Synergistic effects of EMPs and PMPs on pulmonary vascular leakage and lung injury after ischemia/reperfusion

Cell Commun Signal. 2020 Nov 23;18(1):184. doi: 10.1186/s12964-020-00672-0.

Abstract

Background: Vascular leakage is an important pathophysiological process of critical conditions such as shock and ischemia-reperfusion (I/R)-induced lung injury. Microparticles (MPs), including endothelial cell-derived microparticles (EMPs), platelet-derived microparticles (PMPs) and leukocyte-derived microparticles (LMPs), have been shown to participate in many diseases. Whether and which of these MPs take part in pulmonary vascular leakage and lung injury after I/R and whether these MPs have synergistic effect and the underlying mechanism are not known.

Methods: Using hemorrhage/transfusion (Hemo/Trans) and aorta abdominalis occlusion-induced I/R rat models, the role of EMPs, PMPs and LMPs and the mechanisms in pulmonary vascular leakage and lung injury were observed.

Results: The concentrations of EMPs, PMPs and LMPs were significantly increased after I/R. Intravenous administration of EMPs and PMPs but not LMPs induced pulmonary vascular leakage and lung injury. Furthermore, EMPs induced pulmonary sequestration of platelets and promoted more PMPs production, and played a synergistic effect on pulmonary vascular leakage. MiR-1, miR-155 and miR-542 in EMPs, and miR-126 and miR-29 in PMPs, were significantly increased after hypoxia/reoxygenation (H/R). Of which, inhibition of miR-155 in EMPs and miR-126 in PMPs alleviated the detrimental effects of EMPs and PMPs on vascular barrier function and lung injury. Overexpression of miR-155 in EMPs down-regulated the expression of tight junction related proteins such as ZO-1 and claudin-5, while overexpression of miR-126 up-regulated the expression of caveolin-1 (Cav-1), the trans-cellular transportation related protein such as caveolin-1 (Cav-1). Inhibiting EMPs and PMPs production with blebbistatin (BLE) and amitriptyline (AMI) alleviated I/R induced pulmonary vascular leakage and lung injury.

Conclusions: EMPs and PMPs contribute to the pulmonary vascular leakage and lung injury after I/R. EMPs mediate pulmonary sequestration of platelets, producing more PMPs to play synergistic effect. Mechanically, EMPs carrying miR-155 that down-regulates ZO-1 and claudin-5 and PMPs carrying miR-126 that up-regulates Cav-1, synergistically mediate pulmonary vascular leakage and lung injury after I/R. Video Abstract.

Keywords: Emps; Pmps; Pulmonary vascular permeability.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amitriptyline / pharmacology
  • Animals
  • Blood Platelets / drug effects
  • Blood Platelets / metabolism*
  • Capillary Permeability / drug effects
  • Caveolin 1 / metabolism
  • Cell-Derived Microparticles / drug effects
  • Cell-Derived Microparticles / metabolism*
  • Claudin-5 / metabolism
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Heterocyclic Compounds, 4 or More Rings / pharmacology
  • Leukocytes / drug effects
  • Leukocytes / metabolism
  • Lung / blood supply*
  • Lung / pathology
  • Lung Injury / etiology*
  • Lung Injury / metabolism*
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Rats, Sprague-Dawley
  • Reperfusion Injury / complications*
  • Zonula Occludens-1 Protein / metabolism

Substances

  • Caveolin 1
  • Claudin-5
  • Heterocyclic Compounds, 4 or More Rings
  • MicroRNAs
  • Zonula Occludens-1 Protein
  • Amitriptyline
  • blebbistatin