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

Alex R. Generous, Oliver J. Harrison, Regina B. Troyanovsky, Mathieu Mateo, Chanakha K. Navaratnarajah, Ryan C. Donohue, Christian K. Pfaller, Olga Alekhina, Alina P. Sergeeva, Indrajyoti Indra, Theresa Thornburg, Irina Kochetkova, Daniel D. Billadeau, Matthew P. Taylor, Sergey M. Troyanovsky, Barry Honig, Lawrence Shapiro, Roberto Cattaneo

Research output: Contribution to journalArticle

8 Scopus citations

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.

Original languageEnglish (US)
JournalJournal of cell science
Volume132
Issue number16
DOIs
StatePublished - Aug 23 2019

Keywords

  • Cell adhesion
  • Cell communication
  • Cytoplasm transfer
  • Measles virsus
  • Nectin
  • Neuronal entry
  • Trans-endocytosis
  • Virus receptor

ASJC Scopus subject areas

  • Cell Biology

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  • Cite this

    Generous, A. R., Harrison, O. J., Troyanovsky, R. B., Mateo, M., Navaratnarajah, C. K., Donohue, R. C., Pfaller, C. K., Alekhina, O., Sergeeva, A. P., Indra, I., Thornburg, T., Kochetkova, I., Billadeau, D. D., Taylor, M. P., Troyanovsky, S. M., Honig, B., Shapiro, L., & Cattaneo, R. (2019). Trans-endocytosis elicited by nectins transfers cytoplasmic cargo, including infectious material, between cells. Journal of cell science, 132(16). https://doi.org/10.1242/jcs.235507