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Peptostreptococcus anaerobius promotes colorectal carcinogenesis and modulates tumour immunity
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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“Some members of this signature, such as F. nucleatum and P. anaerobius, have been shown to promote colorectal carcinogenesis and modulate tumour immunity74,75”
From Gut OncoMicrobiome Signatures (GOMS) as next-generation biomarkers for cancer immunotherapy (2023) · cites this paper as [75]
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The gut microbiota can orchestrate the signaling pathways in colorectal cancer
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Fecal Bacteria as Non-Invasive Biomarkers for Colorectal Adenocarcinoma
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“It has been reported that peptostreptococcus anaerobius, an anaerobic bacterium enriched in the fecal and mucosal microbiota from CRC patients, promotes CRC (23).”
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“Simultaneously, it modulates the frequencies of regulatory T cells, Th-17 cells, and CD8+ T cells (Figure 3C) (72).”
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“stomatis and Treponema denticola in the surveyed ESCC samples is also consistent with previous studies examining bacteria-associated oncogenic pathways.(29,34) We discerned that some species of the genus Porphyromonas exhibited opposite trends of dominance in the upper aerodigestive tract SCC.”
ResultThe role of microbiomes in gastrointestinal cancers: new insights
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“Subsequent examinations of functional nature revealed that P. anaerobius expedited the progression of AOM-induced CRC by augmenting the synthesis of cholesterol through the activation of TLR2/TLR4 signaling, thereby bolstering the proliferation of CRC cells (85, 86).”
BackgroundGut microbiome in tumorigenesis and therapy of colorectal cancer
Wang, L., Yu, K., Hou, Y., Guo, M., Yao, F., & Chen, Z. (2022) · Journal of Cellular Physiology · doi:10.1002/jcp.30917 · Cited by 31
“For instance, Peptostreptococcus anaerobius, an anaerobic bacterium, can activate PI3K‐Akt and NF‐κB signaling pathways to enhance pro‐inflammatory factor release from epithelial (Long et al., 2019).”
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“anaerobius modulated the integrin α2/β1-phosphoinositide 3-kinase-Akt-NF-κB signaling pathway [47].”
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Effect of gut microbiota in the colorectal cancer and potential target therapy
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“ing inflammation and DNA damage and protecting cancer from immune attack [16, 17].”
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“These effects promoted tumor progression (Long et al., 2019).”
Dingenen, L. V., Segers, C., Wouters, S., Mysara, M., Leys, N., Kumar‐Singh, S., Malhotra‐Kumar, S., & Houdt, R. V. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1298264 · Cited by 29
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“Interestingly, Fusobacterium nucleatum [30,39–42] and Peptostreptococcus anaerobius [43,44] have also been implicated in the development of colorectal cancer.”
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“[17] BBR, a common isoquinoline alkaloid, was originally extracted from the rhizome of Coptis and has been used to treat bacterial diarrhea in China for thousands of years.”
BackgroundFeng, C., Li, N., Gao, G., He, Q., Kwok, L., & Zhang, H. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25073768 · Cited by 27
“For example, typical Fusobacterium nucleatum could recruit tumor-infiltrating bone marrow cells, inhibiting T cells and natural killer cells [42]; Peptostreptococcus anaerobius could increase tumor-associated macrophages and neutrophils, ultimately leading to tumor progression [43].”
BackgroundAhmad, A., Mahmood, N., Raza, M. A., Mushtaq, Z., Saeed, F., Afzaal, M., Hussain, M., Amjad, H., & Al-Awadi, H. M. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e29495 · Cited by 32
The Role of Gut Microbiota in Modulating Tumor Growth and Anticancer Agent Efficacy
Kim, J.-H., & Lee, H. K. (2021) · Molecules and Cells · doi:10.14348/molcells.2021.0032 · Cited by 27
“In a colorectal cancer mouse model, this strain was found to accelerate tumor growth (Long et al., 2019).”
BackgroundLegaria, M. C., Nastro, M., Camporro, J., Heger, F., Barberis, C. M., Stecher, D., Rodríguez, C. H., & Vay, C. A. (2021) · Anaerobe · doi:10.1016/j.anaerobe.2021.102461 · Cited by 26
Mohammadi, M., Mirzaei, H., & Motallebi, M. (2021) · Anaerobe · doi:10.1016/j.anaerobe.2021.102501 · Cited by 26
The Tissue-Associated Microbiota in Colorectal Cancer: A Systematic Review
da Costa, C. P., Vieira, P. F., Mendes-Rocha, M., Pereira‐Marques, J., Ferreira, R. M., & Figueiredo, C. (2022) · Cancers · doi:10.3390/cancers14143385 · Cited by 29
“Peptostreptococcus anaerobius surface protein PCWBR2 interacts with host cell α2/β1 integrins, enhancing cell proliferation and a pro-inflammatory immune environment, which promotes CRC development in mice [85].”
BackgroundLin, J., Huang, M., Sun, Z., Chen, L., Lei, Y., Huang, Y., Qi, M., Fan, S.-R., Chen, S.-G., Chung, C., et al. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.121715 · Cited by 26
Dong, Y., Meng, F., Wang, J., Wei, J., Zhang, K., Qin, S., Li, M., Wang, F., Wang, B., Liu, T., et al. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2446376 · Cited by 28
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Implication of gut microbes and its metabolites in colorectal cancer
Kumar, A., Ali, A., Kapardar, R. K., Dar, G. M., Nimisha, Apurva, A., Sharma, A. K., Verma, R., Sattar, R. S. A., Ahmad, E., et al. (2022) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-022-04422-2 · Cited by 26
Zhang, H., Jin, K., Xiong, K., Jing, W., Pang, Z., Feng, M., & Cheng, X. (2023) · Cancer Medicine · doi:10.1002/cam4.6194 · Cited by 23
Zeng, W., Wang, Y., Wang, Z., Yu, M., Liu, K., Zhao, C., Pan, Y., & Ma, S. (2023) · Discover Oncology · doi:10.1007/s12672-023-00748-6 · Cited by 27
“Peptostreptococcus anaerobius induces adhesion to colonic epithelial cells by binding membrane protein PCWBR2 to integrin α2/β1, which induces downstream PI3K/NF-κB signaling cascade activation to promote colon cancer growth (29).”
BackgroundWang, S., Xu, B., Zhang, Y., Chen, G., Zhao, P., Gao, Q., & Yuan, L. (2023) · Cancer Biology and Medicine · doi:10.20892/j.issn.2095-3941.2023.0376 · Cited by 24
Gut microbiota and immune alteration in cancer development: implication for immunotherapy
Lau, H. C.-H., Zhang, X., & Yu, J. (2023) · eGastroenterology · doi:10.1136/egastro-2023-100007 · Cited by 24
“30 Parvi-monas micra is another pathogenic bacterium that is enriched in patients with CRC, and it has been identified by several studies as an independent risk factor of CRC with poor survival.”
Self-citationMicrobe-based management for colorectal cancer
Gao, Z.-Y., Cui, Z., Yan, Y.-Q., Ning, L.-J., Wang, Z.-H., & Hong, J. (2021) · Chinese Medical Journal · doi:10.1097/cm9.0000000000001887 · Cited by 26
“This specific axis might become a potential therapeutic target for CRC.([49])”
BackgroundGut Microbiota and Colorectal Cancer Risk Factors
Feizi, H., Rezaee, M. A., Ghotaslou, R., Sadrkabir, M., Jadidi‐Niaragh, F., Gholizadeh, P., Taghizadeh, S., Ghanbarov, K., Yousefi, M., & Kafil, H. S. (2022) · Current Pharmaceutical Biotechnology · doi:10.2174/1389201023666221005103340 · Cited by 25
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“Meanwhile, we performed biotinylated L. acidophilus pull-down assay to characterize L. acid-ophilus interacting epithelial proteins by mass spectrometry 38,39 .”
Gut dysbiosis in cancer immunotherapy: microbiota-mediated resistance and emerging treatments
Eiman, L., Moazzam, K., Anjum, S., Kausar, H., Sharif, E. A. M., & Ibrahim, W. N. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1575452 · Cited by 28
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“Additionally, when compared with two commonly used colorectal cancer cell lines (HT-29 and Caco-2), the human normal colon mucosal epithelial cell line, NCM460, generated different functions [18].”
ResultStatistical modeling of gut microbiota for personalized health status monitoring
Zhu, J., Xie, H., Yang, Z., Chen, J., Yin, J., Tian, P., Wang, H., Zhao, J., Zhang, H., Lu, W., et al. (2023) · Microbiome · doi:10.1186/s40168-023-01614-x · Cited by 24
Epidemiology and early screening strategies for colorectal cancer in China
Yang, Y., Gao, Z., Huang, A., Shi, J., Sun, Z. Z., Hong, H., & Gu, J. (2023) · Chinese Journal of Cancer Research · doi:10.21147/j.issn.1000-9604.2023.06.05 · Cited by 23
Zhang, W., Jin, C., Liu, S., Wan, X., Li, Y., Liu, J., Duan, Z., Ma, J., & Gao, Y. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1757513 · Cited by 22
“Its surface protein PCWBR2 binds integrin a 2/ b 1 on tumor epithelium, activating PI3K – Akt – NF-k B signaling and promoting in fl ammatory and suppressive-cell in fi ltration (110).”
Modulating the gut microbiota: A novel perspective in colorectal cancer treatment
Bai, X., Liu, B., Fan, D., Lu, Y., & Zhao, X. (2025) · Cancer Letters · doi:10.1016/j.canlet.2025.217459 · Cited by 23
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“Peptostreptococcus promotes colorectal carcinogenesis and modulates tumor immunity (39).”
BackgroundCorrelation between Olive Oil Intake and Gut Microbiota in Colorectal Cancer Prevention
Memmola, R., Petrillo, A., Lorenzo, S. D., Altuna, S. C., Habeeb, B. S., Soggiù, A., Bonizzi, L., Garrone, O., & Ghidini, M. (2022) · Nutrients · doi:10.3390/nu14183749 · Cited by 25
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“NCM460 is a normal human colonic mucosal epithelial cell line and has become an important in vitro experimental model for intestinal research owning to its potential characteristics before carcinogenesis when the culture is in vitro [33,34].”
BackgroundCrosstalk between gut microbiota and RNA N6-methyladenosine modification in cancer
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Modifications of microbiome-derived cell-free RNA in plasma discriminates colorectal cancer samples
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Metadata
- 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
- Venue
- Nature Microbiology
- Published
- 2019-09-09
- Volume
- 4
- Issue
- 12
- Pages
- 2319-2330
- ISSN
- 2058-5276 (ISSN-L)
- 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
- 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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