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Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer

Author

Listed:
  • Janelle C. Arthur

    (University of North Carolina at Chapel Hill)

  • Raad Z. Gharaibeh

    (University of North Carolina at Charlotte
    University of North Carolina at Charlotte)

  • Marcus Mühlbauer

    (University of North Carolina at Chapel Hill)

  • Ernesto Perez-Chanona

    (University of North Carolina at Chapel Hill
    University of Florida)

  • Joshua M. Uronis

    (University of North Carolina at Chapel Hill
    Present address: Division of Medical Oncology, Department of Medicine, Duke University, PO Box 3382, 2141 CIEMAS Building, Durham, North Carolina 27708, USA)

  • Jonathan McCafferty

    (University of North Carolina at Charlotte)

  • Anthony A. Fodor

    (University of North Carolina at Charlotte)

  • Christian Jobin

    (University of Florida
    University of Florida)

Abstract

Enterobacteria, especially Escherichia coli, are abundant in patients with inflammatory bowel disease or colorectal cancer (CRC). However, it is unclear whether cancer is promoted by inflammation-induced expansion of E. coli and/or changes in expression of specific microbial genes. Here we use longitudinal (2, 12 and 20 weeks) 16S rRNA sequencing of luminal microbiota from ex-germ-free mice to show that inflamed Il10−/− mice maintain a higher abundance of Enterobacteriaceae than healthy wild-type mice. Experiments with mono-colonized Il10−/− mice reveal that host inflammation is necessary for E. coli cancer-promoting activity. RNA-sequence analysis indicates significant changes in E. coli gene catalogue in Il10−/− mice, with changes mostly driven by adaptation to the intestinal environment. Expression of specific genes present in the tumour-promoting E. coli pks island are modulated by inflammation/CRC development. Thus, progression of inflammation in Il10−/− mice supports Enterobacteriaceae and alters a small subset of microbial genes important for tumour development.

Suggested Citation

  • Janelle C. Arthur & Raad Z. Gharaibeh & Marcus Mühlbauer & Ernesto Perez-Chanona & Joshua M. Uronis & Jonathan McCafferty & Anthony A. Fodor & Christian Jobin, 2014. "Microbial genomic analysis reveals the essential role of inflammation in bacteria-induced colorectal cancer," Nature Communications, Nature, vol. 5(1), pages 1-11, December.
    • Handle: RePEc:nat:natcom:v:5:y:2014:i:1:d:10.1038_ncomms5724
    DOI: 10.1038/ncomms5724
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