Biology Bulletin

, Volume 45, Issue 1, pp 73–81 | Cite as

Stress Reaction and Biochemical Shock as Interrelated and Unavoidable Components in the Formation of High Radioresistance of the Body in Acute Hypoxia

Animal and Human Physiology
  • 6 Downloads

Abstract

Stress reactions with activation of the sympathetic-adrenal system due to acute hypoxia reflects the degree of sensitivity of the body to this extreme factor. Succinate dehydrogenase (SDH) activation in cells as an adaptive response to acute hypoxia is closely associated with the degree of disturbance of tissue respiration through a lack of oxygen in the tissues, including the manifestation of “biochemical shock,” which is an unavoidable component of implementation of the protective effect of radioprotectors. In experiments on mice, rats, and dogs, the correlation between the manifestation of the radioprotective effect of acute hypoxia and SDH activation in blood lymphocytes, caused primarily by adrenergic stimulation during stress reactions, is confirmed. The degree of SDH activation in blood lymphocytes by hypoxia of different origins including that induced by radioprotectors may indicate its radioprotective potential irrespective of the differences in the oxygen consumption intensity and the resistance to acute hypoxia in animals and humans.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Akopova, O., Nosar, V., and Gavenauskas, B., The effect of ATP-dependent potassium uptake on mitochondrial functions under acute hypoxia, J. Bioenerg. Biomembr., 2016, vol. 48, no. 1, pp. 67–75.CrossRefPubMedGoogle Scholar
  2. Allalunis-Turner, M.J., Reduced bone marrow pO2 following treatment with radioprotective drugs, Radiat. Res., 1990, vol. 122, no. 3, pp. 262–267.CrossRefPubMedGoogle Scholar
  3. Allalunis-Turner, M.J., Walden, T.J., and Sawich, C., Induction of marrow hypoxia by radioprotective agents, Radiat. Res., 1989, vol. 118, no. 3, pp. 581–586.CrossRefPubMedGoogle Scholar
  4. Antipov, V.V., Vasin, M.V., and Gaidamakin, A.N., Species-specific reactions of succinate dehydrogenase of lym- phocytes in animals to acute hypoxic hypoxia and its relation to the radiation resistance of the body, Kosm. Biol. Aviakosm. Med., 1989, vol. 23, no. 2, pp. 63–66.PubMedGoogle Scholar
  5. Ariza, A.C., Deen, P.M., and Robben, J.H., The succinate receptor as a novel therapeutic target for oxidative and metabolic stress-related conditions, Front. Endocrinol. (Lausanne), 2012, vol. 3, p. 22.Google Scholar
  6. Bacq, Z.M., Beaumariage, M.L., and Van Caneghem, P., Importance for radioprotective effect in mammals of pharmacological and biochemical actions of cysteamine and related substances, Ann. Ist. Super Sanita, 1965, vol. 1, no. 9, pp. 639–645.PubMedGoogle Scholar
  7. Bacq, Z.M., Beaumariage, M.L., Goutier, R., and Van Caneghem, P., The state of shock induced by cystamine and cysteamine, Br. J. Pharmacol., 1968, vol. 34, no. 1, p. 202–203.Google Scholar
  8. Cavanagh, H.D. and Colley, A.M., Cholinergic, adrenergic, and PGE1 effects on cyclic nucleotides and growth in cultured corneal epithelium, Metab. Pediatr. Syst. Ophthalmol., 1982, vol. 6, no. 2, pp. 63–74.PubMedGoogle Scholar
  9. Dawson, T.L., Gores, G.J., Nieminen, A.L., Herman, B., and Lemasters, J.J., Mitochondria as a source of reactive oxygen species during reductive stress in rat hepatocytes, Am. J. Physiol. Cell Physiol., 1993, vol. 264, no. 4, pt 1, pp. C961–C967.CrossRefGoogle Scholar
  10. Duong, T.T., Witting, P.K., Antao, S.T., Parry, S.N., Kennerson, M., Lai, B., Vogt, S., Lay, P.A., and Harris, H.H., Multiple protective activities of neuroglobin in cultured neuronal cells exposed to hypoxia re-oxygenation injury, J. Neurochem., 2009, vol. 108, no. 5, pp. 1143–1154.CrossRefPubMedGoogle Scholar
  11. Feldkamp, T., Kribben, A., Roeser, N.F., Senter, R.A., Kemner, S., Venkatachalam, M.A., Nissim, I., and Weinberg, J.M., Preservation of complex I function during hypoxia-reoxygenation-induced mitochondrial injury in proximal tubules, Am. J. Physiol. Renal. Physiol., 2004, vol. 286, no. 4, pp. F749–F759.CrossRefPubMedGoogle Scholar
  12. Fernandez-Gomez, F.J., Galindo, M.F., Gómez-Lázaro, M., Yuste, V.J., Camello, J.X., Aguirre, N., and Jordan, J., Malonate induces cell death via mitochondrial potential collapse and delayed swelling through an ROS-dependent pathway, Br. J. Pharmacol., 2005, vol. 144, no. 4, pp. 528–537.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Firket, H. and Beaumariage, M.L., Ultrastructural modifications of mitochondria and rough endoplasmic reticulum of liver and spleen after a period of hypoxia, Virchows Arch. Cell Pathol., 1971, vol. 8, no. 4, pp. 342–349.Google Scholar
  14. Firket, H. and Lelièvre, P., Effect of cystamine on the respiration, oxidative phosphorylation and ultrastructure of the mitochondria of the rat, Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 1966, vol. 10, no. 4, pp. 403–415.CrossRefPubMedGoogle Scholar
  15. Fujishiro, N., Endo, Y., Warashina, A., and Inoue, M., Mechanisms for hypoxia detection in O2-sensitive cells, Jpn. J. Physiol., 2004, vol. 54, no. 2, pp. 109–123.CrossRefPubMedGoogle Scholar
  16. Gaidamakin, A.N. and Abramov, M.M., Comparison of changes in succinate dehydrogenase activity in blood lymphocytes and modification of radiosensitivity by exogenous hypoxia, Radiobiologiya, 1987, vol. 27, no. 4, pp. 524–528.Google Scholar
  17. Garlid, K.D. and Paucek, P., The mitochondrial potassium cycle, IUBMB Life, 2001, vol. 52, pp. 153–158.CrossRefPubMedGoogle Scholar
  18. Haass, M., Richardt, G., and Schömig, A., Potentiation of potassium-evoked noradrenaline and neuropeptide Y corelease by cardiac energy depletion: role of calcium channels and sodium-proton exchange, Naunyn Schmiedebergs Arch. Pharmacol., 1992, vol. 346, no. 4, pp. 410–418.CrossRefPubMedGoogle Scholar
  19. Hakak, Y., Lehmann-Bruinsma, K., Phillips, S., Le, T., Liaw, C., Connolly, D.T., and Behan, D.P., The role of the GPR91 ligand succinate in hematopoiesis, J. Leukocyte Biol., 2009, vol. 85, no. 5, pp. 837–843.CrossRefPubMedGoogle Scholar
  20. Hasegawa, A.T. and Landahl, H.D., Studies on spleen oxygen tension and radioprotection in mice with hypoxia, serotonin and p-aminopropiophenone, Radiat. Res., 1967, vol. 31, no. 3, pp. 389–399.CrossRefGoogle Scholar
  21. Hawkins, B.J., Levin, M.D., Doonan, P.J., Petrenko, N.B., Davis, C.W., Patel, V.V., and Madesh, M., Mitochondrial complex IIprevents hypoxic but not calcium- and proapoptotic Bcl-2 protein-induced mitochondrial membrane potential loss, J. Biol. Chem., 2010, vol. 285, no. 34, pp. 26494–26505.CrossRefPubMedPubMedCentralGoogle Scholar
  22. He, W., Miao, F.J., Lin, D.C., Schwandner, R.T., Wang, Z., Gao, J., Chen, J.L., Tian, H., and Ling, L., Citric acid cycle intermediates as ligands for orphan G-protein-coupled receptors, Nature, 2004, vol. 429, no. 6988, pp. 188–193.CrossRefPubMedGoogle Scholar
  23. Hu, J., Bernardini, A., and Fandrey, J., Optical analysis of hypoxia inducible factor (HIF)-1 complex assembly: imaging of cellular oxygen sensing, Adv. Exp. Med. Biol., 2016, vol. 903, pp. 247–258.CrossRefPubMedGoogle Scholar
  24. Jones, D.P. and Mason, H.S., Gradients of O2 concentration in hepatocytes, J. Biol. Chem., 1978, vol. 253, no. 14, pp. 4874–4880.PubMedGoogle Scholar
  25. Kaasik, A., Safiulina, D., Zharkovsky, A., and Veksler, V., Regulation of mitochondrial matrix volume, Am. J. Physiol. Cell Physiol., 2007, vol. 292, no. 1, pp. C157–C163.CrossRefPubMedGoogle Scholar
  26. Kawada, T., Yamazaki, T., Akiyama, T., Sato, T., Shishido, T., Inagaki, M., Tatewaki, T., Yanagiya, Y., Sugimachi, M., and Sunagawa, K., Cyanide intoxication induced exocytotic epinephrine release in rabbit myocardium, J. Auton. Nerv. Syst., 2000, vol. 80, no. 3, pp. 137–141.CrossRefPubMedGoogle Scholar
  27. Kehrer, J.P. and Lund, L.G., Cellular reducing equivalents and oxidative stress, Free Radic. Biol. Med., 1994, vol. 17, no. 1, pp. 65–75.CrossRefPubMedGoogle Scholar
  28. Kondrasheva, M.N., Activation of succinate dehydrogenase as the basis for anaerobic performance and resistance to hypoxia, in Mitokhondrial’nye protsessy vo vremennoi organizatsii zhiznedeyatel’nosti (Mitochondrial Processes in the Temporal Organization of Life Activity), Kondrasheva, M.N. and Maevskii, E.I., Eds., Pushchino, 1978, pp. 6–12.Google Scholar
  29. Kondrasheva, M.N. and Chagovets, N.R., Succinic acid in the skeletal muscles during intense load and relaxation, Dokl. Akad. Nauk SSSR, 1971, vol. 198, no. 1, pp. 243–246.Google Scholar
  30. Kondrasheva, M.N., Maevskii, E.I., Babayan, E.I., and Akhmerov, R.N., Adaptation to hypoxia by switching metabolism to the conversion of succinic acid, in Mitokhondriya. Biokhimiya i ul’trastruktura (Mitochondrion: Biochemistry and Ultrastructure), Moscow: Nauka, 1973, pp. 112–129.Google Scholar
  31. Kondrashova, M., Zakharchenko, M., and Khunderyakova, N., Preservation of the in vivo state of mitochondrial network for ex vivo physiological study of mitochondria, Int. J. Biochem. Cell Biol., 2009, vol. 41, no. 10, pp. 2036–2050.CrossRefPubMedGoogle Scholar
  32. Konstantinova, M.M. and Graevskii, E.I., Tissue hypoxia as a mechanism of radioprotective action of adrenaline, heroin, and morphine, Dokl. Akad. Nauk SSSR, 1960, vol. 133, pp. 1427–1430.Google Scholar
  33. Koroleva, L.V. and Vasin, M.V., Effect of adrenaline on the succinate dehydrogenase activity of peripheral blood lymphocytes of rats following exposure to ionizing radiation, Radiobiologiya, 1988, vol. 28, no. 2, pp. 228–230.Google Scholar
  34. Kraus-Friedmann, N., Glucagon-stimulated respiration and intracellular Ca2+, FEBS Lett., 1986, vol. 201, no. 1, pp. 133–136.CrossRefPubMedGoogle Scholar
  35. Kulinskii, V.I., Kuntsevich, A.K., and Trufanova, L.V., Activation succinate dehydrogenation in rat liver by noradrenaline, cAMP and acute cooling, Byul. Eksp. Biol. Med., 1981, vol. 92, no. 8, pp. 33–34.Google Scholar
  36. Kurz, T., Richardt, G., Seyfarth, M., and Schömig, A., Nonexocytotic noradrenaline release induced by pharmacological agents or anoxia in human cardiac tissue, Naunyn Schmiedebergs Arch. Pharmacol., 1996, vol. 354, no. 1, pp. 7–16.CrossRefPubMedGoogle Scholar
  37. Kvetnansky, R., Lu, X., and Ziegler, M.G., Stress-triggered changes in peripheral catecholaminergic systems, Adv. Pharmacol., 2013, vol. 68, pp. 359–397.CrossRefPubMedGoogle Scholar
  38. Laszczyca, P., The activity of mitochondrial enzymes in the muscles of rats subjected to physical training and subchronical intoxication with lead and zinc, Acta Physiol. Pol., 1989, vol. 40, nos. 5–6, pp. 544–551.PubMedGoogle Scholar
  39. Lehninger, A.L. and Remmert, L.F., An endogenous uncoupling and swelling agent in liver mitochondria and its enzymic formation, J. Biol. Chem., 1959, vol. 234, pp. 2459–2464.PubMedGoogle Scholar
  40. Lehninger, A.L. and Schneider, M., Mitochondrial swelling induced by glutathione, J. Biophys. Biochem. Cytol., 1959, vol. 5, no. 1, pp. 109–116.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Lelièvre, P., Action of cystamine and cysteamine on the oxygen consumption and coupled oxidative phosphorylation of the liver mitochondria of rats, Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 1965, vol. 9, pp. 107–113.CrossRefPubMedGoogle Scholar
  42. Luk’yanova, L.D., Mitochondrial signaling pathways in adaptation to hypoxia, Fiziol. Zh. im. I.M. Sechenova, 2013, vol. 59, no. 6, pp. 141–154.Google Scholar
  43. Maevskii, E.I., Grishina, E.V., Rozenfel’d, A.S., Zyakun, A.M., Kondrashova, M.N., and Vereshchagina, V.M., Anaerobic conversion of succinate and enhancement of its oxidation. Possible mechanisms of cellular adaptation to oxygen deficiency, Biofizika, 2000, vol. 45, no. 3, pp. 509–513.PubMedGoogle Scholar
  44. Van der Meer, C. and van Bekkum, D.W., The mechanism of radiation protection by hystamine and other biological amines, Int. J. Radiat. Biol., 1959, vol. 1, pp. 5–12.Google Scholar
  45. Van der Meer, C. and van Bekkum, D., A study on the mechanism of radiation protection by 5-hydroxytryptamine and tryptamine, Int. J. Radiat. Biol., 1961, vol. 4, pp. 105–110.Google Scholar
  46. Mohan, C., Memon, R.A., and Bessman, S.P., Differential effects of insulin, epinephrine, and glucagon on rat hepatocyte mitochondrial activity, Arch. Biochem. Biophys., 1991, vol. 287, no. 1, pp. 18–23.CrossRefPubMedGoogle Scholar
  47. Mojet, M.H., Mills, E., and Duchen, M.R., Hypoxiainduced catecholamine secretion in isolated newborn rat adrenal chromaffin cells is mimicked by inhibition of mitochondrial respiration, J. Physiol., 1997, vol. 504, no. 1, pp. 175–189.CrossRefPubMedPubMedCentralGoogle Scholar
  48. Nartsissov, R.P., The use of N-nitrotetrazolium violet for quantitative cytometry of dehydrogenases in human lymphocytes, Arkh. Anat. Gistol. Embriol., 1969, vol. 56, no. 5, pp. 85–91.PubMedGoogle Scholar
  49. Newmeyer, D.D. and Ferguson-Miller, S., Mitochondria: releasing power for life and unleashing the machineries of death, Cell, 2003, vol. 112, no. 4, pp. 481–490.CrossRefPubMedGoogle Scholar
  50. Ovakimov, V.N. and Yarmonenko, S.P., Adaptation to hypoxia as a factor modifying its radioprotective effect, Med. Radiol., 1974, vol. 19, no. 6, pp. 49–53.Google Scholar
  51. Pistollato, F., Abbadi, S., Rampazzo, E., Viola, G., Della, Puppa A., Cavallini, L., Frasson, C., Persano, L., Panchision, D.M., and Basso, G., Hypoxia and succinate antagonize 2-deoxyglucose effect glioblastoma, Biochem. Pharmacol., 2010, vol. 80, no. 10, pp. 1517–1527.CrossRefPubMedGoogle Scholar
  52. Richardt, G., Lumpp, U., Haass, M., and Schömig, A., Propranolol inhibits nonexocytotic noradrenaline release in myocardial ischemia, Naunyn Schmiedebergs Arch. Pharmacol., 1990, vol. 341, nos. 1–2, pp. 50–55.PubMedGoogle Scholar
  53. Schömig, A., Haass, M., and Richardt, G., Catecholamine release and arrhythmias in acute myocardial ischaemia, Eur. Heart J., 1991, vol. 12, suppl. F, pp. 38–47.CrossRefPubMedGoogle Scholar
  54. Schömig, A., Richardt, G., and Kurz, T., Sympatho-adrenergic activation of the ischemic myocardium and its arrhythmogenic impact, Herz, 1995, vol. 20, no. 3, pp. 169–186.PubMedGoogle Scholar
  55. Sivaramakrishnan, S. and Ramasarma, T., Noradrenaline stimulates succinate dehydrogenase through beta-adrenergic receptors, Indian J. Biochem. Biophys., 1983a, vol. 1983, no. 20, pp. 1–16.Google Scholar
  56. Sivaramakrishnan, S., Panini, S.R., and Ramasarma, T., Activation of succinate dehydrogenase in isolated mitochondria by noradrenaline, Indian J. Biochem. Biophys., 1983b, vol. 1983, no. 20, pp. 1–23.Google Scholar
  57. Skrede, S., Effects of cystamine and cysteamine on the adenosine- triphosphatase activity and oxidative phosphorylation of rat-liver mitochondria, Biochem. J., 1966, vol. 98, no. 3, pp. 702–710.CrossRefPubMedPubMedCentralGoogle Scholar
  58. Souvannakitti, D., Kumar, G.K., Fox, A., and Prabhakar, N.R., Neonatal intermittent hypoxia leads to long-lasting facilitation of acute hypoxia-evoked catecholamine secretion from rat chromaffin cells, J. Neurophysiol., 2009, vol. 101, no. 6, pp. 2837–2846.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Ushakov, I.B., Abramov, M.M., Khunandov, L.L., and Zuev, V.G., Radioprotektory i gipoksiya: mekhanizmy kombinirovannoi zashchity (Radioprotectors and Hypoxia: Mechanisms of Combined Protection), Moscow: Vooruzhenie. Politika. Konversiya, 1996.Google Scholar
  60. Vasin, M.V., Comparative characteristics of the modification of radiosensitivity of mice and rats by a hypoxic mixture, Radiobiologiya, 1986, vol. 26, no. 4, pp. 563–565.Google Scholar
  61. Vasin, M.V., Classification of radioprotective agents as a reflection of the current state and prospects of development of radiation pharmacology?, Radiats. Biol. Radioekol., 2013, vol. 53, no. 5, pp. 459–467.Google Scholar
  62. Vasin, M.V. and Ushakov, I.B., Comparative efficacy and the window of radioprotection for adrenergic and serotoninergic agents and aminothiols in experiments with small and large animals, J. Radiat. Res., 2015, vol. 56, no. 1, pp. 1–10.CrossRefPubMedGoogle Scholar
  63. Vasin, M.V., Antipov, V.V., Suvorov, N.N., Abramov, M.M., and Gorelova, N.V., Characteristics of the role of the hydroxyl group in serotonin in the pharmacological and antiradiation effect of serotonin, Radiobiologiya, 1984, vol. 24, no. 3, pp. 411–414.Google Scholar
  64. Vasin, M.V., Suvorov, N.N., Abramov, M.M., and Gordeev, E.N., Changes in the therapeutic spectrum with respect to the pharmacological and radioprotective activity after O-alkylation of serotonin and 5(2-hydroxyethoxytryptamine), Radiobiologiya, 1987, vol. 27, no. 5, pp. 700–703.Google Scholar
  65. Vasin, M.V., Petrova, T.V., and Koroleva, L.V., The effect of adrenaline on the cyclic nucleotides and succinate dehydrogenase activity, Fiziol. Zh. SSSR im. I.M. Sechenova, 1991, vol. 77, no. 4, pp. 106–108.PubMedGoogle Scholar
  66. Vasin, M.V., Chernov, G.A., Koroleva, L.V., L’vova, T.S., Abramov, M.M., Antipov, V.V., and Suvorov, N.N., Mechanism of the radiation-protective effect of indralin, Radiats. Biol. Radioekol., 1996, vol. 36, no. 1, pp. 36–46.Google Scholar
  67. Vasin, M.V., Antipov, V.V., Chernov, G.A., Abramov, M.M., Gavrilyuk, D.N., L’vova, T.S., and Suvorov, N.N., The role of the vasoconstrictor effect in realizing the radioprotective properties of indralin in experiments on dogs, Radiats. Biol. Radioekol., 1997, vol. 37, no. 1, pp. 46–55.Google Scholar
  68. Vasin, M.V., Ushakov, I.B., Koroleva, L.V., and Antipov, V.V., The role of cell hypoxia in the effect of radiation protectors, Radiats. Biol. Radioekol., 1999, vol. 39, nos. 2–3, pp. 238–248.Google Scholar
  69. Vasin, M.V., Ushakov, I.B., Semenova, L.A., and Kovtun, V.Yu., Pharmacologic analysis of the radiation-protecting effect of indraline, Radiats. Biol. Radioekol., 2001, vol. 41, no. 3, pp. 307–309.Google Scholar
  70. Vasin, M.V., Ushakov, I.B., Koroleva, L.V., and Stepanov, V.K., Participation of succinate dehydrogenase cell system in adaptive processes during human breathing with a hypoxic gas mixture, Aviakosm. Ekol. Med., 2002a, vol. 2002, no. 36, pp. 6–35.Google Scholar
  71. Vasin, M.V., Ushakov, I.B., Koroleva, L.V., Lairov, I.A., and Radchenko, S.N., In vitro response of mitochondrial succinate oxidase system to epinephrine in human blood lymphocytes from health individuals and patients with neurocirculatory dystonia, Byull. Eksp. Biol. Med., 2002b, vol. 2002, no. 134, pp. 4–393.Google Scholar
  72. Vasin, M.V., Ushakov, I.B., and Antipov, V.V., Potential role of catecholamine response to acute hypoxia in the modification of the effects of radioprotectors, Byull. Eksp. Biol. Med., 2015, vol. 159, no. 5, pp. 549–552.CrossRefGoogle Scholar
  73. Vladimirov, V.G., The effect of cystamine on oxidative phosphorylation in the spleen of irradiated rats, Byull. Eksp. Biol. Med., 1962, vol. 54, no. 11, pp. 55–58.Google Scholar
  74. Wittenberger, T., Schaller, H.C., and Hellebrand, S., An expressed sequence tag (EST) data mining strategy succeeding in the discovery of new G-protein coupled receptors, J. Mol. Biol., 2001, vol. 307, pp. 799–813.CrossRefPubMedGoogle Scholar
  75. Yang, L., Yu, D., Fan, H.H., Feng, Y., Hu, L., Zhang, W.Y., Zhou, K., and Mo, X.M., Triggering the succinate receptor GPR91 enhances pressure overload-induced right ventricular hypertrophy, Int. J. Clin. Exp. Pathol., 2014, vol. 7, no. 9, pp. 5415–5428.PubMedPubMedCentralGoogle Scholar
  76. Yarmonenko, S.P. and Epshtein, I.M., Oxygen effect and the intracellular oxygen content (the adaptation hypothesis), Radiobiologiya, 1977, vol. 17, no. 3, pp. 323–335.Google Scholar
  77. Yarmonenko, S.P., Rampan, Yu.I., Karochkin, B.B., Berezhnova, L.I., Ovakimov, V.G., and Aupanetyan, G.M., Oxygen tension kinetics in critical organs under the effects of mexamine in comparison with its radiation-protective effect, Radiobiologiya, 1970, vol. 10, no. 6, pp. 700–705.Google Scholar
  78. Yarmonenko, S.P., Vainson, A.A., and Magdon, E., Kislorodnyi effekt i luchevaya terapiya opukholei (Oxygen Effect and Radiation Therapy of Tumors), Moscow: Meditsina, 1980.Google Scholar
  79. Yuhas, J.M., Proctor, J.O., and Smith, L.H., Some pharmacologic effects of WR-2721: their role in toxicity and radioprotection, Radiat. Res., 1973, vol. 54, pp. 222–233.CrossRefPubMedGoogle Scholar
  80. Zakharchenko, M.V., Zakharchenko, A.V., Khunderyakova, N.V., Tutukina, M.N., Simonova, M.A., Vasilieva, A.A., Romanova, O.I., Fedotcheva, N.I., Litvinova, E.G., Maevsky, E.I., Zinchenko, V.P., Berezhnov, A.V., Morgunov, I.G., Gulayev, A.A., and Kondrashova, M.N., Burst of succinate dehydrogenase and α-ketoglutarate dehydrogenase activity in concert with the expression of genes coding for respiratory chain proteins underlies shortterm beneficial physiological stress in mitochondria, Int. J. Biochem. Cell Biol., 2013, vol. 45, no. 1, pp. 190–200.CrossRefPubMedGoogle Scholar
  81. Zepeda, A.B., Pessoa, A., Castillo, R.L., Figueroa, C.A., Pulgar, V.M., and Farías, J.G., Cellular and molecular mechanisms in the hypoxic tissue: role of HIF-1 and ROS, Cell Biochem. Funct., 2013, vol. 31, no. 6, pp. 451–459.CrossRefPubMedGoogle Scholar
  82. Zherebchenko, P.G. and Suvorov, N.N., The relationship between the radioprotective and vasoconstrictor effects of indolylalkylamines, Radiobiologiya, 1963, vol. 3, pp. 595–602.Google Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • M. V. Vasin
    • 1
  • I. B. Ushakov
    • 1
  • I. V. Bukhtiyarov
    • 1
  1. 1.Research Institute of Medicine of LaborRussian Academy of SciencesMoscowRussia

Personalised recommendations