SQSTM1/p62/A170 regulates the severity of Legionella pneumophila pneumonia by modulating inflammasome activity

Eur J Immunol. 2014 Apr;44(4):1084-92. doi: 10.1002/eji.201344091. Epub 2014 Jan 28.

Abstract

Sequestosome1/A170/p62 (SQSTM1) is a scaffold multifunctional protein involved in several cellular events, such as signal transduction, cell survival, cell death, and inflammation. SQSTM1 expression by macrophages is induced in response to environmental stresses; however, its role in macrophage-mediated host responses to environmental stimuli, such as infectious pathogens, remains unclear. In this study, we investigated the role of SQSTM1 in host responses to Legionella pneumophila, an intra-cellular pathogen that infects macrophages, in both an SQSTM1-deficient (SQSTM1(-/-) ) mouse model and macrophages from these mice. Compared with wild-type (WT) macrophages, the production and secretion of the proinflammatory cytokine IL-1β was significantly enhanced in SQSTM1(-/-) macrophages after infection with L. pneumophila. Inflammasome activity, indicated by the level of IL-18 and caspase-1 activity, was also elevated in SQSTM1(-/-) macrophages after infection with L. pneumophila. SQSTM1 may interact with nucleotide-binding oligomerization domain-like receptor family, caspase recruitment domain-containing 4 and nucleotide-binding oligomerization domain like receptor family, pyrin domain containing 3 proteins to inhibit their self-dimerization. Acute pulmonary inflammation induced by L. pneumophila and silica was enhanced in SQSTM1(-/-) mice with an increase in IL-1β levels in the bronchoalveolar lavage fluids. These findings suggest that SQSTM1 is a negative regulator of acute pulmonary inflammation, possibly by regulating inflammasome activity and subsequent proinflammatory cytokine production.

Keywords: Inflammasome; Legionella; Macrophages; Pneumonia; Sequestosome1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / deficiency
  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / immunology*
  • Animals
  • Bronchoalveolar Lavage Fluid / chemistry
  • Bronchoalveolar Lavage Fluid / immunology
  • Bronchoalveolar Lavage Fluid / microbiology
  • Caspase 1 / immunology
  • Caspase 1 / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Heat-Shock Proteins / deficiency
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / immunology*
  • Host-Pathogen Interactions / immunology
  • Immunoblotting
  • Inflammasomes / immunology*
  • Inflammasomes / metabolism
  • Interleukin-18 / immunology
  • Interleukin-18 / metabolism
  • Interleukin-1beta / immunology
  • Interleukin-1beta / metabolism
  • Legionella pneumophila / immunology*
  • Legionella pneumophila / physiology
  • Legionnaires' Disease / immunology*
  • Legionnaires' Disease / microbiology
  • Legionnaires' Disease / pathology
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / microbiology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • NF-kappa B / immunology
  • NF-kappa B / metabolism
  • Pneumonia / immunology*
  • Pneumonia / microbiology
  • Pneumonia / pathology
  • Sequestosome-1 Protein
  • Severity of Illness Index

Substances

  • Adaptor Proteins, Signal Transducing
  • Heat-Shock Proteins
  • Inflammasomes
  • Interleukin-18
  • Interleukin-1beta
  • NF-kappa B
  • Sequestosome-1 Protein
  • Sqstm1 protein, mouse
  • Caspase 1