Cited by 565Gut microbiota and healthBacterial Cancer TherapyCancer Immunotherapy and Biomarkers

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Peptostreptococcus anaerobius promotes colorectal carcinogenesis and modulates tumour immunity

Long, Xiaohang, Wong, Chi Chun, Tong, Li, Chu, Eagle S. H., Ho Szeto, Chun, Go, Minne Y. Y., Coker, Olabisi Oluwabukola, Chan, Anthony W. H., Chan, Francis K. L., Sung, Joseph J. Y., Yu, Jun·2019·Nature Microbiology

DOI 10.1038/s41564-019-0541-3

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Abstract

Emerging evidence implicates a role of the gut microbiota in colorectal cancer (CRC). Peptostreptococcus anaerobius (P. anaerobius) is an anaerobic bacterium selectively enriched in the faecal and mucosal microbiota from patients with CRC, but its causative role and molecular mechanism in promoting tumorigenesis remain unestablished. We demonstrate that P. anaerobius adheres to the CRC mucosa and accelerates CRC development in Apc Min/+ mice. In vitro assays and transmission electron microscopy revealed that P. anaerobius selectively adheres to CRC cell lines (HT-29 and Caco-2) compared to normal colonic epithelial cells (NCM460). We identified a P. anaerobius surface protein, putative cell wall binding repeat 2 (PCWBR2), which directly interacts with colonic cell lines via α 2/β 1 integrin, a receptor frequently overexpressed in human CRC tumours and cell lines. Interaction between PCWBR2 and integrin α 2/β 1 induces the activation of the PI3K-Akt pathway in CRC cells via phospho-focal adhesion kinase, leading to increased cell proliferation and nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κB) activation. NF-κB in turn triggers a pro-inflammatory response as indicated by increased levels of cytokines, such as interleukin-10 and interferon-γ in the tumours of P. anaerobius-treated Apc Min/+ mice. Analyses of tumour-infiltrating immune cell populations in P. anaerobius-treated Apc Min/+ mice revealed significant expansion of myeloid-derived suppressor cells, tumour-associated macrophages and granulocytic tumour-associated neutrophils, which are associated with chronic inflammation and tumour progression. Blockade of integrin α 2/β 1 by RGDS peptide, small interfering RNA or antibodies all impair P. anaerobius attachment and abolish P. anaerobius-mediated oncogenic response in vitro and in vivo. Collectively, we show that P. anaerobius drives CRC via a PCWBR2-integrin α 2/β 1-PI3K-Akt-NF-κB signalling axis and identify the PCWBR2-integrin α 2/β 1 axis as a potential therapeutic target for CRC.

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Influential
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“The following primers were used: F. nucleatum , forward 5 ′ -CTG TAT TGC GTT GGA AAC TGT GTA A-3 ′ and reverse 5 ′ -TAC CAG GGT ATC TAA TCC TGT TTG C-3 ′ ; P. anaerobius , forward 5 ′ -AGA CGA ATT CAA GTC AGT AAA TAC A-3 ′ and reverse 5 ′ -CTC CTA TCC ACC AGG ATA TCA A-3 ′ [38].”
Influential

Authors: Long, X., Wong, C. C., Tong, L., Chu, E. S. H., Ho Szeto, C., Go, M. Y. Y., Coker, O. O., Chan, A. W. H., Chan, F. K. L., Sung, J. J. Y., & Yu, J.
Affiliations: Chinese University of Hong Kong (HK)
Corresponding author: Yu, Jun
ORCID: Long, Xiaohang
Wong, Chi Chun
Chu, Eagle S. H.
Coker, Olabisi Oluwabukola
Chan, Anthony W. H.
Chan, Francis K. L.
Sung, Joseph J. Y.
Yu, Jun
Venue: Nature Microbiology
Publisher: Springer Science and Business Media LLC
Published: 2019-09-09
Volume: 4
Issue: 12
Pages: 2319-2330
ISSN: 2058-5276 (ISSN-L)
DOI: 10.1038/s41564-019-0541-3
OpenAlex: W2972734154
Cited by: 557
References: 34
Citations by year: 2026: 88 · 2025: 101 · 2024: 87 · 2023: 112 · 2022: 72 · 2021: 64 · 2020: 31
FWCI: 13.90
Type: journal article
Language: en
Open access: closed
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Nature Microbiology (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Bacterial Cancer Therapy
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Keywords: Peptostreptococcus anaerobius, colorectal cancer, colorectal carcinogenesis, gut microbiota, bacterial adhesion, PI3K/Akt signaling, NF-κB, focal adhesion kinase, tumour immunity, myeloid-derived suppressor cells, tumour-associated macrophages, tumor-associated neutrophils, chronic inflammation, ApcMin/+ mice, RGDS peptide, therapeutic target, tumor microenvironment
MeSH terms: Animals, Biotin, Cell Survival, Colon, Disease Models, Animal, Humans, Male, Mice, Inbred C57BL, Peptostreptococcus, Colorectal Neoplasms, Signal Transduction, Cytokines, NF-kappa B, Caco-2 Cells, HT29 Cells, Phosphatidylinositol 3-Kinases, Gene Expression Profiling, Integrin alpha2beta1, Cell Proliferation, Mice, Focal Adhesion Protein-Tyrosine Kinases, Gene Knockdown Techniques, Carcinogenesis

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Peptostreptococcus anaerobius promotes colorectal carcinogenesis and modulates tumour immunity

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