Isoflurane selectively inhibits distal mitochondrial complex I in Caenorhabditis elegans

Anesth Analg. 2011 Jun;112(6):1321-9. doi: 10.1213/ANE.0b013e3182121d37. Epub 2011 Apr 5.

Abstract

Background: Complex I of the electron transport chain (ETC) is a possible target of volatile anesthetics (VAs). Complex I enzymatic activities are inhibited by VAs, and dysfunction of complex I can lead to hypersensitivity to VAs in worms and in people. Mutant analysis in Caenorhabditis (C.) elegans suggests that VAs may specifically interfere with complex I function at the binding site for its substrate ubiquinone. We hypothesized that isoflurane inhibits electron transport by competing with ubiquinone for binding to complex I.

Methods: Wildtype and mutant C. elegans were used to study the effects of isoflurane on isolated mitochondria. Enzymatic activities of the ETC were assayed and dose-response curves determined using established techniques. Two-dimensional native gels of mitochondrial proteins were performed after exposure of mitochondria to isoflurane.

Results: Complex I is the most sensitive component of the ETC to isoflurane inhibition; however, the proximal portion of complex I (the flavoprotein) is relatively insensitive to isoflurane. Isoflurane and quinone do not compete for a common binding site on complex I. The absolute rate of complex I enzymatic activity in vitro does not predict immobilization of the animal by isoflurane. Isoflurane had no measurable effect on stability of mitochondrial supercomplexes. Reduction of ubiquinone by complex I displayed positive cooperative kinetics not disrupted by isoflurane.

Conclusions: Isoflurane directly inhibits complex I at a site distal to the flavoprotein subcomplex. However, we have excluded our original hypothesis that isoflurane and ubiquinone compete for a common hydrophobic binding site on complex I. In addition, immobilization of the nematode by isoflurane is not due to limiting absolute amounts of complex I electron transport as measured in isolated mitochondria.

Publication types

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

MeSH terms

  • Anesthetics, Inhalation / pharmacology*
  • Animals
  • Binding Sites
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins / metabolism
  • Cytochromes c / metabolism
  • Electron Transport
  • Electron Transport Complex I / metabolism*
  • Electrophoresis, Gel, Two-Dimensional / methods
  • Electrophoresis, Polyacrylamide Gel
  • Horses
  • Hydrophobic and Hydrophilic Interactions
  • Isoflurane / chemistry
  • Isoflurane / pharmacology*
  • Kinetics
  • Mitochondria / metabolism
  • Mutation
  • NADH Dehydrogenase / metabolism
  • Solubility
  • Ubiquinone / chemistry
  • Water / chemistry

Substances

  • Anesthetics, Inhalation
  • Caenorhabditis elegans Proteins
  • Water
  • Ubiquinone
  • Cytochromes c
  • Isoflurane
  • NADH Dehydrogenase
  • Electron Transport Complex I
  • GAS-1 protein, C elegans