Extracellular matrix assembly stress initiates Drosophila central nervous system morphogenesis

• Published in: Developmental cell Vol. 58; no. 10; pp. 825 - 835.e6
• Main Authors: Serna-Morales, Eduardo, Sánchez-Sánchez, Besaiz J., Marcotti, Stefania, Nichols, Angus, Bhargava, Anushka, Dragu, Anca, Hirvonen, Liisa M., Díaz-de-la-Loza, María-del-Carmen, Mink, Matyas, Cox, Susan, Rayfield, Emily, Lee, Rachel M., Hobson, Chad M., Chew, Teng-Leong, Stramer, Brian M.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 22.05.2023; Cell Press
• Subjects: Animals; basement membrane; Central Nervous System; collagen IV; Drosophila; Drosophila - genetics; embryonic development; extracellular matix; Extracellular Matrix - physiology; morphogenesis; Morphogenesis - physiology; Short; surface tension; basement membrane; morphogenesis; Drosophila; extracellular matix; embryonic development; collagen IV; surface tension; central nervous system
• ISSN: 1534-5807; 1878-1551
• DOI: 10.1016/j.devcel.2023.03.019

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. [Display omitted] •Sudden uneven Col4 assembly surrounding the fly VNC initiates tissue condensation•Col4 flows coherently on the tissue surface independently of cellular contractility•Modeling indicates that a BM-dependent increase in surface tension drives morphogenesis•Perturbations of Col4 assembly affect the rate of VNC condensation Serna-Morales et al. demonstrate that the initiation of Drosophila VNC condensation is triggered by sudden basement membrane assembly around the tissue, which increases the surface tension independently of cellular contractile activity. Their work suggests that intrinsic stresses in an assembling basement membrane network can actively contribute forces that drive tissue morphogenesis.