Evolutionary plasticity in the requirement for force exerted by ligand endocytosis to activate C. elegans Notch proteins

Curr Biol. 2022 May 23;32(10):2263-2271.e6. doi: 10.1016/j.cub.2022.03.025. Epub 2022 Mar 28.

Abstract

The conserved transmembrane receptor Notch has diverse and profound roles in controlling cell fate during animal development. In the absence of ligand, a negative regulatory region (NRR) in the Notch ectodomain adopts an autoinhibited confirmation, masking an ADAM protease cleavage site;1,2 ligand binding induces cleavage of the NRR, leading to Notch ectodomain shedding as the first step of signal transduction.3,4 In Drosophila and vertebrates, recruitment of transmembrane Delta/Serrate/LAG-2 (DSL) ligands by the endocytic adaptor Epsin, and their subsequent internalization by Clathrin-mediated endocytosis, exerts a "pulling force" on Notch that is essential to expose the cleavage site in the NRR.4-6 Here, we show that Epsin-mediated endocytosis of transmembrane ligands is not essential to activate the two C. elegans Notch proteins, LIN-12 and GLP-1. Using an in vivo force sensing assay in Drosophila,6 we present evidence (1) that the LIN-12 and GLP-1 NRRs are tuned to lower force thresholds than the NRR of Drosophila Notch, and (2) that this difference depends on the absence of a "leucine plug" that occludes the cleavage site in the Drosophila and vertebrate Notch NRRs.1,2 Our results thus establish an unexpected evolutionary plasticity in the force-dependent mechanism of Notch activation and implicate a specific structural element, the leucine plug, as a determinant.

Keywords: ADAM protease; C. elegans; Drosophila; Epsin; NRR; Notch; ectodomain shedding; force sensor; ligand endocytosis; mechano-receptor; negative regulatory region.

Publication types

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

MeSH terms

  • Animals
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / metabolism
  • Caenorhabditis elegans Proteins* / genetics
  • Drosophila / metabolism
  • Drosophila Proteins* / genetics
  • Drosophila Proteins* / metabolism
  • Endocytosis
  • Glucagon-Like Peptide 1
  • Leucine
  • Ligands
  • Receptors, Notch / genetics
  • Receptors, Notch / metabolism

Substances

  • Caenorhabditis elegans Proteins
  • Drosophila Proteins
  • Ligands
  • Receptors, Notch
  • Glucagon-Like Peptide 1
  • Leucine