Nanoparticle-Mediated Delivery of Mitochondrial Division Inhibitor 1 to the Myocardium Protects the Heart From Ischemia-Reperfusion Injury Through Inhibition of Mitochondria Outer Membrane Permeabilization: A New Therapeutic Modality for Acute Myocardial Infarction

J Am Heart Assoc. 2016 Jul 22;5(7):e003872. doi: 10.1161/JAHA.116.003872.

Abstract

Background: Mitochondria-mediated cell death plays a critical role in myocardial ischemia-reperfusion (IR) injury. We hypothesized that nanoparticle-mediated drug delivery of mitochondrial division inhibitor 1 (Mdivi1) protects hearts from IR injury through inhibition of mitochondria outer membrane permeabilization (MOMP), which causes mitochondrial-mediated cell death.

Methods and results: We formulated poly (lactic-co-glycolic acid) nanoparticles containing Mdivi1 (Mdivi1-NP). We recently demonstrated that these nanoparticles could be successfully delivered to the cytosol and mitochondria of cardiomyocytes under H2O2-induced oxidative stress that mimicked IR injury. Pretreatment with Mdivi1-NP ameliorated H2O2-induced cell death in rat neonatal cardiomyocytes more potently than Mdivi1 alone, as indicated by a lower estimated half-maximal effective concentration and greater maximal effect on cell survival. Mdivi1-NP treatment of Langendorff-perfused mouse hearts through the coronary arteries at the time of reperfusion reduced infarct size after IR injury more effectively than Mdivi1 alone. Mdivi1-NP treatment also inhibited Drp1-mediated Bax translocation to the mitochondria and subsequent cytochrome c leakage into the cytosol, namely, MOMP, in mouse IR hearts. MOMP inhibition was also observed in cyclophilin D knockout (CypD-KO) mice, which lack the mitochondrial permeability transition pore (MPTP) opening. Intravenous Mdivi1-NP treatment in vivo at the time of reperfusion reduced IR injury in wild-type and CypD-KO mice, but not Bax-KO mice.

Conclusions: Mdivi1-NP treatment reduced IR injury through inhibition of MOMP, even in the absence of a CypD/MPTP opening. Thus, nanoparticle-mediated drug delivery of Mdivi1 may be a novel treatment strategy for IR injury.

Keywords: drug delivery system; ischemia‐reperfusion injury; mitochondria; myocardial infarction; nanoparticle.

MeSH terms

  • Animals
  • Biocompatible Materials / therapeutic use
  • Cell Survival / drug effects
  • Cytochromes c / drug effects
  • Cytochromes c / metabolism
  • Drug Carriers
  • Drug Delivery Systems
  • Dynamins / metabolism
  • Heart / drug effects*
  • Hydrogen Peroxide / pharmacology*
  • Isolated Heart Preparation
  • Lactic Acid / therapeutic use
  • Mice
  • Mitochondrial Membranes / drug effects*
  • Mitochondrial Membranes / metabolism
  • Myocardial Infarction*
  • Myocardial Reperfusion Injury / prevention & control*
  • Myocytes, Cardiac / drug effects*
  • Myocytes, Cardiac / metabolism
  • Nanoparticles / therapeutic use*
  • Oxidants / pharmacology*
  • Permeability / drug effects*
  • Polyglycolic Acid / therapeutic use
  • Polylactic Acid-Polyglycolic Acid Copolymer
  • Protein Transport / drug effects
  • Quinazolinones / administration & dosage
  • Quinazolinones / pharmacology*
  • Rats
  • bcl-2-Associated X Protein / drug effects
  • bcl-2-Associated X Protein / metabolism

Substances

  • 3-(2,4-dichloro-5-methoxyphenyl)-2-sulfanyl-4(3H)-quinazolinone
  • Bax protein, mouse
  • Biocompatible Materials
  • Drug Carriers
  • Oxidants
  • Quinazolinones
  • bcl-2-Associated X Protein
  • Polylactic Acid-Polyglycolic Acid Copolymer
  • Polyglycolic Acid
  • Lactic Acid
  • Cytochromes c
  • Hydrogen Peroxide
  • Dnm1l protein, mouse
  • Dynamins