Membrane prewetting by condensates promotes tight-junction belt formation

Nature. 2024 Aug;632(8025):647-655. doi: 10.1038/s41586-024-07726-0. Epub 2024 Aug 7.

Abstract

Biomolecular condensates enable cell compartmentalization by acting as membraneless organelles1. How cells control the interactions of condensates with other cellular structures such as membranes to drive morphological transitions remains poorly understood. We discovered that formation of a tight-junction belt, which is essential for sealing epithelial tissues, is driven by a wetting phenomenon that promotes the growth of a condensed ZO-1 layer2 around the apical membrane interface. Using temporal proximity proteomics in combination with imaging and thermodynamic theory, we found that the polarity protein PATJ mediates a transition of ZO-1 into a condensed surface layer that elongates around the apical interface. In line with the experimental observations, our theory of condensate growth shows that the speed of elongation depends on the binding affinity of ZO-1 to the apical interface and is constant. Here, using PATJ mutations, we show that ZO-1 interface binding is necessary and sufficient for tight-junction belt formation. Our results demonstrate how cells exploit the collective biophysical properties of protein condensates at membrane interfaces to shape mesoscale structures.

MeSH terms

  • Animals
  • Biomolecular Condensates* / chemistry
  • Biomolecular Condensates* / metabolism
  • Cell Compartmentation
  • Cell Membrane* / chemistry
  • Cell Membrane* / metabolism
  • Dogs
  • Epithelium
  • HEK293 Cells
  • Humans
  • Madin Darby Canine Kidney Cells
  • Mutation
  • Protein Binding
  • Proteomics
  • Thermodynamics
  • Tight Junction Proteins / metabolism
  • Tight Junctions* / chemistry
  • Tight Junctions* / metabolism
  • Wettability*
  • Zonula Occludens-1 Protein / genetics
  • Zonula Occludens-1 Protein / metabolism

Substances

  • PATJ protein, human
  • Tight Junction Proteins
  • TJP1 protein, human
  • Zonula Occludens-1 Protein