Directed cell invasion and asymmetric adhesion drive tissue elongation and turning in C. elegans gonad morphogenesis

Priti Agarwal, Tom Shemesh*, Ronen Zaidel-Bar*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

Abstract

Development of the C. elegans gonad has long been studied as a model of organogenesis driven by collective cell migration. A somatic cell named the distal tip cell (DTC) is thought to serve as the leader of following germ cells; yet, the mechanism for DTC propulsion and maneuvering remains elusive. Here, we demonstrate that the DTC is not self-propelled but rather is pushed by the proliferating germ cells. Proliferative pressure pushes the DTC forward, against the resistance of the basement membrane in front. The DTC locally secretes metalloproteases that degrade the impeding membrane, resulting in gonad elongation. Turning of the gonad is achieved by polarized DTC-matrix adhesions. The asymmetrical traction results in a bending moment on the DTC. Src and Cdc42 regulate integrin adhesion polarity, whereas an external netrin signal determines DTC orientation. Our findings challenge the current view of DTC migration and offer a distinct framework to understand organogenesis.

Original languageEnglish
Pages (from-to)2111-2126.e6
JournalDevelopmental Cell
Volume57
Issue number17
DOIs
StatePublished - 12 Sep 2022

Funding

FundersFunder number
United States-Israel Binational Science Foundation2021014, 2751/20
Israel Science Foundation3308/20, 767/20

    Keywords

    • cell adhesion
    • cell invasion
    • cell migration
    • cell polarity
    • extracellular matrix degradation
    • integrins
    • organogenesis
    • proliferative pressure
    • tissue elongation
    • tissue mechanics

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