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Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis

There is growing evidence that individuals with colonic adenomas and carcinomas harbor a distinct microbiota. Alterations to the gut microbiota may allow the outgrowth of bacterial populations that induce genomic mutations or exacerbate tumor-promoting inflammation. In addition, it is likely that th...

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Detalles Bibliográficos
Autores principales: Zackular, Joseph P., Baxter, Nielson T., Chen, Grace Y., Schloss, Patrick D.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4863627/
https://www.ncbi.nlm.nih.gov/pubmed/27303681
http://dx.doi.org/10.1128/mSphere.00001-15
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author Zackular, Joseph P.
Baxter, Nielson T.
Chen, Grace Y.
Schloss, Patrick D.
author_facet Zackular, Joseph P.
Baxter, Nielson T.
Chen, Grace Y.
Schloss, Patrick D.
author_sort Zackular, Joseph P.
collection PubMed
description There is growing evidence that individuals with colonic adenomas and carcinomas harbor a distinct microbiota. Alterations to the gut microbiota may allow the outgrowth of bacterial populations that induce genomic mutations or exacerbate tumor-promoting inflammation. In addition, it is likely that the loss of key bacterial populations may result in the loss of protective functions that are normally provided by the microbiota. We explored the role of the gut microbiota in colon tumorigenesis by using an inflammation-based murine model. We observed that perturbing the microbiota with different combinations of antibiotics reduced the number of tumors at the end of the model. Using the random forest machine learning algorithm, we successfully modeled the number of tumors that developed over the course of the model on the basis of the initial composition of the microbiota. The timing of antibiotic treatment was an important determinant of tumor outcome, as colon tumorigenesis was arrested by the use of antibiotics during the early inflammation period of the murine model. Together, these results indicate that it is possible to predict colon tumorigenesis on the basis of the composition of the microbiota and that altering the gut microbiota can alter the course of tumorigenesis. IMPORTANCE Mounting evidence indicates that alterations to the gut microbiota, the complex community of bacteria that inhabits the gastrointestinal tract, are strongly associated with the development of colorectal cancer. We used antibiotic perturbations to a murine model of inflammation-driven colon cancer to generate eight starting communities that resulted in various severities of tumorigenesis. Furthermore, we were able to quantitatively predict the final number of tumors on the basis of the initial composition of the gut microbiota. These results further bolster the evidence that the gut microbiota is involved in mediating the development of colorectal cancer. As a final proof of principle, we showed that perturbing the gut microbiota in the midst of tumorigenesis could halt the formation of additional tumors. Together, alteration of the gut microbiota may be a useful therapeutic approach to preventing and altering the trajectory of colorectal cancer.
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spelling pubmed-48636272016-06-14 Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis Zackular, Joseph P. Baxter, Nielson T. Chen, Grace Y. Schloss, Patrick D. mSphere Research Article There is growing evidence that individuals with colonic adenomas and carcinomas harbor a distinct microbiota. Alterations to the gut microbiota may allow the outgrowth of bacterial populations that induce genomic mutations or exacerbate tumor-promoting inflammation. In addition, it is likely that the loss of key bacterial populations may result in the loss of protective functions that are normally provided by the microbiota. We explored the role of the gut microbiota in colon tumorigenesis by using an inflammation-based murine model. We observed that perturbing the microbiota with different combinations of antibiotics reduced the number of tumors at the end of the model. Using the random forest machine learning algorithm, we successfully modeled the number of tumors that developed over the course of the model on the basis of the initial composition of the microbiota. The timing of antibiotic treatment was an important determinant of tumor outcome, as colon tumorigenesis was arrested by the use of antibiotics during the early inflammation period of the murine model. Together, these results indicate that it is possible to predict colon tumorigenesis on the basis of the composition of the microbiota and that altering the gut microbiota can alter the course of tumorigenesis. IMPORTANCE Mounting evidence indicates that alterations to the gut microbiota, the complex community of bacteria that inhabits the gastrointestinal tract, are strongly associated with the development of colorectal cancer. We used antibiotic perturbations to a murine model of inflammation-driven colon cancer to generate eight starting communities that resulted in various severities of tumorigenesis. Furthermore, we were able to quantitatively predict the final number of tumors on the basis of the initial composition of the gut microbiota. These results further bolster the evidence that the gut microbiota is involved in mediating the development of colorectal cancer. As a final proof of principle, we showed that perturbing the gut microbiota in the midst of tumorigenesis could halt the formation of additional tumors. Together, alteration of the gut microbiota may be a useful therapeutic approach to preventing and altering the trajectory of colorectal cancer. American Society for Microbiology 2015-11-04 /pmc/articles/PMC4863627/ /pubmed/27303681 http://dx.doi.org/10.1128/mSphere.00001-15 Text en Copyright © 2015 Zackular et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Zackular, Joseph P.
Baxter, Nielson T.
Chen, Grace Y.
Schloss, Patrick D.
Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis
title Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis
title_full Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis
title_fullStr Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis
title_full_unstemmed Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis
title_short Manipulation of the Gut Microbiota Reveals Role in Colon Tumorigenesis
title_sort manipulation of the gut microbiota reveals role in colon tumorigenesis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4863627/
https://www.ncbi.nlm.nih.gov/pubmed/27303681
http://dx.doi.org/10.1128/mSphere.00001-15
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