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. 1988 Aug 1;107(2):481–495. doi: 10.1083/jcb.107.2.481

Coupling membranes as energy-transmitting cables. I. Filamentous mitochondria in fibroblasts and mitochondrial clusters in cardiomyocytes

PMCID: PMC2115217  PMID: 3417757

Abstract

An hypothesis considering mitochondria as intracellular power- transmitting protonic cables was tested in human fibroblasts where mitochondria are thin and long and in rat cardiomyocytes where they show cluster organization. Mitochondria in the cell were specifically stained with fluorescent-penetrating cation ethylrhodamine, which electrophoretically accumulates in the mitochondrial matrix. A 40- micron-long mitochondrial filament of fibroblast was illuminated by a very narrow (less than or equal to 0.5 micron) laser beam to induce local damage of the mitochondrial membranes. Such a treatment was found to induce quenching of the ethylrhodamine fluorescence in the entire filament. According to the electron microscope examination, the laser- treated filament retained its continuity after the laser illumination. Other mitochondrial filaments (some of which were localized at a distance less than 10 micron from the laser-treated one) remained fluorescent. In a cell where mitochondrial filaments seemed to be united in a network, laser illumination of one filament resulted in fluorescence quenching in the whole network, whereas fluorescence of small mitochondria not connected with the network was unaffected. The illumination of cardiomyocyte was found to result in the fluorescence quenching not only in a laser-illuminated mitochondrion but also in a large cluster of organelles composed of many mitochondria. Electron microscopy showed that all the mitochondria in the cluster change from the orthodox to the condensed state. It was also found that mitochondria in the cluster are connected to one another with specific junctions. If a mitochondrion did not form junctions with a quenched cluster, its fluorescence was not decreased even when this mitochondrion was localized close to an illuminated one. The size of the mitochondrial cluster may be as long as 50 micron. The cluster is formed by branched chains of contacting mitochondria, which may be defined as Streptio mitochondriale. In the cardiomyocyte there are several mitochondrial clusters or, alternatively, the quenched cluster is a result of decomposition of a supercluster uniting all the mitochondria of the cell. Cluster organization of mitochondria could also be revealed when a single mitochondrion was punctured in situ with a microcapillary. The obtained data are in agreement with the idea that mitochondrial junctions are H+ permeable so that, within the cluster, delta psi may be transmitted from one mitochondrion to another. The above results are consistent with the assumption that mitochondrial filaments or networks represent a united electrical system.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Bakeeva L. E., Chentsov YuS, Skulachev V. P. Intermitochondrial contacts in myocardiocytes. J Mol Cell Cardiol. 1983 Jul;15(7):413–420. doi: 10.1016/0022-2828(83)90261-4. [DOI] [PubMed] [Google Scholar]
  2. Bakeeva L. E., Chentsov YuS, Skulachev V. P. Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle. Biochim Biophys Acta. 1978 Mar 13;501(3):349–369. doi: 10.1016/0005-2728(78)90104-4. [DOI] [PubMed] [Google Scholar]
  3. Chen L. B., Summerhayes I. C., Johnson L. V., Walsh M. L., Bernal S. D., Lampidis T. J. Probing mitochondria in living cells with rhodamine 123. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 1):141–155. doi: 10.1101/sqb.1982.046.01.018. [DOI] [PubMed] [Google Scholar]
  4. Drachev V. A., Zorov D. B. Mitokhondriia kak élektricheskii kabel'. Eksperimental'naia proverka gipotezy. Dokl Akad Nauk SSSR. 1986;287(5):1237–1238. [PubMed] [Google Scholar]
  5. Fischkoff S., Vanderkooi J. M. Oxygen diffusion in biological and artificial membranes determined by the fluorochrome pyrene. J Gen Physiol. 1975 May;65(5):663–676. doi: 10.1085/jgp.65.5.663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Johnson L. V., Walsh M. L., Chen L. B. Localization of mitochondria in living cells with rhodamine 123. Proc Natl Acad Sci U S A. 1980 Feb;77(2):990–994. doi: 10.1073/pnas.77.2.990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Jones D. P. Effect of mitochondrial clustering on O2 supply in hepatocytes. Am J Physiol. 1984 Jul;247(1 Pt 1):C83–C89. doi: 10.1152/ajpcell.1984.247.1.C83. [DOI] [PubMed] [Google Scholar]
  8. Keith A. D., Snipes W. Viscosity of cellular protoplasm. Science. 1974 Feb 15;183(4125):666–668. doi: 10.1126/science.183.4125.666. [DOI] [PubMed] [Google Scholar]
  9. Kennedy F. G., Jones D. P. Oxygen dependence of mitochondrial function in isolated rat cardiac myocytes. Am J Physiol. 1986 Mar;250(3 Pt 1):C374–C383. doi: 10.1152/ajpcell.1986.250.3.C374. [DOI] [PubMed] [Google Scholar]
  10. Kirkwood S. P., Munn E. A., Brooks G. A. Mitochondrial reticulum in limb skeletal muscle. Am J Physiol. 1986 Sep;251(3 Pt 1):C395–C402. doi: 10.1152/ajpcell.1986.251.3.C395. [DOI] [PubMed] [Google Scholar]
  11. Levin S. A., Potapova T. V., Skulachev V. P., Chailakhian L. M. Rasprostraniaiushchiesia izmeneniia élekltricheskogo potentsiala u nitchatykh tsianobakterii. Biofizika. 1982 Mar-Apr;27(2):280–284. [PubMed] [Google Scholar]
  12. Mitchell P. Chemiosmotic coupling in oxidative and photosynthetic phosphorylation. Biol Rev Camb Philos Soc. 1966 Aug;41(3):445–502. doi: 10.1111/j.1469-185x.1966.tb01501.x. [DOI] [PubMed] [Google Scholar]
  13. Severina I. I., Skulachev V. P., Zorov D. B. Coupling membranes as energy-transmitting cables. II. Cyanobacterial trichomes. J Cell Biol. 1988 Aug;107(2):497–501. doi: 10.1083/jcb.107.2.497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Shimada T., Horita K., Murakami M., Ogura R. Morphological studies of different mitochondrial populations in monkey myocardial cells. Cell Tissue Res. 1984;238(3):577–582. doi: 10.1007/BF00219874. [DOI] [PubMed] [Google Scholar]
  15. Skulachev V. P. Integrating functions of biomembranes. Problems of lateral transport of energy, metabolites and electrons. Biochim Biophys Acta. 1980 Dec 31;604(3):297–310. doi: 10.1016/0005-2736(80)90576-3. [DOI] [PubMed] [Google Scholar]
  16. Skulachev V. P. Membrane electricity as a convertible energy currency for the cell. Can J Biochem. 1980 Mar;58(3):161–175. doi: 10.1139/o80-023. [DOI] [PubMed] [Google Scholar]
  17. Sumper M., Träuble H. Membranes as acceptors for palmitoyl CoA in fatty acid biosynthesis. FEBS Lett. 1973 Feb 15;30(1):29–34. doi: 10.1016/0014-5793(73)80612-x. [DOI] [PubMed] [Google Scholar]
  18. Vorobjev I. A., Zorov D. B. Diazepam inhibits cell respiration and induces fragmentation of mitochondrial reticulum. FEBS Lett. 1983 Nov 14;163(2):311–314. doi: 10.1016/0014-5793(83)80842-4. [DOI] [PubMed] [Google Scholar]
  19. Wittenberg B. A., Wittenberg J. B. Oxygen pressure gradients in isolated cardiac myocytes. J Biol Chem. 1985 Jun 10;260(11):6548–6554. [PubMed] [Google Scholar]

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