Abstract
Using fluorescent and electron microscopy a comparative analysis was performed of components of the protein-synthesizing system of hippocampal neurons both in ground squirrels in various phases of the torpor-activity cycle and in rats cooled under the hypoxia-hypercapnia conditions. Results of the study have shown that in hippocampal neurons of the ground squirrels entering the natural torpor state and of rats under conditions of artificial hypothermia to 17°C, similar mechanisms might be possible to function, one of their obligatory components being a generalized decrease of activity of the protein-synthesizing system with its subsequent restoration at the exit from hypothermia. Cessation of hypoxia-hypercapnia even under conditions of a further temperature decrease restored the rat neuronal protein-synthesizing activity, which seems to indicate the presence of a potential possibility of adaptation of brain neurons in vivo to low temperatures, at which the integral organism of non-hibernating homoeothermic animals does not survive.
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References
Gordon, R.Ya., Study of Generalized Metabolic Response of Nerve Cells to Change of the Functional State and to Action of Damaging Factors, Doctorate Sci. Dissertation, Pushchino, 2000.
Manina, A.A., Ultrastukturnye izmeneniya i reparativnye protsessy v tsentralnoi nervnoi sisteme pri razlichnykh vozdeistviyakh (Ultrastructural Changes and Reparative Processes in the Central Nervous System under Various Actions), Leningrad, 1971.
Demin, N.N., Shartanova, T.Kh., and Emirbekov, E.Z., Neirokhimiya zimnei spyachki mlekopitayushchikh (Neurochemistry of Hibernation in Mammals), Leningrad, 1988.
Gordon, R.Ya., Bocharova, L.S., Arkhipov, V.I., and Karnaukhov, V.N., RNA Metabolism and Uridine Transport in the Brain of Hibernators, Evolutionary Aspects of Hibernation, Kreps, E.M., Ed., Leningrad, 1986, pp. 73–79.
Bocharova, L.S., Gordon, R.Ya., and Popov, V.I., RNA Metabolism in the Brain of Hibernators. 2. Rapid Changes in the Neuronal Ribosome RNA Content, Mechanisms of Natural Hypometabolic States, Kovaleva, S., Popova, N., Solomonov, N., and Wang, L., Eds., Pushchino, 1992, pp. 125–132.
Popov, V.I. and Bocharova, L.S., Hibernation-Induced Structural Changes in Synaptic Contacts between Mossy Fibres and Hippocampal Pyramidal Neurons, Neurosci., 1992, vol. 48, pp. 53–62.
Planas, A.M., Soriano, M.A., Estrada, A., Estrada, A., Sanz, O., Martin, F., and Ferrer, I., The Heat Shock Stress Response after Brain Lesions: Induction of 72 kDa Heat Shock Protein (Cell Types Involved, Axonal Transport, Transcriptional Regulation) and Protein Synthesis Inhibition, Progr. Neurobiol., 1997, vol. 51, pp. 607–636.
Black, A.B. and Subject, J.E., Involvement of rRNA Synthesis in the Enhanced Survival and Recovery of Proteins Synthesis Seen in Thermotolerance, J. Cell Physiol., 1989, vol. 138, pp. 439–449.
Frerichs, K.U. and Hallenbeck, J.M., Hibernation in Ground Squirrels Induced State and Species-Specific Tolerance to Hypoxia and Glycemia: An in vitro Study in Hippocampal Slices, J. Cerebr. Blood Flow Met., 1998, vol. 18, pp. 168–175.
Krilovicz, B.L., Glotzbach, S.F., and Heller, H.C., Neuronal Activity during Sleep and Complete Bouts of Hibernation, Am. J. Physiol., 1988, vol. 255 pp. 1008–1019.
Fischer, S., et al., Hypothermia Abolishes Hypoxia-Induced Hyperpermeability in Brain Microvessel Endothelial Cells, Mol. Brain Res., 1999, vol. 74, pp. 135–144.
Zhang, Z., Sobel, R.A., Cheng, D., Steinberg, G.K., and Yenari, M.A., Mild Hypothermia Increases Bcl-2 Protein Expression following Global Cerebral Ischemia, Mol. Brain Res., 2001, vol. 95, pp. 75–85.
Drew, K.L., Rice, M.E., Kuhn, T.B., and Smith, M.A., Neuroprotective Adaptations in Hibernation: Therapeutic Implication for Ischemia-Reperfusion, Traumatic Brain Injury and Neurodegenerative Diseases, Free Radic. Biol. Med., 2001, vol. 31, pp. 563–573.
Ignatiev, D.A., Sukhova, G.S., and Sukhov, V.P., Analysis of Changes of Heart Rate and Temperature in the Ground Squirrel Citellus undulatus in Various Physiological States, Zh. Obshch. Biol., 2001, vol. 62, No. 1, pp. 66–67.
Maistrakh, E.V., Gipotermiya i gipobios (Hypothermia and Hypobiosis), Moscow, 1964.
Shtark, M.B., Mozg zimnespyashchikh (Brain of Hibernators), Novosibirsk, 1970.
Heller, H.C., Hibernation: Neuronal Aspects, Ann. Rev. Physiol., 1979, vol. 40, pp. 305–332.
Bekman, A.L. and Stanton, T.L., Properties of the CNS during the State of Hibernation, The Neural Basis of Behavior, Bekman, A.L., Ed., New York, 1982, pp. 19–45.
Vinogradova, O.S., Gippokamp i pamyat’ (Hyppocampus and Memory), Moscow, 1975.
Matson, M.P. and Kater, S.B., Development and Selective Neurodegeneration in Cell Cultures from Different Hippocampal Regions, Brain Res., 1989, vol. 490, pp. 110–125.
Giaja, J., Hypothermie, Hibernation et Poikilothermie Experimentale, Biol. Med., 1953, vol. 42, pp. 545–552.
Timofeev, M.N., Iskusstvennyi gipobioz (Artificial Hypobiosis), Moscow, 1983.
Vinokurov, V.N. and Akhremenko, A.K., Populyatsionnaya ekologiya dlinnokhvostykh suslikov Yakutii (Population Ecology of the Yakutia Long-Tail Ground Squirrels), 1982.
Gordon, R.Ya., Bocharova, L.S., Kruman, I.I., Kruman, I.I., Popov, V.I., Kazantsev, A.P., Khutzian, S.S., and Karnaukhov, V.N., Acridine Orange as an Indicator of the Cytoplasmic Ribosome State, Cytometry, 1997, vol. 29, pp. 215–221.
Karnaukhov, V.I., Yashin, V.A., Kazantsev, A.P., Karnaukhova, N.A., and Kulakov, V.I., Two-Wave Microfluorimeter—Photometer Based on Standard Equipment, Tsitologiya, 1987, vol. 29, pp. 113–118.
Chelidze, I.V. and Zatsepina, O.V., Morpofunctional Classification of Nucleoli, Tsiologiya, 1987, vol. 105, pp. 252–268.
Frerichs, K.U., Smith, C.B., Brenner, M., DeGracia, D.J., Krause, G.S., Marrone, L., Dever, T.E., and Hallenbeck, J.V., Supression of Proteins Synthesis in Brain during Hibernation Involves Inhibition of Protein Initiation and Elongation, Proc. Natl Acad. Sci. USA, 1998, vol. 95, pp. 14 511–14 516.
Krause, G.S. and Tiffany, B.R., Suppression of Protein Synthesis in the Reperfused Brain, Stroke, 1993, vol. 24, pp. 747–756.
Doutheil, J., Gissel, C., Oshlies, U., Hossmann, K.-A., and Pashen, W., Relation of Neuronal Endoplasmic Reticulum Calcium Homeostasis to Ribosomal Aggregation and Protein Synthesis: Implications for Stress-Induced Suppression of Protein Synthesis, Brain Res., 1997, vol. 772, pp. 43–51.
Ignatiev, D.A., Vorobiev, V.V., Sukhova, G.S., Ziganshin, R.Kh., Sukhov, V.P., Temnov, A.V., Temnova, A.A., and Ashmarin, I.P., Hibernation and Artificial Hypobiosis, Neirokhim., 1998, no. 3, pp. 240–263.
Bullard, F.W., David, G., and Nichols, C.T., The Mechanism of Hypoxic Tolerance in Hibernating and Non-Hibernating Mammals, Mammalian Hibernation, Bulletin of the Museum of Comparative Zoology at Harvard Colledge, Lyman, C.P. and Dawe, A.R., Eds., Cambridge, MA., 1960, pp. 322–335.
Lust, W.D., Whaton, A.B., Feussuer, G., and Passonneau, J., Metabolism in the Hamster Brain during Hibernation and Arousal, Brain Res., 1989, vol. 486, pp. 12–20.
Haak, L.L., Mignot, E., Kilduff, T.S., Dement, W.C., and Heller, H.C., Regional Changes in Central Monoamine and Metabolite Levels during the Hibernation Cycle in the Golden-Mantled Ground Squirrel, Brain Res., 1991, vol. 563, pp. 215–220.
Osborne, P.G., Hu, Y., Covey, D.N., Barns, B.N., Katz, Z., and Drew, K.L., Determination of Striatal Extracellular Gamma-Aminobutyric Acid in Non-Hibernating and Hibernating Arctic Ground Squirrels using Quantitative Microdialysis, Brain Res., 1999, vol. 839, pp. 1–6.
Choi, D.W., Cerebral Hypoxia: Some New Approaches and Unanswered Questions, J. Neurosci., 1990, vol. 10, pp. 2493–2501.
Shaver, E.G., Welsh, F.A., Sutton, L.N., Mora, G., Gennarelli, L.M., and Norwood, C.R., Deep Hypothemia Diminishes the Ischemic Induction of Heat-Shock Protein-72 mRNA in Piglet Brain, Stroke, 1995, vol. 26, pp. 1273–1278.
Ivanov, K.P., Changes of Physiological Functions, Mechanisms of their Restoration and Temperature Life Limits during Hypothermia, Usp. Fiziol. Nauk, 1996, vol. 27. pp. 84–105.
Andjus, R.K., Suspended Animation in Cooled, Supercooled and Frozen Rats, J. Physiol. (England), 1955, vol. 128, pp. 547–556.
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Original Russian Text © R. Ya. Gordon, D. A. Ignatiev, V. V. Rogachevskii, N. I. Medvedev, I. V. Kraev, I. V. Patrushev, S. S. Khutsyan, and V. I. Popov, 2006, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2006, Vol. 42, No. 3, pp. 237–243.
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Gordon, R.Y., Ignatiev, D.A., Rogachevskii, V.V. et al. Changes of activity of the protein-synthesizing system of brain neurons of the ground squirrel Citellus undulatus during hibernation and hypothermia. J Evol Biochem Phys 42, 299–307 (2006). https://doi.org/10.1134/S0022093006030082
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DOI: https://doi.org/10.1134/S0022093006030082