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Matters of the heart in bioenergetics: mitochondrial fusion into continuous reticulum is not needed for maximal respiratory activity

Journal of Bioenergetics and Biomembranes volume 45, pages 319–331 (2013)Cite this article

Abstract

Mitochondria are dynamic structures for which fusion and fission are well characterized for rapidly dividing cells in culture. Based on these data, it has recently been proposed that high respiratory activity is the result of fusion and formation of mitochondrial reticulum, while fission results in fragmented mitochondria with low respiratory activity. In this work we test the validity of this new hypothesis by analyzing our own experimental data obtained in studies of isolated heart mitochondria, permeabilized cells of cardiac phenotype with different mitochondrial arrangement and dynamics. Additionally, we reviewed published data including electron tomographic investigation of mitochondrial membrane-associated structures in heart cells. Oxygraphic studies show that maximal ADP-dependent respiration rates are equally high both in isolated heart mitochondria and in permeabilized cardiomyocytes. On the contrary, these rates are three times lower in NB HL-1 cells with fused mitochondrial reticulum. Confocal and electron tomographic studies show that there is no mitochondrial reticulum in cardiac cells, known to contain 5,000–10,000 individual, single mitochondria, which are regularly arranged at the level of sarcomeres and are at Z-lines separated from each other by membrane structures, including the T-tubular system in close connection to the sarcoplasmic reticulum. The new structural data in the literature show a principal role for the elaborated T-tubular system in organization of cell metabolism by supplying calcium, oxygen and substrates from the extracellular medium into local domains of the cardiac cells for calcium cycling within Calcium Release Units, associated with respiration and its regulation in Intracellular Energetic Units.

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Affiliations

  1. Laboratory of Bioenergetics, National Institute of Chemical Physics and Biophysics, Tallinn, Estonia

    Minna Varikmaa, Tuuli Kaambre & Valdur Saks

  2. INSERM U1055, Laboratory of Fundamental and Applied Bioenergetics, Joseph Fourier University, Grenoble, France

    Rita Guzun, Marcela Gonzalez-Granillo & Valdur Saks

  3. Life Science Imaging–In Vitro Platform, IAB CRI U823 Inserm/Joseph Fourier University, Grenoble, France

    Alexei Grichine & Yves Usson

  4. Experimental, Theoretical and Applied Cardio-Respiratory Physiology, Laboratory TIMC-IMAG, Joseph Fourier University, Grenoble, France

    François Boucher

  5. Laboratory of Bioenergetics, Joseph Fourier University, 2280, Rue de la Piscine, BP53X-38041 Grenoble Cedex 9, France

    Valdur Saks

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  1. Minna Varikmaa
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  2. Rita Guzun
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  3. Alexei Grichine
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  4. Marcela Gonzalez-Granillo
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  5. Yves Usson
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  6. François Boucher
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  7. Tuuli Kaambre
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Varikmaa, M., Guzun, R., Grichine, A. et al. Matters of the heart in bioenergetics: mitochondrial fusion into continuous reticulum is not needed for maximal respiratory activity. J Bioenerg Biomembr 45, 319–331 (2013). https://doi.org/10.1007/s10863-012-9494-4

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  • DOI: https://doi.org/10.1007/s10863-012-9494-4

Keywords

  • Cardiac cells
  • Respiration
  • Mitochondria
  • Fusion-fission
  • Calcium metabolism
  • Energy metabolism