Distinct cellular and junctional dynamics independently regulate the rotation and elongation of the embryonic gut in Drosophila

Complex organ structures are formed with high reproducibility. To achieve such intricate morphologies, the responsible epithelium undergoes multiple simultaneous shape changes, such as elongation and folding. However, these changes have typically been assessed separately. In this study, we revealed how distinct shape changes are controlled during internal organ morphogenesis. The Drosophila embryonic hindgut undergoes left-right asymmetric rotation and anteroposterior elongation in a tissue-autonomous manner driven by cell sliding and convergent extension, respectively, in the hindgut epithelia. However, the regulation of these processes remains unclear. Through genetic analysis and live imaging, we demonstrated that cell sliding and convergent extension are independently regulated by Myosin1D and E-cadherin, and Par-3, respectively, whereas both require MyosinII activity. Using a mathematical model, we demonstrated that independently regulated cellular dynamics can simultaneously cause shape changes in a single mechanical system using anisotropic edge contraction. Our findings indicate that distinct cellular dynamics sharing a common apparatus can be independently and simultaneously controlled to form complex organ shapes. This suggests that such a mechanism may be a general strategy during complex tissue morphogenesis.

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Publication Details

Journal
PLoS Genetics
Published
2024-10-07
DOI
https://doi.org/10.1371/journal.pgen.1011422
Citations
1
Primary Topic
Cellular Mechanics and Interactions
Type
article
Field-Weighted Citation Impact
0.33

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article

Distinct cellular and junctional dynamics independently regulate the rotation and elongation of the embryonic gut in Drosophila

Kenji Matsuno, Satoru Okuda, Mikiko Inaki, Takamasa Higashi
1 citations
PLoS Genetics
Cellular Mechanics and Interactions
0.33
article

Distinct cellular and junctional dynamics independently regulate the rotation and elongation of the embryonic gut in Drosophila

Kenji Matsuno, Satoru Okuda, Mikiko Inaki, Takamasa Higashi
article en
1 citations

Abstract

Complex organ structures are formed with high reproducibility. To achieve such intricate morphologies, the responsible epithelium undergoes multiple simultaneous shape changes, such as elongation and folding. However, these changes have typically been assessed separately. In this study, we revealed how distinct shape changes are controlled during internal organ morphogenesis. The Drosophila embryonic hindgut undergoes left-right asymmetric rotation and anteroposterior elongation in a tissue-autonomous manner driven by cell sliding and convergent extension, respectively, in the hindgut epithelia. However, the regulation of these processes remains unclear. Through genetic analysis and live imaging, we demonstrated that cell sliding and convergent extension are independently regulated by Myosin1D and E-cadherin, and Par-3, respectively, whereas both require MyosinII activity. Using a mathematical model, we demonstrated that independently regulated cellular dynamics can simultaneously cause shape changes in a single mechanical system using anisotropic edge contraction. Our findings indicate that distinct cellular dynamics sharing a common apparatus can be independently and simultaneously controlled to form complex organ shapes. This suggests that such a mechanism may be a general strategy during complex tissue morphogenesis.

PLoS GeneticsVol. 20(10)
Kanazawa University (JP), University of Hyogo (JP), Life Science Institute (JP)
Naito Foundation, Shiseido Group, Japan Society for the Promotion of Science
Openalex Percentile: Top 41%
Cellular Mechanics and Interactions
0.33
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Distinct cellular and junctional dynamics independently regulate the rotation and elongation of the embryonic gut in Drosophila — Kenji Matsuno, Satoru Okuda, et al. · PLoS Genetics (2024) | TGRS Research Map | TGRS