Nonredundant protective properties of FPR2/ALX in polymicrobial murine sepsis

Proc Natl Acad Sci U S A. 2014 Dec 30;111(52):18685-90. doi: 10.1073/pnas.1410938111. Epub 2014 Dec 15.

Abstract

Sepsis is characterized by overlapping phases of excessive inflammation temporally aligned with an immunosuppressed state, defining a complex clinical scenario that explains the lack of successful therapeutic options. Here we tested whether the formyl-peptide receptor 2/3 (Fpr2/3)--ortholog to human FPR2/ALX (receptor for lipoxin A4)--exerted regulatory and organ-protective functions in experimental sepsis. Coecal ligature and puncture was performed to obtain nonlethal polymicrobial sepsis, with animals receiving antibiotics and analgesics. Clinical symptoms, temperature, and heart function were monitored up to 24 h. Peritoneal lavage and plasma samples were analyzed for proinflammatory and proresolving markers of inflammation and organ dysfunction. Compared with wild-type mice, Fpr2/3(-/-) animals exhibited exacerbation of disease severity, including hypothermia and cardiac dysfunction. This scenario was paralleled by higher levels of cytokines [CXCL1 (CXC receptor ligand 1), CCL2 (CC receptor ligand 2), and TNFα] as quantified in cell-free biological fluids. Reduced monocyte recruitment in peritoneal lavages of Fpr2/3(-/-) animals was reflected by a higher granulocyte/monocyte ratio. Monitoring Fpr2/3(-/-) gene promoter activity with a GFP proxy marker revealed an over threefold increase in granulocyte and monocyte signals at 24 h post-coecal ligature and puncture, a response mediated by TNFα. Treatment with a receptor peptido-agonist conferred protection against myocardial dysfunction in wild-type, but not Fpr2/3(-/-), animals. Therefore, coordinated physio-pharmacological analyses indicate nonredundant modulatory functions for Fpr2/3 in experimental sepsis, opening new opportunities to manipulate the host response for therapeutic development.

Keywords: ALX; annexin peptide; cardiac dysfunction; resolution of inflammation; therapeutic innovation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism
  • Chemokine CXCL1 / genetics
  • Chemokine CXCL1 / metabolism
  • Disease Models, Animal
  • Granulocytes / metabolism*
  • Granulocytes / pathology
  • Humans
  • Mice
  • Mice, Knockout
  • Monocytes / metabolism*
  • Monocytes / pathology
  • Peritoneum / metabolism
  • Peritoneum / pathology
  • Receptors, Formyl Peptide / genetics
  • Receptors, Formyl Peptide / metabolism*
  • Sepsis / genetics
  • Sepsis / metabolism*
  • Sepsis / pathology
  • Signal Transduction*
  • Time Factors
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Adaptor Proteins, Signal Transducing
  • Ccl2 protein, mouse
  • Chemokine CCL2
  • Chemokine CXCL1
  • Cxcl1 protein, mouse
  • HSH2 protein, mouse
  • Receptors, Formyl Peptide
  • Tumor Necrosis Factor-alpha
  • formyl peptide receptor 2, mouse