Neutrophil-derived IL-1β is sufficient for abscess formation in immunity against Staphylococcus aureus in mice

PLoS Pathog. 2012;8(11):e1003047. doi: 10.1371/journal.ppat.1003047. Epub 2012 Nov 29.

Abstract

Neutrophil abscess formation is critical in innate immunity against many pathogens. Here, the mechanism of neutrophil abscess formation was investigated using a mouse model of Staphylococcus aureus cutaneous infection. Gene expression analysis and in vivo multispectral noninvasive imaging during the S. aureus infection revealed a strong functional and temporal association between neutrophil recruitment and IL-1β/IL-1R activation. Unexpectedly, neutrophils but not monocytes/macrophages or other MHCII-expressing antigen presenting cells were the predominant source of IL-1β at the site of infection. Furthermore, neutrophil-derived IL-1β was essential for host defense since adoptive transfer of IL-1β-expressing neutrophils was sufficient to restore the impaired neutrophil abscess formation in S. aureus-infected IL-1β-deficient mice. S. aureus-induced IL-1β production by neutrophils required TLR2, NOD2, FPR1 and the ASC/NLRP3 inflammasome in an α-toxin-dependent mechanism. Taken together, IL-1β and neutrophil abscess formation during an infection are functionally, temporally and spatially linked as a consequence of direct IL-1β production by neutrophils.

Publication types

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

MeSH terms

  • Abscess / genetics
  • Abscess / immunology*
  • Abscess / metabolism
  • Abscess / microbiology
  • Abscess / pathology
  • Adoptive Transfer
  • Animals
  • Carrier Proteins / genetics
  • Carrier Proteins / immunology
  • Carrier Proteins / metabolism
  • Inflammasomes / genetics
  • Inflammasomes / immunology
  • Inflammasomes / metabolism
  • Interleukin-1beta / biosynthesis
  • Interleukin-1beta / genetics
  • Interleukin-1beta / immunology*
  • Mice
  • Mice, Mutant Strains
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Neutrophils / immunology*
  • Neutrophils / metabolism
  • Neutrophils / pathology
  • Nod2 Signaling Adaptor Protein / genetics
  • Nod2 Signaling Adaptor Protein / immunology
  • Nod2 Signaling Adaptor Protein / metabolism
  • Receptors, Formyl Peptide / genetics
  • Receptors, Formyl Peptide / immunology
  • Receptors, Formyl Peptide / metabolism
  • Staphylococcal Skin Infections / genetics
  • Staphylococcal Skin Infections / immunology*
  • Staphylococcal Skin Infections / metabolism
  • Staphylococcal Skin Infections / microbiology
  • Staphylococcal Skin Infections / pathology
  • Staphylococcus aureus / immunology*
  • Toll-Like Receptor 2 / genetics
  • Toll-Like Receptor 2 / immunology
  • Toll-Like Receptor 2 / metabolism

Substances

  • Carrier Proteins
  • Fpr1 protein, mouse
  • Inflammasomes
  • Interleukin-1beta
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Nod2 Signaling Adaptor Protein
  • Nod2 protein, mouse
  • Receptors, Formyl Peptide
  • Tlr2 protein, mouse
  • Toll-Like Receptor 2