Neutrophil mobilization from the bone marrow during polymicrobial sepsis is dependent on CXCL12 signaling

J Immunol. 2011 Jul 15;187(2):911-8. doi: 10.4049/jimmunol.1100588. Epub 2011 Jun 20.

Abstract

Neutrophils are essential for successful host eradication of bacterial pathogens and for survival to polymicrobial sepsis. During inflammation, the bone marrow provides a large reserve of neutrophils that are released into the peripheral circulation where they traverse to sites of infection. Although neutrophils are essential for survival, few studies have investigated the mechanisms responsible for neutrophil mobilization from the bone marrow during polymicrobial sepsis. Using a cecal ligation and puncture model of polymicrobial sepsis, we demonstrated that neutrophil mobilization from the bone marrow is not dependent on TLR4, MyD88, TRIF, IFNARα/β, or CXCR2 pathway signaling during sepsis. In contrast, we observed that bone marrow CXCL12 mRNA abundance and specific CXCL12 levels are sharply reduced, whereas splenic CXCR4 mRNA and cell surface expression are increased during sepsis. Blocking CXCL12 activity significantly reduced blood neutrophilia by inhibiting bone marrow release of granulocytes during sepsis. However, CXCL12 inhibition had no impact on the expansion of bone marrow neutrophil precursors and hematopoietic progenitors. Bone marrow neutrophil retention by CXCL12 blockade prevented blood neutrophilia, inhibited peritoneal neutrophil accumulation, allowed significant peritoneal bacterial invasion, and increased polymicrobial sepsis mortality. We concluded that changes in the pattern of CXCL12 signaling during sepsis are essential for neutrophil bone marrow mobilization and host survival but have little impact on bone marrow granulopoiesis.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Acute Disease
  • Animals
  • Bone Marrow Cells / immunology*
  • Bone Marrow Cells / microbiology
  • Bone Marrow Cells / pathology*
  • Chemokine CXCL12 / genetics
  • Chemokine CXCL12 / physiology*
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C3H
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Mice, Transgenic
  • Myelopoiesis / genetics
  • Myelopoiesis / immunology
  • Neutrophil Infiltration / genetics
  • Neutrophil Infiltration / immunology*
  • Sepsis / immunology*
  • Sepsis / microbiology*
  • Sepsis / mortality
  • Signal Transduction / genetics
  • Signal Transduction / immunology*
  • Survival Analysis

Substances

  • Chemokine CXCL12
  • Cxcl12 protein, mouse