Yersinia enterocolitica inhibits Salmonella enterica serovar Typhimurium and Listeria monocytogenes cellular uptake

Infect Immun. 2014 Jan;82(1):174-83. doi: 10.1128/IAI.00984-13. Epub 2013 Oct 14.

Abstract

Yersinia enterocolitica biovar 1B employs two type three secretion systems (T3SS), Ysa and Ysc, which inject effector proteins into macrophages to prevent phagocytosis. Conversely, Salmonella enterica serovar Typhimurium uses a T3SS encoded by Salmonella pathogenicity island 1 (SPI1) to actively invade cells that are normally nonphagocytic and a second T3SS encoded by SPI2 to survive within macrophages. Given the distinctly different outcomes that occur with regard to host cell uptake of S. Typhimurium and Y. enterocolitica, we investigated how each pathogen influences the internalization outcome of the other. Y. enterocolitica reduces S. Typhimurium invasion of HeLa and Caco-2 cells to a level similar to that observed using an S. Typhimurium SPI1 mutant alone. However, Y. enterocolitica had no effect on S. Typhimurium uptake by J774.1 or RAW264.7 macrophage-like cells. Y. enterocolitica was also able to inhibit the invasion of epithelial and macrophage-like cells by Listeria monocytogenes. Y. enterocolitica mutants lacking either the Ysa or Ysc T3SS were partially defective, while double mutants were completely defective, in blocking S. Typhimurium uptake by epithelial cells. S. Typhimurium encodes a LuxR homolog, SdiA, which detects N-acylhomoserine lactones (AHLs) produced by Y. enterocolitica and upregulates the expression of an invasin (Rck) and a putative T3SS effector (SrgE). Two different methods of constitutively activating the S. Typhimurium SdiA regulon failed to reverse the uptake blockade imposed by Y. enterocolitica.

Publication types

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

MeSH terms

  • Analysis of Variance
  • Bacterial Secretion Systems / immunology
  • Bacterial Secretion Systems / physiology
  • Caco-2 Cells
  • Cells, Cultured
  • HeLa Cells
  • Host-Pathogen Interactions / immunology*
  • Humans
  • Listeria monocytogenes / immunology*
  • Listeria monocytogenes / pathogenicity
  • Salmonella typhimurium / immunology*
  • Salmonella typhimurium / pathogenicity
  • Yersinia enterocolitica / immunology*
  • Yersinia enterocolitica / pathogenicity

Substances

  • Bacterial Secretion Systems