Abstract
Animal development consists of a cascade of tissue differentiation and shape change. Associated mechanical signals regulate tissue differentiation. Here we demonstrate that endogenous mechanical cues also trigger biochemical pathways, generating the active morphogenetic movements shaping animal development through a mechanotransductive cascade of Myo-II medio-apical stabilization. To mimic physiological tissue deformation with a cell scale resolution, liposomes containing magnetic nanoparticles are injected into embryonic epithelia and submitted to time-variable forces generated by a linear array of micrometric soft magnets. Periodic magnetically induced deformations quantitatively phenocopy the soft mechanical endogenous snail-dependent apex pulsations, rescue the medio-apical accumulation of Rok, Myo-II and subsequent mesoderm invagination lacking in sna mutants, in a Fog-dependent mechanotransductive process. Mesoderm invagination then activates Myo-II apical accumulation, in a similar Fog-dependent mechanotransductive process, which in turn initiates endoderm invagination. This reveals the existence of a highly dynamic self-inductive cascade of mesoderm and endoderm invaginations, regulated by mechano-induced medio-apical stabilization of Myo-II.
Highlights
Animal development consists of a cascade of tissue differentiation and shape change
Such a response to a non-physiological mechanical perturbation suggested that the mechanotransductive mechanical induction of medio-apical stabilization of Myo-II by the physiological mechanical strains resulting from sna-dependent pulsations could regulate the interplay between sna and twi pathways, which in turn leads to mesoderm morphogenesis
In sna RNA interference (RNAi) injected Spider–GFP Sqh–mCherry embryos, both the pulsating and stably constricting phases are absent, no characteristic period emerges from the spectral signature and there was no apical accumulation of Myo-II (Figs 1e–g and 2g)[28]
Summary
Animal development consists of a cascade of tissue differentiation and shape change. Associated mechanical signals regulate tissue differentiation. We demonstrate that endogenous mechanical cues trigger biochemical pathways, generating the active morphogenetic movements shaping animal development through a mechanotransductive cascade of Myo-II medio-apical stabilization. Mesoderm invagination activates Myo-II apical accumulation, in a similar Fog-dependent mechanotransductive process, which in turn initiates endoderm invagination This reveals the existence of a highly dynamic self-inductive cascade of mesoderm and endoderm invaginations, regulated by mechano-induced medio-apical stabilization of Myo-II. This stimulates a mechanosensitive pathway, Folded gastrulation (Fog), that is downstream of twist[18] Such a response to a non-physiological mechanical perturbation suggested that the mechanotransductive mechanical induction of medio-apical stabilization of Myo-II by the physiological mechanical strains resulting from sna-dependent pulsations could regulate the interplay between sna and twi pathways, which in turn leads to mesoderm morphogenesis
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