCenter for Medical Chemistry, Faculty of Medicine Clínica Alemana-Universidad del DesarrolloCenter for Regenerative Medicine, Faculty of Medicine Clínica Alemana-Universidad del DesarrolloCenter for Regenerative Medicine, Faculty of Medicine Clínica Alemana-Universidad del DesarrolloDepartment of Neuroscience, Faculty of Medicine, Universidad de ChileMolecular and Clinical Pharmacology Program, Institute of Biomedical Sciences, Faculty of Medicine, Universidad de ChileCenter for Regenerative Medicine, Faculty of Medicine Clínica Alemana-Universidad del DesarrolloAbstract Alcohol use disorder (AUD) represents a public health crisis with few FDA-approved medications for its treatment. Growing evidence supports the key role of the bidirectional communication between the gut microbiota and the central nervous system (CNS) during the initiation and progression of alcohol use disorder. Among the different protective molecules that could mediate this communication, short chain fatty acids (SCFAs) have emerged as attractive candidates, since these gut microbiota-derived molecules have multi-target effects that could normalize several of the functional and structural parameters altered by chronic alcohol abuse. The present study, conducted in male alcohol-preferring UChB rats, shows that the initiation of voluntary ethanol intake was inhibited in 85% by the intragastric administration of a combination of SCFAs (acetate, propionate and butyrate) given before ethanol exposure, while SCFAs administration after two months of ethanol intake induced a 90% reduction in its consumption. These SCFAs therapeutic effects were associated with (1) a significant reduction of ethanol-induced intestinal inflammation and damage; (2) reduction of plasma lipopolysaccharide levels and hepatic inflammation; (3) reduction of ethanol-induced astrocyte and microglia activation; and (4) attenuation of the ethanol-induced gene expression changes within the nucleus accumbens. Finally, we determined that among the different SCFAs evaluated, butyrate was the most potent, reducing chronic ethanol intake in a dose–response manner. These findings support a key role of SCFAs, and especially butyrate, in regulating AUD, providing a simple, inexpensive, and safe approach as a preventive and intervention-based strategy to address this devastating disease.https://doi.org/10.1038/s41598-024-80228-1Alcohol abuseGut microbiota-brain axisSCFAsButyrateAlcohol use disorder treatment
spellingShingle María Elena Quintanilla
Daniela Santapau
Eugenio Diaz
Ignacio Valenzuela Martinez
Nicolas Medina
Glauben Landskron
Antonia Dominguez
Paola Morales
David Ramírez
Marcela Hermoso
Belén Olivares
Pablo Berríos-Cárcamo
Marcelo Ezquer
Mario Herrera-Marschitz
Yedy Israel
Fernando Ezquer
Intragastric administration of short chain fatty acids greatly reduces voluntary ethanol intake in rats
Scientific Reports
Alcohol abuse
Gut microbiota-brain axis
SCFAs
Butyrate
Alcohol use disorder treatment
title Intragastric administration of short chain fatty acids greatly reduces voluntary ethanol intake in rats
title_full Intragastric administration of short chain fatty acids greatly reduces voluntary ethanol intake in rats
title_fullStr Intragastric administration of short chain fatty acids greatly reduces voluntary ethanol intake in rats
title_full_unstemmed Intragastric administration of short chain fatty acids greatly reduces voluntary ethanol intake in rats
title_short Intragastric administration of short chain fatty acids greatly reduces voluntary ethanol intake in rats
title_sort intragastric administration of short chain fatty acids greatly reduces voluntary ethanol intake in rats
topic Alcohol abuse
Gut microbiota-brain axis
SCFAs
Butyrate
Alcohol use disorder treatment
url https://doi.org/10.1038/s41598-024-80228-1
work_keys_str_mv AT mariaelenaquintanilla intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT danielasantapau intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT eugeniodiaz intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT ignaciovalenzuelamartinez intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT nicolasmedina intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT glaubenlandskron intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT antoniadominguez intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT paolamorales intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT davidramirez intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT marcelahermoso intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT belenolivares intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT pabloberrioscarcamo intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT marceloezquer intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT marioherreramarschitz intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT yedyisrael intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats
AT fernandoezquer intragastricadministrationofshortchainfattyacidsgreatlyreducesvoluntaryethanolintakeinrats