Yes-associated protein (YAP) signaling regulates lipopolysaccharide-induced tissue factor expression in human endothelial cells

Surgery. 2016 May;159(5):1436-48. doi: 10.1016/j.surg.2015.12.008. Epub 2016 Jan 12.

Abstract

Background: Sepsis-induced acute lung injury (ALI) is characterized by fibrin deposition, which indicates the local activation of coagulation. Tissue factor (TF), expressed in the pulmonary microvasculature, acts as a critical initiator of blood coagulation and ALI in sepsis. The molecular mechanism of lipopolysaccharide (LPS)-induced TF expression in endothelial cells (ECs), however, has not been determined. In this study, we implicate the Rho-associated protein kinase (ROCK)/Yes associated protein (YAP)/early growth response (Egr-1) signaling pathway in LPS-induced TF expression in vitro and in sepsis-induced ALI in vivo.

Methods: Human umbilical vein ECs incubated with LPS were pretreated with or without the ROCK inhibitor Y-27632, a YAP small, interfering RNA (siRNA) and an Egr-1 siRNA. ROCK, YAP and Egr-1 signaling-induced protein expression was investigated by Western blot. The LPS-induced activation of YAP was analyzed by an immunofluorescent assay. Furthermore, we intratracheally injected YAP siRNA to assess septic ALI in mice by hematoxylin and eosin staining.

Results: LPS rapidly induced ROCK activation and increased TF expression in ECs. LPS caused YAP shuttling into the nuclei of ECs and combined with Egr-1 via the activation of ROCK. Furthermore, the LPS-mediated TF expression increase was prevented by ROCK inactivation, YAP knockdown and Egr-1 depletion, suggesting that LPS-induced TF expression is closely associated with the ROCK/YAP/Egr-1 signaling pathway in ECs. Finally, an intratracheal injection of YAP siRNA relieved lung injury in septic mice.

Conclusion: This study not only suggests that ROCK/YAP/Egr-1 signaling regulates TF expression after stimulation with LPS in ECs, but it also indicates that LPS-induced activation of YAP signaling plays an important role in septic ALI in mice. Our findings provide a new insight into the pathogenic mechanism of TF expression, which is closely linked to septic ALI, and YAP signaling is considered to be a novel target for therapeutic intervention under septic conditions.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Lung Injury / etiology
  • Acute Lung Injury / metabolism*
  • Adaptor Proteins, Signal Transducing / antagonists & inhibitors
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Animals
  • Biomarkers / metabolism
  • Blotting, Western
  • Cell Cycle Proteins
  • Early Growth Response Protein 1 / metabolism*
  • Human Umbilical Vein Endothelial Cells / metabolism*
  • Humans
  • Lipopolysaccharides
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Phosphoproteins / antagonists & inhibitors
  • Phosphoproteins / metabolism*
  • Sepsis / complications*
  • Signal Transduction
  • Thromboplastin / metabolism*
  • Transcription Factors
  • YAP-Signaling Proteins
  • rho-Associated Kinases / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Biomarkers
  • Cell Cycle Proteins
  • EGR1 protein, human
  • Early Growth Response Protein 1
  • Lipopolysaccharides
  • Phosphoproteins
  • Transcription Factors
  • YAP-Signaling Proteins
  • YAP1 protein, human
  • Yap1 protein, mouse
  • Thromboplastin
  • rho-Associated Kinases