Ex vivo fecal fermentation of human ileal fluid collected after raspberry consumption modifies (poly)phenolics and modulates genoprotective effects in colonic epithelial cells

Diets rich in fruit and vegetables are associated with a decreased incidence of colorectal cancer (CRC) due, in part, to the bioactive (poly)phenolic components and their microbiota-mediated metabolites. This study investigated how such compounds, derived from ingested raspberries in the gastrointes...

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Main Authors: Sara Dobani, Cheryl Latimer, Gordon J. McDougall, J. William Allwood, Gema Pereira-Caro, José Manuel Moreno-Rojas, Nigel G. Ternan, L. Kirsty Pourshahidi, Roger Lawther, Kieran M. Tuohy, Daniele Del Rio, Gloria O'Connor, Ian Rowland, Tahani Mazyad Almutairi, Alan Crozier, Chris I.R. Gill
Format: Article
Language:English
Published: Elsevier 2021-04-01
Series:Redox Biology
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2213231721000100
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language English
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author Sara Dobani
Cheryl Latimer
Gordon J. McDougall
J. William Allwood
Gema Pereira-Caro
José Manuel Moreno-Rojas
Nigel G. Ternan
L. Kirsty Pourshahidi
Roger Lawther
Kieran M. Tuohy
Daniele Del Rio
Gloria O'Connor
Ian Rowland
Tahani Mazyad Almutairi
Alan Crozier
Chris I.R. Gill
spellingShingle Sara Dobani
Cheryl Latimer
Gordon J. McDougall
J. William Allwood
Gema Pereira-Caro
José Manuel Moreno-Rojas
Nigel G. Ternan
L. Kirsty Pourshahidi
Roger Lawther
Kieran M. Tuohy
Daniele Del Rio
Gloria O'Connor
Ian Rowland
Tahani Mazyad Almutairi
Alan Crozier
Chris I.R. Gill
Ex vivo fecal fermentation of human ileal fluid collected after raspberry consumption modifies (poly)phenolics and modulates genoprotective effects in colonic epithelial cells
Redox Biology
Ileostomy
Gastrointestinal microbiota
Raspberry (poly)phenols
Phenolic catabolites
Fecal fermentation
DNA damage
author_facet Sara Dobani
Cheryl Latimer
Gordon J. McDougall
J. William Allwood
Gema Pereira-Caro
José Manuel Moreno-Rojas
Nigel G. Ternan
L. Kirsty Pourshahidi
Roger Lawther
Kieran M. Tuohy
Daniele Del Rio
Gloria O'Connor
Ian Rowland
Tahani Mazyad Almutairi
Alan Crozier
Chris I.R. Gill
author_sort Sara Dobani
title Ex vivo fecal fermentation of human ileal fluid collected after raspberry consumption modifies (poly)phenolics and modulates genoprotective effects in colonic epithelial cells
title_short Ex vivo fecal fermentation of human ileal fluid collected after raspberry consumption modifies (poly)phenolics and modulates genoprotective effects in colonic epithelial cells
title_full Ex vivo fecal fermentation of human ileal fluid collected after raspberry consumption modifies (poly)phenolics and modulates genoprotective effects in colonic epithelial cells
title_fullStr Ex vivo fecal fermentation of human ileal fluid collected after raspberry consumption modifies (poly)phenolics and modulates genoprotective effects in colonic epithelial cells
title_full_unstemmed Ex vivo fecal fermentation of human ileal fluid collected after raspberry consumption modifies (poly)phenolics and modulates genoprotective effects in colonic epithelial cells
title_sort ex vivo fecal fermentation of human ileal fluid collected after raspberry consumption modifies (poly)phenolics and modulates genoprotective effects in colonic epithelial cells
publisher Elsevier
series Redox Biology
issn 2213-2317
publishDate 2021-04-01
description Diets rich in fruit and vegetables are associated with a decreased incidence of colorectal cancer (CRC) due, in part, to the bioactive (poly)phenolic components and their microbiota-mediated metabolites. This study investigated how such compounds, derived from ingested raspberries in the gastrointestinal tract, may exert protective effects by reducing DNA damage. Ileal fluids collected pre- and post-consumption of 300 g of raspberries by ileostomists (n = 11) were subjected to 24 h ex vivo fermentation with fecal inoculum to simulate interaction with colonic microbiota. The impact of fermentation on (poly)phenolics in ileal fluid was determined and the bioactivity of ileal fluids pre- and post fermentation investigated. (Poly)phenolic compounds including sanguiin H-6, sanguiin H-10 and cyanidin-3-O-sophoroside decreased significantly during fermentation while, in contrast, microbial catabolites, including 3-(3′-hydroxyphenyl)propanoic acid, 3-hydroxybenzoic acid and benzoic acid increased significantly. The post-raspberry ileal fermentate from 9 of the 11 ileostomates significantly decreased DNA damage (~30%) in the CCD 841 CoN normal cell line using an oxidative challenge COMET assay. The raspberry ileal fermentates also modulated gene expression of the nuclear factor 2–antioxidant responsive element (Nrf2-ARE) pathway involved in oxidative stress cytoprotection, namely Nrf2, NAD(P)H dehydrogenase, quinone-1 and heme oxygenase-1. Four of the phenolic catabolites were assessed individually, each significantly reducing DNA damage from an oxidative challenge over a physiologically relevant 10–100 μM range. They also induced a differential pattern of expression of key genes in the Nrf2-ARE pathway in CCD 841 CoN cells. The study indicates that the colon-available raspberry (poly)phenols and their microbial-derived catabolites may play a role in protection against CRC in vivo.
topic Ileostomy
Gastrointestinal microbiota
Raspberry (poly)phenols
Phenolic catabolites
Fecal fermentation
DNA damage
url http://www.sciencedirect.com/science/article/pii/S2213231721000100
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spelling doaj-95536c9da11c40739337597ffb3cf5082021-01-22T04:49:56ZengElsevierRedox Biology2213-23172021-04-0140101862Ex vivo fecal fermentation of human ileal fluid collected after raspberry consumption modifies (poly)phenolics and modulates genoprotective effects in colonic epithelial cellsSara Dobani0Cheryl Latimer1Gordon J. McDougall2J. William Allwood3Gema Pereira-Caro4José Manuel Moreno-Rojas5Nigel G. Ternan6L. Kirsty Pourshahidi7Roger Lawther8Kieran M. Tuohy9Daniele Del Rio10Gloria O'Connor11Ian Rowland12Tahani Mazyad Almutairi13Alan Crozier14Chris I.R. Gill15Nutrition Innovation Centre for Food and Health, University of Ulster, Coleraine, Northern Ireland, UKNutrition Innovation Centre for Food and Health, University of Ulster, Coleraine, Northern Ireland, UKEnvironmental and Biochemical Sciences Department, The James Hutton Institute, Invergowrie, Dundee, Scotland, UKEnvironmental and Biochemical Sciences Department, The James Hutton Institute, Invergowrie, Dundee, Scotland, UKDepartment of Food Science and Health, IFAPA-Alameda Del Obispo, SN, Córdoba, SpainDepartment of Food Science and Health, IFAPA-Alameda Del Obispo, SN, Córdoba, SpainNutrition Innovation Centre for Food and Health, University of Ulster, Coleraine, Northern Ireland, UKNutrition Innovation Centre for Food and Health, University of Ulster, Coleraine, Northern Ireland, UKAltnagelvin Area Hospital, Londonderry, Northern Ireland, UKFood Quality and Nutrition Department, Fondazione Edmund Mach, San Michele All'Adige, ItalyDepartment of Veterinary Science, University of Parma, Parma, ItalyAltnagelvin Area Hospital, Londonderry, Northern Ireland, UKDepartment of Food and Nutritional Sciences, University of Reading, Reading, UKDepartment of Chemistry, King Saud University, Riyadh, Saudi ArabiaDepartment of Chemistry, King Saud University, Riyadh, Saudi Arabia; Department of Nutrition University of California, Davis, CA, USANutrition Innovation Centre for Food and Health, University of Ulster, Coleraine, Northern Ireland, UK; Corresponding author.Diets rich in fruit and vegetables are associated with a decreased incidence of colorectal cancer (CRC) due, in part, to the bioactive (poly)phenolic components and their microbiota-mediated metabolites. This study investigated how such compounds, derived from ingested raspberries in the gastrointestinal tract, may exert protective effects by reducing DNA damage. Ileal fluids collected pre- and post-consumption of 300 g of raspberries by ileostomists (n = 11) were subjected to 24 h ex vivo fermentation with fecal inoculum to simulate interaction with colonic microbiota. The impact of fermentation on (poly)phenolics in ileal fluid was determined and the bioactivity of ileal fluids pre- and post fermentation investigated. (Poly)phenolic compounds including sanguiin H-6, sanguiin H-10 and cyanidin-3-O-sophoroside decreased significantly during fermentation while, in contrast, microbial catabolites, including 3-(3′-hydroxyphenyl)propanoic acid, 3-hydroxybenzoic acid and benzoic acid increased significantly. The post-raspberry ileal fermentate from 9 of the 11 ileostomates significantly decreased DNA damage (~30%) in the CCD 841 CoN normal cell line using an oxidative challenge COMET assay. The raspberry ileal fermentates also modulated gene expression of the nuclear factor 2–antioxidant responsive element (Nrf2-ARE) pathway involved in oxidative stress cytoprotection, namely Nrf2, NAD(P)H dehydrogenase, quinone-1 and heme oxygenase-1. Four of the phenolic catabolites were assessed individually, each significantly reducing DNA damage from an oxidative challenge over a physiologically relevant 10–100 μM range. They also induced a differential pattern of expression of key genes in the Nrf2-ARE pathway in CCD 841 CoN cells. The study indicates that the colon-available raspberry (poly)phenols and their microbial-derived catabolites may play a role in protection against CRC in vivo.http://www.sciencedirect.com/science/article/pii/S2213231721000100IleostomyGastrointestinal microbiotaRaspberry (poly)phenolsPhenolic catabolitesFecal fermentationDNA damage