Angiogenic impairment of the vascular endothelium: a novel mechanism and potential therapeutic target in muscular dystrophy

Arterioscler Thromb Vasc Biol. 2013 Dec;33(12):2867-76. doi: 10.1161/ATVBAHA.112.301172. Epub 2013 Sep 26.

Abstract

Objective: Dystrophin, the missing or defective protein in Duchenne muscular dystrophy, is expressed not only in muscle cells but also in vascular endothelial cells (ECs). In this study, we assessed the effects of dystrophin deficiency on the angiogenic capacities of ECs.

Approach and results: We isolated vascular ECs from mdx mice, the murine equivalent of Duchenne muscular dystrophy in humans, and wild-type controls, and we found that mdx-derived ECs have impaired angiogenic properties, in terms of migration, proliferation, and tube formation. They also undergo increased apoptosis in vitro compared with wild-type cells and have increased senescence-associated β-galactosidase activity. Mdx-derived ECs also display reduced ability to support myoblast proliferation when cocultured with satellite cell-derived primary myoblasts. These endothelial defects are mirrored by systemic impairment of angiogenesis in vivo, both on induction of ischemia, stimulation with growth factors in the corneal model and matrigel plug assays, and tumor growth. We also found that dystrophin forms a complex with endothelial NO synthase and caveolin-1 in ECs, and that NO production and cGMP formation are compromised in ECs isolated from mdx mice. Interestingly, treatment with aspirin enhances production of both cGMP and NO in dystrophic ECs, whereas low-dose aspirin improves the dystrophic phenotype of mdx mice in vivo, in terms of resistance to physical exercise, muscle fiber permeability, and capillary density.

Conclusions: These findings demonstrate that impaired angiogenesis is a novel player and potential therapeutic target in Duchenne muscular dystrophy.

Keywords: angiogenesis inhibitors; endothelium, vascular; muscle diseases, inflammatory; nitric oxide synthase type III.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis
  • Aspirin / pharmacology
  • Carcinoma, Lewis Lung / blood supply
  • Carcinoma, Lewis Lung / metabolism
  • Carcinoma, Lewis Lung / pathology
  • Caveolin 1 / metabolism
  • Cell Movement
  • Cell Proliferation
  • Cells, Cultured
  • Cellular Senescence
  • Coculture Techniques
  • Corneal Neovascularization / metabolism
  • Corneal Neovascularization / pathology
  • Corneal Neovascularization / physiopathology
  • Cyclic GMP / metabolism
  • Disease Models, Animal
  • Dystrophin / genetics
  • Dystrophin / metabolism*
  • Endothelial Cells / drug effects
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / metabolism*
  • Endothelium, Vascular / pathology
  • Endothelium, Vascular / physiopathology
  • Ischemia / metabolism
  • Ischemia / pathology
  • Ischemia / physiopathology
  • Mice
  • Mice, Inbred mdx
  • Muscular Dystrophy, Duchenne / drug therapy
  • Muscular Dystrophy, Duchenne / genetics
  • Muscular Dystrophy, Duchenne / metabolism*
  • Muscular Dystrophy, Duchenne / pathology
  • Muscular Dystrophy, Duchenne / physiopathology
  • Mutation
  • Myoblasts, Skeletal / metabolism
  • Myoblasts, Skeletal / pathology
  • Neovascularization, Pathologic
  • Neovascularization, Physiologic* / drug effects
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type III / metabolism
  • Time Factors

Substances

  • Cav1 protein, mouse
  • Caveolin 1
  • Dystrophin
  • Nitric Oxide
  • Nitric Oxide Synthase Type III
  • Nos3 protein, mouse
  • Cyclic GMP
  • Aspirin