Mechanical forces drive neuroblast morphogenesis and are required for epidermal closure

Dev Biol. 2016 Apr 15;412(2):261-77. doi: 10.1016/j.ydbio.2016.02.023. Epub 2016 Feb 27.

Abstract

Tissue morphogenesis requires myosin-dependent events such as cell shape changes and migration to be coordinated between cells within a tissue, and/or with cells from other tissues. However, few studies have investigated the simultaneous morphogenesis of multiple tissues in vivo. We found that during Caenorhabditis elegans ventral enclosure, when epidermal cells collectively migrate to cover the ventral surface of the embryo, the underlying neuroblasts (neuronal precursor cells) also undergo morphogenesis. We found that myosin accumulates as foci along the junction-free edges of the ventral epidermal cells to form a ring, whose closure is myosin-dependent. We also observed the accumulation of myosin foci and the adhesion junction proteins E-cadherin and α-catenin in the underlying neuroblasts. Myosin may help to reorganize a subset of neuroblasts into a rosette-like pattern, and decrease their surface area as the overlying epidermal cells constrict. Since myosin is required in the neuroblasts for ventral enclosure, we propose that mechanical forces in the neuroblasts influence constriction of the overlying epidermal cells. In support of this model, disrupting neuroblast cell division or altering their fate influences myosin localization in the overlying epidermal cells. The coordination of myosin-dependent events and forces between cells in different tissues could be a common theme for coordinating morphogenetic events during metazoan development.

Keywords: Adhesion junctions; Anillin; C. elegans; Cell migration; Epidermal morphogenesis; Myosin; Neuronal development; RhoA.

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Biomechanical Phenomena
  • Cadherins / genetics
  • Cadherins / metabolism
  • Caenorhabditis elegans / cytology
  • Caenorhabditis elegans / embryology
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Cell Movement
  • Cell Proliferation
  • Embryo, Nonmammalian / cytology
  • Embryo, Nonmammalian / embryology
  • Embryo, Nonmammalian / metabolism*
  • Epidermis / embryology
  • Epidermis / metabolism*
  • Luminescent Proteins* / genetics
  • Luminescent Proteins* / metabolism
  • Microscopy, Fluorescence / methods
  • Morphogenesis*
  • Mutation
  • Myosins / genetics
  • Myosins / metabolism
  • Neural Stem Cells / metabolism*
  • RNA Interference
  • Time-Lapse Imaging / methods
  • alpha Catenin / genetics
  • alpha Catenin / metabolism

Substances

  • Cadherins
  • Caenorhabditis elegans Proteins
  • Luminescent Proteins
  • alpha Catenin
  • Myosins