Suppression of α-catenin and adherens junctions enhances epithelial cell proliferation and motility via TACE-mediated TGF-α autocrine/paracrine signaling

Sustained cell migration is essential for wound healing and cancer metastasis. The epidermal growth factor receptor (EGFR) signaling cascade is known to drive cell migration and proliferation. While the signal transduction downstream of EGFR has been extensively investigated, our knowledge of the in...

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Published inMolecular biology of the cell Vol. 32; no. 4; pp. 348 - 361
Main Authors Bunker, Eric N, Wheeler, Graycen E, Chapnick, Douglas A, Liu, Xuedong
Format Journal Article
LanguageEnglish
Published United States The American Society for Cell Biology 15.02.2021
Subjects
ADAM17 Protein - metabolism
ADAM17 Protein - physiology
Adherens Junctions - metabolism
Adherens Junctions - physiology
alpha Catenin - metabolism
alpha Catenin - physiology
Cell Line, Tumor
Cell Movement - physiology
Cell Proliferation
Epidermal Growth Factor - metabolism
Epithelial Cells - metabolism
ErbB Receptors - metabolism
HaCaT Cells
Humans
Metalloproteases - metabolism
Paracrine Communication - physiology
Phosphorylation
Signal Transduction
Transforming Growth Factor alpha - metabolism
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Abstract Sustained cell migration is essential for wound healing and cancer metastasis. The epidermal growth factor receptor (EGFR) signaling cascade is known to drive cell migration and proliferation. While the signal transduction downstream of EGFR has been extensively investigated, our knowledge of the initiation and maintenance of EGFR signaling during cell migration remains limited. The metalloprotease TACE (tumor necrosis factor alpha converting enzyme) is responsible for producing active EGFR family ligands in the via ligand shedding. Sustained TACE activity may perpetuate EGFR signaling and reduce a cell's reliance on exogenous growth factors. Using a cultured keratinocyte model system, we show that depletion of α-catenin perturbs adherens junctions, enhances cell proliferation and motility, and decreases dependence on exogenous growth factors. We show that the underlying mechanism for these observed phenotypical changes depends on enhanced autocrine/paracrine release of the EGFR ligand transforming growth factor alpha in a TACE-dependent manner. We demonstrate that proliferating keratinocyte epithelial cell clusters display waves of oscillatory extracellular signal-regulated kinase (ERK) activity, which can be eliminated by TACE knockout, suggesting that these waves of oscillatory ERK activity depend on autocrine/paracrine signals produced by TACE. These results provide new insights into the regulatory role of adherens junctions in initiating and maintaining autocrine/paracrine signaling with relevance to wound healing and cellular transformation.
AbstractList Sustained cell migration is essential for wound healing and cancer metastasis. The epidermal growth factor receptor (EGFR) signaling cascade is known to drive cell migration and proliferation. While the signal transduction downstream of EGFR has been extensively investigated, our knowledge of the initiation and maintenance of EGFR signaling during cell migration remains limited. The metalloprotease TACE (tumor necrosis factor alpha converting enzyme) is responsible for producing active EGFR family ligands in the via ligand shedding. Sustained TACE activity may perpetuate EGFR signaling and reduce a cell's reliance on exogenous growth factors. Using a cultured keratinocyte model system, we show that depletion of α-catenin perturbs adherens junctions, enhances cell proliferation and motility, and decreases dependence on exogenous growth factors. We show that the underlying mechanism for these observed phenotypical changes depends on enhanced autocrine/paracrine release of the EGFR ligand transforming growth factor alpha in a TACE-dependent manner. We demonstrate that proliferating keratinocyte epithelial cell clusters display waves of oscillatory extracellular signal-regulated kinase (ERK) activity, which can be eliminated by TACE knockout, suggesting that these waves of oscillatory ERK activity depend on autocrine/paracrine signals produced by TACE. These results provide new insights into the regulatory role of adherens junctions in initiating and maintaining autocrine/paracrine signaling with relevance to wound healing and cellular transformation.
The loss of adherens junctions elevates autocrine TGF-α signaling in a TACE-dependent manner. Keratinocyte epithelial sheets depend on this signaling to propagate ERK activity for proliferation and motility signaling. Sustained cell migration is essential for wound healing and cancer metastasis. The epidermal growth factor receptor (EGFR) signaling cascade is known to drive cell migration and proliferation. While the signal transduction downstream of EGFR has been extensively investigated, our knowledge of the initiation and maintenance of EGFR signaling during cell migration remains limited. The metalloprotease TACE (tumor necrosis factor alpha converting enzyme) is responsible for producing active EGFR family ligands in the via ligand shedding. Sustained TACE activity may perpetuate EGFR signaling and reduce a cell’s reliance on exogenous growth factors. Using a cultured keratinocyte model system, we show that depletion of α-catenin perturbs adherens junctions, enhances cell proliferation and motility, and decreases dependence on exogenous growth factors. We show that the underlying mechanism for these observed phenotypical changes depends on enhanced autocrine/paracrine release of the EGFR ligand transforming growth factor alpha in a TACE-dependent manner. We demonstrate that proliferating keratinocyte epithelial cell clusters display waves of oscillatory extracellular signal–regulated kinase (ERK) activity, which can be eliminated by TACE knockout, suggesting that these waves of oscillatory ERK activity depend on autocrine/paracrine signals produced by TACE. These results provide new insights into the regulatory role of adherens junctions in initiating and maintaining autocrine/paracrine signaling with relevance to wound healing and cellular transformation.
Author Bunker, Eric N
Wheeler, Graycen E
Chapnick, Douglas A
Liu, Xuedong
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  surname: Wheeler
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content type line 23
Competing interests: X.L. and the University of Colorado–Boulder have a financial interest in development of HDAC inhibitors for therapeutics and own equity in OnKure. X.L. is a cofounder and member of the board of directors of OnKure, which has licensed proprietary HDAC inhibitors from the University of Colorado–Boulder. OnKure has neither involvement in the experimental design nor funding of this study.
Co–first author.
Author contributions: E.N.B., G.E.W., and D.A.C. developed the codes for data analysis. E.N.B., G.E.W., D.A.C., and X. L. performed the experiments. E.N.B., G.E.W., and X. L. designed the studies. E.N.B., G.E.W., and X. L. wrote the manuscript.
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Snippet Sustained cell migration is essential for wound healing and cancer metastasis. The epidermal growth factor receptor (EGFR) signaling cascade is known to drive...
The loss of adherens junctions elevates autocrine TGF-α signaling in a TACE-dependent manner. Keratinocyte epithelial sheets depend on this signaling to...
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SubjectTerms ADAM17 Protein - metabolism
ADAM17 Protein - physiology
Adherens Junctions - metabolism
Adherens Junctions - physiology
alpha Catenin - metabolism
alpha Catenin - physiology
Cell Line, Tumor
Cell Movement - physiology
Cell Proliferation
Epidermal Growth Factor - metabolism
Epithelial Cells - metabolism
ErbB Receptors - metabolism
HaCaT Cells
Humans
Metalloproteases - metabolism
Paracrine Communication - physiology
Phosphorylation
Signal Transduction
Transforming Growth Factor alpha - metabolism
Title Suppression of α-catenin and adherens junctions enhances epithelial cell proliferation and motility via TACE-mediated TGF-α autocrine/paracrine signaling
URI https://www.ncbi.nlm.nih.gov/pubmed/33378218
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