Skip to main content
SpringerLink
Log in

Isn’t It Time for Establishing Mitochondrial Nomenclature Breaking Mitochondrial Paradigm?

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

Abstract

In this work, we decided to initiate a discussion concerning heterogeneity of mitochondria, suggesting that it is time to build classification of mitochondria, like the one that exists for their progenitors, α-proteobacteria, proposing possible separation of mitochondrial strains and maybe species. We continue to adhere to the general line that mitochondria are friends and foes: on the one hand, they provide the cell and organism with the necessary energy and signaling molecules, and, on the other hand, participate in destruction of the cell and the organism. Current understanding that the activity of mitochondria is not only limited to energy production, but also that these alternative non-energetic functions are unique and irreplaceable in the cell, allowed us to speak about the strong subordination of the entire cellular metabolism to characteristic functional manifestations of mitochondria. Mitochondria are capable of producing not only ATP, but also iron–sulfur clusters, steroid hormones, heme, reactive oxygen and nitrogen species, participate in thermogenesis, regulate cell death, proliferation and differentiation, participate in detoxification, etc. They are a mandatory attribute of eukaryotic cells, and, so far, no eukaryotic cells performing a non-parasitic or non-symbiotic life style have been found that lack mitochondria. We believe that the structural-functional intracellular, intercellular, inter-organ, and interspecific diversity of mitochondria is large enough to provide grounds for creating a mitochondrial nomenclature. The arguments for this are given in this analytical work.

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

Similar content being viewed by others

Abbreviations

mtDNA:

mitochondrial DNA

References

  1. 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  Google Scholar 

  2. 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  Google Scholar 

  3. 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  Google Scholar 

  4. Popkov, V. A., Silachev, D. N., Jankauskas, S. S., Zorova, L. D., Pevzner, I. B., Babenko, V. A., Plotnikov, E. Y., and Zorov, D. B. (2016) Molecular and cellular interactions between mother and fetus. Pregnancy as a rejuvenating factor, Biochemistry (Moscow), 81, 1480-1487, https://doi.org/10.1134/S0006297916120099.

    Article  CAS  Google Scholar 

  5. 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  Google Scholar 

  6. 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  Google Scholar 

  7. Snyder, G. K., and Sheafor, B. A. (1999) Red blood cells: centerpiece in the evolution of the vertebrate circulatory system, Am. Zool., 39, 189-198, https://doi.org/10.1093/icb/39.2.189.

    Article  Google Scholar 

  8. Gaehtgens, P., Schmidt, F., and Will, G. (1981) Comparative rheology of nucleated and non-nucleated red blood cells. I. Microrheology of avian erythrocytes during capillary flow, Pflugers Arch., 390, 278-282, https://doi.org/10.1007/BF00658276.

    Article  CAS  Google Scholar 

  9. Dzierzak, E., and Philipsen, S. (2013) Erythropoiesis: development and differentiation, Cold Spring Harb. Perspect. Med., 3, a011601, https://doi.org/10.1101/cshperspect.a011601.

    Article  CAS  Google Scholar 

  10. Dubiel, W., and Rapoport, S. M. (1989) ATP-dependent proteolysis of mitochondria of reticulocytes, Rev. Biol. Cell., 21, 505-521.

    CAS  Google Scholar 

  11. Klionsky, D. J., and Emr, S. D. (2000) Autophagy as a regulated pathway of cellular degradation, Science, 290, 1717-1721, https://doi.org/10.1126/science.290.5497.1717.

    Article  CAS  Google Scholar 

  12. Johnstone, R. M., Mathew, A., Mason, A. B., and Teng, K. (1991) Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins, J. Cell Physiol., 147, 27-36, https://doi.org/10.1002/jcp.1041470105.

    Article  CAS  Google Scholar 

  13. Yang, C., Endoh, M., Tan, D. Q., Nakamura-Ishizu, A., Takihara, Y., Matsumura, T., and Suda, T. (2021) Mitochondria transfer from early stages of erythroblasts to their macrophage niche via tunnelling nanotube, Br. J. Haematol., 193, 1260-1274, https://doi.org/10.1111/bjh.17531.

    Article  CAS  Google Scholar 

  14. Géminard, C., de Gassart, A., and Vidal, M. (2002) Reticulocyte maturation: mitoptosis and exosome release, Biocell, 26, 205-215, https://doi.org/10.32604/biocell.2002.26.205.

    Article  Google Scholar 

  15. Tovar, J., León-Avila, G., Sánchez, L. B., Sutak, R., Tachezy, J., van der Giezen, M., Hernández, M., Müller, M., and Lucocq, J. M. (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation, Nature, 426, 172-176, https://doi.org/10.1038/nature01945.

    Article  CAS  Google Scholar 

  16. Karnkowska, A., Vacek, V., Zubáčová, Z., Treitli, S. C., Petrželková, R., Eme, L., Novák, L., Žárský, V., Barlow, L. D., Herman, E. K., Soukal, P., Hroudová, M., Doležal, P., Stairs, C. W., Roger, A. J., Eliáš, M., Dacks, J. B., Vlček, Č., and Hampl, V. (2016) A eukaryote without a mitochondrial organelle, Curr Biol, 26, 1274-1284, https://doi.org/10.1016/j.cub.2016.03.053.

    Article  CAS  Google Scholar 

  17. John, U., Lu, Y., Wohlrab, S., Growth, M., Janouškovec, J., Kohli, G. S., Mark, F. C., Bickmeyer, U., Farhat, S., Felder, M., Frickenhaus, S., Guillou, L., Keeling, P. J., Moustafa, A., Porcel, B. M., Valentin, K., and Glöckner, G. (2019) An aerobic eukaryotic parasite with functional mitochondria that likely lacks a mitochondrial genome, Sci. Adv., 5, eaav1110, https://doi.org/10.1126/sciadv.aav1110.

    Article  CAS  Google Scholar 

  18. Kayal, E., and Smith, D. R. (2021) Is the dinoflagellate Amoebophrya really missing an mtDNA? Mol. Biol. Evol., 38, 2493-2496, https://doi.org/10.1093/molbev/msab041.

    Article  CAS  Google Scholar 

  19. Burki, F. (2016) Mitochondrial evolution: going, going, gone, Curr. Biol., 26, R410-R412, https://doi.org/10.1016/j.cub.2016.04.032.

    Article  CAS  Google Scholar 

  20. Rouault, T. A. (2012) Biogenesis of iron-sulfur clusters in mammalian cells: new insights and relevance to human disease, Dis. Model Mech., 5, 155-164, https://doi.org/10.1242/dmm.009019.

    Article  CAS  Google Scholar 

  21. Dempsey, M. E. (1974) Regulation of steroid biosynthesis, Annu. Rev. Biochem., 43, 967-990, https://doi.org/10.1146/annurev.bi.43.070174.004535.

    Article  CAS  Google Scholar 

  22. Salinas, G., Langelaan, D. N., and Shepherd, J. N. (2020) Rhodoquinone in bacteria and animals: Two distinct pathways for biosynthesis of this key electron transporter used in anaerobic bioenergetics, Biochim. Biophys. Acta Bioenerg., 1861, 148278, https://doi.org/10.1016/j.bbabio.2020.148278.

    Article  CAS  Google Scholar 

  23. Koppenol, W. H., Bounds, P. L., and Dang, C. V. (2011) Otto Warburg’s contributions to current concepts of cancer metabolism, Nat. Rev. Cancer, 11, 325-337, https://doi.org/10.1038/nrc3038.

    Article  CAS  Google Scholar 

  24. Mereschkowsky, C. (1905) Uber Natur und Ursprung der Chromatophoren im Pflanzenreiche [in Deutsch], Biologisches Zentralblatt, XXV (18), 593-604.

    Google Scholar 

  25. Famintsyn, A. S. (1907) On the Role of Symbiosis in the Evolution of Organisms [in Russian], Proc. Botanic. Lab. Imperial Acad. Sci., 20, 1-14.

    Google Scholar 

  26. Margulis, L. (1981) Symbiosis in Cell Evolution: Life and Its Environment on the Early Earth, Publisher: W. H. Freeman and Company, San Franscisco.

  27. Sagan, L. (1967) On the origin of mitosing cells, J. Theor. Biol., 14, 225-274, https://doi.org/10.1016/0022-5193(67)90079-3.

    Article  CAS  Google Scholar 

  28. Margulis, L., and Bermudes, D. (1985) Symbiosis as a mechanism of evolution: status of cell symbiosis theory, Symbiosis, 1, 101-124.

    CAS  Google Scholar 

  29. Gray, M. W. (1983) The bacterial ancestry of plastids and mitochondria, BioScience, 33, 693-699, https://doi.org/10.2307/1309349.

    Article  CAS  Google Scholar 

  30. 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 (Pt 1), 1-13, https://doi.org/10.1113/jphysiol.1995.sp020786.

    Article  Google Scholar 

  31. Roger, A. J., Muñoz-Gómez, S. A., and Kamikawa, R. (2017) The origin and diversification of mitochondria, Curr. Biol., 27, R1177-R1192, https://doi.org/10.1016/j.cub.2017.09.015.

    Article  CAS  Google Scholar 

  32. Zorov, D. B., Isaev, N. K., Plotnikov, E. Y., 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  Google Scholar 

  33. Abele, D. (2002) Toxic oxygen: The radical life-giver, Nature, 420, 27-27, https://doi.org/10.1038/420027a.

    Article  CAS  Google Scholar 

  34. Martin, W., and Mentel, M. (2010) The origin of mitochondria, Nat. Education, 3, 58.

    Google Scholar 

  35. Viale, A. M., and Arakaki, A. K. (1994) The chaperone connection to the origins of the eukaryotic organelles, FEBS Lett., 341, 146-151, https://doi.org/10.1016/0014-5793(94)80446-X.

    Article  CAS  Google Scholar 

  36. McLean, J. S., Bor, B., Kerns, K. A., Liu, Q., To, T. T., Solden, L., Hendrickson, E. L., Wrighton, K., Shi, W., and He, X. (2020) Acquisition and adaptation of ultra-small parasitic reduced genome bacteria to mammalian hosts, Cell Rep., 32, 107939, https://doi.org/10.1016/j.celrep.2020.107939.

    Article  CAS  Google Scholar 

  37. He, X., McLean, J. S., Edlund, A., Yooseph, S., Hall, A. P., Liu, S.-Y., Dorrestein, P. C., Esquenazi, E., Hunter, R. C., Cheng, G., et al. (2015) Cultivation of a human-associated TM7 phylotype reveals a reduced genome and epibiotic parasitic lifestyle, Proc. Natl. Acad. Sci. USA, 112, 244-249, https://doi.org/10.1073/pnas.1419038112.

    Article  CAS  Google Scholar 

  38. Amann, R., Ludwig, W., and Schleifer, K.-H. (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation, Microbiol. Rev., 59, 143-169, https://doi.org/10.1128/mr.59.1.143-169.1995.

    Article  CAS  Google Scholar 

  39. Vartoukian, S. R., Palmer, R. M., and Wade, W. G. (2010) Strategies for culture of “unculturable” bacteria, FEMS Microbiol. Lett., 309, 1-7, https://doi.org/10.1111/j.1574-6968.2010.02000.x.

    Article  CAS  Google Scholar 

  40. Portier, P. J. (1918) Les Symbiotes. French Edition, Masson (Paris), 1.

  41. Wallin, I. E. (1925) On the nature of mitochondria. IX. Demonstration of the bacterial nature of mitochondria, Am. J. Anat., 36, 131, https://doi.org/10.1002/aja.1000360106.

    Article  Google Scholar 

  42. Masuzawa, A., Black, K. M., Pacak, C. A., Ericsson, M., Barnett, R. J., Drumm, C., Seth, P., Bloch, D. B., Levitsky, S., Cowan, D. B., et al. (2013) Transplantation of autologously derived mitochondria protects the heart from ischemia-reperfusion injury, Am. J. Physiol. Heart Circ. Physiol., 304, H966-H982, https://doi.org/10.1152/ajpheart.00883.2012.

    Article  CAS  Google Scholar 

  43. 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., et al. (2018) Mitochondrial membrane potential, Anal. Biochem., 552, 50-59, https://doi.org/10.1016/j.ab.2017.07.009.

    Article  CAS  Google Scholar 

  44. Zorova, L. D., Demchenko, E. A., Korshunova, G. A., Tashlitsky, V. N., Zorov, S. D., Andrianova, N. V., Popkov, V. A., Babenko, V. A., Pevzner, I. B., Silachev, D. N., et al. (2022) Is the mitochondrial membrane potential (∆Ψ) correctly assessed? Intracellular and intramitochondrial modifications of the ∆Ψ probe, rhodamine 123, Int. J. Mol. Sci., 23, 482, https://doi.org/10.3390/ijms23010482.

    Article  CAS  Google Scholar 

  45. Andersson, S. G. E., Zomorodipour, A., Andersson, J. O., Sicheritz-Pontén, T., Alsmark, U. C. M., Podowski, R. M., Näslund, A. K., Eriksson, A.-S., Winkler, H. H., and Kurland, C. G. (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria, Nature, 396, 133-140, https://doi.org/10.1038/24094.

    Article  CAS  Google Scholar 

  46. Kurland, C. G., and Andersson, S. G. (2000) Origin and evolution of the mitochondrial proteome, Microbiol. Mol. Biol. Rev., 64, 786-820, https://doi.org/10.1128/MMBR.64.4.786-820.2000.

    Article  CAS  Google Scholar 

  47. Emelyanov, V. V. (2001) Evolutionary relationship of Rickettsiae and mitochondria, FEBS Lett., 501, 11-18, https://doi.org/10.1016/S0014-5793(01)02618-7.

    Article  CAS  Google Scholar 

  48. Emelyanov, V. V. (2003) Mitochondrial connection to the origin of the eukaryotic cell, Eur. J. Biochem., 270, 1599-1618, https://doi.org/10.1046/j.1432-1033.2003.03499.x.

    Article  CAS  Google Scholar 

  49. Fitzpatrick, D. A., Creevey, C. J., and McInerney, J. O. (2006) Genome phylogenies indicate a meaningful alpha-proteobacterial phylogeny and support a grouping of the mitochondria with the Rickettsiales, Mol. Biol. Evol., 23, 74-85, https://doi.org/10.1093/molbev/msj009.

    Article  CAS  Google Scholar 

  50. Driscoll, T. P., Verhoeve, V. I., Guillotte, M. L., Lehman, S. S., Rennoll, S. A., Beier-Sexton, M., Rahman, M. S., Azad, A. F., and Gillespie, J. J. (2017) Wholly Rickettsia! Reconstructed metabolic profile of the quintessential bacterial parasite of eukaryotic cells, mBio, 8, e00859-17, https://doi.org/10.1128/mBio.00859-17.

    Article  Google Scholar 

  51. Pallen, M. J. (2011) Time to recognize that mitochondria are bacteria? Trends Microbiol, 19, 58-64, https://doi.org/10.1016/j.tim.2010.11.001.

    Article  CAS  Google Scholar 

  52. Winkler, H. H., Neuhaus, H. E. (1999) Non-mitochondrial ATP transport, Trends Biochem. Sci., 24, 64-68, https://doi.org/10.1016/S0968-0004(98)01334-6.

    Article  CAS  Google Scholar 

  53. 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  CAS  Google Scholar 

  54. 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  Google Scholar 

  55. Skulachev, V. P., Bakeeva, L. E., Chernyak, B. V., Domnina, L. V., Minin, A. A., Pletjushkina, O. Y., Saprunova, V. B., Skulachev, I. V., Tsyplenkova, V. G., Vasiliev, J. M., et al. (2004) Thread-grain transition of mitochondrial reticulum as a step of mitoptosis and apoptosis, Mol. Cell Biochem., 256-257, 341-358, https://doi.org/10.1023/B:MCBI.0000009880.94044.49.

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  57. Youle, R. J., and van der Bliek, A. M. (2012) Mitochondrial fission, fusion, and stress, Science, 337, 1062-1065, https://doi.org/10.1126/science.1219855.

    Article  CAS  Google Scholar 

  58. Chen, H., Vermulst, M., Wang, Y. E., Chomyn, A., Prolla, T. A., McCaffery, J. M., and Chan, D. C. (2010) Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations, Cell, 141, 280-289, https://doi.org/10.1016/j.cell.2010.02.026.

    Article  CAS  Google Scholar 

  59. Drachev, V. A., and Zorov, D. B. (1986) Mitochondria as an electric cable. Experimental testing of a hypothesis, Dokl. Akad. Nauk SSSR, 287, 1237-1238.

    CAS  Google Scholar 

  60. 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.

    Article  CAS  Google Scholar 

  61. Skulachev, V. P. (2001) Mitochondrial filaments and clusters as intracellular power-transmitting cables, Trends Biochem. Sci., 26, 23-29, https://doi.org/10.1016/S0968-0004(00)01735-7.

    Article  CAS  Google Scholar 

  62. Bakeeva, L. E., Chentsov, Yu. 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  Google Scholar 

  63. Bakeeva, L. E., Chentsov, Y. S., and Skulachev, V. P. (1981) Ontogenesis of mitochondrial reticulum in rat diaphragm muscle, Eur. J. Cell Biol., 25, 175-181.

    CAS  Google Scholar 

  64. Eldarov, C. M., Vangely, I. M., Vays, V. B., Sheval, E. V., Holtze, S., Hildebrandt, T. B., Kolosova, N. G., Popkov, V. A., Plotnikov, E. Y., Zorov, D. B., et al. (2020) Mitochondria in the nuclei of rat myocardial cells, Cells, 9, 712, https://doi.org/10.3390/cells9030712.

    Article  CAS  Google Scholar 

  65. Khryapenkova, T. G., Plotnikov, E. Y., Korotetskaya, M. V., Sukhikh, G. T., and Zorov, D. B. (2008) Heterogeneity of mitochondrial potential as a marker for isolation of pure cardiomyoblast population, Bull. Exp. Biol. Med., 146, 506-511, https://doi.org/10.1007/s10517-009-0327-3.

    Article  CAS  Google Scholar 

  66. Popkov, V. A., Plotnikov, E. Y., Lyamzaev, K. G., Silachev, D. N., Zorova, L. D., Pevzner, I. B., Jankauskas, S. S., Zorov, S. D., Babenko, V. A., and Zorov, D. B. (2015) Mitodiversity, Biochemistry (Moscow), 80, 532-541, https://doi.org/10.1134/S000629791505003X.

    Article  CAS  Google Scholar 

  67. Smith, R. A., and Ord, M. J. (1983) Mitochondrial form and function relationships in vivo: their potential in toxicology and pathology, Int. Rev. Cytol., 83, 63-134, https://doi.org/10.1016/S0074-7696(08)61686-1.

    Article  CAS  Google Scholar 

  68. Wikstrom, J. D., Twig, G., and Shirihai, O. S. (2009) What can mitochondrial heterogeneity tell us about mitochondrial dynamics and autophagy? Int. J. Biochem. Cell Biol., 41, 1914-1927, https://doi.org/10.1016/j.biocel.2009.06.006.

    Article  CAS  Google Scholar 

  69. Kuznetsov, A. V., and Margreiter, R. (2009) Heterogeneity of mitochondria and mitochondrial function within cells as another level of mitochondrial complexity, Int. J. Mol. Sci., 10, 1911-1929, https://doi.org/10.3390/ijms10041911.

    Article  CAS  Google Scholar 

  70. Wikstrom, J. D., Katzman, S. M., Mohamed, H., Twig, G., Graf, S. A., Heart, E., Molina, A. J. A., Corkey, B. E., de Vargas, L. M., Danial, N. N., et al. (2007) beta-Cell mitochondria exhibit membrane potential heterogeneity that can be altered by stimulatory or toxic fuel levels, Diabetes, 56, 2569-2578, https://doi.org/10.2337/db06-0757.

    Article  CAS  Google Scholar 

  71. 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  CAS  Google Scholar 

  72. Hackenbrock, C. R. (1966) Ultrastructural bases for metabolically linked mechanical activity in mitochondria. I. Reversible ultrastructural changes with change in metabolic steady state in isolated liver mitochondria, J. Cell Biol., 30, 269-297, https://doi.org/10.1083/jcb.30.2.269.

    Article  CAS  Google Scholar 

  73. Hackenbrock, C. R. (1968) Ultrastructural bases for metabolically linked mechanical activity in mitochondria. II. Electron transport-linked ultrastructural transformations in mitochondria, J. Cell Biol., 37, 345-369, https://doi.org/10.1083/jcb.37.2.345.

    Article  CAS  Google Scholar 

  74. Hackenbrock, C. R. (1972) States of activity and structure in mitochondrial membranes, Ann. N Y Acad. Sci., 195, 492-504, https://doi.org/10.1111/j.1749-6632.1972.tb54831.x.

    Article  CAS  Google Scholar 

  75. 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  Google Scholar 

  76. Anusha-Kiran, Y., Mol, P., Dey, G., Bhat, F. A., Chatterjee, O., Deolankar, S. C., Philip, M., Prasad, T. S. K., Srinivas Bharath, M. M., and Mahadevan, A. (2022) Regional heterogeneity in mitochondrial function underlies region specific vulnerability in human brain ageing: Implications for neurodegeneration, Free Radic. Biol. Med., 193, 34-57, https://doi.org/10.1016/j.freeradbiomed.2022.09.027.

    Article  CAS  Google Scholar 

  77. Sakai, C., Tomitsuka, E., Esumi, H., Harada, S., and Kita, K. (2012) Mitochondrial fumarate reductase as a target of chemotherapy: from parasites to cancer cells, Biochim. Biophys. Acta, 1820, 643-651, https://doi.org/10.1016/j.bbagen.2011.12.013.

    Article  CAS  Google Scholar 

  78. Plotnikov, E. Y., Babenko, V. A., Silachev, D. N., Zorova, L. D., Khryapenkova, T. G., Savchenko, E. S., Pevzner, I. B., and Zorov, D. B. (2015) Intercellular transfer of mitochondria, Biochemistry (Moscow), 80, 542-548, https://doi.org/10.1134/S0006297915050041.

    Article  CAS  Google Scholar 

  79. Babenko, V. A., Silachev, D. N., Popkov, V. A., Zorova, L. D., Pevzner, I. B., Plotnikov, E. Y., Sukhikh, G. T., and Zorov, D. B. (2018) Miro1 enhances mitochondria transfer from multipotent mesenchymal stem cells (MMSC) to neural cells and improves the efficacy of cell recovery, Molecules, 23, 687, https://doi.org/10.3390/molecules23030687.

    Article  CAS  Google Scholar 

  80. Plotnikov, E. Y., Khryapenkova, T. G., Galkina, S. I., Sukhikh, G. T., and Zorov, D. B. (2010) Cytoplasm and organelle transfer between mesenchymal multipotent stromal cells and renal tubular cells in co-culture, Exp. Cell Res., 316, 2447-2455, https://doi.org/10.1016/j.yexcr.2010.06.009.

    Article  CAS  Google Scholar 

  81. Plotnikov, E. Y., Khryapenkova, T. G., Vasileva, A. K., Marey, M. V., Galkina, S. I., Isaev, N. K., Sheval, E. V., Polyakov, V. Y., Sukhikh, G. T., and Zorov, D. B. (2008) Cell-to-cell cross-talk between mesenchymal stem cells and cardiomyocytes in co-culture, J. Cell Mol. Med., 12, 1622-1631, https://doi.org/10.1111/j.1582-4934.2007.00205.x.

    Article  CAS  Google Scholar 

  82. Koyanagi, M., Brandes, R. P., Haendeler, J., Zeiher, A. M., and Dimmeler, S. (2005) Cell-to-cell connection of endothelial progenitor cells with cardiac myocytes by nanotubes: a novel mechanism for cell fate changes? Circ. Res., 96, 1039-1041, https://doi.org/10.1161/01.RES.0000168650.23479.0c.

    Article  CAS  Google Scholar 

  83. Rustom, A., Saffrich, R., Markovic, I., Walther, P., and Gerdes, H.-H. (2004) Nanotubular highways for intercellular organelle transport, Science, 303, 1007-1010, https://doi.org/10.1126/science.1093133.

    Article  CAS  Google Scholar 

  84. Plotnikov, E. Y., Silachev, D. N., Popkov, V. A., Zorova, L. D., Pevzner, I. B., Zorov, S. D., Jankauskas, S. S., Babenko, V. A., Sukhikh, G. T., and Zorov, D. B. (2017) Intercellular signalling cross-talk: To kill, to heal and to rejuvenate, Heart Lung Circ., 26, 648-659, https://doi.org/10.1016/j.hlc.2016.12.002.

    Article  Google Scholar 

  85. Babenko, V. A., Silachev, D. N., Zorova, L. D., Pevzner, I. B., Khutornenko, A. A., Plotnikov, E. Y., Sukhikh, G. T., and Zorov, D. B. (2015) Improving the post-stroke therapeutic potency of mesenchymal multipotent stromal cells by cocultivation with cortical neurons: The role of crosstalk between cells, Stem Cells Transl. Med., 4, 1011-1020, https://doi.org/10.5966/sctm.2015-0010.

    Article  CAS  Google Scholar 

  86. Frankenberg, G., Rogers, A. V., Mak, J. C. W., Halayko, A. J., Hui, C. K. M., Xu, B., Chung, K. F., Rodriguez, T., Michaeloudes, C., and Bhavsar, P. K. (2022) Mitochondrial transfer regulates bioenergetics in healthy and chronic obstructive pulmonary disease airway smooth muscle, Am. J. Respir. Cell. Mol. Biol., 67, 471-481, https://doi.org/10.1165/rcmb.2022-0041OC.

    Article  Google Scholar 

  87. Sinha, P., Islam, M.N., Bhattacharya, S., and Bhattacharya, J. (2016) Intercellular mitochondrial transfer: bioenergetic crosstalk between cells, Curr. Opin. Genet. Dev., 38, 97-101, https://doi.org/10.1016/j.gde.2016.05.002.

    Article  CAS  Google Scholar 

  88. Masuzawa, A., Black, K. M., Pacak, C. A., Ericsson, M., Barnett, R. J., Drumm, C., Seth, P., Bloch, D. B., Levitsky, S., Cowan, D. B., et al. (2013) Transplantation of autologously derived mitochondria protects the heart from ischemia-reperfusion injury, Am. J. Physiol. Heart Circ. Physiol., 304, H966-H982, https://doi.org/10.1152/ajpheart.00883.2012.

    Article  CAS  Google Scholar 

  89. Willingham, T. B., Ajayi, P. T., and Glancy, B. (2021) Subcellular specialization of mitochondrial form and function in skeletal muscle cells, Front. Cell Dev. Biol., 9, 757305, https://doi.org/10.3389/fcell.2021.757305.

    Article  Google Scholar 

  90. Ngo, J., Osto, C., Villalobos, F., and Shirihai, O. S. (2021) Mitochondrial heterogeneity in metabolic diseases, Biology (Basel), 10, 927, https://doi.org/10.3390/biology10090927.

    Article  CAS  Google Scholar 

  91. Gureev, A. P., Andrianova, N. V., Pevzner, I. B., Zorova, L. D., Chernyshova, E. V., Sadovnikova, I. S., Chistyakov, D. V., Popkov, V. A., Semenovich, D. S., Babenko, V. A., et al. (2022) Dietary restriction modulates mitochondrial DNA damage and oxylipin profile in aged rats, FEBS J., 289, 5697-5713, https://doi.org/10.1111/febs.16451.

    Article  CAS  Google Scholar 

  92. Santamaria, M., Lanave, C., Vicario, S., and Saccone, C. (2007) Variability of the mitochondrial genome in mammals at the inter-species/intra-species boundary, Biol. Chem., 388, 943-946, https://doi.org/10.1515/BC.2007.121.

    Article  CAS  Google Scholar 

  93. Aryaman, J., Johnston, I. G., and Jones, N. S. (2019) Mitochondrial heterogeneity, Front. Genet., 9, 718, https://doi.org/10.3389/fgene.2018.00718.

    Article  CAS  Google Scholar 

  94. Kopinski, P. K., Singh, L. N., Zhang, S., Lott, M. T., and Wallace, D. C. (2021) Mitochondrial DNA variation and cancer, Nat. Rev. Cancer, 21, 431-445, https://doi.org/10.1038/s41568-021-00358-w.

    Article  CAS  Google Scholar 

  95. Wallace, D. C. (2018) Mitochondrial genetic medicine, Nat. Genet., 50, 1642-1649, https://doi.org/10.1038/s41588-018-0264-z.

    Article  CAS  Google Scholar 

  96. Anderson, S., Bankier, A. T., Barrell, B. G., de Bruijn, M. H., Coulson, A. R., Drouin, J., Eperon, I. C., Nierlich, D. P., Roe, B. A., Sanger, F., et al. (1981) Sequence and organization of the human mitochondrial genome, Nature, 290, 457-465, https://doi.org/10.1038/290457a0.

    Article  CAS  Google Scholar 

  97. Van Goethem, G., Dermaut, B., Löfgren, A., Martin, J. J., and van Broeckhoven, C. (2001) Mutation of POLG is associated with progressive external ophthalmoplegia characterized by mtDNA deletions, Nat. Genet., 28, 211-212, https://doi.org/10.1038/90034.

    Article  CAS  Google Scholar 

  98. Spelbrink, J. N., Li, F. Y., Tiranti, V., Nikali, K., Yuan, Q. P., Tariq, M., Wanrooij, S., Garrido, N., Comi, G., Morandi, L., et al. (2001) Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria, Nat. Genet., 28, 223-231, https://doi.org/10.1038/90058.

    Article  CAS  Google Scholar 

  99. Goffart, S., Cooper, H. M., Tyynismaa, H., Wanrooij, S., Suomalainen, A., and Spelbrink, J. N. (2009) Twinkle mutations associated with autosomal dominant progressive external ophthalmoplegia lead to impaired helicase function and in vivo mtDNA replication stalling, Hum. Mol. Genet., 18, 328-340, https://doi.org/10.1093/hmg/ddn359.

    Article  CAS  Google Scholar 

  100. Holt, I. J., Harding, A. E., and Morgan-Hughes, J. A. (1988) Deletions of muscle mitochondrial DNA in patients with mitochondrial myopathies, Nature, 331, 717-719, https://doi.org/10.1038/331717a0.

    Article  CAS  Google Scholar 

  101. Moraes, C. T., DiMauro, S., Zeviani, M., Lombes, A., Shanske, S., Miranda, A. F., Nakase, H., Bonilla, E., Werneck, L. C., and Servidei, S. (1989) Mitochondrial DNA deletions in progressive external ophthalmoplegia and Kearns-Sayre syndrome, N. Engl. J. Med., 320, 1293-1299, https://doi.org/10.1056/NEJM198905183202001.

    Article  CAS  Google Scholar 

  102. Poulton, J., Deadman, M. E., and Gardiner, R. M. (1989) Duplications of mitochondrial DNA in mitochondrial myopathy, Lancet, 333, 236-240, https://doi.org/10.1016/S0140-6736(89)91256-7.

    Article  Google Scholar 

  103. Zaidi, A. A., Wilton, P. R., Su, M. S.-W., Paul, I. M., Arbeithuber, B., Anthony, K., Nekrutenko, A., Nielsen, R., and Makova, K. D. (2019) Bottleneck and selection in the germline and maternal age influence transmission of mitochondrial DNA in human pedigrees, Proc. Natl. Acad. Sci. USA, 116, 25172-25178, https://doi.org/10.1073/pnas.1906331116.

    Article  CAS  Google Scholar 

  104. Beck, E. A., Bassham, S., Cresko, W. A. (2022) Extreme intraspecific divergence in mitochondrial haplotypes makes the threespine stickleback fish an emerging evolutionary mutant model for mito-nuclear interactions, Front. Genet., 13, 925786, https://doi.org/10.3389/fgene.2022.925786.

    Article  CAS  Google Scholar 

  105. Torroni, A., Huoponen, K., Francalacci, P., Petrozzi, M., Morelli, L., Scozzari, R., Obinu, D., Savontaus, M. L., Wallace, D. C. (1996) Classification of european mtDNAs from an analysis of tree european populations, Genetics, 144, 1835-1850, https://doi.org/10.1093/genetics/144.4.1835.

    Article  CAS  Google Scholar 

  106. Van Oven, M., Kayser, M. (2009) Updated comprehensive phylogenetic tree of global human mitochondrial DNA variation, Hum. Mutat., 30, 386-394, https://doi.org/10.1002/humu.20921.

    Article  Google Scholar 

  107. Shapiro, L., McAdams, H. H., and Losick, R. (2002) Generating and exploiting polarity in bacteria, Science, 298, 1942-1946, https://doi.org/10.1126/science.1072163.

    Article  CAS  Google Scholar 

  108. Jazwinski, S. M. (2002) Growing old: metabolic control and yeast aging, Annu. Rev. Microbiol., 56, 769-792, https://doi.org/10.1146/annurev.micro.56.012302.160830.

    Article  CAS  Google Scholar 

  109. 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  Google Scholar 

Download references

Funding

The work was financially supported by the Russian Science Foundation (grant no. 19-14-00173-P).

Author information

Authors and Affiliations

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

    Dmitry B. Zorov, Ljubava D. Zorova, Nadezda V. Andrianova, Valentina A. Babenko, Savva D. Zorov, Irina B. Pevzner & Denis N. Silachev

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

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

  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. Ljubava D. Zorova
    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. Savva D. Zorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Irina B. Pevzner
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gennady T. Sukhikh
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Denis N. Silachev
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D. B. Zorov, G. T. Sukhikh, D. N. Silachev – concept; D. B. Zorov, N. V. Andrianova, V. A. Babenko, L. D. Zorova, S. D. Zorov, I. B. Pevzner, D. N. Silachev – discussion, editing of the concept, writing of the text; D. B. Zorov, D. N. Silachev – editing the text of the article.

Corresponding author

Correspondence to Dmitry B. Zorov.

Ethics declarations

The authors declare no conflict of interest in financial or any other sphere. This article does not describe any studies involving humans or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zorov, D.B., Zorova, L.D., Andrianova, N.V. et al. Isn’t It Time for Establishing Mitochondrial Nomenclature Breaking Mitochondrial Paradigm?. Biochemistry Moscow 87, 1487–1497 (2022). https://doi.org/10.1134/S0006297922120069

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297922120069

Keywords

Search

Navigation