Contractile epithelial tubes are found in various organs, such as lung airways and blood capillaries. Their ability to sense luminal pressure and respond with adequate contractility is essential for their physiology, and its mis-regulation results in diseases such as asthma and hypertension. Here, we describe a mechanoresponsive regulatory pathway downstream of tissue stretching that controls contraction of the C. elegans spermatheca, a tubular structure where fertilization occurs. Using live-imaging, we show that ovulation-induced stretching of spermathecal cells leads to recruitment of the RhoGEF RHGF-1 to stress fibers, which activates RHO-1 and myosin II in a positive feedback loop. Through deletion analysis, we identified the PDZ domain of RHGF-1 as responsible for F-actin binding, and genetic epistasis analysis with the RhoGAP spv-1 demonstrated that tension-dependent recruitment of RHGF-1 to F-actin is required for robust spermathecal contractility. Our study illustrates how mechanosensitive regulators of Rho GTPases provide epithelial tubes the ability to tune their contractility in response to internal pressure.
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December 27 2022
Tension-dependent RHGF-1 recruitment to stress fibers drives robust spermathecal tissue contraction
Shiri Avivi Kela
,
Shiri Avivi Kela
(Conceptualization, Formal analysis, Investigation, Validation, Visualization, Writing - original draft, Writing - review & editing)
1
Department of Cell and Developmental Biology, Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
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Kriti Sethi
,
Kriti Sethi
(Conceptualization, Data curation, Formal analysis, Investigation, Resources, Validation, Visualization, Writing - original draft)
2
Mechanobiology Institute, National University of Singapore, Singapore, Singapore
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Pei Yi Tan
,
Pei Yi Tan
(Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing - review & editing)
2
Mechanobiology Institute, National University of Singapore, Singapore, Singapore
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Danesha Suresh
,
Danesha Suresh
(Investigation)
2
Mechanobiology Institute, National University of Singapore, Singapore, Singapore
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Hui Ting Ong
,
Hui Ting Ong
(Data curation, Resources, Software, Writing - original draft)
2
Mechanobiology Institute, National University of Singapore, Singapore, Singapore
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Perla G. Castaneda
,
Perla G. Castaneda
(Conceptualization, Investigation, Visualization, Writing - original draft, Writing - review & editing)
3
Department of Biology, Northeastern University, Boston, MA, USA
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Mustafi R. Amin
,
Mustafi R. Amin
(Formal analysis, Investigation, Validation, Visualization, Writing - review & editing)
3
Department of Biology, Northeastern University, Boston, MA, USA
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Tal Laviv
,
Tal Laviv
(Formal analysis, Investigation, Visualization)
4
Department of Physiology and Pharmacology, Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
5
Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel
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Erin J. Cram
,
Erin J. Cram
(Formal analysis, Funding acquisition, Writing - review & editing)
3
Department of Biology, Northeastern University, Boston, MA, USA
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Jan Faix
,
Jan Faix
(Formal analysis, Investigation, Validation, Writing - review & editing)
6
Institute for Biophysical Chemistry, Hannover Medical School, Hannover, Germany
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Ronen Zaidel-Bar
(Conceptualization, Funding acquisition, Supervision, Writing - original draft, Writing - review & editing)
1
Department of Cell and Developmental Biology, Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
Correspondence to Ronen Zaidel-Bar: zaidelbar@tauex.tau.ac.il
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Shiri Avivi Kela
Conceptualization, Formal analysis, Investigation, Validation, Visualization, Writing - original draft, Writing - review & editing
1
Department of Cell and Developmental Biology, Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
Kriti Sethi
Conceptualization, Data curation, Formal analysis, Investigation, Resources, Validation, Visualization, Writing - original draft
2
Mechanobiology Institute, National University of Singapore, Singapore, Singapore
Pei Yi Tan
Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing - review & editing
2
Mechanobiology Institute, National University of Singapore, Singapore, Singapore
Danesha Suresh
Investigation
2
Mechanobiology Institute, National University of Singapore, Singapore, Singapore
Hui Ting Ong
Data curation, Resources, Software, Writing - original draft
2
Mechanobiology Institute, National University of Singapore, Singapore, Singapore
Perla G. Castaneda
Conceptualization, Investigation, Visualization, Writing - original draft, Writing - review & editing
3
Department of Biology, Northeastern University, Boston, MA, USA
Mustafi R. Amin
Formal analysis, Investigation, Validation, Visualization, Writing - review & editing
3
Department of Biology, Northeastern University, Boston, MA, USA
Tal Laviv
Formal analysis, Investigation, Visualization
4
Department of Physiology and Pharmacology, Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel
5
Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel
Erin J. Cram
Formal analysis, Funding acquisition, Writing - review & editing
3
Department of Biology, Northeastern University, Boston, MA, USA
Jan Faix
Formal analysis, Investigation, Validation, Writing - review & editing
6
Institute for Biophysical Chemistry, Hannover Medical School, Hannover, Germany
Correspondence to Ronen Zaidel-Bar: zaidelbar@tauex.tau.ac.il
Disclosures: The authors declare no competing financial interests.
Received:
March 24 2022
Revision Received:
October 03 2022
Accepted:
November 08 2022
Online Issn: 1540-8140
Print Issn: 0021-9525
Funding
Funder(s):
Israel Science Foundation
- Award Id(s): 1293/17,767/20
Funder(s):
National Science Foundation
- Award Id(s): 1816640
Funder(s):
Israel Binational Science Foundation award
- Award Id(s): 2017657
Funder(s):
Deutsche Forschungsgemeinschaft
- Award Id(s): Fa330/12-3
Funder(s):
Office of Research Infrastructure Programs, National Institutes of Health
- Award Id(s): P40 OD010440
Funder(s):
Joan and Jaime Constantiner Institute for Molecular Genetics
© 2022 Kela et al.
2022
Kela et al.
This article is distributed under the terms of an Attribution–Noncommercial–Share Alike–No Mirror Sites license for the first six months after the publication date (see http://www.rupress.org/terms/). After six months it is available under a Creative Commons License (Attribution–Noncommercial–Share Alike 4.0 International license, as described at https://creativecommons.org/licenses/by-nc-sa/4.0/).
J Cell Biol (2023) 222 (2): e202203105.
Article history
Received:
March 24 2022
Revision Received:
October 03 2022
Accepted:
November 08 2022
Citation
Shiri Avivi Kela, Kriti Sethi, Pei Yi Tan, Danesha Suresh, Hui Ting Ong, Perla G. Castaneda, Mustafi R. Amin, Tal Laviv, Erin J. Cram, Jan Faix, Ronen Zaidel-Bar; Tension-dependent RHGF-1 recruitment to stress fibers drives robust spermathecal tissue contraction. J Cell Biol 6 February 2023; 222 (2): e202203105. doi: https://doi.org/10.1083/jcb.202203105
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