Trans-endocytosis elicited by nectins transfers cytoplasmic cargo, including infectious material, between cells

J Cell Sci. 2019 Aug 23;132(16):jcs235507. doi: 10.1242/jcs.235507.

Abstract

Here, we show that cells expressing the adherens junction protein nectin-1 capture nectin-4-containing membranes from the surface of adjacent cells in a trans-endocytosis process. We find that internalized nectin-1-nectin-4 complexes follow the endocytic pathway. The nectin-1 cytoplasmic tail controls transfer: its deletion prevents trans-endocytosis, while its exchange with the nectin-4 tail reverses transfer direction. Nectin-1-expressing cells acquire dye-labeled cytoplasmic proteins synchronously with nectin-4, a process most active during cell adhesion. Some cytoplasmic cargo remains functional after transfer, as demonstrated with encapsidated genomes of measles virus (MeV). This virus uses nectin-4, but not nectin-1, as a receptor. Epithelial cells expressing nectin-4, but not those expressing another MeV receptor in its place, can transfer infection to nectin-1-expressing primary neurons. Thus, this newly discovered process can move cytoplasmic cargo, including infectious material, from epithelial cells to neurons. We name the process nectin-elicited cytoplasm transfer (NECT). NECT-related trans-endocytosis processes may be exploited by pathogens to extend tropism. This article has an associated First Person interview with the first author of the paper.

Keywords: Cell adhesion; Cell communication; Cytoplasm transfer; Measles virsus; Nectin; Neuronal entry; Trans-endocytosis; Virus receptor.

Publication types

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

MeSH terms

  • Biological Transport, Active / genetics
  • Cell Adhesion / genetics
  • Cell Adhesion Molecules / genetics
  • Cell Adhesion Molecules / metabolism*
  • Cell Line
  • Endocytosis*
  • Epithelial Cells / metabolism*
  • Humans
  • Measles virus / genetics
  • Measles virus / metabolism*
  • Nectins / genetics
  • Nectins / metabolism*
  • Virus Internalization*

Substances

  • Cell Adhesion Molecules
  • NECTIN1 protein, human
  • Nectins
  • NECTIN4 protein, human