Skip to main content
SpringerLink
Log in

Mitocentricity

  • REVIEW
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Worldwide, interest in mitochondria is constantly growing, as evidenced by scientific statistics, and studies of the functioning of these organelles are becoming more prevalent than studies of other cellular structures. In this analytical review, mitochondria are conditionally placed in a certain cellular center, which is responsible for both energy production and other non-energetic functions, without which the existence of not only the eukaryotic cell itself, but also the entire organism is impossible. Taking into account the high multifunctionality of mitochondria, such a fundamentally new scheme of cell functioning organization, including mitochondrial management of processes that determine cell survival and death, may be justified. Considering that this issue is dedicated to the memory of V. P. Skulachev, who can be called mitocentric, due to the history of his scientific activity almost entirely aimed at studying mitochondria, this work examines those aspects of mitochondrial functioning that were directly or indirectly the focus of attention of this outstanding scientist. We list all possible known mitochondrial functions, including membrane potential generation, synthesis of Fe-S clusters, steroid hormones, heme, fatty acids, and CO2. Special attention is paid to the participation of mitochondria in the formation and transport of water, as a powerful biochemical cellular and mitochondrial regulator. The history of research on reactive oxygen species that generate mitochondria is subject to significant analysis. In the section “Mitochondria in the center of death”, special emphasis is placed on the analysis of what role and how mitochondria can play and determine the program of death of an organism (phenoptosis) and the contribution made to these studies by V. P. Skulachev.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Abbreviations

ROS:

reactive oxygen species

References

  1. Zorov, D. B., Isaev, N. K., Plotnikov, E. Yu., Zorova, L. D., Stelmashook, E. V., Vasileva, A. K., Arkhangelskaya, A. A., and Khrjapenkova, T. G. (2007) The mitochondrion as Janus bifrons, Biochemistry (Moscow), 72, 1115-1126, https://doi.org/10.1134/S0006297907100094.

    Article  CAS  PubMed  Google Scholar 

  2. Picard, M., and Shirihai, O. S. (2022) Mitochondrial signal transduction, Cell Metab., 34, 1620-1653, https://doi.org/10.1016/j.cmet.2022.10.008.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Zorov, D. B., Krasnikov, B. F., Kuzminova, A. E., Vysokikh, M. Yu., and Zorova, L. D. (1997) Mitochondria Revisited. Alternative functions of mitochondria, Biosci. Rep., 17, 507-520, https://doi.org/10.1023/A:1027304122259.

    Article  CAS  PubMed  Google Scholar 

  4. Skou, J. C. (1998) The identification of the sodium pump, Biosci. Rep., 18, 155-169, https://doi.org/10.1023/A:1020196612909.

    Article  CAS  PubMed  Google Scholar 

  5. Klingenberg, M. (2008) The ADP and ATP transport in mitochondria and its carrier, Biochim. Biophys. Acta Biomembr., 1778, 1978-2021, https://doi.org/10.1016/j.bbamem.2008.04.011.

    Article  CAS  Google Scholar 

  6. Zorova, L. D., Popkov, V. A., Plotnikov, E. Y., Silachev, D. N., Pevzner, I. B., Jankauskas, S. S., Babenko, V. A., Zorov, S. D., Balakireva, A. V., Juhaszova, M., Sollott, S. J., and Zorov, D. B. (2018) Mitochondrial membrane potential, Anal. Biochem., 552, 50-59, https://doi.org/10.1016/j.ab.2017.07.009.

    Article  CAS  PubMed  Google Scholar 

  7. Di Lisa, F., Blank, P. S., Colonna, R., Gambassi, G., Silverman, H. S., Stern, M. D., and Hansford, R. G. (1995) Mitochondrial membrane potential in single living adult rat cardiac myocytes exposed to anoxia or metabolic inhibition, J. Physiol., 486, 1-13, https://doi.org/10.1113/jphysiol.1995.sp020786.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Weinberg, J. M., Venkatachalam, M. A., Roeser, N. F., and Nissim, I. (2000) Mitochondrial dysfunction during hypoxia/reoxygenation and its correction by anaerobic metabolism of citric acid cycle intermediates, Proc. Natl. Acad. Sci. USA, 97, 2826-2831, https://doi.org/10.1073/pnas.97.6.2826.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  9. Takahashi, E., and Sato, M. (2014) Anaerobic respiration sustains mitochondrial membrane potential in a prolyl hydroxylase pathway-activated cancer cell line in a hypoxic microenvironment, Am. J. Physiol. Cell Physiol., 306, C334-C342, https://doi.org/10.1152/ajpcell.00255.2013.

    Article  CAS  PubMed  Google Scholar 

  10. Jin, S. M., Lazarou, M., Wang, C., Kane, L. A., Narendra, D. P., and Youle, R. J. (2010) Mitochondrial membrane potential regulates PINK1 import and proteolytic destabilization by PARL, J. Cell Biol., 191, 933-942, https://doi.org/10.1083/jcb.201008084.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Mokranjac, D., and Neupert, W. (2008) Energetics of protein translocation into mitochondria, Biochim. Biophys. Acta Bioener., 1777, 758-762, https://doi.org/10.1016/j.bbabio.2008.04.009.

    Article  CAS  Google Scholar 

  12. Gunter, T. E., and Pfeiffer, D. R. (1990) Mechanisms by which mitochondria transport calcium, Am. J. Physiol. Cell Physiol., 258, C755-C786, https://doi.org/10.1152/ajpcell.1990.258.5.C755.

    Article  CAS  Google Scholar 

  13. Cortassa, S., Juhaszova, M., Aon, M. A., Zorov, D. B., and Sollott, S. J. (2021) Mitochondrial Ca2+, redox environment and ROS emission in heart failure: two sides of the same coin? J. Mol. Cell Cardiol., 151, 113-125, https://doi.org/10.1016/j.yjmcc.2020.11.013.

    Article  CAS  PubMed  Google Scholar 

  14. Liberman, E. A., Topaly, V. P., Tsofina, L. M., Jasaitis, A. A., and Skulachev, V. P. (1969) Mechanism of coupling of oxidative phosphorylation and the membrane potential of mitochondria, Nature, 222, 1076-1078, https://doi.org/10.1038/2221076a0.

    Article  ADS  CAS  PubMed  Google Scholar 

  15. Plotnikov, E. Y., Silachev, D. N., Chupyrkina, A. A., Danshina, M. I., Jankauskas, S. S., Morosanova, M. A., Stelmashook, E. V., Vasileva, A. K., Goryacheva, E. S., Pirogov, Y. A., Isaev, N. K., and Zorov, D. B. (2010) New-generation Skulachev ions exhibiting nephroprotective and neuroprotective properties, Biochemistry (Moscow), 75, 145-150, https://doi.org/10.1134/S0006297910020045.

    Article  CAS  PubMed  Google Scholar 

  16. Johnson, D. C., Dean, D. R., Smith, A. D., and Johnson, M. K. (2005) Structure, function, and formation of biological iron-sulfur clusters, Annu. Rev. Biochem., 74, 247-281, https://doi.org/10.1146/annurev.biochem.74.082803.133518.

    Article  CAS  PubMed  Google Scholar 

  17. Wächtershäuser, G. (1988) Before enzymes and templates: theory of surface metabolism, Microbiol. Rev., 52, 452-484, https://doi.org/10.1128/MMBR.52.4.452-484.1988.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Wächtershäuser, G. (1990) Evolution of the first metabolic cycles, Proc. Natl. Acad. Sci. USA, 87, 200-204, https://doi.org/10.1073/pnas.87.1.200.

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  19. Tsaousis, A. D. (2019) On the origin of iron/sulfur cluster biosynthesis in eukaryotes, Front. Microbiol., 10, 2478, https://doi.org/10.3389/fmicb.2019.02478.

    Article  PubMed  PubMed Central  Google Scholar 

  20. Lill, R., Diekert, K., Kaut, A., Lange, H., Pelzer, W., Prohl, C., and Kispal, G. (1999) The essential role of mitochondria in the biogenesis of cellular iron-sulfur proteins, Biol. Chem., 380, 1157-1166, https://doi.org/10.1515/BC.1999.147.

    Article  CAS  PubMed  Google Scholar 

  21. Braymer, J. J., and Lill, R. (2017) Iron-sulfur cluster biogenesis and trafficking in mitochondria, J. Biol. Chem., 292, 12754-12763, https://doi.org/10.1074/jbc.R117.787101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Rouault, T. A., and Maio, N. (2017) Biogenesis and functions of mammalian iron-sulfur proteins in the regulation of iron homeostasis and pivotal metabolic pathways, J. Biol. Chem., 292, 12744-12753, https://doi.org/10.1074/jbc.R117.789537.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Peña-Diaz, P., and Lukeš, J. (2018) Fe-S cluster assembly in the supergroup Excavata, J. Biol. Inorg. Chem., 23, 521-541, https://doi.org/10.1007/s00775-018-1556-6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Miller, W. L. (2013) Steroid hormone synthesis in mitochondria, Mol. Cell. Endocrinol., 379, 62-73, https://doi.org/10.1016/j.mce.2013.04.014.

    Article  CAS  PubMed  Google Scholar 

  25. Yeliseev, A. A., and Kaplan, S. (1995) A sensory transducer homologous to the mammalian peripheral-type benzodiazepine receptor regulates photosynthetic membrane complex formation in Rhodobacter sphaeroides 2.4.1., J. Biol. Chem., 270, 21167-21175, https://doi.org/10.1074/jbc.270.36.21167.

    Article  CAS  PubMed  Google Scholar 

  26. Baker, M. E., and Fanestil, D. D. (1991) Mammalian peripheral-type benzodiazepine receptor is homologous to CrtK protein of rhodobacter capsulatus, a photosynthetic bacterium, Cell, 65, 721-722, https://doi.org/10.1016/0092-8674(91)90379-D.

    Article  CAS  PubMed  Google Scholar 

  27. Zorov, D. B., Andrianova, N. V., Babenko, V. A., Bakeeva, L. E., Zorov, S. D., Zorova, L. D., Pevsner, I. B., Popkov, V. A., Plotnikov, E. Yu., and Silachev, D. N. (2020) Nonphosphorylating oxidation in mitochondria and related processes, Biochemistry (Moscow), 85, 1570-1577, https://doi.org/10.1134/S0006297920120093.

    Article  CAS  PubMed  Google Scholar 

  28. Acin-Perez, R., Salazar, E., Kamenetsky, M., Buck, J., Levin, L. R., and Manfredi, G. (2009) Cyclic AMP produced inside mitochondria regulates oxidative phosphorylation, Cell Metab., 9, 265-276, https://doi.org/10.1016/j.cmet.2009.01.012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Zeylemaker, W. P., Klaasse, A. D. M., Slater, E. C., and Veeger, C. (1970) Studies on Succinate Dehydrogenase. VI. Inhibition by monocarboxylic acids, Biochim. Biophys. Acta Enzymol., 198, 415-422, https://doi.org/10.1016/0005-2744(70)90120-8.

    Article  CAS  Google Scholar 

  30. Kasho, V. N., and Boyer, P. D. (1984) Relationships of inosine triphosphate and bicarbonate effects on F1 ATPase to the binding change mechanism, J. Bioenerg. Biomembr., 16, 407-419, https://doi.org/10.1007/BF00743235.

    Article  CAS  PubMed  Google Scholar 

  31. Roveri, O. A., and Calcaterra, N. B. (1985) Steady-state kinetics of F1-ATPase, FEBS Lett., 192, 123-127, https://doi.org/10.1016/0014-5793(85)80056-9.

    Article  CAS  PubMed  Google Scholar 

  32. Lodeyro, A. F., Calcaterra, N. B., and Roveri, O. A. (2001) Inhibition of steady-state mitochondrial ATP synthesis by bicarbonate, an activating anion of ATP hydrolysis, Biochim. Biophys. Acta Bioenergetics, 1506, 236-243, https://doi.org/10.1016/S0005-2728(01)00221-3.

    Article  CAS  Google Scholar 

  33. Khailova, L. S., Vygodina, T. V., Lomakina, G. Y., Kotova, E. A., and Antonenko, Y. N. (2020) Bicarbonate suppresses mitochondrial membrane depolarization induced by conventional uncouplers, Biochem. Biophys. Res. Commun., 530, 29-34, https://doi.org/10.1016/j.bbrc.2020.06.131.

    Article  CAS  PubMed  Google Scholar 

  34. Poňka, P., and Neuwirt, J. (1974) Haem synthesis and iron uptake by reticulocytes, Br. J. Haematol., 28, 1-5, https://doi.org/10.1111/j.1365-2141.1974.tb06634.x.

    Article  PubMed  Google Scholar 

  35. Kikuchi, G., and Hayashi, N. (1981) Regulation by heme of synthesis and intracellular translocation of δ-aminolevulinate synthase in the liver, Mol. Cell Biochem., 37, 27-41, https://doi.org/10.1007/BF02355885.

    Article  CAS  PubMed  Google Scholar 

  36. Azzi, A. (1984) Mitochondria: the utilization of oxygen for cell life, Experientia, 40, 901-906, https://doi.org/10.1007/BF01946437.

    Article  CAS  PubMed  Google Scholar 

  37. Mead, J. F. (1963) Lipid metabolism, Annu. Rev. Biochem., 32, 241-268, https://doi.org/10.1146/annurev.bi.32.070163.001325.

    Article  CAS  PubMed  Google Scholar 

  38. Severin, F. F., Severina, I. I., Antonenko, Y. N., Rokitskaya, T. I., Cherepanov, D. A., Mokhova, E. N., Vyssokikh, M. Yu., Pustovidko, A. V., Markova, O. V., Yaguzhinsky, L. S., Korshunova, G. A., Sumbatyan, N. V., Skulachev, M. V., and Skulachev, V. P. (2010) Penetrating cation/fatty acid anion pair as a mitochondria-targeted protonophore, Proc. Natl. Acad. Sci. USA, 107, 663-668, https://doi.org/10.1073/pnas.0910216107.

    Article  ADS  PubMed  Google Scholar 

  39. Andreyev, A. Yu., Bondareva, T. O., Dedukhova, V. I., Mokhova, E. N., Skulachev, V. P., Tsofina, L. M., Volkov, N. I., and Vygodina, T. V. (1989) The ATP/ADP-antiporter Is involved in the uncoupling effect of fatty acids on mitochondria, Eur. J. Biochem., 182, 585-592, https://doi.org/10.1111/j.1432-1033.1989.tb14867.x.

    Article  Google Scholar 

  40. Skulachev, V. P. (1998) Uncoupling: new approaches to an old problem of bioenergetics, Biochim. Biophys. Acta Bioenerg., 1363, 100-124, https://doi.org/10.1016/S0005-2728(97)00091-1.

    Article  CAS  Google Scholar 

  41. Zorov, D. B. (1996) Mitochondrial damage as a source of diseases and aging: a strategy of how to fight these, Biochim. Biophys. Acta Bioenerg., 1275, 10-15, https://doi.org/10.1016/0005-2728(96)00042-4.

    Article  Google Scholar 

  42. Schmidt, B., McCracken, J., and Ferguson-Miller, S. (2003) A discrete water exit pathway in the membrane protein cytochrome c oxidase, Proc. Natl. Acad. Sci. USA, 100, 15539-15542, https://doi.org/10.1073/pnas.2633243100.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  43. Buckberg, G. D., Fixler, D. E., Archie, J. P., and Hoffman, J. I. E. (1972) Experimental subendocardial ischemia in dogs with normal coronary arteries, Circ. Res., 30, 67-81, https://doi.org/10.1161/01.RES.30.1.67.

    Article  CAS  PubMed  Google Scholar 

  44. Hoffman, J. I. E., and Buckberg, G. D. (1978) The myocardial supply:demand ratio – a critical review, Am. J Cardiol., 41, 327-332, https://doi.org/10.1016/0002-9149(78)90174-1.

    Article  CAS  PubMed  Google Scholar 

  45. Newsholme, E. A., and Leech, A. R. (1983) Biochemistry for the Medical Sciences, Wiley, p. 952.

  46. Yaniv, Y., Juhaszova, M., Nuss, H. B., Wang, S., Zorov, D. B., Lakatta, E. G., and Sollott, S. J. (2010) Matching ATP supply and demand in mammalian heart, Ann. NY Acad. Sci., 1188, 133-142, https://doi.org/10.1111/j.1749-6632.2009.05093.x.

    Article  ADS  CAS  PubMed  Google Scholar 

  47. Bakeeva, L. E., Grinius, L. L., Jasaitis, A. A., Kuliene, V. V., Levitsky, D. O., Liberman, E. A., Severina, I. I., and Skulachev, V. P. (1970) Conversion of biomembrane-produced energy into electric form. II. Intact mitochondria, Biochim. Biophys. Acta, 216, 13-21, https://doi.org/10.1016/0005-2728(70)90154-4.

    Article  CAS  PubMed  Google Scholar 

  48. Bakeeva, L. E., Chentsov, Y. S., Jasaitis, A. A., and Skulachev, V. P. (1972) The effect of oncotic pressure on heart muscle mitochondria, Biochim. Biophys. Acta, 275, 319-332, https://doi.org/10.1016/0005-2728(72)90213-7.

    Article  CAS  PubMed  Google Scholar 

  49. Hackenbrock, C. R. (1966) Ultrastuctural bases for metabolically-linked mechanical activity in mitochondria, J. Cell. Biol., 30, 269-297, https://doi.org/10.1083/jcb.30.2.269.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Harris, R. A., Penniston, J. T., Asai, J., and Green, D. E. (1986) The conformational basis of energy conservation in membrane systems. II. Correlation between conformational change and functional states, Proc. Natl. Acad. Sci USA, 59, 830-837, https://doi.org/10.1073/pnas.59.3.830.

    Article  ADS  Google Scholar 

  51. Wrigglesworth, J. M., and Packer, L. (1968) Optical rotary dispersion and circular dichroism studies on mitochondria: correlation of ultrastructure and metabolic state with molecular conformational changes, Arch. Biochem. Biophys., 128, 790-801, https://doi.org/10.1016/0003-9861(68)90087-8.

    Article  CAS  PubMed  Google Scholar 

  52. Beavis, A. D., Brannan, R. D., and Garlid, K. D. (1985) Swelling and contraction of the mitochondrial matrix. I. A Structural interpretation of the relationship between light scattering and matrix volume, J. Biol. Chem., 260, 13424-13433.

    Article  CAS  PubMed  Google Scholar 

  53. Allmann, D. W., Munroe, J., Wakabayashi, T., and Green, D. E. (1970) Studies on the transition of the cristal membrane from the orthodox to the aggregated configuration. III. Loss of coupling ability of adrenal cortex mitochondria in the orthodox configuration, J. Bioenerg., 1, 331-353, https://doi.org/10.1007/BF01654572.

    Article  CAS  PubMed  Google Scholar 

  54. Packer, L. (1963) Size and shape transformations correlated with oxidative phosphorylation in mitochondria, J. Cell. Biol., 18, 487-494, https://doi.org/10.1083/jcb.18.3.487.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Petit, P. X., Zamzami, N., Vayssière, J. L., Mignotte, B., Kroemer, G., and Castedo, M. (1997) Implication of mitochondria in apoptosis, Mol. Cell. Biochem., 174, 185-188.

    Article  CAS  PubMed  Google Scholar 

  56. Petit, P. X., Goubern, M., Diolez, P., Susin, S. A., Zamzami, N., and Kroemer, G. (1998) Disruption of the outer mitochondrial membrane as a result of large amplitude swelling: the impact of irreversible permeability transition, FEBS Lett., 426, 111-116, https://doi.org/10.1016/S0014-5793(98)00318-4.

    Article  CAS  PubMed  Google Scholar 

  57. Lehninger, A. L. (1962) Water uptake and extrusion by mitochondria in relation to oxidative phosphorylation, Physiol. Rev., 42, 467-517, https://doi.org/10.1152/physrev.1962.42.3.467.

    Article  CAS  PubMed  Google Scholar 

  58. Green, D. E., Asai, J., Harris, R. A., and Penniston, J. T. (1968) Conformational basis of energy transformations in membrane systems, Arch. Biochem. Biophys., 125, 684-705, https://doi.org/10.1016/0003-9861(68)90626-7.

    Article  CAS  PubMed  Google Scholar 

  59. Hackenbrock, C. R. (1968) Chemical and physical fixation of isolated mitochondria in low-energy and high-energy states, Proc. Natl. Acad. Sci. USA, 61, 598-605, https://doi.org/10.1073/pnas.61.2.598.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  60. Garlid, K. D. (1976) Aqueous phase structure in cells and organelles, in Proceedings of the Cell-Associated Water, Boston, Massachusetts, pp. 293-362.

  61. Garlid, K. D. (1999) The state of water in biological systems, Int. Rev. Cytol., 192, 281-302, https://doi.org/10.1016/s0074-7696(08)60530-6.

    Article  Google Scholar 

  62. Srere, P. A. (1981) Protein Crystals as a model for mitochondrial matrix proteins, Trends Biochem. Sci., 6, 4-7, https://doi.org/10.1016/0968-0004(81)90003-7.

    Article  CAS  Google Scholar 

  63. Fulton, A. B. (1982) How crowded is the cytoplasm? Cell, 30, 345-347, https://doi.org/10.1016/0092-8674(82)90231-8.

    Article  CAS  PubMed  Google Scholar 

  64. Takahashi, S., and Sugimoto, N. (2020) Stability prediction of canonical and non-canonical structures of nucleic acids in various molecular environments and cells, Chem. Soc. Rev., 49, 8439-8468, https://doi.org/10.1039/D0CS00594K.

    Article  CAS  PubMed  Google Scholar 

  65. Minton, A. P. (1983) The effect of volume occupancy upon the thermodynamic activity of proteins: some biochemical consequences, Mol. Cell. Biochem., 55, 119-140, https://doi.org/10.1007/BF00673707.

    Article  CAS  PubMed  Google Scholar 

  66. Minton, A. P. (1990) Holobiochemistry: the effect of local environment upon the equilibria and rates of biochemical reactions, Int. J. Biochem., 22, 1063-1067, https://doi.org/10.1016/0020-711X(90)90102-9.

    Article  CAS  PubMed  Google Scholar 

  67. Bentzel, C. J., and Solomon, A. K. (1967) Osmotic properties of mitochondria, J. Gen. Physiol., 50, 1547-1563, https://doi.org/10.1085/jgp.50.6.1547.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Cooke, R., and Kuntz, I. D. (1974) The properties of water in biological systems, Annu. Rev. Biophys. Bioeng., 3, 95-126, https://doi.org/10.1146/annurev.bb.03.060174.000523.

    Article  CAS  PubMed  Google Scholar 

  69. Drost-Hansen, W. (1969) Structure of water near solid unterfaces, Ind. Eng. Chem., 61, 10-47, https://doi.org/10.1021/ie50719a005.

    Article  CAS  Google Scholar 

  70. Juhaszova, M., Zorov, D. B., Kim, S. H., Pepe, S., Fu, Q., Fishbein, K. W., Ziman, B. D., Wang, S., Ytrehus, K., Antos, C. L., Olson, E. N., and Sollott, S. J. (2004) Glycogen synthase kinase-3β mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore, J. Clin. Invest., 113, 1535-1549, https://doi.org/10.1172/JCI19906.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Srere, P. A. (1980) The infrastructure of the mitochondrial matrix, Trends Biochem. Sci., 5, 120-121, https://doi.org/10.1016/0968-0004(80)90051-1.

    Article  CAS  Google Scholar 

  72. Matlib, M. A., and Srere, P. A. (1976) Oxidative properties of swollen rat liver mitochondria, Arch. Biochem. Biophys., 174, 705-712, https://doi.org/10.1016/0003-9861(76)90401-X.

    Article  CAS  PubMed  Google Scholar 

  73. Srere, P. A. (1982) The structure of the mitochondrial inner membrane-matrix compartment, Trends Biochem. Sci., 7, 375-378, https://doi.org/10.1016/0968-0004(82)90119-0.

    Article  CAS  Google Scholar 

  74. Srere, P. A., Mattiasson, B., and Mosbach, K. (1973) An immobilized three-enzyme system: a model for microenvironmental compartmentation in mitochondria, Proc. Natl. Acad. Sci. USA, 70, 2534-2538, https://doi.org/10.1073/pnas.70.9.2534.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  75. Letts, J. A., Fiedorczuk, K., and Sazanov, L. A. (2016) The architecture of respiratory supercomplexes, Nature, 537, 644-648, https://doi.org/10.1038/nature19774.

    Article  ADS  CAS  PubMed  Google Scholar 

  76. Guo, R., Zong, S., Wu, M., Gu, J., and Yang, M. (2017) Architecture of human mitochondrial respiratory megacomplex I2III2IV2, Cell, 170, 1247-1257.e12, https://doi.org/10.1016/J.CELL.2017.07.050.

    Article  CAS  PubMed  Google Scholar 

  77. Gu, J., Wu, M., Guo, R., Yan, K., Lei, J., Gao, N., and Yang, M. (2016) The architecture of the mammalian respirasome, Nature, 537, 639-643, https://doi.org/10.1038/nature19359.

    Article  ADS  CAS  PubMed  Google Scholar 

  78. Ing, G., Hartley, A. M., Pinotsis, N., and Maréchal, A. (2022) Cryo-EM structure of a monomeric yeast S. cerevisiae complex IV isolated with maltosides: implications in supercomplex formation, Biochim. Biophys. Acta Bioenerg., 1863, 148591, https://doi.org/10.1016/J.BBABIO.2022.148591.

    Article  CAS  PubMed  Google Scholar 

  79. Vercellino, I., and Sazanov, L. A. (2022) The assembly, regulation and function of the mitochondrial respiratory chain, Nat. Rev. Mol. Cell. Biol., 23, 141-161, https://doi.org/10.1038/s41580-021-00415-0.

    Article  CAS  PubMed  Google Scholar 

  80. Bhatia, V. K., Hatzakis, N. S., and Stamou, D. (2010) A Unifying mechanism accounts for sensing of membrane curvature by BAR domains, amphipathic helices and membrane-anchored proteins, Semin. Cell Dev. Biol., 21, 381-390, https://doi.org/10.1016/j.semcdb.2009.12.004.

    Article  CAS  PubMed  Google Scholar 

  81. Madsen, K. L., Bhatia, V. K., Gether, U., and Stamou, D. (2010) BAR domains, amphipathic helices and membrane-anchored proteins use the same mechanism to sense membrane curvature, FEBS Lett., 584, 1848-1855, https://doi.org/10.1016/j.febslet.2010.01.053.

    Article  CAS  PubMed  Google Scholar 

  82. Drin, G., and Antonny, B. (2010) Amphipathic helices and membrane curvature, FEBS Lett., 584, 1840-1847, https://doi.org/10.1016/j.febslet.2009.10.022.

    Article  CAS  PubMed  Google Scholar 

  83. Ikon, N., and Ryan, R. O. (2017) Cardiolipin and mitochondrial cristae organization, Biochim. Biophys. Acta Biomembranes, 1859, 1156-1163, https://doi.org/10.1016/j.bbamem.2017.03.013.

    Article  CAS  PubMed  Google Scholar 

  84. Blum, T. B., Hahn, A., Meier, T., Davies, K. M., and Kühlbrandt, W. (2019) Dimers of mitochondrial ATP synthase induce membrane curvature and self-assemble into rows, Proc. Natl. Acad. Sci. USA, 116, 4250-4255, https://doi.org/10.1073/pnas.1816556116.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  85. Ohnishi, T. (1962) Extraction of actin- and myosin-like proteins from erythrocyte membrane, J. Biochemistry, 52, 307-308, https://doi.org/10.1093/oxfordjournals.jbchem.a127620.

    Article  CAS  Google Scholar 

  86. Neifakh, S. A., and Kazakova, T. B. (1963) Actomyosin-like protein in mitochondria of the mouse liver, Nature, 197, 1106-1107, https://doi.org/10.1038/1971106a0.

    Article  ADS  CAS  PubMed  Google Scholar 

  87. Bartley, W., Dean, B., and Ferdinand, W. (1969) Maintenance of mitochondrial volume and the effects of phosphate and ATP in producing swelling and shrinking, J. Theor. Biol., 24, 192-202, https://doi.org/10.1016/S0022-5193(69)80045-7.

    Article  ADS  CAS  PubMed  Google Scholar 

  88. Zorov, D., Vorobjev, I., Popkov, V., Babenko, V., Zorova, L., Pevzner, I., Silachev, D., Zorov, S., Andrianova, N., and Plotnikov, E. (2019) Lessons from the discovery of mitochondrial fragmentation (fission): a review and update, Cells, 8, 175, https://doi.org/10.3390/cells8020175.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Pihl, E., and Bahr, G. (1970) Matrix structure of critical-point dried mitochondria, Exp. Cell. Res., 63, 391-403, https://doi.org/10.1016/0014-4827(70)90228-4.

    Article  CAS  PubMed  Google Scholar 

  90. Juhaszova, M., Kobrinsky, E., Zorov, D. B., Nuss, H. B., Yaniv, Y., Fishbein, K. W., de Cabo, R., Montoliu, L., Gabelli, S. B., Aon, M. A., Cortassa, S., and Sollott, S. J. (2022) ATP Synthase K+- and H+-fluxes drive ATP synthesis and enable mitochondrial K+-“Uniporter” function: I. Characterization of ion fluxes, Function, 3, zqab065, https://doi.org/10.1093/function/zqab065.

    Article  PubMed  Google Scholar 

  91. Juhaszova, M., Kobrinsky, E., Zorov, D. B., Nuss, H. B., Yaniv, Y., Fishbein, K. W., de Cabo, R., Montoliu, L., Gabelli, S. B., Aon, M. A., Cortassa, S., and Sollott, S. J. (2022) ATP synthase K+- and H+-fluxes drive ATP synthesis and enable mitochondrial K+-“uniporter” function: II. Ion and ATP synthase flux regulation, Function, 3, zqac001, https://doi.org/10.1093/function/zqac001.

    Article  PubMed  PubMed Central  Google Scholar 

  92. Sobti, M., Walshe, J. L., Wu, D., Ishmukhametov, R., Zeng, Y. C., Robinson, C. V., Berry, R. M., and Stewart, A. G. (2020) Cryo-EM structures provide insight into how E. coli F1Fo ATP synthase accommodates symmetry mismatch, Nat. Commun., 11, 2615, https://doi.org/10.1038/s41467-020-16387-2.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  93. Lai, Y., Zhang, Y., Zhou, S., Xu, J., Du, Z., Feng, Z., Yu, L., Zhao, Z., Wang, W., Tang, Y., Yang, X., Guddat, L. W., Liu, F., Gao, Y., Rao, Z., and Gong, H. (2023) Structure of the human ATP synthase, Mol. Cell, 83, 2137-2147.e4, https://doi.org/10.1016/j.molcel.2023.04.029.

    Article  CAS  PubMed  Google Scholar 

  94. Pfeffermann, J., and Pohl, P. (2023) Tutorial for stopped-flow water flux measurements: why a report about “ultrafast water permeation through nanochannels with a densely fluorous interior surface” is flawed, Biomolecules, 13, 431, https://doi.org/10.3390/biom13030431.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Boytsov, D., Brescia, S., Chaves, G., Koefler, S., Hannesschlaeger, C., Siligan, C., Goessweiner-Mohr, N., Musset, B., and Pohl, P. (2023) Trapped pore waters in the open proton channel HV1, Small, 19, 2205968, https://doi.org/10.1002/smll.202205968.

    Article  CAS  Google Scholar 

  96. Pfeffermann, J., Goessweiner-Mohr, N., and Pohl, P. (2021) The energetic barrier to single-file water flow through narrow channels, Biophys. Rev., 13, 913-923, https://doi.org/10.1007/s12551-021-00875-w.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Zeuthen, T., and MacAulay, N. (2012) Transport of water against its concentration gradient: fact or fiction? Wiley Interdiscip. Rev. Membr. Transp. Signal., 1, 373-381, https://doi.org/10.1002/wmts.54.

    Article  CAS  Google Scholar 

  98. Loo, D. D. F., Hirayama, B. A., Meinild, A., Chandy, G., Zeuthen, T., and Wright, E. M. (1999) Passive water and ion transport by cotransporters, J. Physiol., 518, 195-202, https://doi.org/10.1111/j.1469-7793.1999.0195r.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Skulachev, V. P. (1995) Nonphosphorylating respiration as the mechanism preventing the formation of active forms of oxygen, Mol. Biol., 29, 1199-1209.

    CAS  Google Scholar 

  100. Chance, B. (1965) The respiratory chain as a model for metabolic control in multi-enzyme systems, in Control of Energy Metabolism, Academic Press, pp. 9-12.

  101. Skulachev, V. P. (1996) Role of uncoupled and non-coupled oxidations in maintenance of safely low levels of oxygen and its one-electron reductants, Q. Rev. Biophys., 29, 169-202, https://doi.org/10.1017/S0033583500005795.07.

    Article  CAS  PubMed  Google Scholar 

  102. Edwards, S. W. (1996) The O−2 generating NADPH oxidase of phagocytes: structure and methods of detection, Methods, 9, 563-577, https://doi.org/10.1006/meth.1996.0064.

    Article  CAS  PubMed  Google Scholar 

  103. Skulachev, V. P. (2005) How to clean the dirtiest place in the cell: cationic antioxidants as intramitochondrial ROS scavengers, IUBMB Life, 57, 305-310, https://doi.org/10.1080/15216540500092161.

    Article  CAS  PubMed  Google Scholar 

  104. Dröge, W. (2002) Free radicals in the physiological control of cell function, Physiol. Rev., 82, 47-95, https://doi.org/10.1152/physrev.00018.2001.

    Article  PubMed  Google Scholar 

  105. Michaelis, L. (1946) Fundamentals of oxidation and respiration, Am. Sci., 34, 573-596.

    CAS  PubMed  Google Scholar 

  106. Gerschman, R., Gilbert, D. L., Nye, S. W., Dwyer, P., and Fenn, W. O. (1954) Oxygen poisoning and X-irradiation: a mechanism in common, Science, 119, 623-626, https://doi.org/10.1126/science.119.3097.623.

    Article  ADS  CAS  PubMed  Google Scholar 

  107. Harman, D. (1995) Aging: a theory based on free radical and radiation chemistry, J. Gerontol., 11, 298-300, https://doi.org/10.1093/geronj/11.3.298.

    Article  Google Scholar 

  108. Franceschi, C. (1989) Cell proliferation, cell death and aging, Aging Clin. Exp. Res., 1, 3-15, https://doi.org/10.1007/BF03323871.

    Article  CAS  Google Scholar 

  109. Franceschi, C., Bonafe, M., Valensis, S., Oliveri, F., De Luca, M., Ottaviani, E., and De Benedictis, G. (2000) Inflamm-aging: an evolutionary perspective on immunosenescence, Ann. N Y Acad. Sci., 908, 244-254, https://doi.org/10.1111/j.1749-6632.2000.tb06651.x.

    Article  ADS  CAS  PubMed  Google Scholar 

  110. Franceschi, C., Garagnani, P., Vitale, G., Capri, M., and Salvioli, S. (2017) Inflammaging and ‘Garb-Aging’, Trends Endocrinol. Metab., 28, 199-212, https://doi.org/10.1016/j.tem.2016.09.005.

    Article  CAS  PubMed  Google Scholar 

  111. Ferrucci, L., and Fabbri, E. (2018) Inflammageing: chronic inflammation in ageing, cardiovascular disease, and frailty, Nat. Rev. Cardiol., 15, 505-522, https://doi.org/10.1038/s41569-018-0064-2.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Zhang, Q., Raoof, M., Chen, Y., Sumi, Y., Sursal, T., Junger, W., Brohi, K., Itagaki, K., and Hauser, C. J. (2010) Circulating mitochondrial DAMPs cause inflammatory responses to injury, Nature, 464, 104-107, https://doi.org/10.1038/nature08780.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  113. Pinti, M., Cevenini, E., Nasi, M., De Biasi, S., Salvioli, S., Monti, D., Benatti, S., Gibellini, L., Cotichini, R., Stazi, M. A., Trenti, T., Franceschi, C., and Cossarizza, A. (2014) Circulating mitochondrial DNA increases with age and is a familiar trait: implications for “inflamm-aging”, Eur. J Immunol., 44, 1552-1562, https://doi.org/10.1002/eji.201343921.

    Article  CAS  PubMed  Google Scholar 

  114. Shimada, K., Crother, T. R., Karlin, J., Dagvadorj, J., Chiba, N., Chen, S., Ramanujan, V. K., Wolf, A. J., Vergnes, L., Ojcius, D. M., Rentsendorj, A., Vargas, M., Guerrero, C., Wang, Y., Fitzgerald, K. A., Underhill, D. M., Town, T., and Arditi, M. (2012) Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis, Immunity, 36, 401-414, https://doi.org/10.1016/j.immuni.2012.01.009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Iyer, S. S., He, Q., Janczy, J. R., Elliott, E. I., Zhong, Z., Olivier, A. K., Sadler, J. J., Knepper-Adrian, V., Han, R., Qiao, L., Eisenbarth, S. C., Nauseef, W. M., Cassel, S. L., and Sutterwala, F. S. (2013) Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation, Immunity, 39, 311-323, https://doi.org/10.1016/j.immuni.2013.08.001.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Zorov, D. B., Bannikova, S. Y., Belousov, V. V., Vyssokikh, M. Y., Zorova, L. D., Isaev, N. K., Krasnikov, B. F., and Plotnikov, E. Y. (2005) Reactive oxygen and nitrogen species: friends or foes? Biochemistry (Moscow), 70, 215-221, https://doi.org/10.1007/s10541-005-0103-6.

    Article  CAS  PubMed  Google Scholar 

  117. Boveris, A., Oshino, N., and Chance, B. (1972) The cellular production of hydrogen peroxide, Biochem. J., 128, 617-630, https://doi.org/10.1042/bj1280617.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Korshunov, S. S., Skulachev, V. P., and Starkov, A. A. (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria, FEBS Lett., 416, 15-18, https://doi.org/10.1016/S0014-5793(97)01159-9.

    Article  CAS  PubMed  Google Scholar 

  119. Vyssokikh, M. Y., Holtze, S., Averina, O. A., Lyamzaev, K. G., Panteleeva, A. A., Marey, M. V., Zinovkin, R. A., Severin, F. F., Skulachev, M. V., Fasel, N., Hildebrandt, T. B., and Skulachev, V. P. (2020) Mild depolarization of the inner mitochondrial membrane is a crucial component of an anti-aging program, Proc. Natl. Acad. Sci. USA, 117, 6491-6501, https://doi.org/10.1073/pnas.1916414117.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  120. Plotnikov, E. Y., Silachev, D. N., Jankauskas, S. S., Rokitskaya, T. I., Chupyrkina, A. A., Pevzner, I. B., Zorova, L. D., Isaev, N. K., Antonenko, Y. N., Skulachev, V. P., and Zorov, D. B. (2012) Mild uncoupling of respiration and phosphorylation as a mechanism providing nephro- and neuroprotective effects of penetrating cations of the SkQ family, Biochemistry (Moscow), 77, 1029-1037, https://doi.org/10.1134/S0006297912090106.

    Article  CAS  PubMed  Google Scholar 

  121. Skulachev, V. P. (1991) Fatty acid circuit as a physiological mechanism of uncoupling of oxidative phosphorylation, FEBS Lett., 294, 158-162, https://doi.org/10.1016/0014-5793(91)80658-P.

    Article  CAS  PubMed  Google Scholar 

  122. Isaev, N. K., Zorov, D. B., Stelmashook, E. V., Uzbekov, R. E., Kozhemyakin, M. B., and Victorov, I. V. (1996) Neurotoxic Glutamate treatment of cultured cerebellar granule cells induces Ca2+-dependent collapse of mitochondrial membrane potential and ultrastructural alterations of mitochondria, FEBS Lett., 392, 143-147, https://doi.org/10.1016/0014-5793(96)00804-6.

    Article  CAS  PubMed  Google Scholar 

  123. Weidinger, A., Milivojev, N., Hosmann, A., Duvigneau, J. C., Szabo, C., Törö, G., Rauter, L., Vaglio-Garro, A., Mkrtchyan, G. V., Trofimova, L., Sharipov, R. R., Surin, A. M., Krasilnikova, I. A., Pinelis, V. G., Tretter, L., Moldzio, R., Bayır, H., Kagan, V. E., Bunik, V. I., and Kozlov, A. V. (2023) Oxoglutarate dehydrogenase complex controls glutamate-mediated neuronal death, Redox Biol., 62, 102669, https://doi.org/10.1016/j.redox.2023.102669.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Li, X., and May, J. M. (2002) Catalase-dependent measurement of H2O2 in intact mitochondria, Mitochondrion, 1, 447-453, https://doi.org/10.1016/S1567-7249(02)00010-7.

    Article  CAS  PubMed  Google Scholar 

  125. Palma, F. R., He, C., Danes, J. M., Paviani, V., Coelho, D. R., Gantner, B. N., and Bonini, M. G. (2020) Mitochondrial superoxide dismutase: what the established, the intriguing, and the novel reveal about a key cellular redox switch, Antioxid. Redox Signal., 32, 701-714, https://doi.org/10.1089/ars.2019.7962.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Kang, S. W., Chae, H. Z., Seo, M. S., Kim, K., Baines, I. C., and Rhee, S. G. (1998) Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-α, J. Biol. Chem., 273, 6297-6302, https://doi.org/10.1074/JBC.273.11.6297.

    Article  CAS  PubMed  Google Scholar 

  127. Arnér, E. S. J., and Holmgren, A. (2000) Physiological functions of thioredoxin and thioredoxin reductase, Eur. J Biochem., 267, 6102-6109, https://doi.org/10.1046/j.1432-1327.2000.01701.x.

    Article  PubMed  Google Scholar 

  128. Sohal, R. S., and Brunk, U. T. (1992) Mitochondrial production of pro-oxidants and cellular senescence, Mutat. Res., 275, 295-304, https://doi.org/10.1016/0921-8734(92)90033-L.

    Article  CAS  PubMed  Google Scholar 

  129. Zorov, D. B., Juhaszova, M., and Sollott, S. J. (2014) Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release, Physiol. Rev., 94, 909-950, https://doi.org/10.1152/physrev.00026.2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. Silachev, D. N., Plotnikov, E. Y., Pevzner, I. B., Zorova, L. D., Babenko, V. A., Zorov, S. D., Popkov, V. A., Jankauskas, S. S., Zinchenko, V. P., Sukhikh, G. T., and Zorov, D. B. (2014) The mitochondrion as a key regulator of ischaemic tolerance and injury, Heart Lung Circ., 23, 897-904, https://doi.org/10.1016/j.hlc.2014.05.022.

    Article  PubMed  Google Scholar 

  131. Zorov, D. B., Isaev, N. K., Plotnikov, E. Y., Silachev, D. N., Zorova, L. D., Pevzner, I. B., Morosanova, M. A., Jankauskas, S. S., Zorov, S. D., and Babenko, V. A. (2013) Perspectives of mitochondrial medicine, Biochemistry (Moscow), 78, 979-990, https://doi.org/10.1134/S0006297913090034.

    Article  CAS  PubMed  Google Scholar 

  132. Miller, J. W., Selhub, J., and Joseph, J. A. (1996) Oxidative damage caused by free radicals produced during catecholamine autoxidation: protective effects of O-methylation and melatonin, Free Radic. Biol. Med., 21, 241-249, https://doi.org/10.1016/0891-5849(96)00033-0.

    Article  CAS  PubMed  Google Scholar 

  133. Seiter, C. H. A., Margalit, R., and Perreault, R. A. (1979) The cytochrome c binding site on cytochrome c oxidase, Biochem. Biophys. Res. Commun., 86, 473-477, https://doi.org/10.1016/0006-291X(79)91738-8.

    Article  CAS  PubMed  Google Scholar 

  134. Vyssokikh, M., Zorova, L., Zorov, D., Heimlich, G., Jürgensmeier, J., Schreiner, D., and Brdiczka, D. (2004) The intra-mitochondrial cytochrome c distribution varies correlated to the formation of a complex between VDAC and the adenine nucleotide translocase: this affects Bax-dependent cytochrome c release, Biochim. Biophys. Acta Mol. Cell. Res., 1644, 27-36, https://doi.org/10.1016/j.bbamcr.2003.10.007.

    Article  CAS  Google Scholar 

  135. Vyssokikh, M. Y., Zorova, L., Zorov, D., Heimlich, G., Jürgensmeier, J. J., and Brdiczka, D. (2002) Bax releases cytochrome c preferentially from a complex between porin and adenine nucleotide translocator. Hexokinase activity suppresses this effect, Mol. Biol. Rep., 29, 93-96, https://doi.org/10.1023/a:1020383108620.

    Article  CAS  PubMed  Google Scholar 

  136. Kagan, V. E., Bayır, H. A., Belikova, N. A., Kapralov, O., Tyurina, Y. Y., Tyurin, V. A., Jiang, J., Stoyanovsky, D. A., Wipf, P., Kochanek, P. M., Greenberger, J. S., Pitt, B., Shvedova, A. A., and Borisenko, G. (2009) Cytochrome c/cardiolipin relations in mitochondria: a kiss of death, Free Radic. Biol. Med., 46, 1439-1453, https://doi.org/10.1016/j.freeradbiomed.2009.03.004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Pereverzev, M. O., Vygodina, T. V., Konstantinov, A. A., and Skulachev, V. P. (2003) Cytochrome c, an ideal antioxidant, Biochem. Soc. Trans., 31, 1312-1315, https://doi.org/10.1042/bst0311312.

    Article  CAS  PubMed  Google Scholar 

  138. Skulachev, V. P. (1998) Cytochrome c in the apoptotic and antioxidant cascades, FEBS Lett., 423, 275-280, https://doi.org/10.1016/S0014-5793(98)00061-1.

    Article  CAS  PubMed  Google Scholar 

  139. Abramicheva, P. A., Andrianova, N. V., Babenko, V. A., Zorova, L. D., Zorov, S. D., Pevzner, I. B., Popkov, V. A., Semenovich, D. S., Yakupova, E. I., Silachev, D. N., Plotnikov, E. Y., Sukhikh, G. T., and Zorov, D. B. (2023) Mitochondrial network: electric cable and more, Biochemistry (Moscow), 88, 1596-1607, https://doi.org/10.1134/S0006297923100140.

    Article  CAS  PubMed  Google Scholar 

  140. Skulachev, V. P. (1971) Energy transformations in the respiratory chain, Curr. Top. Bioenergetics, 4, 127-190, https://doi.org/10.1016/B978-0-12-152504-0.50010-1.

    Article  CAS  Google Scholar 

  141. Bakeeva, L. E., Chentsov, Y. S., and Skulachev, V. P. (1978) Mitochondrial framework (reticulum mitochondriale) in rat diaphragm muscle, Biochim. Biophys. Acta, 501, 349-369, https://doi.org/10.1016/0005-2728(78)90104-4.

    Article  CAS  PubMed  Google Scholar 

  142. Drachev, V. A., and Zorov, D. B. (1986) Mitochondria are like an electrical cable. Experimental testing of the hypothesis, Dokl. Acad. Nauk. USSR, 287, 1237-1238.

    CAS  Google Scholar 

  143. Amchenkova, A. A., Bakeeva, L. E., Chentsov, Y. S., Skulachev, V. P., and Zorov, D. B. (1988) Coupling membranes as energy-transmitting cables. I. Filamentous mitochondria in fibroblasts and mitochondrial clusters in cardiomyocytes, J. Cell. Biol., 107, 481-495, https://doi.org/10.1083/jcb.107.2.481.148.

    Article  CAS  PubMed  Google Scholar 

  144. Vitale, I., Pietrocola, F., Guilbaud, E., Aaronson, S. A., Abrams, J. M., Adam, D., Agostini, M., Agostinis, P., Alnemri, E. S., Altucci, L., et al. (2023) Apoptotic cell death in disease – current understanding of the NCCD 2023, Cell Death Differ., 30, 1097-1154, https://doi.org/10.1038/s41418-023-01153-w.

    Article  PubMed  PubMed Central  Google Scholar 

  145. Zorov, D. B., Popkov, V. A., Zorova, L. D., Vorobjev, I. A., Pevzner, I. B., Silachev, D. N., Zorov, S. D., Jankauskas, S. S., Babenko, V. A., and Plotnikov, E. Y. (2017) Mitochondrial aging: is there a mitochondrial clock? J. Gerontol. A Biol. Sci. Med. Sci., 72, 1171-1179, https://doi.org/10.1093/gerona/glw184.

    Article  CAS  PubMed  Google Scholar 

  146. Twig, G., Elorza, A., Molina, A. J. A., Mohamed, H., Wikstrom, J. D., Walzer, G., Stiles, L., Haigh, S. E., Katz, S., Las, G., Alroy, J., Wu, M., Py, B. F., Yuan, J., Deeney, J. T., Corkey, B. E., and Shirihai, O. S. (2008) Fission and selective fusion govern mitochondrial segregation and elimination by autophagy, EMBO J., 27, 433-446, https://doi.org/10.1038/sj.emboj.7601963.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Vorobjev, I. A., and Zorov, D. B. (1983) Diazepam inhibits cell respiration and induces fragmentation of mitochondrial reticulum, FEBS Lett., 163, 311-314, https://doi.org/10.1016/0014-5793(83)80842-4.

    Article  ADS  CAS  PubMed  Google Scholar 

  148. Plotnikov, E. Y., Vasileva, A. K., Arkhangelskaya, A. A., Pevzner, I. B., Skulachev, V. P., and Zorov, D. B. (2008) Interrelations of mitochondrial fragmentation and cell death under ischemia/reoxygenation and UV-irradiation: protective effects of SkQ1, lithium ions and insulin, FEBS Lett., 582, 3117-3124, https://doi.org/10.1016/j.febslet.2008.08.002.

    Article  CAS  PubMed  Google Scholar 

  149. Hunter, D. R., Haworth, R. A. (1979) The Ca2+-induced membrane transition in mitochondria: I. The protective mechanisms, Arch. Biochem. Biophys., 195, 453-459, https://doi.org/10.1016/0003-9861(79)90371-0.

    Article  CAS  PubMed  Google Scholar 

  150. Haworth, R. A., and Hunter, D. R. (1979) The Ca2+-induced membrane transition in mitochondria: II. Nature of the Ca2+ trigger site, Arch. Biochem. Biophys., 195, 460-467, https://doi.org/10.1016/0003-9861(79)90372-2.

    Article  CAS  PubMed  Google Scholar 

  151. Hunter, D. R., and Haworth, R. A. (1979) The Ca2+-induced membrane transition in mitochondria: III. Transitional Ca2+ release, Arch. Biochem. Biophys., 195, 468-477, https://doi.org/10.1016/0003-9861(79)90373-4.

    Article  CAS  PubMed  Google Scholar 

  152. Novgorodov, S. A., Gudz, T. I., Kushnareva, Y. E., Zorov, D. B., and Kudrjashov, Y. B. (1990) Effect of cyclosporine A and oligomycin on non-specific permeability of the inner mitochondrial membrane, FEBS Lett., 270, 108-110, https://doi.org/10.1016/0014-5793(90)81245-j.

    Article  CAS  PubMed  Google Scholar 

  153. Novgorodov, S. A., Gudz, T. I., Kushnareva, Y. E., Zorov, D. B., and Kudrjashov, Y. B. (1990) Effect of ADP/ATP antiporter conformational state on the suppression of the nonspecific permeability of the inner mitochondrial membrane by cyclosporine A, FEBS Lett., 277, 123-126, https://doi.org/10.1016/0014-5793(90)80824-3.

    Article  CAS  PubMed  Google Scholar 

  154. Kinnally, K. W., Zorov, D., Antonenko, Y., and Perini, S. (1991) Calcium modulation of mitochondrial inner membrane channel activity, Biochem. Biophys. Res. Commun., 176, 1183-1188, https://doi.org/10.1016/0006-291x(91)90410-9.

    Article  CAS  PubMed  Google Scholar 

  155. Szabó, I., and Zoratti, M. (1992) The mitochondrial megachannel is the permeability transition pore, J. Bioenerg. Biomembr., 24, 111-117, https://doi.org/10.1007/BF00769537.

    Article  PubMed  Google Scholar 

  156. Zoratti, M., and Szabò, I. (1995) The mitochondrial permeability transition, Biochim. Biophys. Acta, 1241, 139-176, https://doi.org/10.1016/0304-4157(95)00003-a.

    Article  PubMed  Google Scholar 

  157. Krasnikov, B. F., Zorov, D. B., Antonenko, Y. N., Zaspa, A. A., Kulikov, I. V., Kristal, B. S., Cooper, A. J., and Brown, A. M. (2005) Comparative kinetic analysis reveals that inducer-specific ion release precedes the mitochondrial permeability transition, Biochim. Biophys. Acta, 1708, 375-392, https://doi.org/10.1016/j.bbabio.2005.05.009.

    Article  CAS  PubMed  Google Scholar 

  158. Zorov, D. B., Juhaszova, M., Yaniv, Y., Nuss, H. B., Wang, S., and Sollott, S. J. (2009) Regulation and pharmacology of the mitochondrial permeability transition pore, Cardiovasc. Res., 83, 213-225, https://doi.org/10.1093/cvr/cvp151.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Skulachev, V. P. (1996) Why are mitochondria involved in apoptosis? Permeability transition pores and apoptosis as selective mechanisms to eliminate superoxide-producing mitochondria and cell, FEBS Lett., 397, 7-10, https://doi.org/10.1016/0014-5793(96)00989-1.

    Article  CAS  PubMed  Google Scholar 

  160. Kluck, R. M., Esposti, M. D., Perkins, G., Renken, C., Kuwana, T., Bossy-Wetzel, E., Goldberg, M., Allen, T., Barber, M. J., Green, D. R., and Newmeyer, D. D. (1999) The pro-apoptotic proteins, Bid and Bax, cause a limited permeabilization of the mitochondrial outer membrane that is enhanced by cytosol, J. Cell Biol., 147, 809-822, https://doi.org/10.1083/jcb.147.4.809.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Zorov, D. B., Kinnally, K. W., and Tedeschi, H. (1992) Voltage activation of heart inner mitochondrial membrane channels, J. Bioenerg. Biomembr., 24, 119-124, https://doi.org/10.1007/BF00769538.

    Article  CAS  PubMed  Google Scholar 

  162. Lemasters, J. J. (1999) Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis, Am. J. Physiol. Gastrointest. Liver Physiol., 276, G1-G6, https://doi.org/10.1152/ajpgi.1999.276.1.G1.

    Article  CAS  Google Scholar 

  163. Riedl, S. J., and Salvesen, G. S. (2007) The apoptosome: signalling platform of cell death, Nat. Rev. Mol. Cell Biol., 8, 405-413, https://doi.org/10.1038/nrm2153.

    Article  CAS  PubMed  Google Scholar 

  164. Zorov, D. B., Plotnikov, E. Y., Jankauskas, S. S., Isaev, N. K., Silachev, D. N., Zorova, L. D., Pevzner, I. B., Pulkova, N. V., Zorov, S. D., and Morosanova, M. A. (2012) The phenoptosis problem: what is causing the death of an organism? Lessons from acute kidney injury, Biochemistry (Moscow), 77, 742-753, https://doi.org/10.1134/S0006297912070073.

    Article  CAS  PubMed  Google Scholar 

  165. Plotnikov, E. Y., Morosanova, M. A., Pevzner, I. B., Zorova, L. D., Manskikh, V. N., Pulkova, N. V., Galkina, S. I., Skulachev, V. P., and Zorov, D. B. (2013) Protective effect of mitochondria-targeted antioxidants in an acute bacterial infection, Proc. Natl. Acad. Sci. USA, 110, E3100-E3108, https://doi.org/10.1073/pnas.1307096110.

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  166. Zorov, D. B., Plotnikov, E. Y., Silachev, D. N., Zorova, L. D., Pevzner, I. B., Zorov, S. D., Babenko, V. A., Jankauskas, S. S., Popkov, V. A., and Savina, P. S. (2014) Microbiota and mitobiota. Putting an equal sign between mitochondria and bacteria, Biochemistry (Moscow), 79, 1017-1031, https://doi.org/10.1134/S0006297914100046.

    Article  CAS  PubMed  Google Scholar 

  167. Popkov, V. A., Plotnikov, E. Y., Silachev, D. N., Zorova, L. D., Pevzner, I. B., Jankauskas, S. S., Zorov, S. D., Andrianova, N. V., Babenko, V. A., and Zorov, D. B. (2017) Bacterial therapy and mitochondrial therapy, Biochemistry (Moscow), 82, 1549-1556, https://doi.org/10.1134/S0006297917120148.

    Article  CAS  PubMed  Google Scholar 

  168. Skulachev, V. P. (2012) What is “phenoptosis” and how to fight it? Biochemistry (Moscow), 77, 689-706, https://doi.org/10.1134/S0006297912070012.

    Article  CAS  PubMed  Google Scholar 

  169. Skulachev, V. P. (2002) Programmed death phenomena: from organelle to organism, Ann. NY Acad. Sci., 959, 214-237, https://doi.org/10.1111/j.1749-6632.2002.tb02095.x.

    Article  ADS  CAS  PubMed  Google Scholar 

  170. Skulachev, V. P. (1999) Phenoptosis: programmed death of an organism, Biochemistry (Moscow), 64, 1418-1426.

    CAS  PubMed  Google Scholar 

  171. Skulachev, V. P., Vyssokikh, M. Yu., Chernyak, B. V., Averina, O. A., Andreev-Andrievskiy, A. A., Zinovkin, R. A., Lyamzaev, K. G., Marey, M. V., Egorov, M. V., Frolova, O. J., Zorov, D. B., Skulachev, M. V., and Sadovnichii, V. A. (2023) Mitochondrion-targeted antioxidant SkQ1 prevents rapid animal death caused by highly diverse shocks, Sci. Rep., 13, 4326, https://doi.org/10.1038/s41598-023-31281-9.

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  172. Bakeeva, L. E., Barskov, I. V., Egorov, M. V., Isaev, N. K., Kapelko, V. I., Kazachenko, A. V., Kirpatovsky, V. I., Kozlovsky, S. V., Lakomkin, V. L., Levina, S. B., Pisarenko, O. I., Plotnikov, E. Y., Saprunova, V. B., Serebryakova, L. I., Skulachev, M. V., Stelmashook, E. V., Studneva, I. M., Tskitishvili, O. V., Vasilyeva, A. K., Victorov, I. V., Zorov, D. B., and Skulachev, V. P. (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 2. Treatment of some ROS- and age-related diseases (heart arrhythmia, heart infarctions, kidney ischemia, and stroke), Biochemistry (Moscow), 73, 1288-1299, https://doi.org/10.1134/S000629790812002X.

    Article  CAS  PubMed  Google Scholar 

  173. Roginsky, V. A., Skulachev, V. P., Zorov, D. B., Zamyatnin, A. A., Vyssokikh, M. Y., Shidlovsky, K. M., Tashlitsky, V. N., Shkurat, T. P., Severin, F. F., Severina, I. I., Savchenko, A. Y., Skulachev, M. V., Plotnikov, E. Y., Lyamzaev, K. G., Korshunova, G. A., Kolosova, N. G., Egorov, M. V., Chistyakov, V. A., Cherepanov, D. A., Chernyak, B. V., Anisimov, V. N., and Antonenko, Y. N. (2011) Mitochondrial-targeted plastoquinone derivatives. Effect on senescence and acute age-related pathologies, Curr. Drug. Targets, 12, 800-826, https://doi.org/10.2174/138945011795528859.

    Article  PubMed  Google Scholar 

  174. Weismann, A. (1882) About the Duration of Life [in German], Fischer, Jena.

Download references

Funding

This work was supported by the Ministry of Health of the Russian Federation, State Assignment no. 124013000594-1.

Author information

Authors and Affiliations

  1. Belozersky Research Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119991, Moscow, Russia

    Dmitry B. Zorov, Polina A. Abramicheva, Nadezda V. Andrianova, Valentina A. Babenko, Ljubava D. Zorova, Savva D. Zorov, Irina B. Pevzner, Vasily A. Popkov, Dmitry S. Semenovich, Elmira I. Yakupova, Denis N. Silachev & Egor Y. Plotnikov

  2. Kulakov National Medical Research Center of Obstetrics, Gynecology and Perinatology, 117997, Moscow, Russia

    Dmitry B. Zorov, Valentina A. Babenko, Ljubava D. Zorova, Irina B. Pevzner, Vasily A. Popkov, Denis N. Silachev, Egor Y. Plotnikov & Gennady T. Sukhikh

  3. Faculty of Bioengineering and Bioinformatics, Lomonosov Moscow State University, 119991, Moscow, Russia

    Savva D. Zorov

Authors
  1. Dmitry B. Zorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Polina A. Abramicheva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nadezda V. Andrianova
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Valentina A. Babenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ljubava D. Zorova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Savva D. Zorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Irina B. Pevzner
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Vasily A. Popkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Dmitry S. Semenovich
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Elmira I. Yakupova
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Denis N. Silachev
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Egor Y. Plotnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Gennady T. Sukhikh
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

P.A.A., N.V.A., V.A.B., L.D.Z., S.D.Z., I.B.P., V.A.P., D.S.S., E.I.Y., D.N.S., E.Y.P., G.T.S., and D.B.Z. general discussion of the concept, ideology and plans for the construction of the work; D.B.Z. writing the manuscript; L.D.Z. and S.D.Z. editing and technical design of the manuscript.

Corresponding author

Correspondence to Dmitry B. Zorov.

Ethics declarations

This work does not contain any studies involving human and animal subjects. The authors of this work declare that they have no conflicts of interest.

Additional information

Publisher’s Note. Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zorov, D.B., Abramicheva, P.A., Andrianova, N.V. et al. Mitocentricity. Biochemistry Moscow 89, 223–240 (2024). https://doi.org/10.1134/S0006297924020044

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297924020044

Keywords

Search

Navigation