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Research Article
Multiple feedback mechanisms fine-tune Rho signaling to regulate morphogenetic outcomes
Katy Ong, Camille Collier, Stephen DiNardo
Journal of Cell Science 2019 132: jcs224378 doi: 10.1242/jcs.224378 Published 17 April 2019
Katy Ong
1Cell and Developmental Biology Department, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19146, USA
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  • ORCID record for Katy Ong
Camille Collier
2School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA 19104, USA
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Stephen DiNardo
1Cell and Developmental Biology Department, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19146, USA
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  • For correspondence: sdinardo@pennmedicine.upenn.edu
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ABSTRACT

Rho signaling is a conserved mechanism for generating forces through activation of contractile actomyosin. How this pathway can produce different cell morphologies is poorly understood. In the Drosophila embryonic epithelium, we investigate how Rho signaling controls force asymmetry to drive morphogenesis. We study a distinct morphogenetic process termed ‘alignment’. This process results in striking columns of rectilinear cells connected by aligned cell–cell contacts. We found that this is driven by contractile actomyosin cables that elevate tension along aligning interfaces. Our data show that polarization of Rho effectors, Rok and Dia, directs formation of these cables. Constitutive activation of these effectors causes aligning cells to instead invaginate. This suggests that moderating Rho signaling is essential to producing the aligned geometry. Therefore, we tested for feedback that could fine-tune Rho signaling. We discovered that F-actin exerts negative feedback on multiple nodes in the pathway. Further, we present evidence that suggests that Rok in part mediates feedback from F-actin to Rho in a manner independent of Myo-II. Collectively, our work suggests that multiple feedback mechanisms regulate Rho signaling, which may account for diverse morphological outcomes.

Footnotes

  • Competing interests

    The authors declare no competing or financial interests.

  • Author contributions

    Conceptualization: K.O., S.D.; Methodology: K.O., S.D.; Formal analysis: K.O., C.C.; Investigation: K.O., C.C.; Writing - original draft: K.O.; Writing - review & editing: K.O., C.C., S.D.; Supervision: S.D.; Funding acquisition: K.O., S.D.

  • Funding

    Funding sources include National Institutes of Health grants GM117708 (K.O.), HD083185 (K.O.), GM007229 (K.O.), GM45747 (S.D.), and GM60804 (S.D.). Deposited in PMC for release after 12 months.

  • Supplementary information

    Supplementary information available online at http://jcs.biologists.org/lookup/doi/10.1242/jcs.224378.supplemental

  • Received August 25, 2018.
  • Accepted March 1, 2019.
  • © 2019. Published by The Company of Biologists Ltd
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Keywords

  • Rho signaling
  • Epithelial morphogenesis
  • Actomyosin contractility
  • Developmental mechanics
  • Non-muscle Myosin-II
  • Zipper
  • Drosophila melanogaster

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Research Article
Multiple feedback mechanisms fine-tune Rho signaling to regulate morphogenetic outcomes
Katy Ong, Camille Collier, Stephen DiNardo
Journal of Cell Science 2019 132: jcs224378 doi: 10.1242/jcs.224378 Published 17 April 2019
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Research Article
Multiple feedback mechanisms fine-tune Rho signaling to regulate morphogenetic outcomes
Katy Ong, Camille Collier, Stephen DiNardo
Journal of Cell Science 2019 132: jcs224378 doi: 10.1242/jcs.224378 Published 17 April 2019

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