Snail-induced claudin-11 prompts collective migration for tumour progression

Ching Fei Li; Jia Yang Chen; Yang Hui Ho; Wen Hao Hsu; Liang Chun Wu; Hsin Yi Lan; Dennis Shin Shian Hsu; Shyh Kuan Tai; Ying Chih Chang; Muh Hwa Yang

doi:10.1038/s41556-018-0268-z

Snail-induced claudin-11 prompts collective migration for tumour progression

Ching Fei Li, Jia Yang Chen, Yang Hui Ho, Wen Hao Hsu, Liang Chun Wu, Hsin Yi Lan, Dennis Shin Shian Hsu, Shyh Kuan Tai, Ying Chih Chang, Muh Hwa Yang^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

95 Scopus citations

Abstract

Epithelial–mesenchymal transition (EMT) is a pivotal mechanism for cancer dissemination. However, EMT-regulated individual cancer cell invasion is difficult to detect in clinical samples. Emerging evidence implies that EMT is correlated to collective cell migration and invasion with unknown mechanisms. We show that the EMT transcription factor Snail elicits collective migration in squamous cell carcinoma by inducing the expression of a tight junctional protein, claudin-11. Mechanistically, tyrosine-phosphorylated claudin-11 activates Src, which suppresses RhoA activity at intercellular junctions through p190RhoGAP, maintaining stable cell–cell contacts. In head and neck cancer patients, the Snail–claudin-11 axis prompts the formation of circulating tumour cell clusters, which correlate with tumour progression. Overexpression of snail correlates with increased claudin-11, and both are associated with a worse outcome. This finding extends the current understanding of EMT-mediated cellular migration via a non-individual type of movement to prompt cancer progression.

Original language	English
Pages (from-to)	251-262
Number of pages	12
Journal	Nature Cell Biology
Volume	21
Issue number	2
DOIs	https://doi.org/10.1038/s41556-018-0268-z
State	Published - 1 Feb 2019

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title = "Snail-induced claudin-11 prompts collective migration for tumour progression",

abstract = "Epithelial–mesenchymal transition (EMT) is a pivotal mechanism for cancer dissemination. However, EMT-regulated individual cancer cell invasion is difficult to detect in clinical samples. Emerging evidence implies that EMT is correlated to collective cell migration and invasion with unknown mechanisms. We show that the EMT transcription factor Snail elicits collective migration in squamous cell carcinoma by inducing the expression of a tight junctional protein, claudin-11. Mechanistically, tyrosine-phosphorylated claudin-11 activates Src, which suppresses RhoA activity at intercellular junctions through p190RhoGAP, maintaining stable cell–cell contacts. In head and neck cancer patients, the Snail–claudin-11 axis prompts the formation of circulating tumour cell clusters, which correlate with tumour progression. Overexpression of snail correlates with increased claudin-11, and both are associated with a worse outcome. This finding extends the current understanding of EMT-mediated cellular migration via a non-individual type of movement to prompt cancer progression.",

author = "Li, {Ching Fei} and Chen, {Jia Yang} and Ho, {Yang Hui} and Hsu, {Wen Hao} and Wu, {Liang Chun} and Lan, {Hsin Yi} and Hsu, {Dennis Shin Shian} and Tai, {Shyh Kuan} and Chang, {Ying Chih} and Yang, {Muh Hwa}",

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doi = "10.1038/s41556-018-0268-z",

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AU - Li, Ching Fei

AU - Chen, Jia Yang

AU - Ho, Yang Hui

AU - Hsu, Wen Hao

AU - Wu, Liang Chun

AU - Lan, Hsin Yi

AU - Hsu, Dennis Shin Shian

AU - Tai, Shyh Kuan

AU - Chang, Ying Chih

AU - Yang, Muh Hwa

PY - 2019/2/1

Y1 - 2019/2/1

N2 - Epithelial–mesenchymal transition (EMT) is a pivotal mechanism for cancer dissemination. However, EMT-regulated individual cancer cell invasion is difficult to detect in clinical samples. Emerging evidence implies that EMT is correlated to collective cell migration and invasion with unknown mechanisms. We show that the EMT transcription factor Snail elicits collective migration in squamous cell carcinoma by inducing the expression of a tight junctional protein, claudin-11. Mechanistically, tyrosine-phosphorylated claudin-11 activates Src, which suppresses RhoA activity at intercellular junctions through p190RhoGAP, maintaining stable cell–cell contacts. In head and neck cancer patients, the Snail–claudin-11 axis prompts the formation of circulating tumour cell clusters, which correlate with tumour progression. Overexpression of snail correlates with increased claudin-11, and both are associated with a worse outcome. This finding extends the current understanding of EMT-mediated cellular migration via a non-individual type of movement to prompt cancer progression.

AB - Epithelial–mesenchymal transition (EMT) is a pivotal mechanism for cancer dissemination. However, EMT-regulated individual cancer cell invasion is difficult to detect in clinical samples. Emerging evidence implies that EMT is correlated to collective cell migration and invasion with unknown mechanisms. We show that the EMT transcription factor Snail elicits collective migration in squamous cell carcinoma by inducing the expression of a tight junctional protein, claudin-11. Mechanistically, tyrosine-phosphorylated claudin-11 activates Src, which suppresses RhoA activity at intercellular junctions through p190RhoGAP, maintaining stable cell–cell contacts. In head and neck cancer patients, the Snail–claudin-11 axis prompts the formation of circulating tumour cell clusters, which correlate with tumour progression. Overexpression of snail correlates with increased claudin-11, and both are associated with a worse outcome. This finding extends the current understanding of EMT-mediated cellular migration via a non-individual type of movement to prompt cancer progression.

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Snail-induced claudin-11 prompts collective migration for tumour progression

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