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RESEARCH ARTICLE
Smooth muscle differentiation shapes domain branches during mouse lung development
Katharine Goodwin, Sheng Mao, Tristan Guyomar, Erin Miller, Derek C. Radisky, Andrej Košmrlj, Celeste M. Nelson
Development 2019 146: dev181172 doi: 10.1242/dev.181172 Published 25 November 2019
Katharine Goodwin
Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, NJ 08544, USA
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Sheng Mao
Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544, USA
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Tristan Guyomar
Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544, USADépartement de Physique, Ecole Normale Supérieure de Lyon, F-69342 Lyon, France
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Erin Miller
Department of Cancer Biology, Mayo Clinic Cancer Center, Jacksonville, FL 32224, USA
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Derek C. Radisky
Department of Cancer Biology, Mayo Clinic Cancer Center, Jacksonville, FL 32224, USA
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Andrej Košmrlj
Department of Mechanical and Aerospace Engineering, Princeton University, Princeton, NJ 08544, USA
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Celeste M. Nelson
Department of Chemical and Biological Engineering, Princeton University, Princeton, NJ 08544, USADepartment of Molecular Biology, Princeton University, Princeton, NJ 08544, USA
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  • ORCID record for Celeste M. Nelson
  • For correspondence: celesten@princeton.edu
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ABSTRACT

During branching morphogenesis, a simple cluster of cells proliferates and branches to generate an arborized network that facilitates fluid flow. The overall architecture of the mouse lung is established by domain branching, wherein new branches form laterally off the side of an existing branch. The airway epithelium develops concomitantly with a layer of smooth muscle that is derived from the embryonic mesenchyme. Here, we examined the role of smooth muscle differentiation in shaping emerging domain branches. We found that the position and morphology of domain branches are highly stereotyped, as is the pattern of smooth muscle that differentiates around the base of each branch. Perturbing the pattern of smooth muscle differentiation genetically or pharmacologically causes abnormal domain branching. Loss of smooth muscle results in ectopic branching and decreases branch stereotypy. Increased smooth muscle suppresses branch initiation and extension. Computational modeling revealed that epithelial proliferation is insufficient to generate domain branches and that smooth muscle wrapping is required to shape the epithelium into a branch. Our work sheds light on the physical mechanisms of branching morphogenesis in the mouse lung.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: K.G., C.M.N.; Methodology: K.G., C.M.N.; Software: S.M., T.G., A.K.; Formal analysis: S.M., T.G., A.K.; Investigation: K.G.; Resources: E.M., D.C.R.; Writing - original draft: K.G., A.K., C.M.N.; Writing - review & editing: K.G., C.M.N.; Supervision: C.M.N.; Project administration: C.M.N.; Funding acquisition: C.M.N.

  • Funding

    This work was funded by the National Institutes of Health (HL120142), the National Science Foundation (CMMI-1435853) and a Faculty Scholars Award from the Howard Hughes Medical Institute. Deposited in PMC for release after 12 months.

  • Supplementary information

    Supplementary information available online at http://dev.biologists.org/lookup/doi/10.1242/dev.181172.supplemental

  • Received June 4, 2019.
  • Accepted October 21, 2019.
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Keywords

  • Mechanical stress
  • Symmetry breaking
  • Tissue morphodynamics

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RESEARCH ARTICLE
Smooth muscle differentiation shapes domain branches during mouse lung development
Katharine Goodwin, Sheng Mao, Tristan Guyomar, Erin Miller, Derek C. Radisky, Andrej Košmrlj, Celeste M. Nelson
Development 2019 146: dev181172 doi: 10.1242/dev.181172 Published 25 November 2019
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RESEARCH ARTICLE
Smooth muscle differentiation shapes domain branches during mouse lung development
Katharine Goodwin, Sheng Mao, Tristan Guyomar, Erin Miller, Derek C. Radisky, Andrej Košmrlj, Celeste M. Nelson
Development 2019 146: dev181172 doi: 10.1242/dev.181172 Published 25 November 2019

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