Actin network disassembly powers dissemination of Listeria monocytogenes

J Cell Sci. 2014 Jan 1;127(Pt 1):240-9. doi: 10.1242/jcs.140038. Epub 2013 Oct 23.

Abstract

Several bacterial pathogens hijack the actin assembly machinery and display intracellular motility in the cytosol of infected cells. At the cell cortex, intracellular motility leads to bacterial dissemination through formation of plasma membrane protrusions that resolve into vacuoles in adjacent cells. Here, we uncover a crucial role for actin network disassembly in dissemination of Listeria monocytogenes. We found that defects in the disassembly machinery decreased the rate of actin tail turnover but did not affect the velocity of the bacteria in the cytosol. By contrast, defects in the disassembly machinery had a dramatic impact on bacterial dissemination. Our results suggest a model of L. monocytogenes dissemination in which the disassembly machinery, through local recycling of the actin network in protrusions, fuels continuous actin assembly at the bacterial pole and concurrently exhausts cytoskeleton components from the network distal to the bacterium, which enables membrane apposition and resolution of protrusions into vacuoles.

Keywords: AIP1; ARP2/3; Actin assembly; Actin network disassembly; CFL1; GMFB; Listeria; WDR1.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Actin Cytoskeleton / genetics*
  • Actin Cytoskeleton / metabolism
  • Actin Cytoskeleton / microbiology
  • Actins / antagonists & inhibitors
  • Actins / genetics*
  • Actins / metabolism
  • Cell Membrane / metabolism
  • Cell Membrane / microbiology
  • Cofilin 1 / genetics
  • Cofilin 1 / metabolism
  • Cytosol / metabolism
  • Cytosol / microbiology
  • Gene Expression Regulation
  • Glia Maturation Factor / genetics
  • Glia Maturation Factor / metabolism
  • HeLa Cells
  • Host-Pathogen Interactions
  • Humans
  • Listeria monocytogenes / physiology*
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism
  • Microscopy, Confocal
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Signal Transduction
  • Vacuoles / metabolism
  • Vacuoles / microbiology

Substances

  • Actins
  • CFL1 protein, human
  • Cofilin 1
  • Glia Maturation Factor
  • Microfilament Proteins
  • RNA, Small Interfering
  • WDR1 protein, human