Biochemistry (Moscow)

, Volume 79, Issue 10, pp 1017–1031 | Cite as

Microbiota and mitobiota. Putting an equal sign between mitochondria and bacteria

  • D. B. ZorovEmail author
  • E. Y. Plotnikov
  • D. N. Silachev
  • L. D. Zorova
  • I. B. Pevzner
  • S. D. Zorov
  • V. A. Babenko
  • S. S. Jankauskas
  • V. A. Popkov
  • P. S. Savina


The recent revival of old theories and setting them on modern scientific rails to a large extent are also relevant to mitochondrial science. Given the widespread belief that mitochondria are symbionts of ancient bacterial origin, the processes inherent to mitochondrial physiology can be revised based on their comparative analysis with possible involvement of bacteria. Such comparison combined with discussion of the role of microbiota in pathogenesis allows discussion of the role of “mitobiota” (we introduce this term) as the combination of different phenotypic manifestations of mitochondria in the organism reflecting pathological changes in the mitochondrial genome. When putting an equal sign between mitochondria and bacteria, we find similarity between the mitochondrial and bacterial theories of cancer. The presence of the term “bacterial infection” suggests “mitochondrial infection”, and mitochondrial (oxidative) theory of aging can in some way be transformed into a “bacterial theory of aging”. The possible existence of such processes and the data confirming their presence are discussed in this review. If such a comparison has the right to exist, the homeostasis of “mitobiota” is of not lesser physiological importance than homeostasis of microbiota, which has been so intensively discussed recently.

Key words

mitochondria ultrastructure bacteria microbiota mitobiota mitohormesis diseases inflammation cancer infection aging death phenoptosis 


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  1. 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.Google Scholar
  2. 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.Google Scholar
  3. 3.
    Henle, J. (1841) Mischungs und forbestandteile des menschlichen korpers, in Allgemeine Anatomie, Varlag Leopold Voss, Leipzig, pp. 573–613.Google Scholar
  4. 4.
    Kolliker, A. (1857) Einige bemerkungen uber die endigungen der hautnerven und den bau der muskein, Zwiss Zool., 8, 311–325.Google Scholar
  5. 5.
    Retzius, G. (1890) Muskelfibrille und sarcoplasma, Biol. Untersuchungen Neue Folge, 1, 51–88.Google Scholar
  6. 6.
    Cajal, S. (1888) Observations sur la texture des fibres musculaires des pattes et des ailes des insects, Int. Monatszeitschrift Anat. Physiol., 205–232, 253–276.Google Scholar
  7. 7.
    Regaud, C., and Favre, M. (1909) Granulations interstitielles et mitochondries des fibres musculaires striees, Compt. Rend., 148, 661–664.Google Scholar
  8. 8.
    Benda, C. (1900) Weitere beobachtungen uber die mitochondria und ihr verhaltnus zu sekretgranulationen nebst kritischen bemerkungen, Arch. Anat. Physiol., 24, 166–178.Google Scholar
  9. 9.
    Mereschkowski, C. (1905) Uber natur und ursprung der chromatophoren im pflanzenreiche, Biol. Centralbl., 25, 593–604.Google Scholar
  10. 10.
    Mereschkowsky, K. (1910) Theorie der zwei plasmaarten als grundlage der symbiogenesis, einer neuen lehre von der ent-stehung der organismen, Biol. Centralbl., 30, 353–367.Google Scholar
  11. 11.
    Schimper, A. (1883) Uber die entwicklung der chlorophyllkorner und farbkorper, Bot. Zeitung, 30, 105–114, 121–131, 137–146, 153–162.Google Scholar
  12. 12.
    Wallin, I. (1923) The mitochondria problem, Amer. Nat., 57, 255–261.Google Scholar
  13. 13.
    Wallin, I. (1927) Symbionticism and the origin of species, in The American Naturalist, Williams & Wilkins Company, Baltimore.Google Scholar
  14. 14.
    Sagan, L. (1967) On the origin of mitosing cells, J. Theor. Biol., 14, 255–274.PubMedGoogle Scholar
  15. 15.
    Margulis, L. (1971) Symbiosis and evolution, Sci. Am., 225, 48–57.PubMedGoogle Scholar
  16. 16.
    Harada, S., Inaoka, D. K., Ohmori, J., and Kita, K. (2013) Diversity of parasite complex II, Biochim. Biophys. Acta, 1827, 658–667.PubMedGoogle Scholar
  17. 17.
    Collins, T. J., Berridge, M. J., Lipp, P., and Bootman, M. D. (2002) Mitochondria are morphologically and functionally heterogeneous within cells, EMBO J., 21, 1616–1627.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Sutovsky, P., Moreno, R. D., Ramalho-Santos, J., Dominko, T., Simerly, C., and Schatten, G. (1999) Ubiquitin tag for sperm mitochondria, Nature, 402, 371–372.PubMedGoogle Scholar
  19. 19.
    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.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Hawrelak, J. A., and Myers, S. P. (2004) The causes of intestinal dysbiosis: a review, Altern. Med. Rev., 9, 180–197.PubMedGoogle Scholar
  21. 21.
    Kuhne, L. (1893) Die neue Heilwissenschaft oder die Lehre von der Einheit aller Krankheiten und deren darauf begrundete einheitliche, arzneilose und operationslose Heilung, Verlag von Louis Kuhne, Leipzig.Google Scholar
  22. 22.
    Mechnikov, I. (1915) On the Nature of Man [in Russian], Nauchnoe Slovo.Google Scholar
  23. 23.
    Dominguez, J. A., and Coopersmith, C. M. (2010) Can we protect the gut in critical illness? The role of growth factors and other novel approaches, Crit. Care Clin., 26, 549–565.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Schwartz, R. F., Neu, J., Schatz, D., Atkinson, M. A., and Wasserfall, C. (2007) Comment on: Brugman, S., et al. (2006) Antibiotic treatment partially protects against type 1 diabetes in the bio-breeding diabetes-prone rat. Is the gut flora involved in the development of type 1 diabetes? Diabetologia, 50, 220–221.PubMedGoogle Scholar
  25. 25.
    Cani, P. D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A. M., Delzenne, N. M., and Burcelin, R. (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat-diet-induced obesity and diabetes in mice, Diabetes, 57, 1470–1481.PubMedGoogle Scholar
  26. 26.
    Cani, P. D., Neyrinck, A. M., Fava, F., Knauf, C., Burcelin, R. G., Tuohy, K. M., Gibson, G. R., and Delzenne, N. M. (2007) Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxemia, Diabetologia, 50, 2374–2383.PubMedGoogle Scholar
  27. 27.
    Bukowska, H., Pieczul-Mroz, J., Jastrzebska, M., Chelstowski, K., and Naruszewicz, M. (1998) Decrease in fibrinogen and LDL-cholesterol levels upon supplementation of diet with Lactobacillus plantarum in subjects with moderately elevated cholesterol, Atherosclerosis, 137, 437–438.PubMedGoogle Scholar
  28. 28.
    Shimizu, K., Ogura, H., Goto, M., Asahara, T., Nomoto, K., Morotomi, M., Yoshiya, K., Matsushima, A., Sumi, Y., Kuwagata, Y., Tanaka, H., Shimazu, T., and Sugimoto, H. (2006) Altered gut flora and environment in patients with severe SIRS, J. Trauma, 60, 126–133.PubMedGoogle Scholar
  29. 29.
    Maejima, K., Deitch, E., and Berg, R. (1984) Promotion by burn stress of the translocation of bacteria from the gastrointestinal tracts of mice, Arch. Surg., 119, 166–172.PubMedGoogle Scholar
  30. 30.
    Maejima, K., Deitch, E. A., and Berg, R. D. (1984) Bacterial translocation from the gastrointestinal tracts of rats receiving thermal injury, Infect. Immun., 43, 6–10.PubMedPubMedCentralGoogle Scholar
  31. 31.
    LeVoyer, T., Cioffi, W. G., Jr., Pratt, L., Shippee, R., McManus, W. F., Mason, A. D., Jr., and Pruitt, B. A., Jr. (1992) Alterations in intestinal permeability after thermal injury, Arch. Surg., 127, 26–29, discussion 29–30.PubMedGoogle Scholar
  32. 32.
    Bolte, E. R. (1998) Autism and Clostridium tetani, Med. Hypotheses, 51, 133–144.PubMedGoogle Scholar
  33. 33.
    Finegold, S. M., Molitoris, D., Song, Y., Liu, C., Vaisanen, M. L., Bolte, E., McTeague, M., Sandler, R., Wexler, H., Marlowe, E. M., Collins, M. D., Lawson, P. A., Summanen, P., Baysallar, M., Tomzynski, T. J., Read, E., Johnson, E., Rolfe, R., Nasir, P., Shah, H., Haake, D. A., Manning, P., and Kaul, A. (2002) Gastrointestinal microflora studies in late-onset autism, Clin. Infect. Dis., 35, S6-S16.Google Scholar
  34. 34.
    McKeever, T. M., Lewis, S. A., Smith, C., Collins, J., Heatlie, H., Frischer, M., and Hubbard, R. (2002) Early exposure to infections and antibiotics and the incidence of allergic disease: a birth cohort study with the West Midlands General Practice Research Database, J. Allergy Clin. Immunol., 109, 43–50.PubMedGoogle Scholar
  35. 35.
    Sekirov, I., Russell, S. L., Antunes, L. C., and Finlay, B. B. (2010) Gut microbiota in health and disease, Physiol. Rev., 90, 859–904.PubMedGoogle Scholar
  36. 36.
    Angus, D. C. (2011) The search for effective therapy for sepsis: back to the drawing board? J. Am. Med. Assoc., 306, 2614–2615.Google Scholar
  37. 37.
    Cauwels, A., Rogge, E., Vandendriessche, B., Shiva, S., and Brouckaert, P. (2014) Extracellular ATP drives systemic inflammation, tissue damage and mortality, Cell Death Dis., 5, e1102.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Skulachev, V. P. (2002) Programmed death phenomena: from organelle to organism, Ann. NY Acad. Sci., 959, 214–237.PubMedGoogle Scholar
  39. 39.
    Agteresch, H. J., Dagnelie, P. C., van den Berg, J. W., and Wilson, J. H. (1999) Adenosine triphosphate: established and potential clinical applications, Drugs, 58, 211–232.PubMedGoogle Scholar
  40. 40.
    Murry, C. E., Jennings, R. B., and Reimer, K. A. (1986) Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium, Circulation, 74, 1124–1136.PubMedGoogle Scholar
  41. 41.
    LeBlanc, J., Roberge, C., Valliere, J., and Oakson, G. (1971) The sympathetic nervous system in short-term adaptation to cold, Can. J. Physiol. Pharmacol., 49, 96–101.PubMedGoogle Scholar
  42. 42.
    Yun, J., and Finkel, T. (2014) Mitohormesis, Cell Metab., 19, 757–766.PubMedGoogle Scholar
  43. 43.
    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.PubMedGoogle Scholar
  44. 44.
    Cunha, F. M., Caldeira da Silva, C. C., Cerqueira, F. M., and Kowaltowski, A. J. (2011) Mild mitochondrial uncoupling as a therapeutic strategy, Curr. Drug Targets, 12, 783–789.PubMedGoogle Scholar
  45. 45.
    Abbracchio, M. P., Burnstock, G., Verkhratsky, A., and Zimmermann, H. (2009) Purinergic signalling in the nervous system: an overview, Trends Neurosci., 32, 19–29.PubMedGoogle Scholar
  46. 46.
    Krysko, O., Love Aaes, T., Bachert, C., Vandenabeele, P., and Krysko, D. V. (2013) Many faces of DAMPs in cancer therapy, Cell Death Dis., 4, e631.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Boya, P., Roques, B., and Kroemer, G. (2001) New EMBO members’ review: viral and bacterial proteins regulating apoptosis at the mitochondrial level, EMBO J., 20, 4325–4331.PubMedPubMedCentralGoogle Scholar
  48. 48.
    Kozjak-Pavlovic, V., Ross, K., and Rudel, T. (2008) Import of bacterial pathogenicity factors into mitochondria, Curr. Opin. Microbiol., 11, 9–14.PubMedGoogle Scholar
  49. 49.
    Kroemer, G., Galluzzi, L., and Brenner, C. (2007) Mitochondrial membrane permeabilization in cell death, Physiol. Rev., 87, 99–163.PubMedGoogle Scholar
  50. 50.
    Skulachev, V. P. (2000) Mitochondria in the programmed death phenomena; a principle of biology: “it is better to die than to be wrong”, Life, 49, 365–373.PubMedGoogle Scholar
  51. 51.
    Macbride, D. (1772) A Methodical Introduction to the Theory and Practice of Physic, Science.Google Scholar
  52. 52.
    Onuigbo, W. I. (1975) Some nineteenth century ideas on links between tuberculous and cancerous diseases of the lung, Br. J. Dis. Chest, 69, 207–210.PubMedGoogle Scholar
  53. 53.
    Broxmeyer, L. (2004) Is cancer just an incurable infectious disease? Med. Hypotheses, 63, 986–996.PubMedGoogle Scholar
  54. 54.
    Virchow, R. (1860) Cellular Pathology, Churchill, London.Google Scholar
  55. 55.
    Virchow, R. (1863) Die Krankhaften Geschwulste, August Hirshwald, Berlin.Google Scholar
  56. 56.
    Balkwill, F., and Mantovani, A. (2001) Inflammation and cancer: back to Virchow? Lancet, 357, 539–545.PubMedGoogle Scholar
  57. 57.
    Morrison, W. B. (2012) Inflammation and cancer: a comparative view, J. Vet. Intern. Med., 26, 18–31.PubMedGoogle Scholar
  58. 58.
    Bierne, H., Hamon, M., and Cossart, P. (2014) Epigenetics and bacterial infections, Cold Spring Harb. Perspect. Med., 2, a010272.Google Scholar
  59. 59.
    Gaylord, H. R. (1901) The protozoon of cancer. A preliminary report based upon three years’ work in the New York State Pathological Laboratory of the University of Buffalo, Am. J. Med. Sci., 121, 503–539.Google Scholar
  60. 60.
    Wainwright, A. M. (2006) The potential role of non-virus microorganisms in cancer, Curr. Trends Microbiol., 48-59.Google Scholar
  61. 61.
    Peter, S., and Beglinger, C. (2007) Helicobacter pylori and gastric cancer: the causal relationship, Digestion, 75, 25–35.PubMedGoogle Scholar
  62. 62.
    Correa, P., and Houghton, J. (2007) Carcinogenesis of Helicobacter pylori, Gastroenterology, 133, 659–672.PubMedGoogle Scholar
  63. 63.
    Hussell, T., Isaacson, P. G., Crabtree, J. E., and Spencer, J. (1993) The response of cells from low-grade B-cell gastric lymphomas of mucosa-associated lymphoid tissue to Helicobacter pylori, Lancet, 342, 571–574.PubMedGoogle Scholar
  64. 64.
    Mc, C. W., and Mason, J. M., 3rd (1951) Enterococcal endocarditis associated with carcinoma of the sigmoid: report of a case, J. Med. Assoc. State Ala., 21, 162–166.Google Scholar
  65. 65.
    Littman, A. J., Jackson, L. A., and Vaughan, T. L. (2005) Chlamydia pneumoniae and lung cancer: epidemiological evidence, Cancer Epidemiol. Biomarkers Prev., 14, 773–778.PubMedGoogle Scholar
  66. 66.
    Littman, A. J., White, E., Jackson, L. A., Thornquist, M. D., Gaydos, C. A., Goodman, G. E., and Vaughan, T. L. (2004) Chlamydia pneumoniae infection and risk of lung cancer, Cancer Epidemiol. Biomarkers Prevent., 13, 1624–1630.Google Scholar
  67. 67.
    Kovalchuk, O., Walz, P., and Kovalchuk, I. (2014) Does bacterial infection cause genome instability and cancer in the host cell? Mutat. Res., 761C, 1–14.Google Scholar
  68. 68.
    Parsonnet, J. (1995) Bacterial infection as a cause of cancer, Environ. Health Perspect., 103, Suppl. 8, 263–268.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Szent-Gyorgyi, A. (1977) The living state and cancer, Proc. Natl. Acad. Sci. USA, 74, 2844–2847.PubMedPubMedCentralGoogle Scholar
  70. 70.
    Warburg, O. (1956) On the origin of cancer cells, Science, 123, 309–314.PubMedGoogle Scholar
  71. 71.
    Zorov, D. B. (1996) Mitochondrial damage as a source of diseases and aging: a strategy of how to fight these, Biochim. Biophys. Acta, 1275, 10–15.PubMedGoogle Scholar
  72. 72.
    Zorov, D. B., Krasnikov, B. F., Kuzminova, A. E., Vysokikh, M., and Zorova, L. D. (1997) Mitochondria revisited. Alternative functions of mitochondria, Biosci. Rep., 17, 507–520.PubMedGoogle Scholar
  73. 73.
    Ramanathan, A., Wang, C., and Schreiber, S. L. (2005) Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements, Proc. Natl. Acad. Sci. USA, 102, 5992–5997.PubMedPubMedCentralGoogle Scholar
  74. 74.
    Mayevsky, A. (2009) Mitochondrial function and energy metabolism in cancer cells: past overview and future perspectives, Mitochondrion, 9, 165–179.PubMedGoogle Scholar
  75. 75.
    Seyfried, T. N., and Shelton, L. M. (2010) Cancer as a metabolic disease, Nutr. Metab. (Lond.), 7, 7.Google Scholar
  76. 76.
    Roskelley, R. C., Mayer, N., Horwitt, B. N., and Salter, W. T. (1943) Studies in cancer. VII. Enzyme deficiency in human and experimental cancer, J. Clin. Invest., 22, 743–751.PubMedPubMedCentralGoogle Scholar
  77. 77.
    John, A. P. (2001) Dysfunctional mitochondria, not oxygen insufficiency, cause cancer cells to produce inordinate amounts of lactic acid: the impact of this on the treatment of cancer, Med. Hypotheses, 57, 429–431.PubMedGoogle Scholar
  78. 78.
    Galluzzi, L., Morselli, E., Kepp, O., Vitale, I., Rigoni, A., Vacchelli, E., Michaud, M., Zischka, H., Castedo, M., and Kroemer, G. (2010) Mitochondrial gateways to cancer, Mol. Aspects Med., 31, 1–20.PubMedGoogle Scholar
  79. 79.
    Cuezva, J. M., Krajewska, M., de Heredia, M. L., Krajewski, S., Santamaria, G., Kim, H., Zapata, J. M., Marusawa, H., Chamorro, M., and Reed, J. C. (2002) The bioenergetic signature of cancer: a marker of tumor progression, Cancer Res., 62, 6674–6681.PubMedGoogle Scholar
  80. 80.
    Welter, C., Kovacs, G., Seitz, G., and Blin, N. (1989) Alteration of mitochondrial DNA in human oncocytomas, Genes Chromosomes Cancer, 1, 79–82.PubMedGoogle Scholar
  81. 81.
    Savagner, F., Franc, B., Guyetant, S., Rodien, P., Reynier, P., and Malthiery, Y. (2001) Defective mitochondrial ATP synthesis in oxyphilic thyroid tumors, J. Clin. Endocrinol. Metab., 86, 4920–4925.PubMedGoogle Scholar
  82. 82.
    Simonnet, H., Alazard, N., Pfeiffer, K., Gallou, C., Beroud, C., Demont, J., Bouvier, R., Schagger, H., and Godinot, C. (2002) Low mitochondrial respiratory chain content correlates with tumor aggressiveness in renal cell carcinoma, Carcinogenesis, 23, 759–768.PubMedGoogle Scholar
  83. 83.
    Bonora, E., Porcelli, A. M., Gasparre, G., Biondi, A., Ghelli, A., Carelli, V., Baracca, A., Tallini, G., Martinuzzi, A., Lenaz, G., Rugolo, M., and Romeo, G. (2006) Defective oxidative phosphorylation in thyroid oncocytic carcinoma is associated with pathogenic mitochondrial DNA mutations affecting complexes I and III, Cancer Res., 66, 6087–6096.PubMedGoogle Scholar
  84. 84.
    Demasi, A. P., Furuse, C., Altemani, A., Junqueira, J. L., Oliveira, P. R., and Araujo, V. C. (2009) Peroxiredoxin I is overexpressed in oncocytic lesions of salivary glands, J. Oral Pathol. Med., 38, 514–517.PubMedGoogle Scholar
  85. 85.
    Israel, B. A., and Schaeffer, W. I. (1987) Cytoplasmic suppression of malignancy, In vitro Cell Dev. Biol., 23, 627–632.PubMedGoogle Scholar
  86. 86.
    Raetz, C. R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins, Annu. Rev. Biochem., 71, 635–700.PubMedPubMedCentralGoogle Scholar
  87. 87.
    Wang, X., and Quinn, P. J. (2010) Endotoxins: lipopolysaccharides of gram-negative bacteria, Subcell. Biochem., 53, 3–25.PubMedGoogle Scholar
  88. 88.
    Heumann, D., and Roger, T. (2002) Initial responses to endotoxins and Gram-negative bacteria, Clin. Chim. Acta, 323, 59–72.PubMedGoogle Scholar
  89. 89.
    Remick, D. G., and Ward, P. A. (2005) Evaluation of endotoxin models for the study of sepsis, Shock, 24,Suppl. 1, 7–11.PubMedGoogle Scholar
  90. 90.
    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.PubMedGoogle Scholar
  91. 91.
    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.PubMedGoogle Scholar
  92. 92.
    Plotnikov, E. Y., Pulkova, N. V., Pevzner, I. B., Zorova, L. D., Silachev, D. N., Morosanova, M. A., Sukhikh, G. T., and Zorov, D. B. (2013) Inflammatory pre-conditioning of mesenchymal multipotent stromal cells improves their immunomodulatory potency in acute pyelonephritis in rats, Cytotherapy, 15, 679–689.PubMedGoogle Scholar
  93. 93.
    Prockop, D. J. (2012) Mitochondria to the rescue, Nature Med., 18, 653–654.PubMedGoogle Scholar
  94. 94.
    Spees, J. L., Olson, S. D., Whitney, M. J., and Prockop, D. J. (2006) Mitochondrial transfer between cells can rescue aerobic respiration, Proc. Natl. Acad. Sci. USA, 103, 1283–1288.PubMedPubMedCentralGoogle Scholar
  95. 95.
    Csordas, A. (2006) Mitochondrial transfer between eukaryotic animal cells and its physiologic role, Rejuvenation Res., 9, 450–454.PubMedGoogle Scholar
  96. 96.
    Mileshina, D., Ibrahim, N., Boesch, P., Lightowlers, R. N., Dietrich, A., and Weber-Lotfi, F. (2011) Mitochondrial transfection for studying organellar DNA repair, genome maintenance and aging, Mech. Ageing Dev., 132, 412–423.PubMedGoogle Scholar
  97. 97.
    Zhang, Q., Itagaki, K., and Hauser, C. J. (2010) Mitochondrial DNA is released by shock and activates neutrophils via p38 map kinase, Shock, 34, 55–59.PubMedGoogle Scholar
  98. 98.
    Clark, M. A., and Shay, J. W. (1982) Mitochondrial transformation of mammalian cells, Nature, 295, 605–607.PubMedGoogle Scholar
  99. 99.
    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.PubMedPubMedCentralGoogle Scholar
  100. 100.
    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.PubMedPubMedCentralGoogle Scholar
  101. 101.
    Medzhitov, R., Preston-Hurlburt, P., and Janeway, C. A., Jr. (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity, Nature, 388, 394–397.PubMedGoogle Scholar
  102. 102.
    Wright, S. D. (1999) Toll, a new piece in the puzzle of innate immunity, J. Exp. Med., 189, 605–609.PubMedPubMedCentralGoogle Scholar
  103. 103.
    Krysko, D. V., Agostinis, P., Krysko, O., Garg, A. D., Bachert, C., Lambrecht, B. N., and Vandenabeele, P. (2011) Emerging role of damage-associated molecular patterns derived from mitochondria in inflammation, Trends Immunol., 32, 157–164.PubMedGoogle Scholar
  104. 104.
    Harman, D. (1956) Aging: a theory based on free radical and radiation chemistry, J. Gerontol., 11, 298–300.PubMedGoogle Scholar
  105. 105.
    Harman, D. (1992) Free radical theory of aging, Mutat. Res., 275, 257–266.PubMedGoogle Scholar
  106. 106.
    Vina, J., Borras, C., Abdelaziz, K. M., Garcia-Valles, R., and Gomez-Cabrera, M. C. (2013) The free radical theory of aging revisited: the cell signaling disruption theory of aging, Antioxid. Redox Signal., 19, 779–787.PubMedPubMedCentralGoogle Scholar
  107. 107.
    Barja, G. (2013) Updating the mitochondrial free radical theory of aging: an integrated view, key aspects, and confounding concepts, Antioxid. Redox Signal., 19, 1420–1445.PubMedGoogle Scholar
  108. 108.
    Liochev, S. I. (2013) Reactive oxygen species and the free radical theory of aging, Free Radic. Biol. Med., 60, 1–4.PubMedGoogle Scholar
  109. 109.
    Perez, V. I., Bokov, A., Van Remmen, H., Mele, J., Ran, Q., Ikeno, Y., and Richardson, A. (2009) Is the oxidative stress theory of aging dead? Biochim. Biophys. Acta, 1790, 1005–1014.PubMedPubMedCentralGoogle Scholar
  110. 110.
    Lapointe, J., and Hekimi, S. (2010) When a theory of aging ages badly, Cell Mol. Life Sci., 67, 1–8.PubMedPubMedCentralGoogle Scholar
  111. 111.
    Speakman, J. R., and Selman, C. (2011) The free-radical damage theory: accumulating evidence against a simple link of oxidative stress to ageing and lifespan, BioEssays: News Rev. Mol. Cell. Devel. Biol., 33, 255–259.Google Scholar
  112. 112.
    Gladyshev, V. N. (2014) The free radical theory of aging is dead. Long live the damage theory! Antioxid. Redox Signal., 20, 727–731.PubMedGoogle Scholar
  113. 113.
    Kirkwood, T. B., and Kowald, A. (2012) The free-radical theory of ageing — older, wiser and still alive: modelling positional effects of the primary targets of ROS reveals new support, BioEssays: News Rev. Mol. Cell. Devel. Biol., 34, 692–700.Google Scholar
  114. 114.
    Heintz, C., and Mair, W. (2014) You are what you host: microbiome modulation of the aging process, Cell, 156, 408–411.PubMedGoogle Scholar
  115. 115.
    Zhang, R., and Hou, A. (2013) Host-microbe interactions in Caenorhabditis elegans, ISRN Microbiol., DOI.10.1155/2013/356451.Google Scholar
  116. 116.
    Bakeeva, L. E., Chentsov Yu. S., and Skulachev, V. P. (1983) Intermitochondrial contacts in myocardiocytes, J. Mol. Cell Cardiol., 15, 413–420.PubMedGoogle Scholar
  117. 117.
    Suzuki, T., and Mostofi, F. K. (1967) Intramitochondrial filamentous bodies in the thick limb of henle of the rat kidney, J. Cell Biol., 33, 605–623.PubMedPubMedCentralGoogle Scholar
  118. 118.
    Sarnat, H. B., Flores-Sarnat, L., Casey, R., Scott, P., and Khan, A. (2012) Endothelial ultrastructural alterations of intramuscular capillaries in infantile mitochondrial cytopathies: “mitochondrial angiopathy”, Neuropathology, 32, 617–627.PubMedGoogle Scholar
  119. 119.
    Hawkins, W. E., Howse, H. D., and Foster, C. A. (1980) Prismatic cristae and paracrystalline inclusions in mitochondria of myocardial cells of the oyster Crassostrea virginica Gmelin, Cell Tissue Res., 209, 87–94.PubMedGoogle Scholar
  120. 120.
    Behbehani, A. W., Goebel, H., Osse, G., Gabriel, M., Langenbeck, U., Berden, J., Berger, R., and Schutgens, R. B. (1984) Mitochondrial myopathy with lactic acidosis and deficient activity of muscle succinate cytochrome-c-oxidoreductase, Eur. J. Pediatr., 143, 67–71.PubMedGoogle Scholar
  121. 121.
    Buell, R., Wang, N. S., Seemayer, T. A., and Ahmed, M. N. (1976) Endobronchial plasma cell granuloma (xanthomatous pseudotumor); a light and electron microscopic study, Hum. Pathol., 7, 411–426.PubMedGoogle Scholar
  122. 122.
    Blinzinger, K., Rewcastle, N. B., and Hager, H. (1965) Observations on prismatic-type mitochondria within astrocytes of the Syrian hamster brain, J. Cell Biol., 25, 293–303.PubMedPubMedCentralGoogle Scholar
  123. 123.
    Vital, A., and Vital, C. (2012) Mitochondria and peripheral neuropathies, J. Neuropathol. Exp. Neurol., 71, 1036–1046.PubMedGoogle Scholar
  124. 124.
    Van Ekeren, G. J., Stadhouders, A. M., Egberink, G. J., Sengers, R. C., Daniels, O., and Kubat, K. (1987) Hereditary mitochondrial hypertrophic cardiomyopathy with mitochondrial myopathy of skeletal muscle, congenital cataract and lactic acidosis, Virchows Arch. Pathol. Anat. Histopathol., 412, 47–52.Google Scholar
  125. 125.
    Andersson-Cedergren, E. (1959) Ultrastructure of motor end plate and sarcoplasmic components of mouse skeletal muscle fiber as revealed by three-dimensional reconstructions from serial sections, J. Ultrastruct. Res., 2,Suppl. 1, 5–191.Google Scholar
  126. 126.
    Mannella, C. A., Marko, M., and Buttle, K. (1997) Reconsidering mitochondrial structure: new views of an old organelle, TIBS, 22, 37–38.PubMedGoogle Scholar
  127. 127.
    Daems, W. T., and Wisse, E. (1966) Shape and attachment of the cristae mitochondriales in mouse hepatic cell mitochondria, J. Ultrastruct. Res., 16, 123–140.PubMedGoogle Scholar
  128. 128.
    Sun, C. N., White, H. J., and Thompson, B. W. (1975) Oncocytoma (mitochondrioma) of the parotid gland. An electron microscopical study, Arch. Pathol., 99, 208–214.PubMedGoogle Scholar
  129. 129.
    Bannasch, P., Krech, R., and Zerban, H. (1978) Morphogenese und micromorphologie epithelialer nierentumoren bei nitrosomorpholin-vergifteten ratten. III. Oncocytentubuli und oncocytomas, Zeitschrift Krebsforschung Klin. Onkol. (Cancer Res. Clin. Oncol.), 92, 87–104.Google Scholar
  130. 130.
    Bonikos, D. S., Bensch, K. G., Watt, T., and Northway, W. H. (1977) Pulmonary oncocytes in prolonged hyperoxia, Exp. Mol. Pathol., 26, 92–102.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2014

Authors and Affiliations

  • D. B. Zorov
    • 1
    Email author
  • E. Y. Plotnikov
    • 1
  • D. N. Silachev
    • 1
  • L. D. Zorova
    • 2
  • I. B. Pevzner
    • 3
  • S. D. Zorov
    • 3
  • V. A. Babenko
    • 3
  • S. S. Jankauskas
    • 3
  • V. A. Popkov
    • 3
  • P. S. Savina
    • 4
  1. 1.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia
  2. 2.International Laser CenterLomonosov Moscow State UniversityMoscowRussia
  3. 3.Faculty of Bioengineering and BioinformaticsLomonosov Moscow State UniversityMoscowRussia
  4. 4.Biological FacultyEltsyn Ural Federal UniversityEkaterinburgRussia

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