The compound BTB06584 is an IF1 -dependent selective inhibitor of the mitochondrial F1 Fo-ATPase

Br J Pharmacol. 2014 Sep;171(18):4193-206. doi: 10.1111/bph.12638. Epub 2014 Jul 1.

Abstract

Background and purpose: Ischaemia compromises mitochondrial respiration. Consequently, the mitochondrial F1 Fo-ATPsynthase reverses and acts as a proton-pumping ATPase, so maintaining the mitochondrial membrane potential (ΔΨm ), while accelerating ATP depletion and cell death. Here we have looked for a molecule that can selectively inhibit this activity without affecting ATP synthesis, preserve ATP and delay ischaemic cell death.

Experimental approach: We developed a chemoinformatic screen based on the structure of BMS199264, which is reported to selectively inhibit F1 Fo-ATPase activity and which is cardioprotective. Results suggested the molecule BTB06584 (hereafter referred to as BTB). Fluorescence microscopy was used to study its effects on ΔΨm and on the rate of ATP consumption following inhibition of respiration in several cell types. The effect of BTB on oxygen (O2 ) consumption was explored and protective potential determined using ischaemia/reperfusion assays. We also investigated a potential mechanism of action through its interaction with inhibitor protein of F1 subunit (IF1 ), the endogenous inhibitor of the F1 Fo-ATPase.

Key results: BTB inhibited F1 Fo-ATPase activity with no effect on ΔΨm or O2 consumption. ATP consumption was decreased following inhibition of respiration, and ischaemic cell death was reduced. BTB efficiency was increased by IF1 overexpression and reduced by silencing the protein. In addition, BTB rescued defective haemoglobin synthesis in zebrafish pinotage (pnt) mutants in which expression of the Atpif1a gene is lost.

Conclusions and implications: BTB may represent a valuable tool to selectively inhibit mitochondrial F1 Fo-ATPase activity without compromising ATP synthesis and to limit ischaemia-induced injury caused by reversal of the mitochondrial F1 Fo-ATPsynthase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATPase Inhibitory Protein
  • Adenosine Triphosphate / metabolism
  • Animals
  • Cell Death / drug effects
  • Cell Line
  • Chlorobenzoates / pharmacology*
  • Embryo, Nonmammalian
  • Enzyme Inhibitors / pharmacology*
  • HeLa Cells
  • Hemoglobins / metabolism
  • Hemolysis / drug effects
  • Humans
  • Membrane Potential, Mitochondrial / drug effects
  • Mice
  • Mice, Inbred C57BL
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Neurons / drug effects
  • Oxygen Consumption
  • Proteins / metabolism*
  • Proton-Translocating ATPases / antagonists & inhibitors*
  • Reperfusion Injury / drug therapy
  • Reperfusion Injury / metabolism
  • Sulfones / pharmacology*
  • Zebrafish

Substances

  • 2-nitro-5-(phenylsulfonyl)phenyl 4-chlorobenzoate
  • Chlorobenzoates
  • Enzyme Inhibitors
  • Hemoglobins
  • Proteins
  • Sulfones
  • Adenosine Triphosphate
  • Proton-Translocating ATPases