Increased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria

ABSTRACT Intestinal inflammation is a risk factor for colorectal cancer formation, but the underlying mechanisms remain unknown. Here, we investigated whether colitis alters the colonic microbiota to enhance its cancer-inducing activity. Colitis increased epithelial oxygenation in the colon of mice...

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Autores principales:	Stephanie A. Cevallos, Jee-Yon Lee, Connor R. Tiffany, Austin J. Byndloss, Luana Johnston, Mariana X. Byndloss, Andreas J. Bäumler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Escherichia coli colibactin colorectal cancer microbiome Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/346796bc81864744844fecae69c14abd
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spelling	oai:doaj.org-article:346796bc81864744844fecae69c14abd2021-11-15T15:59:42ZIncreased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria10.1128/mBio.02244-192150-7511https://doaj.org/article/346796bc81864744844fecae69c14abd2019-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02244-19https://doaj.org/toc/2150-7511ABSTRACT Intestinal inflammation is a risk factor for colorectal cancer formation, but the underlying mechanisms remain unknown. Here, we investigated whether colitis alters the colonic microbiota to enhance its cancer-inducing activity. Colitis increased epithelial oxygenation in the colon of mice and drove an expansion of Escherichia coli within the gut-associated microbial community through aerobic respiration. An aerobic expansion of colibactin-producing E. coli was required for the cancer-inducing activity of this pathobiont in a mouse model of colitis-associated colorectal cancer formation. We conclude that increased epithelial oxygenation in the colon is associated with an expansion of a prooncogenic driver species, thereby increasing the cancer-inducing activity of the microbiota. IMPORTANCE One of the environmental factors important for colorectal cancer formation is the gut microbiota, but the habitat filters that control its cancer-inducing activity remain unknown. Here, we show that chemically induced colitis elevates epithelial oxygenation in the colon, thereby driving an expansion of colibactin-producing Escherichia coli, a prooncogenic driver species. These data suggest that elevated epithelial oxygenation is a potential risk factor for colorectal cancer formation because the consequent changes in the gut habitat escalate the cancer-inducing activity of the microbiota.Stephanie A. CevallosJee-Yon LeeConnor R. TiffanyAustin J. ByndlossLuana JohnstonMariana X. ByndlossAndreas J. BäumlerAmerican Society for MicrobiologyarticleEscherichia colicolibactincolorectal cancermicrobiomeMicrobiologyQR1-502ENmBio, Vol 10, Iss 5 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli colibactin colorectal cancer microbiome Microbiology QR1-502
spellingShingle	Escherichia coli colibactin colorectal cancer microbiome Microbiology QR1-502 Stephanie A. Cevallos Jee-Yon Lee Connor R. Tiffany Austin J. Byndloss Luana Johnston Mariana X. Byndloss Andreas J. Bäumler Increased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria
description	ABSTRACT Intestinal inflammation is a risk factor for colorectal cancer formation, but the underlying mechanisms remain unknown. Here, we investigated whether colitis alters the colonic microbiota to enhance its cancer-inducing activity. Colitis increased epithelial oxygenation in the colon of mice and drove an expansion of Escherichia coli within the gut-associated microbial community through aerobic respiration. An aerobic expansion of colibactin-producing E. coli was required for the cancer-inducing activity of this pathobiont in a mouse model of colitis-associated colorectal cancer formation. We conclude that increased epithelial oxygenation in the colon is associated with an expansion of a prooncogenic driver species, thereby increasing the cancer-inducing activity of the microbiota. IMPORTANCE One of the environmental factors important for colorectal cancer formation is the gut microbiota, but the habitat filters that control its cancer-inducing activity remain unknown. Here, we show that chemically induced colitis elevates epithelial oxygenation in the colon, thereby driving an expansion of colibactin-producing Escherichia coli, a prooncogenic driver species. These data suggest that elevated epithelial oxygenation is a potential risk factor for colorectal cancer formation because the consequent changes in the gut habitat escalate the cancer-inducing activity of the microbiota.
format	article
author	Stephanie A. Cevallos Jee-Yon Lee Connor R. Tiffany Austin J. Byndloss Luana Johnston Mariana X. Byndloss Andreas J. Bäumler
author_facet	Stephanie A. Cevallos Jee-Yon Lee Connor R. Tiffany Austin J. Byndloss Luana Johnston Mariana X. Byndloss Andreas J. Bäumler
author_sort	Stephanie A. Cevallos
title	Increased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria
title_short	Increased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria
title_full	Increased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria
title_fullStr	Increased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria
title_full_unstemmed	Increased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria
title_sort	increased epithelial oxygenation links colitis to an expansion of tumorigenic bacteria
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/346796bc81864744844fecae69c14abd
work_keys_str_mv	AT stephanieacevallos increasedepithelialoxygenationlinkscolitistoanexpansionoftumorigenicbacteria AT jeeyonlee increasedepithelialoxygenationlinkscolitistoanexpansionoftumorigenicbacteria AT connorrtiffany increasedepithelialoxygenationlinkscolitistoanexpansionoftumorigenicbacteria AT austinjbyndloss increasedepithelialoxygenationlinkscolitistoanexpansionoftumorigenicbacteria AT luanajohnston increasedepithelialoxygenationlinkscolitistoanexpansionoftumorigenicbacteria AT marianaxbyndloss increasedepithelialoxygenationlinkscolitistoanexpansionoftumorigenicbacteria AT andreasjbaumler increasedepithelialoxygenationlinkscolitistoanexpansionoftumorigenicbacteria
_version_	1718426958041186304

Increased Epithelial Oxygenation Links Colitis to an Expansion of Tumorigenic Bacteria

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