Cargando…
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...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , |
---|---|
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 |
_version_ | 1784874557574742016 |
---|---|
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. |
format | Online Article Text |
id | pubmed-9860326 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | National Academy of Sciences |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT osbornlucasj agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT schultzkarlee agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT masseywilliam agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT deluciabeckey agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT choucairibrahim agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT varadharajanvenkateshwari agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT banerjeerakhee agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT fungkevin agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT horakanthonyj agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT orabidanny agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT nemetina agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT nagylaurae agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT wangzeneng agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT allendedanielas agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT willardbelindab agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT sangwannaseer agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT hajjaradelinem agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT mcdonaldchristine agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT ahernphilipp agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT hazenstanleyl agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT brownjmark agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT claesenjan agutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT osbornlucasj gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT schultzkarlee gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT masseywilliam gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT deluciabeckey gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT choucairibrahim gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT varadharajanvenkateshwari gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT banerjeerakhee gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT fungkevin gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT horakanthonyj gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT orabidanny gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT nemetina gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT nagylaurae gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT wangzeneng gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT allendedanielas gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT willardbelindab gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT sangwannaseer gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT hajjaradelinem gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT mcdonaldchristine gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT ahernphilipp gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT hazenstanleyl gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT brownjmark gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis AT claesenjan gutmicrobialmetaboliteofdietarypolyphenolsreversesobesitydrivenhepaticsteatosis |