Wnt activation disturbs cell competition and causes diffuse invasion of transformed cells through NF-κB-MMP21 pathway

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 e...

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Published inNature communications Vol. 14; no. 1; p. 7048
Main Authors Nakai, Kazuki, Lin, Hancheng, Yamano, Shotaro, Tanaka, Shinya, Kitamoto, Sho, Saitoh, Hitoshi, Sakuma, Kenta, Kurauchi, Junpei, Akter, Eilma, Konno, Masamitsu, Ishibashi, Kojiro, Kamata, Ryo, Ohashi, Akihiro, Koseki, Jun, Takahashi, Hirotaka, Yokoyama, Hideshi, Shiraki, Yukihiro, Enomoto, Atsushi, Abe, Sohei, Hayakawa, Yoku, Ushiku, Tetsuo, Mutoh, Michihiro, Fujita, Yasuyuki, Kon, Shunsuke
Format Journal Article
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Published London Nature Publishing Group UK 03.11.2023
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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. The relevance of cell competition in intestinal epithelial carcinogenesis remains to be explored. Here, the authors find aberrant Wnt activation in RasV12-transformed cells reverses the directionality of cell extrusion mediated by cell competition in intestinal epithelium, causing infiltration into basal lamina rather than apical elimination of transformed cells and consequent development of invasive carcinomas.
AbstractList 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.
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. The relevance of cell competition in intestinal epithelial carcinogenesis remains to be explored. Here, the authors find aberrant Wnt activation in RasV12-transformed cells reverses the directionality of cell extrusion mediated by cell competition in intestinal epithelium, causing infiltration into basal lamina rather than apical elimination of transformed cells and consequent development of invasive carcinomas.
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.The relevance of cell competition in intestinal epithelial carcinogenesis remains to be explored. Here, the authors find aberrant Wnt activation in RasV12-transformed cells reverses the directionality of cell extrusion mediated by cell competition in intestinal epithelium, causing infiltration into basal lamina rather than apical elimination of transformed cells and consequent development of invasive carcinomas.
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.
ArticleNumber 7048
Author Kamata, Ryo
Sakuma, Kenta
Shiraki, Yukihiro
Hayakawa, Yoku
Mutoh, Michihiro
Saitoh, Hitoshi
Ohashi, Akihiro
Koseki, Jun
Yamano, Shotaro
Kitamoto, Sho
Ishibashi, Kojiro
Yokoyama, Hideshi
Ushiku, Tetsuo
Fujita, Yasuyuki
Enomoto, Atsushi
Kurauchi, Junpei
Takahashi, Hirotaka
Lin, Hancheng
Akter, Eilma
Kon, Shunsuke
Abe, Sohei
Nakai, Kazuki
Tanaka, Shinya
Konno, Masamitsu
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PublicationTitle Nature communications
PublicationTitleAbbrev Nat Commun
PublicationYear 2023
Publisher Nature Publishing Group UK
Nature Publishing Group
Nature Portfolio
Publisher_xml – name: Nature Publishing Group UK
– name: Nature Publishing Group
– name: Nature Portfolio
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Snippet Normal epithelial cells exert their competitive advantage over RasV12-transformed cells and eliminate them into the apical lumen via cell competition. However,...
Abstract Normal epithelial cells exert their competitive advantage over RasV12-transformed cells and eliminate them into the apical lumen via cell competition....
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SubjectTerms 631/67/70
631/80
631/80/304
64
64/60
Basal lamina
Carcinogenesis
Carcinogens
Cell activation
Cells
Colorectal carcinoma
Competition
Competitive advantage
Epithelial cells
Epithelium
Extrusion
Humanities and Social Sciences
Intestine
Invasiveness
multidisciplinary
NF-κB protein
Science
Science (multidisciplinary)
Transformed cells
Wnt protein
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Title Wnt activation disturbs cell competition and causes diffuse invasion of transformed cells through NF-κB-MMP21 pathway
URI https://link.springer.com/article/10.1038/s41467-023-42774-6
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https://search.proquest.com/docview/2886328218
https://pubmed.ncbi.nlm.nih.gov/PMC10624923
https://doaj.org/article/6f44e420616648b8bbcf9f4de854cbbb
Volume 14
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