Dia1-dependent adhesions are required by epithelial tissues to initiate invasion

Developing tissues change shape and tumors initiate spreading through collective cell motility. Conserved mechanisms by which tissues initiate motility into their surroundings are not known. We investigated cytoskeletal regulators during collective invasion by mouse tumor organoids and epithelial Ma...

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Published inThe Journal of cell biology Vol. 217; no. 4; pp. 1485 - 1502
Main Authors Fessenden, Tim B., Beckham, Yvonne, Perez-Neut, Mathew, Ramirez-San Juan, Guillermina, Chourasia, Aparajita H., Macleod, Kay F., Oakes, Patrick W., Gardel, Margaret L.
Format Journal Article
LanguageEnglish
Published United States Rockefeller University Press 02.04.2018
Subjects
Actin
Actins - metabolism
Animals
Breast Neoplasms - genetics
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Cancer
Carrier Proteins - genetics
Carrier Proteins - metabolism
Cell Adhesion
Cell adhesion & migration
Cell migration
Cell Movement
Cell Shape
Collagen
Cytoskeleton
Deformation mechanisms
Dogs
Epithelial Cells - drug effects
Epithelial Cells - metabolism
Epithelial Cells - pathology
Female
Fetal Proteins - metabolism
Fibrillar Collagens - metabolism
Fibrils
Formins
Hepatocyte Growth Factor - pharmacology
Madin Darby Canine Kidney Cells
Mammary Glands, Animal - metabolism
Mammary Glands, Animal - pathology
Mice
Morphogenesis
Motility
Myosin
Myosins - metabolism
Nuclear Proteins - metabolism
Organoids
Regulators
Signal Transduction
Time Factors
Tumor Cells, Cultured
Tumors
Online AccessGet full text
ISSN0021-9525
1540-8140
1540-8140
DOI10.1083/jcb.201703145

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Abstract Developing tissues change shape and tumors initiate spreading through collective cell motility. Conserved mechanisms by which tissues initiate motility into their surroundings are not known. We investigated cytoskeletal regulators during collective invasion by mouse tumor organoids and epithelial Madin–Darby canine kidney (MDCK) acini undergoing branching morphogenesis in collagen. Use of the broad-spectrum formin inhibitor SMIFH2 prevented the formation of migrating cell fronts in both cell types. Focusing on the role of the formin Dia1 in branching morphogenesis, we found that its depletion in MDCK cells does not alter planar cell motility either within the acinus or in two-dimensional scattering assays. However, Dia1 was required to stabilize protrusions extending into the collagen matrix. Live imaging of actin, myosin, and collagen in control acini revealed adhesions that deformed individual collagen fibrils and generated large traction forces, whereas Dia1-depleted acini exhibited unstable adhesions with minimal collagen deformation and lower force generation. This work identifies Dia1 as an essential regulator of tissue shape changes through its role in stabilizing focal adhesions.
AbstractList Developing tissues change shape and tumors initiate spreading through collective cell motility. Conserved mechanisms by which tissues initiate motility into their surroundings are not known. We investigated cytoskeletal regulators during collective invasion by mouse tumor organoids and epithelial Madin-Darby canine kidney (MDCK) acini undergoing branching morphogenesis in collagen. Use of the broad-spectrum formin inhibitor SMIFH2 prevented the formation of migrating cell fronts in both cell types. Focusing on the role of the formin Dia1 in branching morphogenesis, we found that its depletion in MDCK cells does not alter planar cell motility either within the acinus or in two-dimensional scattering assays. However, Dia1 was required to stabilize protrusions extending into the collagen matrix. Live imaging of actin, myosin, and collagen in control acini revealed adhesions that deformed individual collagen fibrils and generated large traction forces, whereas Dia1-depleted acini exhibited unstable adhesions with minimal collagen deformation and lower force generation. This work identifies Dia1 as an essential regulator of tissue shape changes through its role in stabilizing focal adhesions.Developing tissues change shape and tumors initiate spreading through collective cell motility. Conserved mechanisms by which tissues initiate motility into their surroundings are not known. We investigated cytoskeletal regulators during collective invasion by mouse tumor organoids and epithelial Madin-Darby canine kidney (MDCK) acini undergoing branching morphogenesis in collagen. Use of the broad-spectrum formin inhibitor SMIFH2 prevented the formation of migrating cell fronts in both cell types. Focusing on the role of the formin Dia1 in branching morphogenesis, we found that its depletion in MDCK cells does not alter planar cell motility either within the acinus or in two-dimensional scattering assays. However, Dia1 was required to stabilize protrusions extending into the collagen matrix. Live imaging of actin, myosin, and collagen in control acini revealed adhesions that deformed individual collagen fibrils and generated large traction forces, whereas Dia1-depleted acini exhibited unstable adhesions with minimal collagen deformation and lower force generation. This work identifies Dia1 as an essential regulator of tissue shape changes through its role in stabilizing focal adhesions.
Developing tissues change shape and tumors initiate spreading through collective cell motility. Conserved mechanisms by which tissues initiate motility into their surroundings are not known. We investigated cytoskeletal regulators during collective invasion by mouse tumor organoids and epithelial Madin–Darby canine kidney (MDCK) acini undergoing branching morphogenesis in collagen. Use of the broad-spectrum formin inhibitor SMIFH2 prevented the formation of migrating cell fronts in both cell types. Focusing on the role of the formin Dia1 in branching morphogenesis, we found that its depletion in MDCK cells does not alter planar cell motility either within the acinus or in two-dimensional scattering assays. However, Dia1 was required to stabilize protrusions extending into the collagen matrix. Live imaging of actin, myosin, and collagen in control acini revealed adhesions that deformed individual collagen fibrils and generated large traction forces, whereas Dia1-depleted acini exhibited unstable adhesions with minimal collagen deformation and lower force generation. This work identifies Dia1 as an essential regulator of tissue shape changes through its role in stabilizing focal adhesions.
How collective cell migration mediates tissue shape changes during the development of normal tissue or tumors is unclear. Fessenden et al. show that the formin Dia1 stabilizes adhesions of protruding MDCK cells during branching morphogenesis, permitting force generation against collagen and eventual tissue shape changes. Developing tissues change shape and tumors initiate spreading through collective cell motility. Conserved mechanisms by which tissues initiate motility into their surroundings are not known. We investigated cytoskeletal regulators during collective invasion by mouse tumor organoids and epithelial Madin–Darby canine kidney (MDCK) acini undergoing branching morphogenesis in collagen. Use of the broad-spectrum formin inhibitor SMIFH2 prevented the formation of migrating cell fronts in both cell types. Focusing on the role of the formin Dia1 in branching morphogenesis, we found that its depletion in MDCK cells does not alter planar cell motility either within the acinus or in two-dimensional scattering assays. However, Dia1 was required to stabilize protrusions extending into the collagen matrix. Live imaging of actin, myosin, and collagen in control acini revealed adhesions that deformed individual collagen fibrils and generated large traction forces, whereas Dia1-depleted acini exhibited unstable adhesions with minimal collagen deformation and lower force generation. This work identifies Dia1 as an essential regulator of tissue shape changes through its role in stabilizing focal adhesions.
Author Oakes, Patrick W.
Chourasia, Aparajita H.
Fessenden, Tim B.
Perez-Neut, Mathew
Ramirez-San Juan, Guillermina
Beckham, Yvonne
Macleod, Kay F.
Gardel, Margaret L.
AuthorAffiliation 2 Committee on Cancer Biology, University of Chicago, Chicago, IL
3 Ben May Department of Cancer Research, University of Chicago, Chicago, IL
5 Department of Bioengineering, Stanford University, Stanford, CA
4 Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA
1 Institute for Biophysical Dynamics, James Franck Institute, and Department of Physics, University of Chicago, Chicago, IL
6 Department of Physics and Astronomy and Department of Biology, University of Rochester, Rochester, NY
AuthorAffiliation_xml – name: 3 Ben May Department of Cancer Research, University of Chicago, Chicago, IL
– name: 1 Institute for Biophysical Dynamics, James Franck Institute, and Department of Physics, University of Chicago, Chicago, IL
– name: 6 Department of Physics and Astronomy and Department of Biology, University of Rochester, Rochester, NY
– name: 4 Department of Biochemistry and Biophysics, University of California, San Francisco, San Francisco, CA
– name: 2 Committee on Cancer Biology, University of Chicago, Chicago, IL
– name: 5 Department of Bioengineering, Stanford University, Stanford, CA
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Tim B. Fessenden’s present address is David H. Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, Cambridge, MA.
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SSID ssj0004743
Score 2.3872106
Snippet Developing tissues change shape and tumors initiate spreading through collective cell motility. Conserved mechanisms by which tissues initiate motility into...
How collective cell migration mediates tissue shape changes during the development of normal tissue or tumors is unclear. Fessenden et al. show that the formin...
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pubmed
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Enrichment Source
StartPage 1485
SubjectTerms Actin
Actins - metabolism
Animals
Breast Neoplasms - genetics
Breast Neoplasms - metabolism
Breast Neoplasms - pathology
Cancer
Carrier Proteins - genetics
Carrier Proteins - metabolism
Cell Adhesion
Cell adhesion & migration
Cell migration
Cell Movement
Cell Shape
Collagen
Cytoskeleton
Deformation mechanisms
Dogs
Epithelial Cells - drug effects
Epithelial Cells - metabolism
Epithelial Cells - pathology
Female
Fetal Proteins - metabolism
Fibrillar Collagens - metabolism
Fibrils
Formins
Hepatocyte Growth Factor - pharmacology
Madin Darby Canine Kidney Cells
Mammary Glands, Animal - metabolism
Mammary Glands, Animal - pathology
Mice
Morphogenesis
Motility
Myosin
Myosins - metabolism
Nuclear Proteins - metabolism
Organoids
Regulators
Signal Transduction
Time Factors
Tumor Cells, Cultured
Tumors
Title Dia1-dependent adhesions are required by epithelial tissues to initiate invasion
URI https://www.ncbi.nlm.nih.gov/pubmed/29437785
https://www.proquest.com/docview/2078822874
https://www.proquest.com/docview/2002211133
https://pubmed.ncbi.nlm.nih.gov/PMC5881494
Volume 217
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