Neutrophil extracellular trap fragments stimulate innate immune responses that prevent lung transplant tolerance

Am J Transplant. 2019 Apr;19(4):1011-1023. doi: 10.1111/ajt.15163. Epub 2018 Dec 13.

Abstract

Neutrophil extracellular traps (NETs) have been shown to worsen acute pulmonary injury including after lung transplantation. The breakdown of NETs by DNAse-1 can help restore lung function, but whether there is an impact on allograft tolerance remains less clear. Using intravital 2-photon microscopy, we analyzed the effects of DNAse-1 on NETs in mouse orthotopic lung allografts damaged by ischemia-reperfusion injury. Although DNAse-1 treatment rapidly degrades intragraft NETs, the consequential release of NET fragments induces prolonged interactions between infiltrating CD4+ T cells and donor-derived antigen presenting cells. DNAse-1 generated NET fragments also promote human alveolar macrophage inflammatory cytokine production and prime dendritic cells for alloantigen-specific CD4+ T cell proliferation through activating toll-like receptor (TLR) - Myeloid Differentiation Primary Response 88 (MyD88) signaling pathways. Furthermore, and in contrast to allograft recipients with a deficiency in NET generation due to a neutrophil-specific ablation of Protein Arginine Deiminase 4 (PAD4), DNAse-1 administration to wild-type recipients promotes the recognition of allo- and self-antigens and prevents immunosuppression-mediated lung allograft acceptance through a MyD88-dependent pathway. Taken together, these data show that the rapid catalytic release of NET fragments promotes innate immune responses that prevent lung transplant tolerance.

Keywords: animal models: murine; basic (laboratory) research/science; cellular biology; immunobiology; innate immunity; lung transplantation/pulmonology; tolerance: mechanisms; translational research/science.

Publication types

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

MeSH terms

  • Animals
  • Cells, Cultured
  • Dendritic Cells / immunology
  • Deoxyribonucleases / metabolism
  • Enzyme-Linked Immunosorbent Assay
  • Extracellular Traps / immunology*
  • Extracellular Traps / metabolism
  • Humans
  • Immunity, Innate / immunology*
  • Inflammation Mediators / metabolism
  • Lung Transplantation*
  • Macrophages, Alveolar / cytology
  • Macrophages, Alveolar / immunology
  • Macrophages, Alveolar / metabolism
  • Mice
  • Mice, Inbred BALB C
  • Reperfusion Injury
  • Transplantation Tolerance*

Substances

  • Inflammation Mediators
  • Deoxyribonucleases