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Research Article

The Gut Microbiome Modulates Colon Tumorigenesis

Joseph P. Zackular, Nielson T. Baxter, Kathryn D. Iverson, William D. Sadler, Joseph F. Petrosino, Grace Y. Chen, Patrick D. Schloss
Martin J. Blaser, Editor
Joseph P. Zackular
Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, USA
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Nielson T. Baxter
Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, USA
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Kathryn D. Iverson
Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, USA
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William D. Sadler
Department of Internal Medicine, Division of Hematology and Oncology, University of Michigan, Ann Arbor, Michigan, USA
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Joseph F. Petrosino
Human Genome Sequencing Center and Department of Molecular Virology and Microbiology, Baylor College of Medicine, Houston, Texas, USA
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Grace Y. Chen
Department of Internal Medicine, Division of Hematology and Oncology, University of Michigan, Ann Arbor, Michigan, USA
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Patrick D. Schloss
Department of Microbiology and Immunology, University of Michigan, Ann Arbor, Michigan, USA
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Martin J. Blaser
New York University
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DOI: 10.1128/mBio.00692-13
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ABSTRACT

Recent studies have shown that individuals with colorectal cancer have an altered gut microbiome compared to healthy controls. It remains unclear whether these differences are a response to tumorigenesis or actively drive tumorigenesis. To determine the role of the gut microbiome in the development of colorectal cancer, we characterized the gut microbiome in a murine model of inflammation-associated colorectal cancer that mirrors what is seen in humans. We followed the development of an abnormal microbial community structure associated with inflammation and tumorigenesis in the colon. Tumor-bearing mice showed enrichment in operational taxonomic units (OTUs) affiliated with members of the Bacteroides, Odoribacter, and Akkermansia genera and decreases in OTUs affiliated with members of the Prevotellaceae and Porphyromonadaceae families. Conventionalization of germfree mice with microbiota from tumor-bearing mice significantly increased tumorigenesis in the colon compared to that for animals colonized with a healthy gut microbiome from untreated mice. Furthermore, at the end of the model, germfree mice colonized with microbiota from tumor-bearing mice harbored a higher relative abundance of populations associated with tumor formation in conventional animals. Manipulation of the gut microbiome with antibiotics resulted in a dramatic decrease in both the number and size of tumors. Our results demonstrate that changes in the gut microbiome associated with inflammation and tumorigenesis directly contribute to tumorigenesis and suggest that interventions affecting the composition of the microbiome may be a strategy to prevent the development of colon cancer.

IMPORTANCE The trillions of bacteria that live in the gut, known collectively as the gut microbiome, are important for normal functioning of the intestine. There is now growing evidence that disruptive changes in the gut microbiome are strongly associated with the development colorectal cancer. However, how the gut microbiome changes with time during tumorigenesis and whether these changes directly contribute to disease have not been determined. We demonstrate using a mouse model of inflammation-driven colon cancer that there are dramatic, continual alterations in the microbiome during the development of tumors, which are directly responsible for tumor development. Our results suggest that interventions that target these changes in the microbiome may be an effective strategy for preventing the development of colorectal cancer.

  • Copyright © 2013 Zackular et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

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The Gut Microbiome Modulates Colon Tumorigenesis
Joseph P. Zackular, Nielson T. Baxter, Kathryn D. Iverson, William D. Sadler, Joseph F. Petrosino, Grace Y. Chen, Patrick D. Schloss
mBio Nov 2013, 4 (6) e00692-13; DOI: 10.1128/mBio.00692-13

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The Gut Microbiome Modulates Colon Tumorigenesis
Joseph P. Zackular, Nielson T. Baxter, Kathryn D. Iverson, William D. Sadler, Joseph F. Petrosino, Grace Y. Chen, Patrick D. Schloss
mBio Nov 2013, 4 (6) e00692-13; DOI: 10.1128/mBio.00692-13
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