An ECM-to-Nucleus Signaling Pathway Activates Lysosomes for C. elegans Larval Development

Dev Cell. 2020 Jan 6;52(1):21-37.e5. doi: 10.1016/j.devcel.2019.10.020. Epub 2019 Nov 14.

Abstract

Lysosomes degrade macromolecular cargos, recycle catabolites, and serve as signaling platforms to maintain cell homeostasis, but their role at the tissue level is unclear. Here, we investigate lysosome regulation and function during C. elegans molting, a specialized extracellular matrix (ECM) remodeling process essential for larval development. We found that lysosomes are specifically activated in the epidermis at molt when the apical ECM (cuticle) is being replaced. Impaired lysosome function affects endocytic cargo degradation, suppresses elevated protein synthesis at molt, and causes molting defects. Disturbance of ECM-epidermis attachments triggers lysosomal activation and induces expression of the vacuolar H+-ATPase (V-ATPase), which is mediated by the GATA transcription factor ELT-3 and the STAT family protein STA-2. Our study reveals an ECM-to-nucleus signaling pathway that activates lysosomes to facilitate ECM remodeling essential for larval development.

Keywords: C. elegans; ECM remodeling; V-ATPase; cuticle; hemidesmosome; innate immune response; larval development; lysosome; molt.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / growth & development*
  • Caenorhabditis elegans / immunology
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism*
  • Cell Nucleus / genetics
  • Cell Nucleus / immunology
  • Cell Nucleus / metabolism*
  • Epidermis / growth & development
  • Epidermis / immunology
  • Epidermis / metabolism
  • Extracellular Matrix / immunology
  • Extracellular Matrix / metabolism*
  • GATA Transcription Factors / genetics
  • GATA Transcription Factors / metabolism
  • Gene Expression Regulation, Developmental
  • Larva / genetics
  • Larva / growth & development*
  • Larva / metabolism
  • Lysosomes / immunology
  • Lysosomes / metabolism*
  • Molting*
  • Vacuolar Proton-Translocating ATPases / genetics
  • Vacuolar Proton-Translocating ATPases / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • GATA Transcription Factors
  • Vacuolar Proton-Translocating ATPases