Wnt activation disturbs cell competition and causes diffuse invasion of transformed cells through NF-κB-MMP21 pathway
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Abstract
Normal epithelial cells exert their competitive advantage over RasV12-transformed cells and eliminate them into the apical lumen via cell competition. However, the internal or external factors that compromise cell competition and provoke carcinogenesis remain elusive. In this study, we examine the effect of sequential accumulation of gene mutations, mimicking multi-sequential carcinogenesis on RasV12-induced cell competition in intestinal epithelial tissues. Consequently, we find that the directionality of RasV12-cell extrusion in Wnt-activated epithelia is reversed, and transformed cells are delaminated into the basal lamina via non-cell autonomous MMP21 upregulation. Subsequently, diffusively infiltrating, transformed cells develop into highly invasive carcinomas. The elevated production of MMP21 is elicited partly through NF-κB signaling, blockage of which restores apical elimination of RasV12 cells. We further demonstrate that the NF-κB-MMP21 axis is significantly bolstered in early colorectal carcinoma in humans. Collectively, this study shows that cells with high mutational burdens exploit cell competition for their benefit by behaving as unfit cells, endowing them with an invasion advantage.
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In colorectal cancer, activation of NF-κB signaling through innate immune receptors RIG-I/TLR3 enhances MMP21 production, enabling RAS-mutant cells to eliminate neighboring cells through cell competition and diffusely invade surrounding tissues.
“The activation of NF-κB signaling through innate immune receptors RIG-I/TLR3 enhances MMP21 production, enabling RAS-mutant cells to eliminate neighboring cells through cell competition and diffusely invade surrounding tissues [32].”
From The Role of KRAS Mutations in Colorectal Cancer: Biological Insights, Clinical Implications, and Future Therapeutic Perspectives (2025) · cites this paper as [32]
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Self-citationIchimura, T., Kakizuka, T., Sato, Y., Fujioka, Y., Ohba, Y., Horikawa, K., & Nagai, T. (2024) · Biophysics and Physicobiology · doi:10.2142/biophysico.bppb-v21.s017 · Cited by 1 · see citing works
Zhou, Z., Zhao, Z., Chen, F., Meng, Y., Zhang, H., Zhu, M., Han, Y., Wang, X., Cao, Z., Zhang, X. L., et al. (2025) · Research Square · doi:10.21203/rs.3.rs-6524135/v1
Winners take it all: turning cell competition into a therapeutic ally
Fantová, T., Warmuzová, M., Charvátová, S., Stošková, K., Jelinek, T., Šimíček, M., Hájek, R., & Bagó, J. R. (2026) · Cell Communication and Signaling · doi:10.1186/s12964-025-02611-3
In vitro models of cell competition: current approaches and future directions
Bağlamış, S., Krawczyk, P. M., Vermeulen, L., van Neerven, S. M., & Lenos, K. (2026) · Oncogene · doi:10.1038/s41388-026-03751-7
RHOA at the intersection of inflammation-driven and sporadic colorectal cancer
Muccioli, S. E., Hidalgo‐Garcia, L., Ngo, P. A., Neurath, M. F., & López-Posadas, R. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1844372
Mo, H., Han, H., O'Dwyer, M. E., Reidy, E., & Ryan, A. E. (2026) · The Journal of Physiology · doi:10.1113/jp291166
- Authors
- Nakai, K., Lin, H., Yamano, S., Tanaka, S., Kitamoto, S., Saitoh, H., Sakuma, K., Kurauchi, J., Akter, E., Konno, M., Ishibashi, K., Kamata, R., Ohashi, A., Koseki, J., Takahashi, H., Yokoyama, H., Shiraki, Y., Enomoto, A., Abe, S., Hayakawa, Y., Ushiku, T., Mutoh, M., Fujita, Y., & Kon, S.
- Affiliations
- Tokyo University of Science (JP)
- Japan Organization of Occupational Health and Safety (JP)
- Kyoto University (JP)
- Immunology Frontier Research Center, The University of Osaka (JP)
- National Cancer Centre Japan (JP)
- Kanazawa University (JP)
- Nagoya University (JP)
- Ehime University (JP)
- Nagoya University Hospital (JP)
- The University of Tokyo (JP)
- Kyoto Prefectural University of Medicine (JP)
- Corresponding author
- Kon, Shunsuke
- ORCID
- Venue
- Nature Communications
- Published
- 2023-11-03
- Volume
- 14
- Issue
- 1
- Pages
- 7048-7048
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC10624923
- OpenAlex
- W4388292909
- Cited by
- 14
- References
- 84
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 1
- FWCI
- 1.24
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- Research Square (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Japan Agency for Medical Research and Development (19217462)
- MEXT | Japan Society for the Promotion of Science (20H03166, 21H00441)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Wnt/β-catenin signaling in development and cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
- Keywords
- Wnt signaling, cell competition, NF-κB, tumor invasion, colorectal cancer, mutational burden, carcinogenesis, intestinal epithelium
- MeSH terms
- Cell Competition, Animals, Dogs, Humans, Signal Transduction, NF-kappa B, Matrix Metalloproteinases, Secreted, Madin Darby Canine Kidney Cells, Carcinogenesis
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