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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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“Peptostreptococcus anaerobius could promote colorectal carcinogenesis and modulate tumor immunity [30].”
BackgroundWang, Z., Qin, X., Hu, D., Huang, J. M., Guo, E., Xiao, R., Li, W., Sun, C., & Chen, G. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111890 · Cited by 72
The Role of the Microbiome in the Etiopathogenesis of Colon Cancer
Tekle, G. E., Andreeva, N., & Garrett, W. S. (2024) · Annual Review of Physiology · doi:10.1146/annurev-physiol-042022-025619 · Cited by 78
Microbe-based therapies for colorectal cancer: Advantages and limitations
Saeed, M., Shoaib, A., Kandimalla, R., Javed, S., Almatroudi, A., Gupta, R. C., & Aqil, F. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.05.018 · Cited by 69
Qian, M., Liu, J., Zhao, D., Cai, P., Pan, C., Jia, W., Gao, Y., Zhang, Y., Zhang, N., Zhang, Y., et al. (2021) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2021.08.014 · Cited by 71
“After incubation for 2 hours anaerobically, the plate was subjected to aerobic conditions for a total of 24 hours.(66) The treated cells were stained with Oil red O or extracted RNA for qPCR analysis.”
MethodYang, Q., Wang, Y., Wei, X., Zhu, J., Wang, X., Xie, X., & Lü, W. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00286 · Cited by 67
“Peptostreptococcus anaerobius and Fusobacterium nucleatum have been reported to promote tumorigenesis in colorectal cancers (Kostic et al., 2013; Tsoi et al., 2017; Long et al., 2019).”
BackgroundRole of Oral Bacteria in the Development of Oral Squamous Cell Carcinoma
Li, Q., Hu, Y., Zhou, X., Liu, S., Han, Q., & Cheng, L. (2020) · Cancers · doi:10.3390/cancers12102797 · Cited by 71
“Peptostreptococcus, Parvimonas, and Campylobacter are anaerobic bacteria reported to participate in the colorectal cancer process [30,31].”
BackgroundThe role of the gut microbiota in tumor, immunity, and immunotherapy
Xie, Y., & Liu, F. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1410928 · Cited by 75
Friend or Foe? Recent Strategies to Target Myeloid Cells in Cancer
Chaib, M., Chauhan, S. C., & Makowski, L. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00351 · Cited by 65
“These findings propose Peptostreptococcus anaerobius-induced PCWBR2-integrin α2/β1 axis as a potential therapeutic target in colorectal cancer (Long et al., 2019).”
BackgroundZhu, R., Lang, T., Yan, W., Zhu, X. G., Huang, X. Y., Yin, Q., & Li, Y. (2021) · Advanced Science · doi:10.1002/advs.202003542 · Cited by 65
Gut mucosal microbiota profiles linked to colorectal cancer recurrence
Huo, R., Wang, Y., Hou, S., Wang, W., Zhang, C.-Z., & Wan, X. (2022) · World Journal of Gastroenterology · doi:10.3748/wjg.v28.i18.1946 · Cited by 69
Association of Cervical Dysbacteriosis, HPV Oncogene Expression, and Cervical Lesion Progression
Liu, H., Liang, H., Li, D., Wang, M., & Li, Y. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.00151-22 · Cited by 70
“responses and the promotion of colorectal carcinogenesis (31).”
BackgroundThe effect of periodontal bacteria infection on incidence and prognosis of cancer
Li, X., Zhang, Q., Peng, Y., Wang, D., & Liu, Y. (2020) · Medicine · doi:10.1097/md.0000000000019698 · Cited by 66
Colon Cancer: From Epidemiology to Prevention
Katsaounou, K., Nicolaou, E., Vogazianos, P., Brown, C., Stavrou, M., Teloni, S., Hatzis, P., Agapiou, A., Fragkou, E., Tsiaoussis, G. I., et al. (2022) · Metabolites · doi:10.3390/metabo12060499 · Cited by 65
“anaerobius generate a pro-inflammatory immune microenvironment in ApcMin/+ mice, leading to the immune cell infiltration of tumours and their progression [92,93].”
BackgroundCrosstalk between autophagy and microbiota in cancer progression
Wang, Y., Du, J., Wu, X., Abdelrehem, A., Ren, Y., Liu, C., Zhou, X., & Wang, S. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01461-0 · Cited by 61
“[70] FadA Fusobacterium adhesin A, STAT3 Signal transducer and activator of transcription3, TLR2 toll-like receptor2, TLR4 toll-like receptor4, ROS reactive oxygen species, PCWBR2 putative cell wall binding repeat 2, SGMB Streptococcus gallolyticus member bacteria, IL-1 interleukin 1, COX-2 cyclooxygenase-2, IL-8 inte…”
BackgroundInfluentialEffects of gut microbiota on immune responses and immunotherapy in colorectal cancer
Hou, X., Zheng, Z., Wei, J., & Zhao, L. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1030745 · Cited by 61
“Tryptophan-derived microbial metabolites activate the aryl hydrocarbon receptor in TAMs to suppress anti-tumor immunity (51).”
BackgroundInfluentialMelatonin–Microbiome Two-Sided Interaction in Dysbiosis-Associated Conditions
Ieșanu, M. I., Zahiu, C. D. M., Dogaru, I.-A., Chiţimuș, D. M., Pîrcălăbioru, G. G., Voiculescu, S. E., Isac, S., Galoş, F., Pavel, B., O’Mahony, S. M., et al. (2022) · Antioxidants · doi:10.3390/antiox11112244 · Cited by 63
Microbiota and Colorectal Cancer: From Gut to Bedside
Silva, M. G., Brunner, V., & Tschurtschenthaler, M. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.760280 · Cited by 61
Bacterial‐Mediated Tumor Therapy: Old Treatment in a New Context
Liu, Y., Niu, L., Li, N., Wang, Y., Liu, M., Su, X., Bao, X., Yin, B., & Shen, S. (2023) · Advanced Science · doi:10.1002/advs.202205641 · Cited by 56
Microbiota-Associated Metabolites and Related Immunoregulation in Colorectal Cancer
Chen, Y., & Chen, Y. (2021) · Cancers · doi:10.3390/cancers13164054 · Cited by 54
Gut microbiota modulation: a tool for the management of colorectal cancer
Wang, Y., & Li, H. (2022) · Journal of Translational Medicine · doi:10.1186/s12967-022-03378-8 · Cited by 58
“anaerobius-treated mice exhibited a significant increase in the population of tumor-associated macrophages (TAMs), granulocytic tumor-associated neutrophils, and myeloidderived suppressor cells, which are involved in chronic inflammation and tumor development [66].”
BackgroundMima, K., Kosumi, K., Baba, Y., Hamada, T., Baba, H., & Ogino, S. (2020) · Human Genetics · doi:10.1007/s00439-020-02235-2 · Cited by 51
“2019) Peptostreptococcus anaerobius can activate the NFKB signaling pathway in colorectal cancer cell lines and inhibit T-cell-mediated immune responses against colorectal tumors through the recruitment of myeloid-derived suppressor cells and tumor-associated macrophages into the tumor microenvironment in the ApcMin/+…”
BackgroundLiu, J., Yan, Q., Li, S., Jiao, J., Hao, Y., Zhang, G., Zhang, Q., Luo, F., Zhang, Y., Lv, Q., et al. (2024) · npj Biofilms and Microbiomes · doi:10.1038/s41522-024-00499-4 · Cited by 58
“The probe sequences used in the FISH experiments were as follows: FAM-conjugated EUB338 universal bacterial probe (GCTGCCTCCCGT AGGAGT) 76 , and Cy3-conjugated speci fi c probes targeting Streptococcus salivarius (GATGACGAATAGGTGTTAG), Roseburia intestinalis (ATTAGAGGCGGTCAAGAA), Bi fi dobacterium…”
MethodStreptococcus Pneumoniae Promotes Lung Cancer Development and Progression
Li, N., Zhou, H., Holden, V. K., Deepak, J., Dhilipkannah, P., Todd, N. W., Stass, S. A., & Jiang, F. (2022) · iScience · doi:10.1016/j.isci.2022.105923 · Cited by 55
Liu, Z., Zhang, D., & Chen, S. (2024) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-024-03034-7 · Cited by 51
“…its distinctive effector molecule, ADP-glycerol-β-D-mannoheptulose [138, 139], Peptostreptococcus anaerobiu s and Bacteroides fragilis which were observed to increase in GC, can activate NF-κB signaling pathway via inducing intra-cellular synthesis of ROS and IL-17 respectively in CRC [140, 141].”
BackgroundTumor microbiome: roles in tumor initiation, progression, and therapy
Zhang, S., Huang, J., Jiang, Z., Tong, H., Ma, X., & Liu, Y. (2025) · Molecular Biomedicine · doi:10.1186/s43556-025-00248-9 · Cited by 58
Gut Microbiota and Colorectal Cancer: A Balance Between Risk and Protection
Ionescu, V. A., Diaconu, C. C., Gheorghe, G., Mihai, M.-M., Diaconu, C. C., Bostan, M., & Bleoţu, C. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26083733 · Cited by 55
“Peptostreptococcus anaerobius interacts via its putative cell wall binding repeat 2 (PCWBR2) surface protein with α 2/ β 1 integrins on colonic epithelial cells [105].”
InfluentialgutMEGA: a database of the human gut MEtaGenome Atlas
Zhang, Q., Yu, K., Li, S., Zhang, X.-L., Zhao, Q., Zhao, X., Liu, Z., Cheng, H. L., Li, X., & Li, X. (2020) · Briefings in Bioinformatics · doi:10.1093/bib/bbaa082 · Cited by 50
Harness the functions of gut microbiome in tumorigenesis for cancer treatment
Lee, M. (2021) · Cancer Communications · doi:10.1002/cac2.12200 · Cited by 50
“In animal studies, its oncogenic role was confirmed to facilitate CRC development in ApcMin/+ mice [35].”
BackgroundInfluentialKabwe, M., Dashper, S. G., Bachrach, G., & Tucci, J. (2021) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuab017 · Cited by 52
Fang, L., Ford-Roshon, D., Russo, M., O’Brien, C., Xiong, X., Gurjao, C., Grandclaudon, M., Raghavan, S., Corsello, S. M., Carr, S. A., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30794-7 · Cited by 49
Prenatal Maternal Stress Exacerbates Experimental Colitis of Offspring in Adulthood
Sun, Y., Xie, R., Lü, L., Jin, G., Zhou, B., Huang, H., Li, M., Yang, Y., Liu, X., Cao, X., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.700995 · Cited by 49
“org 4 Fluorescence In Situ Hybridization Fluorescence in situ hybridization (FISH) was performed as described previously (40).”
Method
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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