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Biochemistry (Moscow)

, Volume 81, Issue 4, pp 329–337 | Cite as

Mitochondria as a signaling Hub and target for phenoptosis shutdown

  • P. V. Zolotukhin
  • A. A. Belanova
  • E. V. Prazdnova
  • M. S. Mazanko
  • M. M. Batiushin
  • V. K. Chmyhalo
  • V. A. ChistyakovEmail author
Review

Abstract

Mitochondria have long been studied as the main energy source and one of the most important generators of reactive oxygen species in the eukaryotic cell. Yet, new data suggest mitochondria serve as a powerful cellular regulator, pathway trigger, and signal hub. Some of these crucial mitochondrial functions appear to be associated with RNP-granules. Deep and versatile involvement of mitochondria in general cellular regulation may be the legacy of parasitic behavior of the ancestors of mitochondria in the host cells. In this regard, we also discuss here the perspectives of using mitochondria-targeted compounds for systemic correction of phenoptotic shifts.

Keywords

mitochondria regulation systems biology mitochondrial targeting Skulachev ions phenoptosis 

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References

  1. 1.
    Emster, L., and Schartz, G. (1981) Mitochondria: a historical review, J. Cell Biol., 91, 227–255.CrossRefGoogle Scholar
  2. 2.
    Skulachev, V. P. (2005) How to clean the dirtiest place in the cell: cationic antioxidants as intramitochondrial ROS scavengers, IUBMB Life, 57, 305–310.CrossRefPubMedGoogle Scholar
  3. 3.
    Skulachev, V. P. (2009) How to cancel the organism aging program? Ros. Khim. Zh., 53, 125–140.Google Scholar
  4. 4.
    Skulachev, V. P. (2011) Aging as a particular case of phenoptosis, the programmed death of an organism (a response to Kirkwood and Melov “On the programmed/non-programmed nature of ageing within the life history”), Aging (Albany, N. Y.), 3, 1120–1123.Google Scholar
  5. 5.
    Skulachev, V. P. (2012) What is phenoptosis and how to fight it? Biochemistry (Moscow), 77, 689–706.PubMedGoogle Scholar
  6. 6.
    Schapira, A. H. (2006) Mitochondrial disease, Lancet, 368, 70–82.CrossRefPubMedGoogle Scholar
  7. 7.
    Otten, A. B., and Smeets, H. J. (2015) Evolutionary defined role of the mitochondrial DNA in fertility, disease and ageing, Hum. Reprod. Update, 21, 671–689.CrossRefPubMedGoogle Scholar
  8. 8.
    Govindaraj, P., Khan, N. A., Gopalakrishna, P., Chandra, R. V., Vanniarajan, A., Reddy, A. A., Singh, S., Kumaresan, R., Srinivas, G., Singh, L., and Thangaraj, K. (2011) Mitochondrial dysfunction and genetic heterogeneity in chronic periodontitis, Mitochondrion, 11, 504–512.CrossRefPubMedGoogle Scholar
  9. 9.
    Schulz, J. B., Lindenau, J., Seyfried, J., and Dichgans, J. (2000) Glutathione, oxidative stress and neurodegeneration, Eur. J. Biochem., 267, 4904–4911.CrossRefPubMedGoogle Scholar
  10. 10.
    Mariani, E., Polidori, M. C., Cherubini, A., and Mecocci, P. (2005) Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview, J. Chromatogr. B Anal. Technol. Biomed. Life Sci., 827, 65–75.CrossRefGoogle Scholar
  11. 11.
    Koopman, W. J., Distelmaier, F., Smeitink, J. A., and Willems, P. H. (2013) OXPHOS mutations and neurodegeneration, EMBO J., 32, 9–29.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Avila, J. (2010) Common mechanisms in neurodegeneration, Nat. Med., 16, 1372.CrossRefPubMedGoogle Scholar
  13. 13.
    Filosto, M., Scarpelli, M., Cotelli, M. S., Vielmi, V., Todeschini, A., Gregorelli, V., Tonin, P., Tomelleri, G., and Padovani, A. (2011) The role of mitochondria in neurodegenerative diseases, J. Neurol., 258, 1763–1774.CrossRefPubMedGoogle Scholar
  14. 14.
    Zhu, X., Perry, G., Smith, M. A., and Wang, X. (2013) Abnormal mitochondrial dynamics in the pathogenesis of Alzheimer’s disease, J. Alzheimer’s Dis., 33, S253–S262.Google Scholar
  15. 15.
    Bonda, D. J., Wang, X., Perry, G., Nunomura, A., Tabaton, M., Zhu, X., and Smith, M. A. (2010) Oxidative stress in Alzheimer’s disease: a possibility for prevention, Neuropharmacology, 59, 290–294.CrossRefPubMedGoogle Scholar
  16. 16.
    Skulachev, V. P. (2007) A biochemical approach to the problem of aging: “megaproject” on membrane-penetrating ions. The first results and prospects, Biochemistry (Moscow), 72, 1385–1396.CrossRefGoogle Scholar
  17. 17.
    Anisimov, V. N., Egorov, M. V., Krasilshchikova, M. S., Lyamzaev, K. G., Manskikh, V. N., Moshkin, M. P., Novikov, E. A., Popovich, I. G., Rogovin, K. A., Shabalina, I. G., Shekarova, O. N., Skulachev, M. V., Titova, T. V., Vygodin, V. A., Vyssokikh, M. Y., Yurova, M. N., Zabezhinsky, M. A., and Skulachev, V. P. (2011) Effects of the mitochondria-targeted antioxidant SkQ1 on lifespan of rodents, Aging (Albany, N. Y.), 3, 1110–1119.Google Scholar
  18. 18.
    Neroev, V. V., Archipova, M. M., Bakeeva, L. E., Fursova, A. Zh., Grigorian, E. N., Grishanova, A. Yu., Iomdina, E. N., Ivashchenko, Zh. N., Katargina, L. A., Khoroshilova Maslova, I. P., Kilina, O. V., Kolosova, N. G., Kopenkin, E. P., Korshunov, S. S., Kovaleva, N. A., Novikova, Yu. P., Philippov, P. P., Pilipenko, D. I., Robustova, O. V., Saprunova, V. B., Senin, I. I., Skulachev, M. V., Sotnikova, L. F., Stefanova, N. A., Tikhomirova, N. K., Tsapenko, I. V., Shchipanova, A. I., Zinovkin, R. A., and Skulachev, V. P. (2008) Mitochondria-targeted plastoquinone derivatives as tools to interrupt execution of the aging program. 4. Age-related eye disease. SkQ1 returns vision to blind animals, Biochemistry (Moscow), 73, 1317–1328.CrossRefGoogle Scholar
  19. 19.
    Khrenkova, V. V., and Aleksandrova, A. A. (2013) Ribonucleoprotein compartments of the eukaryotic cell, Valeology, 4, 19–28.Google Scholar
  20. 20.
    Huang, L., Mollet, S., Souquere, S., Le Roy, F., Ernoult Lange, M., Pierron, G., Dautry, F., and Weil, D. (2011) Mitochondria associate with P-bodies and modulate microRNA-mediated RNA interference, J. Biol. Chem., 286, 24219–24230.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Ernoult-Lange, M., Benard, M., Kress, M., and Weil, D. (2012) P-bodies and mitochondria: which place in RNA interference? Biochimie, 94, 1572–1577.CrossRefPubMedGoogle Scholar
  22. 22.
    Cougot, N., Cavalier, A., Thomas, D., and Gillet, R. (2012) The dual organization of P-bodies revealed by immunoelectron microscopy and electron tomography, J. Mol. Biol., 420, 17–28.CrossRefPubMedGoogle Scholar
  23. 23.
    Aizer, A., and Shav-Tal, Y. (2008) Intracellular trafficking and dynamics of P bodies, Prion, 2, 131–134.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Nijjar, S., and Woodland, H. R. (2013) Protein interactions in Xenopus germ plasm RNP particles, PLoS One, 12, e80077.CrossRefGoogle Scholar
  25. 25.
    Zolotukhin, P., Kozlova, Y., Dovzhik, A., Kovalenko, K., Kutsyn, K., Aleksandrova, A., and Shkurat, T. (2013) Oxidative status interactome map: towards novel approaches in experiment planning, data analysis, diagnostics and therapy, Mol. Biosyst., 9, 2085–2096.CrossRefPubMedGoogle Scholar
  26. 26.
    Lo, S. C., and Hannink, M. (2008) PGAM5 tethers a ternary complex containing Keap1 and Nrf2 to mitochondria, Exp. Cell Res., 314, 1789–1803.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Niture, S. K., Jain, A. K., Shelton, P. M., and Jaiswal, A. K. (2011) Src subfamily kinases regulate nuclear export and degradation of transcription factor Nrf2 to switch off Nrf2mediated antioxidant activation of cytoprotective gene expression, J. Biol. Chem., 286, 28821–28832.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Belanova, A. A., Lebedeva, Yu. A., Kuzminova, O. N., Zolotukhin, P. V., Chmykhalo, V. K., Korihfskaya, S. A., Makarenko, M. S., and Aleksandrova, A. A. (2014) Activator protein 1: structure, function and role in the human oxidative status, Valeologiya, 3, 11–20.Google Scholar
  29. 29.
    Masuko, U.-F., Wayne, R. A., Akers, M., and Griendling, K. K. (1998) p38 mitogen-activated protein kinase is a critical component of the redox-sensitive signaling pathways activated by angiotensin II. Role in vascular smooth muscle cell hypertrophy, J. Biol. Chem., 273, 15022–15029.CrossRefGoogle Scholar
  30. 30.
    Kyriakis, J. M., Banerjee, P., Nikolakaki, E., Dai, T., Rubie, E. A., Ahmad, M. F., Avruch, J., and Woodgett, J. R. (1994) The stress-activated protein kinase subfamily of c-Jun kinases, Nature, 369, 156–160.CrossRefPubMedGoogle Scholar
  31. 31.
    Psarra, A. M., and Sekeris, C. E. (2011) Glucocorticoids induce mitochondrial gene transcription in HepG2 cells: role of the mitochondrial glucocorticoid receptor, Biochim. Biophys. Acta, 1813, 1814–1821.CrossRefPubMedGoogle Scholar
  32. 32.
    Du, Y., Zhang, H., Lu, J., and Holmgren, A. (2012) Glutathione and glutaredoxin act as a backup of human thioredoxin reductase 1 to reduce thioredoxin 1 preventing cell death by aurothioglucose, J. Biol. Chem., 287, 38210–38219.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Olmos, Y., Valle, I., Borniquel, S., Tierrez, A., Soria, E., Lamas, S., and Monsalve, M. (2009) Mutual dependence of Foxo3a and PGC-1alpha in the induction of oxidative stress genes, J. Biol. Chem., 284, 14476–14484.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Scarpulla, R. C. (2008) Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1related coactivator, Ann. N. Y. Acad. Sci., 1147, 321–334.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Patenaude, A., Ven Murthy, M. R., and Mirault, M. E. (2004) Mitochondrial thioredoxin system: effects of TrxR2 overexpression on redox balance, cell growth, and apoptosis, J. Biol. Chem., 279, 27302–27314.CrossRefPubMedGoogle Scholar
  36. 36.
    Hansen, J. M., Zhang, H., and Jones, D. P. (2006) Mitochondrial thioredoxin-2 has a key role in determining tumor necrosis factor-alpha-induced reactive oxygen species generation, NF-kappaB activation, and apoptosis, Toxicol. Sci., 91, 643–650.CrossRefPubMedGoogle Scholar
  37. 37.
    Zhang, H., Go, Y. M., and Jones, D. P. (2007) Mitochondrial thioredoxin-2/peroxiredoxin-3 system functions in parallel with mitochondrial GSH system in protection against oxidative stress, Arch. Biochem. Biophys., 465, 119–126.CrossRefPubMedGoogle Scholar
  38. 38.
    Li, C., Wang, L., Zhang, J., Huang, M., Wong, F., Liu, X., Liu, F., Cui, X., Yang, G., Chen, J., Liu, Y., Wang, J., Liao, S., Gao, M., Hu, X., Shu, X., Wang, Q., Yin, Z., Tang, Z., and Liu, M. (2014) CERKL interacts with mitochondrial TRX2 and protects retinal cells from oxidative stressinduced apoptosis, Biochim. Biophys. Acta, 1842, 1121–1129.CrossRefPubMedGoogle Scholar
  39. 39.
    Vaseva, A. V., Marchenko, N. D., Ji, K., Tsirka, S. E., Holzmann, S., and Moll, U. M. (2012) p53 opens the mitochondrial permeability transition pore to trigger necrosis, Cell, 149, 1536–1548.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Bae, S. H., Sung, S. H., Oh, S. Y., Lim, J. M., Lee, S. K., Park, Y. N., Lee, H. E., Kang, D., and Rhee, S. G. (2013) Sestrins activate Nrf2 by promoting p62-dependent autophagic degradation of Keap1 and prevent oxidative liver damage, Cell Metab., 17, 73–84.CrossRefPubMedGoogle Scholar
  41. 41.
    Budanov, A. V., Shoshani, T., Faerman, A., Zelin, E., Kamer, I., Kalinski, H., Gorodin, S., Fishman, A., Chajut, A., Einat, P., Skaliter, R., Gudkov, A. V., Chumakov, P. M., and Feinstein, E. (2002) Identification of a novel stressresponsive gene Hi95 involved in regulation of cell viability, Oncogene, 21, 6017–6031.CrossRefPubMedGoogle Scholar
  42. 42.
    Dinkova-Kostova, A. T., and Talalay, P. (2010) NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector, Arch. Biochem. Biophys., 501, 116–123.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Asher, G., Lotem, J., Kama, R., Sachs, L., and Shaul, Y. (2002) NQO1 stabilizes p53 through a distinct pathway, Proc. Natl. Acad. Sci. USA, 99, 3099–3104.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Anwar, A., Dehn, D., Siegel, D., Kepa, J. K., Tang, L. J., Pietenpol, J. A., and Ross, D. (2003) Interaction of human NAD(P)H:quinone oxidoreductase 1 (NQO1) with the tumor suppressor protein p53 in cells and cell-free systems, J. Biol. Chem., 278, 10368–10373.CrossRefPubMedGoogle Scholar
  45. 45.
    Chae, S., Ahn, B. Y., Byun, K., Cho, Y. M., Yu, M.-H., and Lee, B. (2013) A systems approach for decoding mitochondrial retrograde signaling pathways, Sci. Signal., 6, rs4.PubMedGoogle Scholar
  46. 46.
    Cloonan, S. M., and Choi, A. M. (2013) Mitochondria: sensors and mediators of innate immune receptor signaling, Curr. Opin. Microbiol., 16, 327–338.CrossRefPubMedGoogle Scholar
  47. 47.
    Julian, M. W., Shao, G., Vangundy, Z. C., Papenfuss, T. L., and Crouser, E. D. (2013) Mitochondrial transcription factor A, an endogenous danger signal, promotes TNFα release via RAGEand TLR9-responsive plasmacytoid dendritic cells, PLoS One, 8, e72354.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Oppenheimer, H., Gabay, O., Meir, H., Haze, A., Kandel, L., Liebergall, M., Gagarina, V., Lee, E. J., and Dvir-Ginzberg, M. (2012) 75-kD sirtuin 1 blocks tumor necrosis factor α-mediated apoptosis in human osteoarthritic chondrocytes, Arthritis Rheum., 64, 718–728.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    O-Uchi, J., Ryu, S. Y., Jhun, B. S., Hurst, S., and Sheu, S. S. (2013) Mitochondrial ion channels/transporters as sensors and regulators of cellular redox signaling, Antioxid. Redox Signal., 21, 987–1006.CrossRefGoogle Scholar
  50. 50.
    Rharass, T., Lemcke, H., Lantow, M., Kuznetsov, S. A., Weiss, D. G., and Panakova, D. (2014) Ca2+-mediated mitochondrial reactive oxygen species metabolism augments Wnt/ß-catenin pathway activation to facilitate cell differentiation, J. Biol. Chem., 289, 27937–27951.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Pavlides, S., Vera, I., Gandara, R., Sneddon, S., Pestell, R. G., Mercier, I., Martinez-Outschoorn, U. E., Whitaker Menezes, D., Howell, A., Sotgia, F., and Lisanti, M. P. (2011) Warburg meets autophagy: cancer-associated fibroblasts accelerate tumor growth and metastasis via oxidative stress, mitophagy, and aerobic glycolysis, Antioxid. Redox Signal., 16, 1264–1284.CrossRefPubMedGoogle Scholar
  52. 52.
    Bellot, G., Garcia-Medina, R., Gounon, P., Chiche, J., Roux, D., Pouyssegur, J., and Mazure, N. M. (2009) Hypoxia-induced autophagy is mediated through hypoxiainducible factor induction of BNIP3 and BNIP3L via their BH3 domains, Mol. Cell. Biol., 29, 2570–2581.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Seton-Rogers, S. (2011) Cancer metabolism: feed it forward, Nat. Rev. Cancer, 11, 461.CrossRefPubMedGoogle Scholar
  54. 54.
    Funato, Y., and Miki, H. (2010) Redox regulation of Wnt signaling via nucleoredoxin, Free Radic. Res., 44, 379–388.CrossRefPubMedGoogle Scholar
  55. 55.
    Funk, J. A., and Schnellmann, R. G. (2013) Accelerated recovery of renal mitochondrial and tubule homeostasis with SIRT1/PGC-1α activation following ischemia-reperfusion injury, Toxicol. Appl. Pharmacol., 273, 345–354.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Zhang, X. H., Wei, H., Saric, T., Hescheler, J., Cleemann, L., and Morad, M. (2015) Regionally diverse mitochondrial calcium signaling regulates spontaneous pacing in developing cardiomyocytes, Cell Calcium, 57, 321–336.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Rosenberg, P. (2004) Mitochondrial dysfunction and heart disease, Mitochondrion, 4, 621–628.CrossRefPubMedGoogle Scholar
  58. 58.
    Doughan, A. K., Harrison, D. G., and Dikalov, S. I. (2008) Molecular mechanisms of angiotensin II-mediated mitochondrial dysfunction: linking mitochondrial oxidative damage and vascular endothelial dysfunction, Circ. Res., 102, 488–496.CrossRefPubMedGoogle Scholar
  59. 59.
    East, D. A., and Campanella, M. (2013) Ca2+ in quality control: an unresolved riddle critical to autophagy and mitophagy, Autophagy, 9, 1710–1719.CrossRefPubMedGoogle Scholar
  60. 60.
    Onyango, P., Celic, I., McCaffery, J. M., Boeke, J. D., and Feinberg, A. P. (2002) SIRT3, a human SIR2 homologue, is an NAD-dependent deacetylase localized to mitochondria, Proc. Natl. Acad. Sci. USA, 99, 13653–13658.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 61.
    Azarashvili, T., Odinokova, I., Bakunts, A., Ternovsky, V., Krestinina, O., Tyynela, J., and Saris, N. E. (2014) Potential role of subunit c of FoF1-ATPase and subunit c of storage body in the mitochondrial permeability transition. Effect of the phosphorylation status of subunitc on pore opening, Cell Calcium, 55, 69–77.CrossRefPubMedGoogle Scholar
  62. 62.
    Alavian, K. N., Beutner, G., Lazrove, E., Sacchetti, S., Park, H. A., Licznerski, P., Li, H., Nabili, P., Hockensmith, K., Graham, M., Porter, G. A., Jr., and Jonas, E. A. (2014) An uncoupling channel within the csubunit ring of the F1Fo ATP synthase is the mitochondrial permeability transition pore, Proc. Natl. Acad. Sci. USA, 111, 10580–10585.CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Jonas, E. A., Porter, G. A., Jr., Beutner, G., Mnatsakanyan, N., and Alavian, K. N. (2015) Cell death disguised: the mitochondrial permeability transition pore as the c-subunit of the F1Fo ATP synthase, Pharmacol. Res., 99, 382–392.CrossRefPubMedGoogle Scholar
  64. 64.
    Lane, N., and Martin, W. (2010) The energetics of genome complexity, Nature, 467, 929–934.CrossRefPubMedGoogle Scholar
  65. 65.
    Wang, Z., and Wu, M. (2014) Phylogenomic reconstruction indicates mitochondrial ancestor was an energy parasite, PLoS One, 9, e110685.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Cole, S. T., Eiglmeier, K., Parkhill, J., James, K. D., Thomson, N. R., Wheeler, P. R., Honore, N., Garnier, T., Churcher, C., Harris, D., Mungall, K., Basham, D., Brown, D., Chillingworth, T., Connor, R., Davies, R. M., Devlin, K., Duthoy, S., Feltwell, T., Fraser, A., Hamlin, N., Holroyd, S., Hornsby, T., Jagels, K., Lacroix, C., Maclean, J., Moule, S., Murphy, L., Oliver, K., Quail, M. A., Rajandream, M. A., Rutherford, K. M., Rutter, S., Seeger, K., Simon, S., Simmonds, M., Skelton, J., Squares, R., Squares, S., Stevens, K., Taylor, K., Whitehead, S., Woodward, J. R., and Barrell, B. G. (2001) Massive gene decay in the leprosy bacillus, Nature, 409, 1007–1011.CrossRefPubMedGoogle Scholar
  67. 67.
    Masaki, T., Qu, J., Cholewa-Waclaw, J., Burr, K., Raaum, R., and Rambukkana, A. (2013) Reprogramming adult Schwann cells to stem cell-like cells by leprosy bacilli promotes dissemination of infection, Cell, 152, 51–67.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Stoner, G. L. (1979) Importance of the neural predilection of Mycobacterium leprae in leprosy, Lancet, 2, 994–996.CrossRefPubMedGoogle Scholar
  69. 69.
    Finzsch, M., Schreiner, S., Kichko, T., Reeh, P., Tamm, E. R., Bösl, M. R., Meijer, D., and Wegner, M. (2010) Sox10 is required for Schwann cell identity and progression beyond the immature Schwann cell stage, J. Cell Biol., 189, 701–712.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Weider, M., Kuspert, M., Bischof, M., Vogl, M. R., Hornig, J., Loy, K., Kosian, T., Muller, J., Hillgartner, S., Tamm, E. R., Metzger, D., and Wegner, M. (2012) Chromatin-remodeling factor Brg1 is required for Schwann cell differentiation and myelination, Dev. Cell, 23, 193–201.CrossRefPubMedGoogle Scholar
  71. 71.
    Hess, S., and Rambukkana, A. (2015) Bacterial-induced cell reprogramming to stem cell-like cells: new premise in hostpathogen interactions, Curr. Opin. Microbiol., 23, 179–188.CrossRefPubMedGoogle Scholar
  72. 72.
    Masaki, T., Mc Glinchey, A., Tomlinson, S. R., Qu, J., and Rambukkana, A. (2013) Reprogramming diminishes retention of Mycobacterium leprae in Schwann cells and elevates bacterial transfer property to fibroblasts, F1000Res., 2, 198.PubMedPubMedCentralGoogle Scholar
  73. 73.
    Masaki, T., Mc Glinchey, A., Cholewa-Waclaw, J., Qu, J., Tomlinson, S. R., and Rambukkana, A. (2014) Innate immune response precedes Mycobacterium leprae-induced reprogramming of adult Schwann cells, Cell. Reprogramm., 16, 9–17.CrossRefGoogle Scholar
  74. 74.
    Kobayashi, Y., Kanesaki, Y., Tanaka, A., Kuroiwa, H., Kuroiwa, T., and Tanaka, K. (2009) Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells, Proc. Natl. Acad. Sci. USA, 106, 803–807.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Caballero, A., Ugidos, A., Liu, B., Oling, D., Kvint, K., Hao, X., Mignat, C., Nachin, L., Molin, M., and Nystrom, T. (2011) Absence of mitochondrial translation control proteins extends life span by activating sirtuin-dependent silencing, Mol. Cell, 42, 390–400.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • P. V. Zolotukhin
    • 1
  • A. A. Belanova
    • 1
  • E. V. Prazdnova
    • 1
  • M. S. Mazanko
    • 1
  • M. M. Batiushin
    • 1
  • V. K. Chmyhalo
    • 1
  • V. A. Chistyakov
    • 1
    Email author
  1. 1.Southern Federal UniversityAcademy of Biology and BiotechnologyRostov-on-DonRussia

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