5-Hydroxydecanoate is metabolised in mitochondria and creates a rate-limiting bottleneck for beta-oxidation of fatty acids

J Physiol. 2005 Jan 15;562(Pt 2):307-18. doi: 10.1113/jphysiol.2004.073932. Epub 2004 Oct 28.

Abstract

5-Hydroxydecanoate (5-HD) blocks pharmacological and ischaemic preconditioning, and has been postulated to be a specific inhibitor of mitochondrial ATP-sensitive K(+) (K(ATP)) channels. However, recent work has shown that 5-HD is activated to 5-hydroxydecanoyl-CoA (5-HD-CoA), which is a substrate for the first step of beta-oxidation. We have now analysed the complete beta-oxidation of 5-HD-CoA using specially synthesised (and purified) substrates and enzymes, as well as isolated rat liver and heart mitochondria, and compared it with the metabolism of the physiological substrate decanoyl-CoA. At the second step of beta-oxidation, catalysed by enoyl-CoA hydratase, enzyme kinetics were similar using either decenoyl-CoA or 5-hydroxydecenoyl-CoA as substrate. The last two steps were investigated using l-3-hydroxyacyl-CoA dehydrogenase (HAD) coupled to 3-ketoacyl-CoA thiolase. V(max) for the metabolite of 5-HD (3,5-dihydroxydecanoyl-CoA) was fivefold slower than for the corresponding metabolite of decanoate (l-3-hydroxydecanoyl-CoA). The slower kinetics were not due to accumulation of d-3-hydroxyoctanoyl-CoA since this enantiomer did not inhibit HAD. Molecular modelling of HAD complexed with 3,5-dihydroxydecanoyl-CoA suggested that the 5-hydroxyl group could decrease HAD turnover rate by interacting with critical side chains. Consistent with the kinetic data, 5-hydroxydecanoyl-CoA alone acted as a weak substrate in isolated mitochondria, whereas addition of 100 mum 5-HD-CoA inhibited the metabolism of decanoyl-CoA or lauryl-carnitine. In conclusion, 5-HD is activated, transported into mitochondria and metabolised via beta-oxidation, albeit with rate-limiting kinetics at the penultimate step. This creates a bottleneck for beta-oxidation of fatty acids. The complex metabolic effects of 5-HD invalidate the use of 5-HD as a blocker of mitochondrial K(ATP) channels in studies of preconditioning.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Biotransformation
  • Coenzyme A / metabolism
  • Decanoic Acids / metabolism*
  • Decanoic Acids / pharmacokinetics
  • Esters / metabolism
  • Fatty Acids / metabolism*
  • Fatty Acids / pharmacokinetics
  • Hydroxy Acids / metabolism*
  • Hydroxy Acids / pharmacokinetics
  • In Vitro Techniques
  • Ischemic Preconditioning, Myocardial
  • Kinetics
  • Mitochondria / enzymology
  • Mitochondria / metabolism*
  • Mitochondria, Heart / enzymology
  • Mitochondria, Heart / metabolism
  • Mitochondria, Liver / enzymology
  • Mitochondria, Liver / metabolism
  • Models, Molecular
  • NAD / metabolism
  • Oxidation-Reduction
  • Rats

Substances

  • Decanoic Acids
  • Esters
  • Fatty Acids
  • Hydroxy Acids
  • NAD
  • 5-hydroxydecanoic acid
  • Coenzyme A