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A gut microbial metabolite of dietary polyphenols reverses obesity-driven hepatic steatosis

The molecular mechanisms by which dietary fruits and vegetables confer cardiometabolic benefits remain poorly understood. Historically, these beneficial properties have been attributed to the antioxidant activity of flavonoids. Here, we reveal that the host metabolic benefits associated with flavono...

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Autores principales: Osborn, Lucas J., Schultz, Karlee, Massey, William, DeLucia, Beckey, Choucair, Ibrahim, Varadharajan, Venkateshwari, Banerjee, Rakhee, Fung, Kevin, Horak, Anthony J., Orabi, Danny, Nemet, Ina, Nagy, Laura E., Wang, Zeneng, Allende, Daniela S., Willard, Belinda B., Sangwan, Naseer, Hajjar, Adeline M., McDonald, Christine, Ahern, Philip P., Hazen, Stanley L., Brown, J. Mark, Claesen, Jan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9860326/
https://www.ncbi.nlm.nih.gov/pubmed/36417437
http://dx.doi.org/10.1073/pnas.2202934119
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author Osborn, Lucas J.
Schultz, Karlee
Massey, William
DeLucia, Beckey
Choucair, Ibrahim
Varadharajan, Venkateshwari
Banerjee, Rakhee
Fung, Kevin
Horak, Anthony J.
Orabi, Danny
Nemet, Ina
Nagy, Laura E.
Wang, Zeneng
Allende, Daniela S.
Willard, Belinda B.
Sangwan, Naseer
Hajjar, Adeline M.
McDonald, Christine
Ahern, Philip P.
Hazen, Stanley L.
Brown, J. Mark
Claesen, Jan
author_facet Osborn, Lucas J.
Schultz, Karlee
Massey, William
DeLucia, Beckey
Choucair, Ibrahim
Varadharajan, Venkateshwari
Banerjee, Rakhee
Fung, Kevin
Horak, Anthony J.
Orabi, Danny
Nemet, Ina
Nagy, Laura E.
Wang, Zeneng
Allende, Daniela S.
Willard, Belinda B.
Sangwan, Naseer
Hajjar, Adeline M.
McDonald, Christine
Ahern, Philip P.
Hazen, Stanley L.
Brown, J. Mark
Claesen, Jan
author_sort Osborn, Lucas J.
collection PubMed
description The molecular mechanisms by which dietary fruits and vegetables confer cardiometabolic benefits remain poorly understood. Historically, these beneficial properties have been attributed to the antioxidant activity of flavonoids. Here, we reveal that the host metabolic benefits associated with flavonoid consumption hinge, in part, on gut microbial metabolism. Specifically, we show that a single gut microbial flavonoid catabolite, 4-hydroxyphenylacetic acid (4-HPAA), is sufficient to reduce diet-induced cardiometabolic disease (CMD) burden in mice. The addition of flavonoids to a high fat diet heightened the levels of 4-HPAA within the portal plasma and attenuated obesity, and continuous delivery of 4-HPAA was sufficient to reverse hepatic steatosis. The antisteatotic effect was shown to be associated with the activation of AMP-activated protein kinase α (AMPKα). In a large survey of healthy human gut metagenomes, just over one percent contained homologs of all four characterized bacterial genes required to catabolize flavonols into 4-HPAA. Our results demonstrate the gut microbial contribution to the metabolic benefits associated with flavonoid consumption and underscore the rarity of this process in human gut microbial communities.
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spelling pubmed-98603262023-02-01 A gut microbial metabolite of dietary polyphenols reverses obesity-driven hepatic steatosis Osborn, Lucas J. Schultz, Karlee Massey, William DeLucia, Beckey Choucair, Ibrahim Varadharajan, Venkateshwari Banerjee, Rakhee Fung, Kevin Horak, Anthony J. Orabi, Danny Nemet, Ina Nagy, Laura E. Wang, Zeneng Allende, Daniela S. Willard, Belinda B. Sangwan, Naseer Hajjar, Adeline M. McDonald, Christine Ahern, Philip P. Hazen, Stanley L. Brown, J. Mark Claesen, Jan Proc Natl Acad Sci U S A Biological Sciences The molecular mechanisms by which dietary fruits and vegetables confer cardiometabolic benefits remain poorly understood. Historically, these beneficial properties have been attributed to the antioxidant activity of flavonoids. Here, we reveal that the host metabolic benefits associated with flavonoid consumption hinge, in part, on gut microbial metabolism. Specifically, we show that a single gut microbial flavonoid catabolite, 4-hydroxyphenylacetic acid (4-HPAA), is sufficient to reduce diet-induced cardiometabolic disease (CMD) burden in mice. The addition of flavonoids to a high fat diet heightened the levels of 4-HPAA within the portal plasma and attenuated obesity, and continuous delivery of 4-HPAA was sufficient to reverse hepatic steatosis. The antisteatotic effect was shown to be associated with the activation of AMP-activated protein kinase α (AMPKα). In a large survey of healthy human gut metagenomes, just over one percent contained homologs of all four characterized bacterial genes required to catabolize flavonols into 4-HPAA. Our results demonstrate the gut microbial contribution to the metabolic benefits associated with flavonoid consumption and underscore the rarity of this process in human gut microbial communities. National Academy of Sciences 2022-11-23 2022-11-29 /pmc/articles/PMC9860326/ /pubmed/36417437 http://dx.doi.org/10.1073/pnas.2202934119 Text en Copyright © 2022 the Author(s). Published by PNAS. https://creativecommons.org/licenses/by-nc-nd/4.0/This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND) (https://creativecommons.org/licenses/by-nc-nd/4.0/) .
spellingShingle Biological Sciences
Osborn, Lucas J.
Schultz, Karlee
Massey, William
DeLucia, Beckey
Choucair, Ibrahim
Varadharajan, Venkateshwari
Banerjee, Rakhee
Fung, Kevin
Horak, Anthony J.
Orabi, Danny
Nemet, Ina
Nagy, Laura E.
Wang, Zeneng
Allende, Daniela S.
Willard, Belinda B.
Sangwan, Naseer
Hajjar, Adeline M.
McDonald, Christine
Ahern, Philip P.
Hazen, Stanley L.
Brown, J. Mark
Claesen, Jan
A gut microbial metabolite of dietary polyphenols reverses obesity-driven hepatic steatosis
title A gut microbial metabolite of dietary polyphenols reverses obesity-driven hepatic steatosis
title_full A gut microbial metabolite of dietary polyphenols reverses obesity-driven hepatic steatosis
title_fullStr A gut microbial metabolite of dietary polyphenols reverses obesity-driven hepatic steatosis
title_full_unstemmed A gut microbial metabolite of dietary polyphenols reverses obesity-driven hepatic steatosis
title_short A gut microbial metabolite of dietary polyphenols reverses obesity-driven hepatic steatosis
title_sort gut microbial metabolite of dietary polyphenols reverses obesity-driven hepatic steatosis
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9860326/
https://www.ncbi.nlm.nih.gov/pubmed/36417437
http://dx.doi.org/10.1073/pnas.2202934119
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