The Danger Signal Extracellular ATP Is Involved in the Immunomediated Damage of α-Sarcoglycan-Deficient Muscular Dystrophy

Am J Pathol. 2019 Feb;189(2):354-369. doi: 10.1016/j.ajpath.2018.10.008. Epub 2018 Nov 16.

Abstract

In muscular dystrophies, muscle membrane fragility results in a tissue-specific increase of danger-associated molecular pattern molecules (DAMPs) and infiltration of inflammatory cells. The DAMP extracellular ATP (eATP) released by dying myofibers steadily activates muscle and immune purinergic receptors exerting dual negative effects: a direct damage linked to altered intracellular calcium homeostasis in muscle cells and an indirect toxicity through the triggering of the immune response and inhibition of regulatory T cells. Accordingly, pharmacologic and genetic inhibition of eATP signaling improves the phenotype in models of chronic inflammatory diseases. In α-sarcoglycanopathy, eATP effects may be further amplified because α-sarcoglycan extracellular domain binds eATP and displays an ecto-ATPase activity, thus controlling eATP concentration at the cell surface and attenuating the magnitude and/or the duration of eATP-induced signals. Herein, we show that in vivo blockade of the eATP/P2X purinergic pathway by a broad-spectrum P2X receptor-antagonist delayed the progression of the dystrophic phenotype in α-sarcoglycan-null mice. eATP blockade dampened the muscular inflammatory response and enhanced the recruitment of forkhead box protein P3-positive immunosuppressive regulatory CD4+ T cells. The improvement of the inflammatory features was associated with increased strength, reduced necrosis, and limited expression of profibrotic factors, suggesting that pharmacologic purinergic antagonism, altering the innate and adaptive immune component in muscle infiltrates, might provide a therapeutic approach to slow disease progression in α-sarcoglycanopathy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / genetics
  • Adenosine Triphosphate / immunology*
  • Animals
  • Calcium / immunology
  • Chronic Disease
  • Inflammation / genetics
  • Inflammation / immunology
  • Inflammation / pathology
  • Mice
  • Mice, Knockout
  • Muscular Dystrophy, Animal* / genetics
  • Muscular Dystrophy, Animal* / immunology
  • Muscular Dystrophy, Animal* / pathology
  • Myofibrils* / immunology
  • Myofibrils* / pathology
  • Receptors, Purinergic P2X / genetics
  • Receptors, Purinergic P2X / immunology
  • Sarcoglycans / deficiency*
  • Sarcoglycans / immunology
  • T-Lymphocytes, Regulatory* / immunology
  • T-Lymphocytes, Regulatory* / pathology

Substances

  • Receptors, Purinergic P2X
  • Sarcoglycans
  • Adenosine Triphosphate
  • Calcium