α-Toxin Regulates Local Granulocyte Expansion from Hematopoietic Stem and Progenitor Cells in Staphylococcus aureus- Infected Wounds

J Immunol. 2017 Sep 1;199(5):1772-1782. doi: 10.4049/jimmunol.1700649. Epub 2017 Jul 21.

Abstract

The immune response to Staphylococcus aureus infection in skin involves the recruitment of polymorphonuclear neutrophils (PMNs) from the bone marrow via the circulation and local granulopoiesis from hematopoietic stem and progenitor cells (HSPCs) that also traffic to infected skin wounds. We focus on regulation of PMN number and function and the role of pore-forming α-toxin (AT), a virulence factor that causes host cell lysis and elicits inflammasome-mediated IL-1β secretion in wounds. Infection with wild-type S. aureus enriched in AT reduced PMN recruitment and resulted in sustained bacterial burden and delayed wound healing. In contrast, PMN recruitment to wounds infected with an isogenic AT-deficient S. aureus strain was unimpeded, exhibiting efficient bacterial clearance and hastened wound resolution. HSPCs recruited to infected wounds were unaffected by AT production and were activated to expand PMN numbers in proportion to S. aureus abundance in a manner regulated by TLR2 and IL-1R signaling. Immunodeficient MyD88-knockout mice infected with S. aureus experienced lethal sepsis that was reversed by PMN expansion mediated by injection of wild-type HSPCs directly into wounds. We conclude that AT-induced IL-1β promotes local granulopoiesis and effective resolution of S. aureus-infected wounds, revealing a potential antibiotic-free strategy for tuning the innate immune response to treat methicillin-resistant S. aureus infection in immunodeficient patients.

Publication types

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

MeSH terms

  • Animals
  • Bacterial Load
  • Bacterial Toxins / genetics
  • Bacterial Toxins / immunology*
  • Cell Differentiation
  • Cell Proliferation
  • Granulocytes / immunology*
  • Granulocytes / microbiology
  • Hematopoietic Stem Cells / physiology*
  • Hemolysin Proteins / genetics
  • Hemolysin Proteins / immunology*
  • Immunomodulation
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mutation / genetics
  • Myeloid Differentiation Factor 88 / genetics
  • Receptors, Interleukin-1 / metabolism
  • Signal Transduction
  • Staphylococcal Infections / immunology*
  • Staphylococcus aureus / physiology*
  • Toll-Like Receptor 2 / metabolism
  • Virulence Factors / genetics
  • Virulence Factors / immunology*
  • Wound Infection / immunology*

Substances

  • Bacterial Toxins
  • Hemolysin Proteins
  • Myd88 protein, mouse
  • Myeloid Differentiation Factor 88
  • Receptors, Interleukin-1
  • Tlr2 protein, mouse
  • Toll-Like Receptor 2
  • Virulence Factors
  • staphylococcal alpha-toxin