Diffusion of tricarboxylic acid cycle enzymes in the mitochondrial matrix in vivo. Evidence for restricted mobility of a multienzyme complex

J Biol Chem. 2002 Oct 25;277(43):40782-8. doi: 10.1074/jbc.M207456200. Epub 2002 Aug 26.

Abstract

It has been proposed that enzymes in many metabolic pathways, including the tricarboxylic acid cycle in the mitochondrial matrix, are physically associated to facilitate substrate channeling and overcome diffusive barriers. We have used fluorescence recovery after photobleaching to measure the diffusional mobilities of chimeras consisting of green fluorescent protein (GFP) fused to the C terminus of four tricarboxylic acid cycle enzymes: malate dehydrogenase, citrate synthase, isocitrate dehydrogenase, and succinyl-CoA synthetase. The GFP-enzyme chimeras were localized selectively in the mitochondrial matrix in transfected Chinese hamster ovary (CHO) and COS7 cells. Laser photobleaching using a 0.7-microm diameter spot demonstrated restricted diffusion of the GFP-enzyme chimeras. Interestingly, all four chimeras had similar diffusional characteristics, approximately 45% of each chimera was mobile and had a diffusion coefficient of 4 x 10(-8) cm(2)/s. In contrast, unconjugated GFP in the mitochondrial matrix (targeted using COX8 leader sequence) diffused freely (nearly 100% mobility) with a greater diffusion coefficient of 20 x 10(-8) cm(2)/s. The mobility of the GFP-enzyme chimeras was insensitive to substrate source, ATP depletion, or inhibition of the adenine nucleotide translocase. These results indicate similar mobility characteristics of unrelated tricarboxylic acid cycle enzymes having different sizes and physical properties, providing biophysical evidence for a diffusible multienzyme complex in the mitochondrial matrix.

Publication types

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

MeSH terms

  • Animals
  • Base Sequence
  • CHO Cells
  • COS Cells
  • Citrate (si)-Synthase / metabolism
  • Citric Acid Cycle*
  • Cricetinae
  • DNA Primers
  • Isocitrate Dehydrogenase / metabolism
  • Malate Dehydrogenase / metabolism
  • Mitochondria / enzymology*
  • Multienzyme Complexes / metabolism
  • Succinate-CoA Ligases / metabolism

Substances

  • DNA Primers
  • Multienzyme Complexes
  • Malate Dehydrogenase
  • Isocitrate Dehydrogenase
  • Citrate (si)-Synthase
  • Succinate-CoA Ligases