Anti-human neutrophil antigen-3a induced transfusion-related acute lung injury in mice by direct disturbance of lung endothelial cells

Arterioscler Thromb Vasc Biol. 2013 Nov;33(11):2538-48. doi: 10.1161/ATVBAHA.113.301206. Epub 2013 Sep 5.

Abstract

Objective: Antibodies against human neutrophil antigen-3a (HNA-3a) located on choline transporter-like protein 2 induce severe transfusion-related acute lung injury (TRALI). This study aims to identify the mechanism implicated in anti-HNA-3a-mediated TRALI.

Approach and results: Our analysis shows that anti-HNA-3a recognizes 2 choline transporter-like protein 2 isoforms (P1 and P2) on human microvascular endothelial cells from lung blood vessels but reacts only with the P1 isoform on neutrophils. Direct treatment of HNA-3a-positive endothelial cells with anti-HNA-3a, but not with anti-HNA-3b, leads to reactive oxygen species production, increased albumin influx, and decreased endothelial resistance associated with the formation of actin stress filaments and loosening of junctional vascular endothelium-cadherin. In a novel in vivo mouse model, TRALI was documented by significant increase in lung water content, albumin concentration, and neutrophil numbers in the bronchoalveolar lavage on injection of human anti-HNA-3a in lipopolysaccharides-treated, as well as nontreated mice. Interestingly, although neutrophil depletion alleviated severity of lung injury, it failed to prevent TRALI in this model. Infusion of anti-HNA-3a F(ab')2 fragments caused moderate TRALI. Finally, mice lacking nicotinamide adenine dinucleotide phosphate oxidase (NOX2(y/-)) were protected from anti-HNA-3a-mediated TRALI.

Conclusions: These data demonstrate the initiation of endothelial barrier dysfunction in vitro and in vivo by direct binding of anti-HNA-3a on endothelial cells. It seems, however, that the presence of neutrophils aggravates barrier dysfunction. This novel mechanism of TRALI primarily mediated by endothelial cell dysfunction via choline transporter-like protein 2 may help to define new treatment strategies to decrease TRALI-related mortality.

Keywords: acute lung injury; endothelium; reactive oxygen species.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Acute Lung Injury / etiology
  • Acute Lung Injury / immunology*
  • Animals
  • Antibodies / immunology
  • Antibodies / pharmacology*
  • Bronchoalveolar Lavage Fluid / cytology
  • Bronchoalveolar Lavage Fluid / immunology
  • Capillary Permeability / immunology
  • Disease Models, Animal
  • Endothelium, Vascular / immunology*
  • Endothelium, Vascular / metabolism
  • Humans
  • Isoantigens / immunology*
  • Lipopolysaccharides / pharmacology
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / immunology
  • Membrane Transport Proteins / immunology
  • Membrane Transport Proteins / metabolism
  • Mice
  • Mice, Knockout
  • NADPH Oxidase 2
  • NADPH Oxidases / genetics
  • Neutrophils / immunology
  • Respiratory Mucosa / cytology
  • Respiratory Mucosa / immunology*
  • Transfusion Reaction*

Substances

  • Actins
  • Antibodies
  • HNA-3a antigen, human
  • Isoantigens
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Membrane Transport Proteins
  • SLC44A2 protein, human
  • SLC44A2 protein, mouse
  • Cybb protein, mouse
  • NADPH Oxidase 2
  • NADPH Oxidases