Inhibition of RNA Helicase Activity Prevents Coxsackievirus B3-Induced Myocarditis in Human iPS Cardiomyocytes

Int J Mol Sci. 2020 Apr 25;21(9):3041. doi: 10.3390/ijms21093041.

Abstract

Aims: Coxsackievirus B3 (CVB3) is known to be an important cause of myocarditis and dilated cardiomyopathy. Enterovirus-2C (E2C) is a viral RNA helicase. It inhibits host protein synthesis. Based on these facts, we hypothesize that the inhibition of 2C may suppress virus replication and prevent enterovirus-mediated cardiomyopathy.

Methods and results: We generated a chemically modified enterovirus-2C inhibitor (E2CI). From the in vitro assay, E2CI was showed strong antiviral effects. For in vivo testing, mice were treated with E2CI intraperitoneally injected daily for three consecutive days at a dose of 8mg/kg per day, after CVB3 post-infection (p.i) (CVB3 + E2CI, n = 33). For the infected controls (CVB3 only, n = 35), mice were injected with PBS (phosphate buffered saline) in a DBA/2 strain to establish chronic myocarditis. The four-week survival rate of E2CI-treated mice was significantly higher than that of controls (92% vs. 71%; p < 0.05). Virus titers and myocardial damage were significantly reduced in the E2CI treated group. In addition, echocardiography indicated that E2CI administration dramatically maintained mouse heart function compared to control at day 28 p.i chronic stage (LVIDD, 3.1 ± 0.08 vs. 3.9 ± 0.09, p < 0.01; LVDS, 2.0 ± 0.07 vs. 2.5 ± 0.07, p < 0.001; FS, 34.8 ± 1.6% vs. 28.5 ± 1.5%; EF, 67. 9 ± 2.9% vs. 54.7 ± 4.7%, p < 0.05; CVB3 + E2CI, n = 6 vs. CVB3, n = 4). Moreover, E2CI is effectively worked in human iPS (induced pluripotent stem cell) derived cardiomyocytes.

Conclusion: Enterovirus-2C inhibitor (E2CI) was significantly reduced viral replication, chronic myocardium damage, and CVB3-induced mortality in DBA/2 mice. These results suggested that E2CI is a novel therapeutic agent for the treatment of enterovirus-mediated diseases.

Keywords: cardiomyopathy; coxsackievirus B3; enterovirus; helicase; iPSC; myocarditis.

MeSH terms

  • Animals
  • Antiviral Agents / chemical synthesis
  • Antiviral Agents / pharmacology*
  • Antiviral Agents / therapeutic use
  • Cardiomyopathy, Dilated / etiology
  • Cardiomyopathy, Dilated / prevention & control
  • Chronic Disease
  • Coxsackievirus Infections / complications
  • Coxsackievirus Infections / drug therapy*
  • Enterovirus B, Human / drug effects
  • Enterovirus B, Human / enzymology*
  • Enterovirus B, Human / physiology
  • HeLa Cells
  • Humans
  • Induced Pluripotent Stem Cells / drug effects*
  • Induced Pluripotent Stem Cells / virology
  • Luciferases, Renilla / analysis
  • Male
  • Mice
  • Mice, Inbred DBA
  • Myocarditis / etiology
  • Myocarditis / prevention & control*
  • Myocarditis / virology
  • Myocytes, Cardiac / drug effects*
  • Myocytes, Cardiac / pathology
  • Myocytes, Cardiac / virology
  • Oxadiazoles / pharmacology
  • Oxadiazoles / therapeutic use
  • Oxazoles / pharmacology
  • Oxazoles / therapeutic use
  • RNA Helicases / antagonists & inhibitors*
  • Recombinant Fusion Proteins / metabolism
  • Ventricular Dysfunction, Left / etiology
  • Ventricular Dysfunction, Left / prevention & control
  • Viral Proteins / antagonists & inhibitors*
  • Virus Replication / drug effects

Substances

  • Antiviral Agents
  • Oxadiazoles
  • Oxazoles
  • Recombinant Fusion Proteins
  • Viral Proteins
  • pleconaril
  • Luciferases, Renilla
  • RNA Helicases