Extracellular matrix assembly stress initiates Drosophila central nervous system morphogenesis

Eduardo Serna Morales, Besaiz Sánchez Sánchez, Stefania Marcotti, Angus Nichols, Anushka Bhargava, Anca Dragu, Liisa Hirvonen, María-del-Carmen Díaz-de-la-Loza, Matyas Mink, Susan Cox, Emily Rayfield, Rachel M Lee, Chad M Hobson, Teng-Leong Chew, Brian Stramer*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

6 Citations (Scopus)

Abstract

Forces controlling tissue morphogenesis are attributed to cellular-driven activities, and any role for extracellular matrix (ECM) is assumed to be passive. However, all polymer networks, including ECM, can develop autonomous stresses during their assembly. Here, we examine the morphogenetic function of an ECM before reaching homeostatic equilibrium by analyzing de novo ECM assembly during Drosophila ventral nerve cord (VNC) condensation. Asymmetric VNC shortening and a rapid decrease in surface area correlate with the exponential assembly of collagen IV (Col4) surrounding the tissue. Concomitantly, a transient developmentally induced Col4 gradient leads to coherent long-range flow of ECM, which equilibrates the Col4 network. Finite element analysis and perturbation of Col4 network formation through the generation of dominant Col4 mutations that affect assembly reveal that VNC morphodynamics is partially driven by a sudden increase in ECM-driven surface tension. These data suggest that ECM assembly stress and associated network instabilities can actively participate in tissue morphogenesis.
Original languageEnglish
Pages (from-to)825-835.e6
JournalDevelopmental Cell
Volume58
Issue number10
Early online date21 Apr 2023
DOIs
Publication statusPublished - 21 Apr 2023

Keywords

  • Drosophila
  • Basement Membrane
  • Collagen IV
  • Morphogenesis
  • Central Nervous System
  • Extracellular Matrix
  • Surface Tension
  • Embryonic Development

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