Thrombospondin-1 triggers macrophage IL-10 production and promotes resolution of experimental lung injury

Mucosal Immunol. 2014 Mar;7(2):440-8. doi: 10.1038/mi.2013.63. Epub 2013 Sep 18.

Abstract

Mononuclear phagocyte recognition of apoptotic cells triggering suppressive cytokine signaling is a key event in inflammation resolution from injury. Mice deficient in thrombospondin (TSP)-1 (thbs1⁻/⁻), an extracellular matrix glycoprotein that bridges cell-cell interactions, are prone to lipopolysaccharide-induced lung injury and show defective macrophage interleukin (IL)-10 production during the resolution phase of inflammation. Reconstitution of IL-10 rescues thbs1⁻/⁻ mice from persistent neutrophilic lung inflammation and injury and thbs1⁻/⁻ alveolar macrophages show defective IL-10 production following intratracheal instillation of apoptotic neutrophils despite intact efferocytosis. Following co-culture with apoptotic neutrophils, thbs1⁻/⁻ macrophages show a selective defect in IL-10 production, whereas prostaglandin E2 and transforming growth factor beta 1 responses remain intact. Full macrophage IL-10 responses require the engagement of TSP-1 structural repeat 2 domain and the macrophage scavenger receptor CD36 LIMP-II Emp sequence homology (CLESH) domain in vitro. Although TSP-1 is not essential for macrophage engulfment of apoptotic neutrophils in vivo, TSP-1 aids in the curtailment of inflammatory responses during the resolution phase of injury in the lungs by providing a means by which apoptotic cells are recognized and trigger optimal IL-10 production by macrophages.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / immunology
  • CD36 Antigens / genetics
  • CD36 Antigens / metabolism
  • Dinoprostone / deficiency
  • Disease Models, Animal
  • Interleukin-10 / biosynthesis*
  • Lipopolysaccharides / adverse effects
  • Lung Injury / chemically induced
  • Lung Injury / genetics
  • Lung Injury / immunology*
  • Lung Injury / metabolism*
  • Lung Injury / pathology
  • Macrophages / immunology*
  • Macrophages / metabolism*
  • Mice
  • Mice, Knockout
  • Neutrophils / immunology
  • Neutrophils / metabolism
  • Pneumonia / genetics
  • Pneumonia / immunology
  • Pneumonia / metabolism
  • Pneumonia / pathology
  • Protein Interaction Domains and Motifs / genetics
  • Signal Transduction
  • Thrombospondin 1 / chemistry
  • Thrombospondin 1 / genetics
  • Thrombospondin 1 / metabolism*
  • Transforming Growth Factor beta1 / metabolism

Substances

  • CD36 Antigens
  • Lipopolysaccharides
  • Thrombospondin 1
  • Transforming Growth Factor beta1
  • Interleukin-10
  • Dinoprostone