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Intracellular colon cancer-associated Escherichia coli promote protumoral activities of human macrophages by inducing sustained COX-2 expression
Open accessAbstract
Intestinal dysbiosis has been reported in patients with colorectal cancer, and there is a high prevalence of Escherichia coli belonging to B2 phylogroup and producing a genotoxin, termed colibactin. Macrophages are one of the predominant tumor-infiltrating immune cells supporting key processes in tumor progression by producing protumoral factors such as cyclooxygenase-2 (COX-2). Here, we investigated whether B2 E. coli colonizing colon tumors could influence protumoral activities of macrophages. In contrast to commensal or nonpathogenic E. coli strains that were efficiently and rapidly degraded by macrophages at 24 h after infection, colon cancer-associated E. coli were able to resist killing by human THP-1 macrophages, to replicate intracellularly, and to persist inside host cells until at least 72 h after infection. Significant increases in COX-2 expression were observed in macrophages infected with colon cancer E. coli compared with macrophages infected with commensal and nonpathogenic E. coli strains or uninfected cells at 72 h after infection. Induction of COX-2 expression required live bacteria and was not due to colibactin production, as similar COX-2 levels were observed in macrophages infected with the wild-type colon cancer-associated E. coli 11G5 strain or a clbQ mutant unable to produce colibactin. Treatment of macrophages with ofloxacin, an antibiotic with intracellular tropism, efficiently decreased the number of intracellular bacteria and suppressed bacteria-induced COX-2 expression. This study provides new insights into the understanding of how tumor- infiltrating bacteria could influence cancer progression through their interaction with immune cells. Manipulation of microbes associated with tumors could have a deep influence on the secretion of protumoral molecules by infiltrating macrophages.
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“In CRC patients, it is known that the composition of the microbiota is one of the factors favoring the development of carcinogenic lesions, notably by the presence of genotoxic bacteria such as Fusobacterium nucleatum or colibactin-producing Escherichia coli (124, 125).”
From Bifidobacteria and Their Health-Promoting Effects (2017) · cites this paper as [124]
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“This is supported by the observation that (i) some bacteria can induce activation of the inflammatory signaling pathway [109]; (ii) COX-2 expression was increased in macrophages infected with the wild-type colon cancer-associated E.”
The Role of Escherichia coli in the Development and Progression of Cancer
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“Moreover, CoPEC infection significantly upregulates COX-2 expression in macrophages, thereby enhancing their pro-tumor activity [56].”
The role of COX-2 and its use as a therapeutic target in IBD and related colorectal cancer
Yang, L., Akanyibah, F. A., Yao, D., Jin, T., & Mao, F. (2025) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2025.110516 · Cited by 13
Correlation between Colon Polyps and Metabolic Syndrome and HP Infection Status
Huang, L., Wu, L., Qiao, Q., & Fang, L. (2019) · Gastroenterology Research and Practice · doi:10.1155/2019/3916154 · Cited by 12
“the proliferation of gastric mucosa, and promote the proliferation and metastasis of gastric tumor cells [19, 20].”
BackgroundGut bacteria, host immunity, and colorectal cancer: From pathogenesis to therapy
Li, Y., Peng, J., & Meng, X. (2024) · European Journal of Immunology · doi:10.1002/eji.202451022 · Cited by 11
“…replicate, and persist inside macrophages, and infected macrophages can activate the JNK/p38 mitogen-activated protein kinase signaling pathway to increase the expression of cyclooxygenase-2, a pivotal risk factor closely linked to the occurrence, progression, and prognosis of CRC [72, 73].”
Sheppe, A. E. F., Santelices, J., Czyż, D. M., & Edelmann, M. J. (2021) · Microbiology Spectrum · doi:10.1128/spectrum.00496-21 · Cited by 11
“way of controlling COX-2 transcription in this process (9, 21, 71, 72), although MEK also”
BackgroundLou, Y., Song, M., Han, M., Zhong, J., Tian, X., Ren, Y., Song, Y., Duan, L., Zhao, P., Song, X., et al. (2022) · Cancer Immunology Research · doi:10.1158/2326-6066.cir-21-0666 · Cited by 10
Microbiota-associated mechanisms in colorectal cancer
González, A., Fullaondo, A., & Odriozola, A. (2024) · Advances in genetics · doi:10.1016/bs.adgen.2024.05.002 · Cited by 8
Nouri, R., Hasani, A., Shirazi, K. M., Sefiadn, F. Y., Mazraeh, F. N., Sattarpour, S., & Rezaee, M. A. (2024) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/j.diagmicrobio.2024.116229 · Cited by 6
Phenotypic characterization and complete genome of a tumorigenic pathobiont Escherichia coli LI60C3
Yu, L. C., Wei, S., Li, Y.-H., Huang, C., Pai, Y.-C., Hung, Y.-M., Lai, L., & Ni, Y. (2025) · Gut Pathogens · doi:10.1186/s13099-025-00732-1 · Cited by 5
“Additionally, colibactin-producing E. coli have been identified for their roles in causing DNA damage and cell senescence in epithelial cells in vitro, as well as promoting severe colitis and invasive tumor growth in chemically induced and genetically modified mice [26–33].”
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Advancements in Understanding and Preventing Obesity-Related Colon Cancer
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“Another study [17] found links between microbes and cancer.”
Advancements in the Pathogenesis, Diagnosis, and Therapeutic Implications of Intestinal Bacteria
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“coli has been reported [7] in addition to mucosal translocation and intracellular persistence in human macrophages [8], which ultimately may lead to invasion of the bloodstream.”
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Role of Bacterial Infection (H. pylori) in Colon Carcinogenesis and Therapeutic Approaches
Singh, P., Tiwari, S. P., Mehdi, M. M., & Sharma, R. (2021) · Springer eBooks · doi:10.1007/978-3-030-64668-4_6 · Cited by 3
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Bacteria-Based Roles in Solid Tumors: Potential for Prevention and Treatment
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Gut microbiota-driven diseases and intervention strategies – lessons from China
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“It has been shown that excessive intake of red meat associated with increased consumption of cholesterol could induce the development of cancers, including CRC.”
InfluentialBioactive lipids and gut microbiota interact to regulate health and disease
Das, U. N. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-821039-0.00011-3 · Cited by 1
Bacteria and cancer: Advances, perspectives and applications
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Dysbiosis Promotes Gastric Diseases and Impede Therapies by Hijacking Gut Immune HomeostasisPreprint
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Additional file 1 of E. coli diversity: low in colorectal cancer
Tang, L. M., Zhou, Y., Zhu, S., Liang, G.-D., Zhuang, H., Zhao, M.-F., Chang, X., Li, H., Liu, Z., Guo, Z., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12097164
Additional file 3 of E. coli diversity: low in colorectal cancer
Tang, L., Zhou, Y., Zhu, S., Liang, G.-D., Zhuang, H., Zhao, M.-F., Chang, X., Li, H., Liu, Z., Guo, Z., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12097173
Additional file 2 of E. coli diversity: low in colorectal cancer
Tang, L., Zhou, Y., Zhu, S., Liang, G.-D., Zhuang, H., Zhao, M.-F., Chang, X., Li, H., Liu, Z., Guo, Z., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12097170
Fecal Microbiota Transplantation and Cancer Immunotherapy: Current Evidence and Future Directions
Mokhtarpour, K., Akbarzadehmoallemkolaei, M., & Rezaei, N. (2024) · Interdisciplinary cancer research · doi:10.1007/16833_2024_419
Additional file 4 of E. coli diversity: low in colorectal cancer
Tang, L., Zhou, Y.-J., Zhu, S., Liang, G.-D., Zhuang, H., Zhao, M.-F., Chang, X.-Y., Li, H.-N., Liu, Z., Guo, Z.-R., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12097182
Rôle de la voie COX-2 au cours de l'infection par Brucella
Gagnaire, A. (2016) · theses.fr (ABES) · doi:10.70675/2f54eb87za0e5z4e1dzb465z168c5d1054de
Metadata
- Authors
- Raisch, J., Rolhion, N., Dubois, A., Darfeuille-Michaud, A., & Bringer, M.-A.
- Affiliations
- Inserm (FR)
- Imperial College London (GB)
- Corresponding author
- Bringer, Marie-Agnès
- Venue
- Laboratory Investigation
- Publisher
- Elsevier BV
- Published
- 2015-03
- Volume
- 95
- Issue
- 3
- Pages
- 296-307
- ISSN
- 0023-6837 (ISSN-L)
- OpenAlex
- W2094274080
- Cited by
- 100
- References
- 62
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 13 · 2023: 6 · 2022: 9 · 2021: 16 · 2020: 11 · 2019: 6 · 2018: 10 · 2017: 10 · 2016: 7 · 2015: 1
- FWCI
- 4.23
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Laboratory Investigation (publishedVersion, other-oa)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Funders
- Imperial College London
- Institut National de la Santé et de la Recherche Médicale (UMR 1071, USC-2018)
- Ligue Contre le Cancer
- Institut National de la Recherche Agronomique (USC-2018)
- Topics
- Life Sciences › Immunology and Microbiology › Microbiology › Escherichia coli research studies
- Life Sciences › Immunology and Microbiology › Immunology › Immune cells in cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Bacterial Cancer Therapy
- Keywords
- colorectal cancer, tumor-associated macrophages, COX-2 expression, intracellular bacterial replication, colibactin, ofloxacin, THP-1 macrophages, gut dysbiosis
- MeSH terms
- Colonic Neoplasms, Escherichia coli, Humans, Macrophages, Peptides, Vacuoles, Immunoblotting, Dinoprostone, Microscopy, Confocal, Cell Line, Tumor, Microscopy, Electron, Transmission, p38 Mitogen-Activated Protein Kinases, Microbial Viability, Cyclooxygenase 2, Host-Pathogen Interactions, Polyketides
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