Heterogeneous bioenergetic behaviour of subsarcolemmal and intermyofibrillar mitochondria in fed and fasted rats

Abstract.

This study was designed to examine energetic behaviour of skeletal muscle subsarcolemmal and intermyofibrillar mitochondrial populations. The data show that subsarcolemmal mitochondria exhibited a lower degree of coupling and efficiency than intermyofibrillar ones, and can therefore be considered less efficient at producing ATP. In addition, subsarcolemmal mitochondria showed an increased sensitivity to palmitate-induced uncoupling, in line with high adenine nucleotide translocator content and decreased oxidative damage. We then determined the effect of 24 h fasting on energetic characteristics of skeletal muscle mitochondrial populations. We found that fasting enhanced proton leak and decreased the degree of coupling and efficiency, both in the absence and in the presence of palmitate only in subsarcolemmal mitochondria. Moreover, this mitochondrial population showed lower oxidative damage, probably due to a counter-regulatory mechanism mediated by uncoupling protein 3. Subsarcolemmal and intermyofibrillar mitochondria appear to exhibit different energetic characteristics and can be differently affected by physiological stimuli.

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Correspondence to G. Liverini.

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Received 28 September 2005; received after revision 9 November 2005; accepted 28 November 2005

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Mollica, M.P., Lionetti, L., Crescenzo, R. et al. Heterogeneous bioenergetic behaviour of subsarcolemmal and intermyofibrillar mitochondria in fed and fasted rats. Cell. Mol. Life Sci. 63, 358–366 (2006). https://doi.org/10.1007/s00018-005-5443-2

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Key words.

  • Subsarcolemmal mitochondria
  • intermyofibrillar mitochondria
  • mitochondrial efficiency
  • palmitate-induced proton leak
  • oxidative damage
  • fed-fasting transition