Actin polymerization as a key innate immune effector mechanism to control Salmonella infection

Proc Natl Acad Sci U S A. 2014 Dec 9;111(49):17588-93. doi: 10.1073/pnas.1419925111. Epub 2014 Nov 24.

Abstract

Salmonellosis is one of the leading causes of food poisoning worldwide. Controlling bacterial burden is essential to surviving infection. Nucleotide-binding oligomerization domain-like receptors (NLRs), such as NLRC4, induce inflammasome effector functions and play a crucial role in controlling Salmonella infection. Inflammasome-dependent production of IL-1β recruits additional immune cells to the site of infection, whereas inflammasome-mediated pyroptosis of macrophages releases bacteria for uptake by neutrophils. Neither of these functions is known to directly kill intracellular salmonellae within macrophages. The mechanism, therefore, governing how inflammasomes mediate intracellular bacterial-killing and clearance in host macrophages remains unknown. Here, we show that actin polymerization is required for NLRC4-dependent regulation of intracellular bacterial burden, inflammasome assembly, pyroptosis, and IL-1β production. NLRC4-induced changes in actin polymerization are physically manifested as increased cellular stiffness, and leads to reduced bacterial uptake, production of antimicrobial molecules, and arrested cellular migration. These processes act in concert to limit bacterial replication in the cell and dissemination in tissues. We show, therefore, a functional link between innate immunity and actin turnover in macrophages that underpins a key host defense mechanism for the control of salmonellosis.

Keywords: ASC; ROS; caspase-1; cytoskeleton; innate immunity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actin Cytoskeleton / metabolism
  • Actins / metabolism*
  • Animals
  • Apoptosis Regulatory Proteins / metabolism
  • Bone Marrow Cells / cytology
  • Calcium-Binding Proteins / metabolism
  • Caspase 1 / metabolism
  • Cytoskeleton / metabolism
  • Hydrogen Peroxide / chemistry
  • Immunity, Innate*
  • Inflammasomes / immunology*
  • Inflammation / immunology
  • Interleukin-1beta / metabolism
  • Macrophages / cytology
  • Macrophages / microbiology*
  • Mice
  • Mice, Transgenic
  • Microscopy, Confocal
  • Neutrophils / immunology
  • Polymerization
  • Reactive Oxygen Species / metabolism
  • Salmonella Infections / immunology*
  • Salmonella typhimurium

Substances

  • Actins
  • Apoptosis Regulatory Proteins
  • Calcium-Binding Proteins
  • Inflammasomes
  • Interleukin-1beta
  • Ipaf protein, mouse
  • Reactive Oxygen Species
  • Hydrogen Peroxide
  • Caspase 1