Cargando…

Butyrate ingestion improves hepatic glycogen storage in the re-fed rat

BACKGROUND: Butyrate naturally produced by intestinal fiber fermentation is the main nutrient for colonocytes, but the metabolic effect of the fraction reaching the liver is not totally known. After glycogen hepatic depletion in the 48-hour fasting rat, we monitored the effect of (butyrate 1.90 mg +...

Descripción completa

Detalles Bibliográficos
Autores principales: Beauvieux, Marie-Christine, Roumes, Hélène, Robert, Nadège, Gin, Henri, Rigalleau, Vincent, Gallis, Jean-Louis
Formato: Texto
Lenguaje:English
Publicado: BioMed Central 2008
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2569010/
https://www.ncbi.nlm.nih.gov/pubmed/18847460
http://dx.doi.org/10.1186/1472-6793-8-19
_version_ 1782160053813379072
author Beauvieux, Marie-Christine
Roumes, Hélène
Robert, Nadège
Gin, Henri
Rigalleau, Vincent
Gallis, Jean-Louis
author_facet Beauvieux, Marie-Christine
Roumes, Hélène
Robert, Nadège
Gin, Henri
Rigalleau, Vincent
Gallis, Jean-Louis
author_sort Beauvieux, Marie-Christine
collection PubMed
description BACKGROUND: Butyrate naturally produced by intestinal fiber fermentation is the main nutrient for colonocytes, but the metabolic effect of the fraction reaching the liver is not totally known. After glycogen hepatic depletion in the 48-hour fasting rat, we monitored the effect of (butyrate 1.90 mg + glucose 14.0 mg)/g body weight versus isocaloric (glucose 18.2 mg/g) or isoglucidic (glucose 14.0 mg/g) control force-feeding on in vivo changes in hepatic glycogen and ATP contents evaluated ex vivo by NMR in the isolated and perfused liver. RESULTS: The change in glycogen was biphasic with (i) an initial linear period where presence of butyrate in the diet increased (P = 0.05) the net synthesis rate (0.20 ± 0.01 μmol/min.g(-1 )liver wet weight, n = 15) versus glucose 14.0 mg/g only (0.16 ± 0.01 μmol/min.g(-1 )liver ww, n = 14), and (ii) a plateau of glycogen store followed by a depletion. Butyrate delayed the establishment of the equilibrium between glycogenosynthetic and glycogenolytic fluxes from the 6(th )to 8(th )hour post-feeding. The maximal glycogen content was then 97.27 ± 10.59 μmol/g liver ww (n = 7) at the 8(th )hour, which was significantly higher than with the isocaloric control diet (64.34 ± 8.49 μmol/g, n = 12, P = 0.03) and the isoglucidic control one (49.11 ± 6.35 μmol/g liver ww, n = 6, P = 0.003). After butyrate ingestion, ATP content increased from 0.95 ± 0.29 to a plateau of 2.14 ± 0.23 μmol/g liver ww at the 8(th )hour post-feeding (n = 8) [P = 0.04 versus isoglucidic control diet (1.45 ± 0.19 μmol/g, n = 8) but was not different from the isocaloric control diet (1.70 ± 0.18 μmol/g, n = 12)]. CONCLUSION: The main hepatic effect of butyrate is a sparing effect on glycogen storage explained (i) by competition between butyrate and glucose oxidation, glucose being preferentially directed to glycogenosynthesis during the post-prandial state; and (ii) by a likely reduced glycogenolysis from the newly synthesized glycogen. This first demonstration of the improvement of liver glycogen storage by acute butyrate supply may be an important contribution to explaining the beneficial effects on glucose homeostasis of nutritional supply increasing butyrate amount such as fiber diets.
format Text
id pubmed-2569010
institution National Center for Biotechnology Information
language English
publishDate 2008
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-25690102008-10-17 Butyrate ingestion improves hepatic glycogen storage in the re-fed rat Beauvieux, Marie-Christine Roumes, Hélène Robert, Nadège Gin, Henri Rigalleau, Vincent Gallis, Jean-Louis BMC Physiol Research Article BACKGROUND: Butyrate naturally produced by intestinal fiber fermentation is the main nutrient for colonocytes, but the metabolic effect of the fraction reaching the liver is not totally known. After glycogen hepatic depletion in the 48-hour fasting rat, we monitored the effect of (butyrate 1.90 mg + glucose 14.0 mg)/g body weight versus isocaloric (glucose 18.2 mg/g) or isoglucidic (glucose 14.0 mg/g) control force-feeding on in vivo changes in hepatic glycogen and ATP contents evaluated ex vivo by NMR in the isolated and perfused liver. RESULTS: The change in glycogen was biphasic with (i) an initial linear period where presence of butyrate in the diet increased (P = 0.05) the net synthesis rate (0.20 ± 0.01 μmol/min.g(-1 )liver wet weight, n = 15) versus glucose 14.0 mg/g only (0.16 ± 0.01 μmol/min.g(-1 )liver ww, n = 14), and (ii) a plateau of glycogen store followed by a depletion. Butyrate delayed the establishment of the equilibrium between glycogenosynthetic and glycogenolytic fluxes from the 6(th )to 8(th )hour post-feeding. The maximal glycogen content was then 97.27 ± 10.59 μmol/g liver ww (n = 7) at the 8(th )hour, which was significantly higher than with the isocaloric control diet (64.34 ± 8.49 μmol/g, n = 12, P = 0.03) and the isoglucidic control one (49.11 ± 6.35 μmol/g liver ww, n = 6, P = 0.003). After butyrate ingestion, ATP content increased from 0.95 ± 0.29 to a plateau of 2.14 ± 0.23 μmol/g liver ww at the 8(th )hour post-feeding (n = 8) [P = 0.04 versus isoglucidic control diet (1.45 ± 0.19 μmol/g, n = 8) but was not different from the isocaloric control diet (1.70 ± 0.18 μmol/g, n = 12)]. CONCLUSION: The main hepatic effect of butyrate is a sparing effect on glycogen storage explained (i) by competition between butyrate and glucose oxidation, glucose being preferentially directed to glycogenosynthesis during the post-prandial state; and (ii) by a likely reduced glycogenolysis from the newly synthesized glycogen. This first demonstration of the improvement of liver glycogen storage by acute butyrate supply may be an important contribution to explaining the beneficial effects on glucose homeostasis of nutritional supply increasing butyrate amount such as fiber diets. BioMed Central 2008-10-10 /pmc/articles/PMC2569010/ /pubmed/18847460 http://dx.doi.org/10.1186/1472-6793-8-19 Text en Copyright © 2008 Beauvieux et al; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( (http://creativecommons.org/licenses/by/2.0) ), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Research Article
Beauvieux, Marie-Christine
Roumes, Hélène
Robert, Nadège
Gin, Henri
Rigalleau, Vincent
Gallis, Jean-Louis
Butyrate ingestion improves hepatic glycogen storage in the re-fed rat
title Butyrate ingestion improves hepatic glycogen storage in the re-fed rat
title_full Butyrate ingestion improves hepatic glycogen storage in the re-fed rat
title_fullStr Butyrate ingestion improves hepatic glycogen storage in the re-fed rat
title_full_unstemmed Butyrate ingestion improves hepatic glycogen storage in the re-fed rat
title_short Butyrate ingestion improves hepatic glycogen storage in the re-fed rat
title_sort butyrate ingestion improves hepatic glycogen storage in the re-fed rat
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2569010/
https://www.ncbi.nlm.nih.gov/pubmed/18847460
http://dx.doi.org/10.1186/1472-6793-8-19
work_keys_str_mv AT beauvieuxmariechristine butyrateingestionimproveshepaticglycogenstorageintherefedrat
AT roumeshelene butyrateingestionimproveshepaticglycogenstorageintherefedrat
AT robertnadege butyrateingestionimproveshepaticglycogenstorageintherefedrat
AT ginhenri butyrateingestionimproveshepaticglycogenstorageintherefedrat
AT rigalleauvincent butyrateingestionimproveshepaticglycogenstorageintherefedrat
AT gallisjeanlouis butyrateingestionimproveshepaticglycogenstorageintherefedrat