Induction of pulmonary hypertensive changes by extracellular vesicles from monocrotaline-treated mice

Cardiovasc Res. 2013 Dec 1;100(3):354-62. doi: 10.1093/cvr/cvt184. Epub 2013 Jul 18.

Abstract

Aims: Circulating endothelium-derived extracellular vesicles (EV) levels are altered in pulmonary arterial hypertension (PAH) but whether they are biomarkers of cellular injury or participants in disease pathogenesis is unknown. Previously, we found that lung-derived EVs (LEVs) induce bone marrow-derived progenitor cells to express lung-specific mRNA and protein. In this study, we sought to determine whether LEV or plasma-derived EV (PEV) alter pulmonary vascular endothelial or marrow progenitor cell phenotype to induce pulmonary vascular remodelling.

Methods and results: LEV, PEV isolated from monocrotaline (MCT-EV)- or vehicle-treated mice (vehicle-EV) were injected into healthy mice. Right ventricular (RV) hypertrophy and pulmonary vascular remodelling were assessed by RV-to-body weight (RV/BW) and blood vessel wall thickness-to-diameter (WT/D) ratios. RV/BW, WT/D ratios were elevated in MCT- vs. vehicle-injected mice (1.99 ± 0.09 vs. 1.04 ± 0.09 mg/g; 0.159 ± 0.002 vs. 0.062 ± 0.009%). RV/BW, WT/D ratios were higher in mice injected with MCT-EV vs. mice injected with vehicle-EV (1.63 ± 0.09 vs. 1.08 ± 0.09 mg/g; 0.113 ± 0.02 vs. 0.056 ± 0.01%). Lineage-depleted bone marrow cells incubated with MCT-EV and marrow cells isolated from mice infused with MCT-EV had greater expression of endothelial progenitor cell mRNAs and mRNAs abnormally expressed in PAH than cells incubated with vehicle-EV or isolated from vehicle-EV infused mice. MCT-EV induced an apoptosis-resistant phenotype in murine pulmonary endothelial cells and lineage-depleted bone marrow cells incubated with MCT-EV induced pulmonary hypertension when injected into healthy mice.

Conclusions: EV from MCT-injured mice contribute to the development of MCT-induced pulmonary hypertension. This effect may be mediated directly by EV on the pulmonary vasculature or by differentiation of bone marrow cells to endothelial progenitor cells that induce pulmonary vascular remodelling.

Keywords: Bone marrow stem/progenitor cells; Endothelium; Microparticles; Monocrotaline; Pulmonary hypertension.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Apoptosis
  • Bone Marrow Cells / metabolism*
  • Bone Marrow Cells / pathology
  • Bone Marrow Transplantation
  • Cell Differentiation
  • Cell Lineage
  • Cells, Cultured
  • Disease Models, Animal
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • Familial Primary Pulmonary Hypertension
  • Hypertension, Pulmonary / blood
  • Hypertension, Pulmonary / chemically induced
  • Hypertension, Pulmonary / genetics
  • Hypertension, Pulmonary / metabolism*
  • Hypertension, Pulmonary / pathology
  • Hypertrophy, Right Ventricular / etiology
  • Hypertrophy, Right Ventricular / metabolism
  • Lung / blood supply*
  • Mice
  • Mice, Inbred C57BL
  • MicroRNAs / metabolism
  • Monocrotaline*
  • Phenotype
  • RNA, Messenger / metabolism
  • Stem Cells / metabolism*
  • Stem Cells / pathology
  • Time Factors
  • Transport Vesicles / metabolism*
  • Transport Vesicles / pathology

Substances

  • MicroRNAs
  • RNA, Messenger
  • Monocrotaline