Chemotherapy-induced thrombin generation via procoagulant endothelial microparticles is independent of tissue factor activity

J Thromb Haemost. 2007 Dec;5(12):2445-52. doi: 10.1111/j.1538-7836.2007.02788.x. Epub 2007 Oct 8.

Abstract

Background: Cisplatin-based chemotherapy predisposes cancer patients to thromboembolic events.

Objectives: To investigate whether endothelial damage, via formation of procoagulant endothelial microparticles (EMPs), contributes to cisplatin-related hypercoagulability.

Methods: Cell viability and caspase-3/7 activities were assessed in two endothelial cell (EC) lines [human umbilical vein ECs (HUVECs) and human pulmonary microvascular ECs (HMVEC-Ls)] after exposure to cisplatin (1, 2.5, 5, 10 and 20 microm) for up to 120 h. Counts and procoagulant activity of EMPs were measured by flow cytometry and a thrombin generation assay, respectively. Tissue factor (TF) antigen and TF-dependent procoagulant activity of EMP were determined by enzyme-linked immunosorbent assay and a novel functional assay.

Results: By inducing apoptosis, cisplatin dose- and time-dependently decreased the viability of confluent HUVECs and HMVEC-Ls. Progression of EC death was accompanied by an increased release of EMPs (relative increase at 20 microm cisplatin for 48 h vs. control: HUVECs 6.5-fold, P < 0.001; HMVEC-Ls 18.4-fold, P < 0.001). EMPs were highly procoagulant (relative increase at 20 microm cisplatin for 48 h vs. control: HUVECs 2.5-fold, P < 0.001; HMVEC-Ls 5.9-fold, P < 0.001). EMP-driven thrombin generation, however, was not dependent on TF: TF expression and TF procoagulant activity levels on microparticles were only marginal and EMP-associated thrombin generation remained unchanged when the extrinsic pathway was blocked by omission of factor VIIa and/or incubation with an anti-human TF antibody. In contrast, blocking of phospholipids by annexin V markedly diminished EMP-associated procoagulant activity.

Conclusions: In vitro, cisplatin induced the release of EMPs that showed TF-independent procoagulant activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antineoplastic Agents / toxicity*
  • Apoptosis / drug effects
  • Blood Coagulation / drug effects*
  • Caspase 3 / metabolism
  • Caspase 7 / metabolism
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Cells, Cultured
  • Cisplatin / toxicity*
  • Dose-Response Relationship, Drug
  • Endothelial Cells / drug effects*
  • Endothelial Cells / enzymology
  • Endothelial Cells / metabolism
  • Factor VIIa / metabolism
  • Humans
  • Phospholipids / metabolism
  • Thrombin / metabolism*
  • Thromboplastin / metabolism*
  • Time Factors
  • Transport Vesicles / drug effects*
  • Transport Vesicles / metabolism

Substances

  • Antineoplastic Agents
  • Phospholipids
  • Thromboplastin
  • Factor VIIa
  • Thrombin
  • CASP7 protein, human
  • Caspase 3
  • Caspase 7
  • Cisplatin