Neutrophil-derived IL-1β Is Sufficient for Abscess Formation in Immunity against Staphylococcus aureus in Mice

John S. Cho, Yi Guo, Romela Irene Ramos, Frank Hebroni, Seema B. Plaisier, Caiyun Xuan, Jennifer L. Granick, Hironori Matsushima, Akira Takashima, Yoichiro Iwakura, Ambrose L. Cheung, Genhong Cheng, Delphine J. Lee, Scott I. Simon, Lloyd S Miller

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Article numbere1003047
JournalPLoS Pathogens
Volume8
Issue number11
DOIs
StatePublished - Nov 2012

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Interleukin-1
Abscess
Staphylococcus aureus
Immunity
Neutrophils
Infection
Inflammasomes
Adoptive Transfer
Neutrophil Infiltration
Antigen-Presenting Cells
Innate Immunity
Monocytes
Macrophages
Gene Expression
Skin

ASJC Scopus subject areas

  • Microbiology
  • Parasitology
  • Virology
  • Immunology
  • Genetics
  • Molecular Biology

Cite this

Neutrophil-derived IL-1β Is Sufficient for Abscess Formation in Immunity against Staphylococcus aureus in Mice. / Cho, John S.; Guo, Yi; Ramos, Romela Irene; Hebroni, Frank; Plaisier, Seema B.; Xuan, Caiyun; Granick, Jennifer L.; Matsushima, Hironori; Takashima, Akira; Iwakura, Yoichiro; Cheung, Ambrose L.; Cheng, Genhong; Lee, Delphine J.; Simon, Scott I.; Miller, Lloyd S.

In: PLoS Pathogens, Vol. 8, No. 11, e1003047, 11.2012.

Research output: Contribution to journalArticle

Cho, JS, Guo, Y, Ramos, RI, Hebroni, F, Plaisier, SB, Xuan, C, Granick, JL, Matsushima, H, Takashima, A, Iwakura, Y, Cheung, AL, Cheng, G, Lee, DJ, Simon, SI & Miller, LS 2012, 'Neutrophil-derived IL-1β Is Sufficient for Abscess Formation in Immunity against Staphylococcus aureus in Mice', PLoS Pathogens, vol. 8, no. 11, e1003047. https://doi.org/10.1371/journal.ppat.1003047
Cho, John S. ; Guo, Yi ; Ramos, Romela Irene ; Hebroni, Frank ; Plaisier, Seema B. ; Xuan, Caiyun ; Granick, Jennifer L. ; Matsushima, Hironori ; Takashima, Akira ; Iwakura, Yoichiro ; Cheung, Ambrose L. ; Cheng, Genhong ; Lee, Delphine J. ; Simon, Scott I. ; Miller, Lloyd S. / Neutrophil-derived IL-1β Is Sufficient for Abscess Formation in Immunity against Staphylococcus aureus in Mice. In: PLoS Pathogens. 2012 ; Vol. 8, No. 11.
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