The DOI matches its Crossref record; 43 of the 43 references it cites were found in a registry or an index.
Fusobacterium nucleatum Potentiates Intestinal Tumorigenesis and Modulates the Tumor-Immune Microenvironment
Open accessAbstract
Increasing evidence links the gut microbiota with colorectal cancer. Metagenomic analyses indicate that symbiotic Fusobacterium spp. are associated with human colorectal carcinoma, but whether this is an indirect or causal link remains unclear. We find that Fusobacterium spp. are enriched in human colonic adenomas relative to surrounding tissues and in stool samples from colorectal adenoma and carcinoma patients compared to healthy subjects. Additionally, in the Apc(Min/+) mouse model of intestinal tumorigenesis, Fusobacterium nucleatum increases tumor multiplicity and selectively recruits tumor-infiltrating myeloid cells, which can promote tumor progression. Tumors from Apc(Min/+) mice exposed to F. nucleatum exhibit a proinflammatory expression signature that is shared with human fusobacteria-positive colorectal carcinomas. However, unlike other bacteria linked to colorectal carcinoma, F. nucleatum does not exacerbate colitis, enteritis, or inflammation-associated intestinal carcinogenesis. Collectively, these data suggest that, through recruitment of tumor-infiltrating immune cells, fusobacteria generate a proinflammatory microenvironment that is conducive for colorectal neoplasia progression.
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“The gut microbiome has been shown to have multiple effects on tumor biology, such as the transformation process, tumor progression, and the response to anticancer therapies including immunotherapy (21-29).”
From The human tumor microbiome is composed of tumor type–specific intracellular bacteria (2020) · cites this paper as [22]
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“The activation of NF-kB promoted the transcription of pro-inflammatory cytokines such as TNF-α and IL-6, which may explain the accumulation of immunosuppressive myeloid cells in TME [59] (Fig. 2).”
From Gut microbiota-mediated immunomodulation in tumor (2021) · cites this paper as [59]
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“Kostic et al. found a correlation between a high abundance of F. nucleatum and activated NF-κB in CRC.”
From Gut microbiota-mediated immunomodulation in tumor (2021) · cites this paper as [59]
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Cites
Jemal, A., Bray, F., Ferlay, J., Ward, E., & Forman, D. (2011) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.20107 · Cited by 55,044
Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation
Vander Heiden, M. G., Cantley, L. C., & Thompson, C. B. (2009) · Science · doi:10.1126/science.1160809 · Cited by 16,197
Structure, function and diversity of the healthy human microbiome
The Human Microbiome Project Consortium (2012) · Nature · doi:10.1038/nature11234 · Cited by 11,726
Comprehensive molecular characterization of human colon and rectal cancer
The Cancer Genome Atlas Network (2012) · Nature · doi:10.1038/nature11252 · Cited by 8,499
Myeloid-derived-suppressor cells as regulators of the immune system
Gabrilovich, D. I., & Nagaraj, S. (2009) · Nature Reviews Immunology · doi:10.1038/nri2506 · Cited by 6,753
Macrophage Diversity Enhances Tumor Progression and Metastasis
Qian, B., & Pollard, J. W. (2010) · Cell · doi:10.1016/j.cell.2010.03.014 · Cited by 5,338
Cancer immunotherapy comes of age
Mellman, I., Coukos, G., & Dranoff, G. (2011) · Nature · doi:10.1038/nature10673 · Cited by 3,893
Coordinated regulation of myeloid cells by tumours
Gabrilovich, D. I., Ostrand-Rosenberg, S., & Bronte, V. (2012) · Nature Reviews Immunology · doi:10.1038/nri3175 · Cited by 3,544
Neutrophils in the activation and regulation of innate and adaptive immunity
Mantovani, A., Cassatella, M. A., Costantini, C., & Jaillon, S. (2011) · Nature reviews. Immunology · doi:10.1038/nri3024 · Cited by 3,159
Regulatory T cells: mechanisms of differentiation and function
Josefowicz, S. Z., Lu, L.-F., & Rudensky, A. Y. (2012) · Annual Review of Immunology · doi:10.1146/annurev.immunol.25.022106.141623 · Cited by 2,866
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Michaud, D. S., Lu, J., Peacock-Villada, A. Y., Barber, J. R., Joshu, C. E., Prizment, A. E., Beck, J. D., Offenbacher, S., & Platz, E. A. (2018) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djx278 · Cited by 171
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Hegarty, J. W., Guinane, C. M., Ross, R. P., Hill, C., & Cotter, P. D. (2016) · F1000Research · doi:10.12688/f1000research.9615.1 · Cited by 141
Periodontal disease, tooth loss and colorectal cancer risk: results from the Nurses’ Health Study
Momen-Heravi, F., Babic, A., Tworoger, S. S., Zhang, L., Wu, K., Smith-Warner, S. A., Ogino, S., Chan, A. T., Meyerhardt, J., Giovannucci, E., et al. (2017) · International Journal of Cancer · doi:10.1002/ijc.30486 · Cited by 137
Self-citationYang, Y., Cai, Q., Shu, X., Steinwandel, M. D., Blot, W. J., Zheng, W., & Long, J. (2019) · International Journal of Cancer · doi:10.1002/ijc.31941 · Cited by 135
Atanasova, K. R., & Yilmaz, Ö. (2014) · Molecular Oral Microbiology · doi:10.1111/omi.12047 · Cited by 129
Gut microbiota-mediated immunomodulation in tumor
Liu, X., Chen, Y., Zhang, S., & Dong, L. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-01983-x · Cited by 112
Raisch, J., Rolhion, N., Dubois, A., Darfeuille-Michaud, A., & Bringer, M.-A. (2015) · Laboratory Investigation · doi:10.1038/labinvest.2014.161 · Cited by 100
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Khan, S. T., Al-Khedhairy, A. A., & Musarrat, J. (2015) · Journal of Nanoparticle Research · doi:10.1007/s11051-015-3074-6 · Cited by 100
The Impact of Intratumoral and Gastrointestinal Microbiota on Systemic Cancer Therapy
Cogdill, A. P., Gaudreau, P. O., Arora, R., Gopalakrishnan, V., & Wargo, J. A. (2018) · Trends in Immunology · doi:10.1016/j.it.2018.09.007 · Cited by 98
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Crosstalk between gut microbiota and Sirtuin-3 in colonic inflammation and tumorigenesis
Zhang, Y., Wang, X.-L., Zhou, M., Kang, C., Lang, H.-D., Chen, M.-T., Hui, S.-C., Wang, B., & Mi, M.-T. (2018) · Experimental & Molecular Medicine · doi:10.1038/s12276-017-0002-0 · Cited by 78
From taxonomy to metabolic output: what factors define gut microbiome health?
Wilmanski, T., Rappaport, N., Diener, C., Gibbons, S. M., & Price, N. D. (2021) · Gut Microbes · doi:10.1080/19490976.2021.1907270 · Cited by 73
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Klimesova, K., Jiraskova Zakostelska, Z., & Tlaskalova-Hogenova, H. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00774 · Cited by 67
Jia, Y.-P., Wang, K., Zhang, Z.-J., Tong, Y.-N., Han, D., Hu, C.-Y., Li, Q., Xiang, Y., Mao, X.-H., & Tang, B. (2017) · PLOS ONE · doi:10.1371/journal.pone.0186179 · Cited by 65
Randrian, V., Evrard, C., & Tougeron, D. (2021) · Cancers · doi:10.3390/cancers13123063 · Cited by 65
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Lehr, K., Nikitina, D., Vilchez-Vargas, R., Steponaitiene, R., Thon, C., Skieceviciene, J., Schanze, D., Zenker, M., Malfertheiner, P., Kupcinskas, J., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-31740-3 · Cited by 54
Gao, Z., Jiang, A., Li, Z., Zhu, L., Mou, W., Shen, W., Luo, P., Tang, B., Zhang, J., & Lin, A. (2025) · Med Research · doi:10.1002/mdr2.70006 · Cited by 51
The role of the gut microbiome in colorectal cancer: Where are we? Where are we going?
Wieczorska, K., Stolarek, M., & Stec, R. (2020) · Clinical Colorectal Cancer · doi:10.1016/j.clcc.2019.07.006 · Cited by 50
Lennard, K. S., Goosen, R. W., & Blackburn, J. M. (2016) · PLOS ONE · doi:10.1371/journal.pone.0166282 · Cited by 45
Metabolic reprogramming: a bridge between aging and tumorigenesis
Drapela, S., Ilter, D., & Gomes, A. P. (2022) · Molecular Oncology · doi:10.1002/1878-0261.13261 · Cited by 41
Gut microbiota imbalance and base excision repair dynamics in colon cancer
Ray, D., & Kidane, D. (2016) · Journal of Cancer · doi:10.7150/jca.15480 · Cited by 37
“For example, Fusobacterium nucleatum increases tumor multiplicity by the infiltration of immune cells and NF-κB activation that potentiate intestinal tumorigenesis [30].”
BackgroundHu, J.-M., Shen, C.-J., Chou, Y.-C., Hung, C.-F., Tian, Y.-F., You, S.-L., Chen, C.-Y., Hsu, C.-H., Hsiao, C.-W., Lin, C.-Y., et al. (2018) · International Journal of Colorectal Disease · doi:10.1007/s00384-018-2965-2 · Cited by 39
Galeano Niño, J. L., Wu, H., LaCourse, K. D., Srinivasan, H., Fitzgibbon, M., Minot, S. S., Sather, C., Johnston, C. D., & Bullman, S. (2023) · Nature Protocols · doi:10.1038/s41596-023-00888-7 · Cited by 36
Greathouse, K. L., White, J. R., Padgett, R. N., Perrotta, B. G., Jenkins, G. D., Chia, N., & Chen, J. (2019) · BMJ Open Gastroenterology · doi:10.1136/bmjgast-2018-000247 · Cited by 35
Microbial factors in inflammatory diseases and cancers
Ong, H. S., & Yim, H. C. H. (2017) · Advances in experimental medicine and biology · doi:10.1007/978-981-10-5987-2_7 · Cited by 29
Bugs as drugs: The role of microbiome in cancer focusing on immunotherapeutics
Araujo, D. V., Watson, G. A., Oliva, M., Heirali, A., Coburn, B., Spreafico, A., & Siu, L. L. (2021) · Cancer Treatment Reviews · doi:10.1016/j.ctrv.2020.102125 · Cited by 29
Fusobacterium nucleatum carcinogenesis and drug delivery interventions
Chen, Z., & Huang, L. (2024) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2024.115319 · Cited by 27
Metadata
- Authors
- Kostic, A. D., Chun, E., Robertson, L., Glickman, J. N., Gallini, C. A., Michaud, M., Clancy, T. E., Chung, D. C., Lochhead, P., Hold, G. L., El-Omar, E. M., Brenner, D., Fuchs, C. S., Meyerson, M., & Garrett, W. S.
- Affiliations
- Broad Institute (US)
- Harvard University (US)
- Brigham and Women's Hospital (US)
- University of Aberdeen (GB)
- University of Michigan (US)
- Corresponding author
- Meyerson, Matthew
- Garrett, Wendy S.
- ORCID
- Venue
- Cell Host & Microbe
- Publisher
- Elsevier BV
- Published
- 2013-08
- Volume
- 14
- Issue
- 2
- Pages
- 207-215
- ISSN
- 1931-3128 (ISSN-L)
- PMC
- PMC3772512
- OpenAlex
- W2096139589
- Cited by
- 2,718
- References
- 43
- Citations by year
- 2026: 274 · 2025: 280 · 2024: 290 · 2023: 294 · 2022: 281 · 2021: 323 · 2020: 225 · 2019: 199 · 2018: 178 · 2017: 119 · 2016: 105 · 2015: 79 · 2014: 56 · 2013: 12
- FWCI
- 37.65
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell Host & Microbe (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Cancer Research Institute
- National Human Genome Research Institute (U54HG003067)
- National Cancer Institute (P50CA127003, RC2CA148317, R01CA154426)
- National Institute of Allergy and Infectious Diseases (K08AI078942)
- National Institute of Diabetes and Digestive and Kidney Diseases (K24DK098311, P30DK043351)
- National Institute of Environmental Health Sciences (T32ES016645)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Bacterial Cancer Therapy
- Keywords
- Fusobacterium nucleatum, colorectal cancer, colorectal adenoma, gut microbiota, intestinal tumorigenesis, tumor microenvironment, tumor-infiltrating myeloid cells, pro-inflammatory microenvironment, ApcMin/+ mice, colonic neoplasia, inflammation-associated carcinogenesis
- MeSH terms
- Adenoma, Animals, Disease Models, Animal, Humans, Leukocytes, Colorectal Neoplasms, Cytokines, Fusobacterium nucleatum, Mice, Carcinogenesis
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