Vascular immunotargeting of glucose oxidase to the endothelial antigens induces distinct forms of oxidant acute lung injury: targeting to thrombomodulin, but not to PECAM-1, causes pulmonary thrombosis and neutrophil transmigration

Am J Pathol. 2002 Mar;160(3):1155-69. doi: 10.1016/S0002-9440(10)64935-8.

Abstract

Oxidative endothelial stress, leukocyte transmigration, and pulmonary thrombosis are important pathological factors in acute lung injury/acute respiratory distress syndrome (ALI/ARDS). Vascular immunotargeting of the H(2)O(2)-generating enzyme glucose oxidase (GOX) to the pulmonary endothelium causes an acute oxidative lung injury in mice.(1) In the present study we compared the pulmonary thrombosis and leukocyte transmigration caused by GOX targeting to the endothelial antigens platelet-endothelial cell adhesion molecule (PECAM) and thrombomodulin (TM). Both anti-PECAM and anti-TM delivered similar amounts of (125)I-GOX to the lungs and caused a dose-dependent, tissue-selective lung injury manifested within 2 to 4 hours by high lethality, vascular congestion, polymorphonuclear neutrophil (PMN) sequestration in the pulmonary vasculature, severe pulmonary edema, and tissue oxidation, yet at an equal dose, anti-TM/GOX inflicted more severe lung injury than anti-PECAM/GOX. Moreover, anti-TM/GOX-induced injury was accompanied by PMN transmigration in the alveolar space, whereas anti-PECAM/GOX-induced injury was accompanied by PMN degranulation within vascular lumen without PMN transmigration, likely because of PECAM blockage. Anti-TM/GOX caused markedly more severe pulmonary thrombosis than anti-PECAM/GOX, likely because of TM inhibition. These results indicate that blocking of specific endothelial antigens by GOX immunotargeting modulates important pathological features of the lung injury initiated by local generation of H(2)O(2) and that this approach provides specific and robust models of diverse variants of human ALI/ARDS in mice. In particular, anti-TM/GOX causes lung injury combining oxidative, prothrombotic, and inflammatory components characteristic of the complex pathological picture seen in human ALI/ARDS.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Disease Models, Animal
  • Endothelium, Vascular* / immunology
  • Endothelium, Vascular* / metabolism
  • Endothelium, Vascular* / pathology
  • Glucose Oxidase / immunology
  • Glucose Oxidase / toxicity*
  • Humans
  • Immunotoxins / immunology
  • Immunotoxins / toxicity*
  • Mice
  • Mice, Inbred BALB C
  • Oxidative Stress* / immunology
  • Platelet Endothelial Cell Adhesion Molecule-1 / immunology
  • Pulmonary Circulation* / immunology
  • Pulmonary Embolism* / etiology
  • Pulmonary Embolism* / immunology
  • Pulmonary Embolism* / metabolism
  • Thrombomodulin / immunology

Substances

  • Immunotoxins
  • Platelet Endothelial Cell Adhesion Molecule-1
  • Thrombomodulin
  • Glucose Oxidase