Complement activation on endothelium initiates antibody-mediated acute lung injury

J Clin Invest. 2020 Nov 2;130(11):5909-5923. doi: 10.1172/JCI138136.

Abstract

Antibodies targeting human leukocyte antigen (HLA)/major histocompatibility complex (MHC) proteins limit successful transplantation and transfusion, and their presence in blood products can cause lethal transfusion-related acute lung injury (TRALI). It is unclear which cell types are bound by these anti-leukocyte antibodies to initiate an immunologic cascade resulting in lung injury. We therefore conditionally removed MHC class I (MHC I) from likely cellular targets in antibody-mediated lung injury. Only the removal of endothelial MHC I reduced lung injury and mortality, related mechanistically to absent endothelial complement fixation and lung platelet retention. Restoration of endothelial MHC I rendered MHC I-deficient mice susceptible to lung injury. Neutrophil responses, including neutrophil extracellular trap (NET) release, were intact in endothelial MHC I-deficient mice, whereas complement depletion reduced both lung injury and NETs. Human pulmonary endothelial cells showed high HLA class I expression, and posttransfusion complement activation was increased in clinical TRALI. These results indicate that the critical source of antigen for anti-leukocyte antibodies is in fact the endothelium, which reframes our understanding of TRALI as a rapid-onset vasculitis. Inhibition of complement activation may have multiple beneficial effects of reducing endothelial injury, platelet retention, and NET release in conditions where antibodies trigger these pathogenic responses.

Keywords: Complement; Immunology; Neutrophils; Platelets; Pulmonology; Vasculitis.

Publication types

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

MeSH terms

  • Animals
  • Cell Line
  • Complement Activation / immunology*
  • Endothelium / immunology*
  • Endothelium / pathology
  • Extracellular Traps / immunology
  • Histocompatibility Antigens Class I / immunology
  • Isoantibodies / immunology*
  • Mice
  • Mice, Inbred BALB C
  • Neutrophils / immunology
  • Neutrophils / pathology
  • Transfusion-Related Acute Lung Injury / immunology*
  • Transfusion-Related Acute Lung Injury / pathology

Substances

  • Histocompatibility Antigens Class I
  • Isoantibodies