Article

Endothelial cell-specific anticoagulation reduces inflammation in a mouse model of acute lung injury

Jian Lou1, Yue Hu1, Min-dan Wu1, Luan-qing Che1, Yin-fang Wu1, Yun Zhao1, Bao-ping Tian1, Zheng-qiang Bao1, Chen Zhu1, Yan-ping Wu1, Lu-lu He1, Chun-xue Bai2,3, Jian Zhou2,3, Song-min Ying1, Wen Li1, Zhi-hua Chen1, Da-xin Chen4, Anthony Dorling4, Hua-hao Shen1,5
1 Key Laboratory of Respiratory Disease of Zhejiang Province, Department of Respiratory and Critical Care Medicine, The Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou 310009, China
2 Department of Pulmonary Medicine, Zhongshan Hospital, Fudan University, Shanghai 200032, China
3 Shanghai Respiratory Research Institute, Shanghai 200032, China
4 MRC Centre for Transplantation, King’s College London, Guy’s Hospital, London, UK
5 State Key Lab for Respiratory Diseases, Guangzhou 510120, China
Correspondence to: Jian Lou: anthony.dorling@kcl.ac.uk, Anthony Dorling: anthony.dorling@kcl.ac.uk, Hua-hao Shen: huahaoshen@zju.edu.cn,
DOI: 10.1038/s41401-018-0175-7
Received: 13 May 2018
Accepted: 24 September 2018
Advance online: 16 November 2018

Abstract

Tissue factor (TF)-dependent coagulation contributes to lung inflammation and the pathogenesis of acute lung injury (ALI). In this study, we explored the roles of targeted endothelial anticoagulation in ALI using two strains of transgenic mice expressing either a membrane-tethered human tissue factor pathway inhibitor (hTFPI) or hirudin fusion protein on CD31+ cells, including vascular endothelial cells (ECs). ALI was induced by intratracheal injection of LPS, and after 24 h the expression of TF and protease-activated receptors (PARs) on EC in lungs were assessed, alongside the extent of inflammation and injury. The expression of TF and PARs on the EC in lungs was upregulated after ALI. In the two strains of transgenic mice, expression of either of hTFPI or hirudin by EC was associated with significant reduction of inflammation, as assessed by the extent of leukocyte infiltration or the levels of proinflammatory cytokines, and promoted survival after LPS-induced ALI. The beneficial outcomes were associated with inhibition of the expression of chemokine CCL2 in lung tissues. The protection observed in the CD31-TFPI-transgenic strain was abolished by injection of an anti-hTFPI antibody, but not by prior engraftment of the transgenic strains with WT bone marrow, confirming that the changes observed were a specific transgenic expression of anticoagulants by EC. These results demonstrate that the inflammation in ALI is TF and thrombin dependent, and that expression of anticoagulants by EC significantly inhibits the development of ALI via repression of leukocyte infiltration, most likely via inhibition of chemokine gradients. These data enhance our understanding of the pathology of ALI and suggest a novel therapeutic strategy for treatment.
Keywords: acute lung injury; lipopolysaccharide; endothelial cells; anticoagulants; human tissue factor pathway inhibitor (hTFPI); hirudin; CCL2; inflammation

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