Human resistin promotes neutrophil proinflammatory activation and neutrophil extracellular trap formation and increases severity of acute lung injury

J Immunol. 2014 May 15;192(10):4795-803. doi: 10.4049/jimmunol.1302764. Epub 2014 Apr 9.

Abstract

Although resistin was recently found to modulate insulin resistance in preclinical models of type II diabetes and obesity, recent studies also suggested that resistin has proinflammatory properties. We examined whether the human-specific variant of resistin affects neutrophil activation and the severity of LPS-induced acute lung injury. Because human and mouse resistin have distinct patterns of tissue distribution, experiments were performed using humanized resistin mice that exclusively express human resistin (hRTN(+/-)(/-)) but are deficient in mouse resistin. Enhanced production of TNF-α or MIP-2 was found in LPS-treated hRtn(+/-/-) neutrophils compared with control Rtn(-/-/-) neutrophils. Expression of human resistin inhibited the activation of AMP-activated protein kinase, a major sensor and regulator of cellular bioenergetics that also is implicated in inhibiting inflammatory activity of neutrophils and macrophages. In addition to the ability of resistin to sensitize neutrophils to LPS stimulation, human resistin enhanced neutrophil extracellular trap formation. In LPS-induced acute lung injury, humanized resistin mice demonstrated enhanced production of proinflammatory cytokines, more severe pulmonary edema, increased neutrophil extracellular trap formation, and elevated concentration of the alarmins HMGB1 and histone 3 in the lungs. Our results suggest that human resistin may play an important contributory role in enhancing TLR4-induced inflammatory responses, and it may be a target for future therapies aimed at reducing the severity of acute lung injury and other inflammatory situations in which neutrophils play a major role.

Publication types

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

MeSH terms

  • AMP-Activated Protein Kinases / genetics
  • AMP-Activated Protein Kinases / immunology
  • Acute Lung Injury / chemically induced
  • Acute Lung Injury / genetics
  • Acute Lung Injury / immunology*
  • Acute Lung Injury / pathology
  • Acute Lung Injury / therapy
  • Animals
  • Chemokine CXCL2 / genetics
  • Chemokine CXCL2 / immunology
  • Disease Models, Animal
  • Female
  • HMGB1 Protein / genetics
  • HMGB1 Protein / immunology
  • Histones / genetics
  • Histones / immunology
  • Humans
  • Lipopolysaccharides / toxicity
  • Lung / immunology
  • Lung / pathology
  • Macrophages, Peritoneal / immunology
  • Macrophages, Peritoneal / pathology
  • Male
  • Mice
  • Mice, Knockout
  • Neutrophil Activation*
  • Neutrophils / immunology*
  • Neutrophils / pathology
  • Resistin / genetics
  • Resistin / immunology*
  • Severity of Illness Index
  • Toll-Like Receptor 4 / genetics
  • Toll-Like Receptor 4 / immunology
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / immunology

Substances

  • Chemokine CXCL2
  • Cxcl2 protein, mouse
  • HMGB1 Protein
  • HMGB1 protein, human
  • HMGB1 protein, mouse
  • Histones
  • Lipopolysaccharides
  • RETN protein, human
  • Resistin
  • Retn protein, mouse
  • TLR4 protein, human
  • Tlr4 protein, mouse
  • Toll-Like Receptor 4
  • Tumor Necrosis Factor-alpha
  • AMP-Activated Protein Kinases