From intravital neuromorphology to hypoxic preconditioning: The scientific path of Prof. Mikhail Samoilov
DOI:
https://doi.org/10.33910/2687-1270-2025-6-4-388-403Keywords:
neuroprotection, intravital brain microscopy, hypoxic preconditioning, anoxia, hypobaric hypoxia, molecular and cellular mechanismsAbstract
Prof. Samoilov’s creative career was inextricably linked with the Pavlov Institute of Physiology of the Russian Academy of Sciences. In the late 1980s, he established methodological foundations for intravital brain microscopy. Under his leadership, the phenomenon of hypoxic neuronal preconditioning was described for the first time — in situ on feline cerebral cortex preparation, in vitro on surviving sections of rat olfactory cortex, and in vivo in a hypobaric hypoxia model in a pressure chamber — and the molecular and cellular mechanisms mediating its neuroprotective effects were characterized. Convincing evidence demonstrated that the calcium, glutamatergic, and polyphosphoinositide systems, together with cooperative activation of transcription factors, play a key role in the adaptive responses of brain neurons to hypoxic insult. On the basis of many years of fundamental research, a method of hypobaric pre‑and postconditioning was developed, in which moderate periodic hypoxia (three 2–hour sessions at 24–hour intervals, 360 mm Hg, corresponding to an altitude of 5,000 m, 10% O₂) exerted a broad spectrum of adaptive effects, increasing both cerebral and systemic resistance to damaging factors and preventing or mitigating the development of posthypoxic and poststress pathologies. The continued development of research on hypoxic pre‑and postconditioning as a foundation for novel biomedical technologies aimed at preserving and restoring health remains a central focus of the Laboratory for the Regulation of Brain Neuron Functions, established by M. O. Samoilov and led by him for more than two decades.
References
ЛИТЕРАТУРА
Баранова, К. А., Рыбникова, Е. А., Самойлов, М. О. (2015) Hейротрофин BDNF вовлекается в формирование и предотвращение постстрессовых психопатологий. Нейрохимия, т. 32, № 2, с. 131–139. https://doi.org/10.7868/S102781331502003X
Беляков, А. В., Семенов, Д. Г. (2018) Стимуляция когнитивных способностей пожилых макак умеренной гипобарической гипоксией. Успехи геронтологии, т. 31, № 6, с. 966–972.
Беляков, А. В., Семенов, Д. Г., Самойлов, М. О. (2018) Опыт исследования и коррекции когнитивных функций макак. Журнал высшей нервной деятельности им. И. П. Павлова, т. 68, № 2, с. 163–175. https://doi.org/10.7868/S004446771802003X
Ватаева, Л. А., Тюлькова, Е. И., Самойлов, М. О. (2004a) Влияние предварительного воздействия умеренной гипоксии на нарушения выработки и воспроизведения условной реакции пассивного избегания, вызываемые тяжелой гипобарической гипоксией у крыс. Журнал высшей нервной деятельности им. И. П. Павлова, т. 54, № 6, с. 835–841.
Ватаева, Л. А., Тюлькова, Е. И., Самойлов, М. О. (2004b) Влияние тяжелой гипоксии на эмоциональное поведение крыс: корректирующий эффект прекондиционирования. Доклады Академии наук, т. 395, № 3, c. 415–417.
Ветровой, О. В., Рыбникова, Е. А., Глущенко, Т. С. и др. (2014) Умеренная гипобарическая гипоксия в режиме посткондиционирования повышает экспрессию HIF-1α и эритропоэтина в СА1 поле гиппокампа крыс, переживших тяжелую гипоксию. Нейрохимия, т. 31, № 2, с. 134–139. https://doi.org/10.7868/S1027813314020137
Ветровой, О. В., Рыбникова, Е. А., Самойлов, М. О. (2017) Церебральные механизмы гипоксического/ ишемического посткондиционирования. Биохимия, т. 82, № 3, с. 542–551.
Дворкин, В. Я., Четвериков, Д. А. (1970) Фосфоинозитиды в нервной системе. Успехи современной биологии, т. 70, № 3, с. 397–412.
Дворкин, В. Я., Четвериков, Д. А., Шмелев, А. А. (1969) Обмен фосфоинозитидов в головном мозге крыс при остром кислородном голодании организма. Доклады Академии наук СССР, т. 185, № 1, с. 218–220.
Евдокимов, С. А., Самойлов, М. О., Семенов, Д. Г. (1976) Микроэлектродное отведение реакций визуально наблюдаемых нейронов коры мозга кошки. Нейрофизиология, т. 8, № 12, с. 122–125.
Кислин, М. С., Строев, С. А., Глущенко, Т. С. и др. (2013) Гипоксическое прекондиционирование модифицирует активность про- и антиоксидантных систем гиппокампа крыс. Биомедицинская химия, т. 59, № 6, с. 673–681. https://doi.org/10.18097/PBMC20135906673
Никитин, В. П., Козырев, С. А., Самойлов, М. О. (1992) Обусловливание и сенситизация у виноградной улитки: нейрофизиологические и метаболические особенности. Журнал высшей нервной деятельности им. И. П. Павлова, т. 42, № 6, с. 1260–1270.
Никитин, В. П., Самойлов, М. О. (1989) Участие кальцийсвязывающих мембранных компонентов в нейрофизиологических механизмах привыкания у виноградной улитки. Нейрофизиология, т. 21, № 5, с. 605–612.
Павлинова, Л. И., Тюлькова, Е. И., Гастева, С. В. (1986) Содержание и обмен полифосфоинозитидов мозга крыс при ишемии и в период рециркуляции. Патологическая физиология и экспериментальная терапия, т. 30, № 5, с. 34–37.
Рыбникова, Е. А., Миронова, В. И., Пивина, С. Г. и др. (2006) Гипоксическое прекондиционирование предотвращает развитие постстрессорных депрессивных состояний у крыс. Доклады Академии наук, т. 411, № 1, с. 122–125.
Рыбникова, Е. А., Миронова, В. И., Пивина, С. Г. и др. (2008) Гормональные механизмы нейропротективных эффектов гипоксического прекондиционирования у крыс. Доклады Академии наук, т. 421, № 5, с. 713–715.
Рыбникова, Е. А., Самойлов, М. О., Миронова, В. И. и др. (2007) Возможности использования гипоксического прекондиционирования для профилактики постстрессовых депрессивных эпизодов. Журнал неврологии и психиатрии им. С. С. Корсакова, т. 107, № 7, с. 43–48.
Рыбникова, Е. А., Хожай, Л. И., Тюлькова, Е. И. и др. (2004) Влияние гипобарической гипоксии на экспрессию белков ранних генов и структурные изменения нейронов мозга: корректирующий эффект прекондиционирования. Морфология, т. 125, № 2, с. 10–15.
Самойлов, М. О. (1985) Реакции нейронов мозга на гипоксию. Л.: Наука, 190 с.
Самойлов, М. О. (1999) Мозг и адаптация: молекулярно-клеточные механизмы. СПб.: Институт физиологии им. И. П. Павлова РАН, 271 с.
Самойлов, М. О., Лазаревич, Е. В., Семенов, Д. Г. и др. (2001a) Адаптивные эффекты гипоксического прекондиционирования нейронов мозга. Российский физиологический журнал им. И. М. Сеченова, т. 87, № 6, с. 714–729.
Самойлов, М. О., Майоров, В. Н., Бодрова, Л. В., Семенов, Д. Г. (1982) Применение контактной микроскопии в прижизненных исследованиях мозга. Цитология, т. 24, № 1, с. 119–123.
Самойлов, М. О., Мокрушин, А. А. (1997) Пептидная модуляция синаптической пластичности, индуцируемая аноксией. Доклады Академии наук, т. 357, № 4, с. 565–567.
Самойлов, М. О., Мокрушин, А. А. (1999) Роль объемной передачи адаптогенных сигналов в формировании приспособительных реакций мозга. Российский физиологический журнал им. И. М. Сеченова, т. 85, № 1, с. 4–20.
Самойлов, М. О., Рыбникова, Е. А. (2012) Молекулярно-клеточные и гормональные механизмы индуцированной толерантности мозга к экстремальным факторам среды. Российский физиологический журнал им. И. М. Сеченова, т. 98, № 1, с. 108–126.
Самойлов, М. О., Рыбникова, Е. А., Тюлькова, Е. И. и др. (2001b) Влияние гипобарической гипоксии на поведенческие реакции и экспрессию ранних генов в мозге крыс: корректирующий эффект прекондиционирующего воздействия. Доклады Академии наук, т. 381, № 1, с. 136–138.
Самойлов, М. О., Рыбникова, Е. А., Чурилова, А. В. (2012) Сигнальные молекулярные и гормональные механизмы формирования протективных эффектов гипоксического прекондиционирования. Патологическая физиология и экспериментальная терапия, т. 56, № 3, с. 3–10.
Самойлов, М. О., Семенов, Д. Г. (1978) Прижизненное морфологическое исследование коры больших полушарий мозга. В кн.: В. Н. Майоров, В. Г. Лукашин, Л. А. Подольская и др. Прижизненная микроскопия нейрона. Л.: Наука, с. 58–72.
Самойлов, М. О., Семенов, Д. Г., Тюлькова, Е. И., Болехан, Е. А. (1992) Вовлечение внутриклеточных регуляторных систем в механизмы восстановления активности нейронов коры головного мозга после аноксии. Российский физиологический журнал им. И. М. Сеченова, т. 78, № 6, с. 11–17.
Самойлов, М. О., Семенов, Д. Г., Тюлькова, Е. И., Болехан, Е. А. (1994a) Влияние краткосрочной аноксии на механизмы внутриклеточной сигнальной трансдукции в коре головного мозга. Российский физиологический журнал им. И. М. Сеченова, т. 80, № 11, с. 37–43.
Самойлов, М. О., Семенов, Д. Г., Тюлькова, Е. И., Болехан, Е. А. (1994b) Молекулярно-клеточные механизмы протектирующего эффекта краткосрочной аноксии. Российский физиологический журнал им. И. М. Сеченова, т. 80, № 12, с. 71–75.
Самойлов, М. О., Ситник, Н. А., Рыбникова, Е. А. и др. (2005) Особенности экспрессии про- и антиапоптических белков Bax и Bcl-2 в нейронах мозга крыс в ответ на тяжелую гипобарическую гипоксию: корректирующий эффект гипоксического прекондиционирования. Доклады Академии наук, т. 402, № 4, с. 563–565.
Самойлов, М. О., Чурилова, А. В., Глущенко, Т. С., Рыбникова, Е. А. (2016) Особенности влияния различных режимов гипобарической гипоксии на содержание эпигенетических факторов в нейронах неокортекса крыс. Бюллетень экспериментальной биологии и медицины, т. 162, № 12, с. 686–690.
Самойлов, М. О., Чурилова, А. В., Глущенко, Т. С., Рыбникова, Е. А. (2017) Влияние различных режимов гипобарической гипоксии на метилирование гистона Н3 в нейронах неокортекса и гиппокампа крыс. Нейрохимия, т. 34, № 3, с. 218–226. https://doi.org/10.7868/S102781331702011X
Семенов, Д. Г. (1978) Мембранный потенциал переживающего нейрона коры головного мозга. Физиологический журнал СССР им. И. М. Сеченова, т. 64, № 3, с. 410–413.
Семенов, Д. Г., Тюлькова, Е. И., Самойлов, М. О. (1995) Внутриклеточные механизмы глутамат- и холинергической сигнальной трансдукции, вовлекаемые в адаптивные реакции коры головного мозга. Российский физиологический журнал им. И. М. Сеченова, т. 81, № 8, с. 51–56.
Семенов, Д. Г., Тюлькова, Е. И., Самойлов, М. О., Лазаревич, Е. В. (1999) Участие внутриклеточных регуляторных систем в адаптивных эффектах краткосрочной аноксии in vitro. Российский физиологический журнал им. И. М. Сеченова, т. 85, № 1, с. 137–145.
Тюлькова, Е. И., Ватаева, Л. А., Самойлов, М. О., Отеллин, В. А. (2010) Механизмы формирования реакций мозга на действие гипобарической гипоксии в различные сроки пренатального периода развития у крыс. Журнал акушерства и женских болезней, т. 59, № 4, с. 99–110.
Тюлькова, Е. И., Семенов, Д. Г., Самойлов, М. О. (1998) Участие кальциевой и фосфоинозитидной систем внутриклеточной регуляции в адаптации нейронов срезов обонятельной коры к гипоксии in vitro. Бюллетень экспериментальной биологии и медицины, т. 125, № 3, с. 259–262.
Bickler, P. E., Hansen, B. M. (1994) Causes of calcium accumulation in rat cortical brain slices during hypoxia and ischemia: Role of ion channels and membrane damage. Brain Research, vol. 665, no. 2, pp. 269–276. https://doi.org/10.1016/0006-8993(94)91347-1
Kirino, T., Tsujita, Y., Tamura, A. (1991) Induced tolerance to ischemia in gerbil hippocampal neurons. Journal of Cerebral Blood Flow & Metabolism, vol. 11, no. 2, pp. 299–307. https://doi.org/10.1038/jcbfm.1991.62
Lazarewicz, J. W., Samoilov, M. O., Semenov, D. G. (1987) Changes of intracellular calcium homeostasis in brain cortical structures during anoxia in vivo and in vitro. Resuscitation, vol. 15, no. 4, pp. 245–255. https://doi.org/10.1016/0300-9572(87)90003-7
Murry, C. E., Jennings, R. B., Reimer, K. A. (1986) Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation, vol. 74, no. 5, pp. 1124–1136. https://doi.org/10.1161/01.cir.74.5.1124
Rybnikova, E. A., Baranova, K. A., Gluschenko, T. S. et al. (2015) Role of HIF-1 in neuronal mechanisms of adaptation to psychoemotional and hypoxic stress. International Journal of Physiology and Pathophysiology, vol. 6, no. 1, pp. 1–11. https://doi.org/10.1615/IntJPhysPathophys.v6.i1.10
Rybnikova, E. A., Baranova, K. A., Zenko, M. Y. (2025) Effect of intermittent hypoxia on the expression of glucocorticoid receptors and hypoxia-inducible factor in rat brain. Bulletin of Experimental Biology and Medicine, vol. 179, no. 1, pp. 94–98. https://doi.org/10.1007/s10517-025-06436-5
Rybnikova, E. A., Samoilov, M. O. (2015) Сurrent insights into the molecular mechanisms of hypoxic pre- and postconditioning using hypobaric hypoxia. Review. Frontiers in Neuroscience, vol. 9, article 388. http://dx.doi.org/10.3389/fnins.2015.00388
Rybnikova, E., Sitnik, N., Gluschenko, T. et al. (2006) The preconditioning modified neuronal expression of apoptosis-related proteins of Bcl-2 superfamily following severe hypobaric hypoxia in rats. Brain Research, vol. 1089, no. 1, pp. 195–202. https://doi.org/10.1016/j.brainres.2006.03.053
Rybnikova, E., Tulkova, E., Pelto-Huikko, M., Samoilov, M. (2002) Mild preconditioning hypoxia modifies nerve growth factor-induced gene A messenger RNA expression in the rat brain induced by severe hypoxia. Neuroscience Letters, vol. 329, no. 1, pp. 49–52. https://doi.org/10.1016/s0304-3940(02)00577-3
Rybnikova, E., Vataeva, L., Tyulkova, E. et al. (2005) Mild hypoxia preconditioning prevents impairment of passive avoidance learning and suppression of brain NGFI-A expression induced by severe hypoxia. Behavioural Brain Research, vol. 160, no. 1, pp. 107–114. https://doi.org/10.1016/j.bbr.2004.11.023
Samoilov, M., Churilova, A., Gluschenko, T. et al. (2016) Acetylation of histones in neocortex and hippocampus of rats exposed to different modes of hypobaric hypoxia: Implications for brain hypoxic injury and tolerance. Acta Histochemica, vol. 118, no. 2, pp. 80–89. https://doi.org/10.1016/j.acthis.2015.11.008
Samoilov, M. O., Rybnikova, E. A., Sitnik, N. A. et al. (2007) Preconditioning modifies the activities of mitogen-activated protein kinases and c-Jun transcription factor in rat hippocampus after severe hypobaric hypoxia. Neurochemical Journal, vol. 1, no. 3, pp. 219–226. https://doi.org/10.1134/S1819712407030087
Samoilov, M. O., Semenov, D. G., Tyulkova, E. I., Lazarevich, J. W. (1992) Early postanoxic changes of polyphosphoinositides and bound Ca2+ content in relation to neuronal activity in brain cortex. Resuscitation, vol. 23, no. 1, pp. 33–43. https://doi.org/10.1016/0300-9572(92)90160-e
Semenov, D. G., Samoilov, M. O., Lazarewicz, J. W. (2002) Calcium transients in the model of rapidly induced anoxic tolerance in rat cortical slices: Involvement of NMDA receptors. Neurosignals, vol. 11, no. 6, pp. 329–335. https://doi.org/10.1159/000068255
Semenov, D. G., Samoilov, M. O., Lazarewicz, J. W. (2009) Preconditioning reduces hypoxia-evoked alterations in glutamatergic Ca2+ signaling in rat cortex. Acta Neurobiologiae Experimentalis, vol. 68, no. 2, pp. 169–179. https://doi.org/10.55782/ane-2008-1686
Semenov, D. G., Samoilov, M. O., Zielonka, P., Lazarewicz, J. W. (2000a) Responses to reversible anoxia of intracellular free and bound Ca2+ in rat cortical slices. Resuscitation, vol. 44, no. 3, pp. 207–214. https://doi.org/10.1016/s0300-9572(00)00136-2
Semenov, D., Tyul’kova, E. I., Samoilov, M. O., Lazarevich, E. V. (2000b). Involvement of intracellular regulatory systems in the adaptive effects of transient anoxia in vitro. Neuroscience and Behavioral Physiology, vol. 30, no. 3, pp. 357–363. https://doi.org/10.1007/BF02471790
Stroev, S. A., Tjulkova, E. I., Gluschenko, T. S. et al. (2004a) The augmentation of brain thioredoxin-1 expression after severe hypobaric hypoxia by the preconditioning in rats. Neuroscience Letters, vol. 370, no. 2–3, pp. 224–229. https://doi.org/10.1016/j.neulet.2004.08.022
Stroev, S. A., Gluschenko, T. S., Tjulkova, E. I. et al. (2004b) Preconditioning enhances the expression of mitochondrial antioxidant thioredoxin-2 in the forebrain of rats exposed to severe hypobaric hypoxia. Journal of Neuroscience Research, vol. 78, no. 4, pp. 563–569. https://doi.org/10.1002/jnr.20282
Vetrovoy, O., Sarieva, K., Galkina, O. et al. (2019) Neuroprotective mechanism of hypoxic post-conditioning involves HIF1-associated regulation of the pentose phosphate pathway activity in rat brain. Neurochemical Research, vol. 44, no. 6, pp. 1425–1436. https://doi.org/10.1007/s11064-018-2681-x
Vetrovoy, O., Sarieva, K., Lomert, E. et al (2020) Pharmacological HIF1 inhibition eliminates downregulation of the pentose phosphate pathway and prevents neuronal apoptosis in rat hippocampus caused by severe hypoxia. Journal of Molecular Neuroscience, vol. 70, no. 5, pp. 635–646. https://doi.org/10.1007/s12031-019-01469-8
Vetrovoy, O., Stratilov, V., Nimiritsky, P. et al. (2021a) Prenatal hypoxia induces premature aging accompanied by impaired function of the glutamatergic system in rat hippocampus. Neurochemical Research, vol. 46, no. 3, pp. 550–563. https://doi.org/10.1007/s11064-020-03191-z
Vetrovoy, O., Tulkova, E., Sarieva, K. et al. (2017) Neuroprotective effect of hypobaric hypoxic postconditioning is accompanied by DNA protection and lipid peroxidation changes in rat hippocampus. Neuroscience Letters, vol. 639, pp. 49–52. https://doi.org/10.1016/j.neulet.2016.12.054
Vetrovoy, O., Tyulkova, E., Stratilov, V. et al. (2021b) Long-term effects of prenatal severe hypoxia on central and peripheral components of the glucocorticoid system in rats. Developmental Neuroscience, vol. 42, no. 2-4, pp. 145–158. https://doi.org/10.1159/000512223
REFERENCES
Baranova, K. A., Rybnikova, E. A., Samoilov, M. O. (2015) Nejrotrofin BDNF vovlekaetsya v formirovanie i predotvrashchenie poststressovykh psikhopatologij [The neurotrophin BDNF is involved in the development and prevention of stress-induced psychopathologies]. Nejrokhimiya, vol. 32, no. 2, pp. 131–139. https://doi.org/10.7868/S102781331502003X (In Russian)
Belyakov, A. V., Semenov, D. G. (2018) Stimulyatsiya kognitivnykh sposobnostej pozhilykh makak umerennoj gipobaricheskoj gipoksiej [Stimulation of cognitive abilities in aged macaques by moderate hypobaric hypoxia]. Uspekhi gerontologii — Advances in Gerontology, vol. 31, no. 6, pp. 966–972. (In Russian)
Belyakov, A. V., Semenov, D. G., Samoilov, M. O. (2018) Opyt issledovaniya i korrektsii kognitivnykh funktsij makak [The experience of investigation and correction of cognitive functions of macaca mulatta]. Zhurnal vysshej nervnoj deyatel’nosti im. I. P. Pavlova, vol. 68, no. 2, pp. 163–175. https://doi.org/10.7868/S004446771802003X (In Russian)
Bickler, P. E., Hansen, B. M. (1994) Causes of calcium accumulation in rat cortical brain slices during hypoxia and ischemia: Role of ion channels and membrane damage. Brain Research, vol. 665, no. 2, pp. 269–276. https://doi.org/10.1016/0006-8993(94)91347-1 (In English)
Dvorkin, V. Ia., Chetverikov, D. A. (1970) Fosfoinozitidy v nervnoj sisteme [Phosphoinositides in the nervous system]. Uspekhi sovremennoj biologii, vol. 70, no. 3, pp. 397–412. (In Russian)
Dvorkin, V. Ya., Chetverikov, D. A., Shmelev, A. A. (1969) Obmen fosfoinozitidov v golovnom mozge krys pri ostrom kislorodnom golodanii organizma [Phosphoinositide metabolism in the rat brain during acute oxygen starvation]. Doklady Akademii nauk SSSR, vol. 185, no. 1, pp. 218–220. (In Russian)
Evdokimov, S. A., Samoilov, M. O., Semenov, D. G. (1976) Mikroelektrodnoe otvedenie reaktsij vizual’no nablyudaemykh nejronov kory mozga koshki [Microelectrode recording of the reactions of visually observed neurons of the cat cerebral cortex]. Nejrofiziologiya, vol. 8, no. 12, pp. 122–125. (In Russian)
Kirino, T., Tsujita, Y., Tamura, A. (1991) Induced tolerance to ischemia in gerbil hippocampal neurons. Journal of Cerebral Blood Flow & Metabolism, vol. 11, no. 2, pp. 299–307. https://doi.org/10.1038/jcbfm.1991.62 (In English)
Kislin, M. S., Stroev, S. A., Gluschenko, T. S. et al. (2013) Gipoksicheskoe prekonditsionirovanie modifitsiruet aktivnost’ pro- i antioksidantnykh sistem gippokampa krys [Hypoxic preconditioning modifies the activity of pro- and antioxidant systems in rat hippocampus]. Biomeditsinskaya khimiya, vol. 59, no. 6, pp. 673–681. https://doi.org/10.18097/PBMC20135906673 (In Russian)
Lazarewicz, J. W., Samoilov, M. O., Semenov, D. G. (1987) Changes of intracellular calcium homeostasis in brain cortical structures during anoxia in vivo and in vitro. Resuscitation, vol. 15, no. 4, pp. 245–255. https://doi.org/10.1016/0300-9572(87)90003-7 (In English)
Murry, C. E., Jennings, R. B., Reimer, K. A. (1986) Preconditioning with ischemia: A delay of lethal cell injury in ischemic myocardium. Circulation, vol. 74, no. 5, pp. 1124–1136. https://doi.org/10.1161/01.cir.74.5.1124 (In English)
Nikitin, V. P., Kozyrev, S. A., Samoilov, M. O. (1992) Obuslovlivanie i sensitizatsiya u vinogradnoj ulitki: nejrofiziologicheskie i metabolicheskie osobennosti [Conditioning and sensitization in the snail: Neurophysiological and metabolic characteristics]. Zhurnal vysshej nervnoj deyatel’nosti im. I. P. Pavlova, vol. 42, no. 6, pp. 1260–1270. (In Russian)
Nikitin, V. P., Samoilov, M. O. (1989) Uchastie kal’tsijsvyazyvayushchikh membrannykh komponentov v nejrofiziologicheskikh mekhanizmakh privykaniya u vinogradnoj ulitki [Involvement of calcium-binding membrane components in neurophysiological mechanics of habituation in Helix pomatia]. Nejrofiziologiya, vol. 21, no. 5, pp. 605–612. (In Russian)
Pavlinova, L. I., Tiul’kova, E. I., Gasteva, S. V. (1986) Soderzhanie i obmen polifosfoinozitidov mozga krys pri ishemii i v period retsirkulyatsii [Polyphosphatidylinositol level and metabolism in the brain in ischemia and in the recirculation period]. Patologicheskaya fiziologiya i eksperimental’naya terapiya, vol. 30, no. 5, pp. 34–37. (In Russian)
Rybnikova, E. A., Baranova, K. A., Gluschenko, T. S. et al. (2015) Role of HIF-1 in neuronal mechanisms of adaptation to psychoemotional and hypoxic stress. International Journal of Physiology and Pathophysiology, vol. 6, no. 1, pp. 1–11. https://doi.org/10.1615/IntJPhysPathophys.v6.i1.10 (In English)
Rybnikova, E. A., Baranova, K. A., Zenko, M. Y. (2025) Effect of intermittent hypoxia on the expression of glucocorticoid receptors and hypoxia-inducible factor in rat brain. Bulletin of Experimental Biology and Medicine, vol. 179, no. 1, pp. 94–98. https://doi.org/10.1007/s10517-025-06436-5 (In English)
Rybnikova, E. A., Khozhai, L. I., Tiul’kova, E. I. et al. (2004) Vliyanie gipobaricheskoj gipoksii na ekspressiyu belkov rannikh genov i strukturnye izmeneniya nejronov mozga: korrektiruyushchij effekt prekonditsionirovaniya [Early genes expression, structural neuron changes in hypobaric hypoxia and correcting effect of preconditioning]. Morfologiya — Morphology, vol. 125, no. 2, pp. 10–15. (In Russian)
Rybnikova, E. A., Mironova, V. I., Pivina, S. G. et al. (2006) Gipoksicheskoe prekonditsionirovanie predotvrashchaet razvitie poststressornykh depressivnykh sostoyanij u krys [Hypoxic preconditioning prevents development of post-stress depressions in rats]. Doklady Akademii nauk, vol. 411, no. 1, pp. 122–125. (In Russian)
Rybnikova, E. A., Mironova, V. I., Pivina, S. G. et al. (2008) Gormonal’nye mekhanizmy nejroprotektivnykh effektov gipoksicheskogo prekonditsionirovaniya u krys [Hormonal mechanisms of neuroprotective effects of the mild hypoxic preconditioning in rats]. Doklady Akademii nauk, vol. 421, no. 5, pp. 713–715. (In Russian)
Rybnikova, E. A., Samoilov, M. O. (2015) Сurrent insights into the molecular mechanisms of hypoxic pre- and postconditioning using hypobaric hypoxia. Review. Frontiers in Neuroscience, vol. 9, article 388. http://dx.doi.org/10.3389/fnins.2015.00388 (In English)
Rybnikova, E. A., Samoilov, M. O., Mironova, V. I. et al (2007) Vozmozhnosti ispol’zovaniya gipoksicheskogo prekonditsionirovaniya dlya profilaktiki poststressovykh depressivnykh epizodov [The feasible applications of hypoxic preconditioning for prevention of post-stress depressive episodes]. Zhurnal nevrologii i psikhiatrii im. S. S. Korsakova — S. S. Korsakov Journal of Neurology and Psychiatry, vol. 107, no. 7, pp. 43–48. (In Russian)
Rybnikova, E., Sitnik, N., Gluschenko, T. et al. (2006) The preconditioning modified neuronal expression of apoptosis-related proteins of Bcl-2 superfamily following severe hypobaric hypoxia in rats. Brain Research, vol. 1089, no. 1, pp. 195–202. https://doi.org/10.1016/j.brainres.2006.03.053 (In English)
Rybnikova, E., Tulkova, E., Pelto-Huikko, M., Samoilov, M. (2002) Mild preconditioning hypoxia modifies nerve growth factor-induced gene A messenger RNA expression in the rat brain induced by severe hypoxia. Neuroscience Letters, vol. 329, no. 1, pp. 49–52. https://doi.org/10.1016/s0304-3940(02)00577-3 (In English)
Rybnikova, E., Vataeva, L., Tyulkova, E. et al. (2005) Mild hypoxia preconditioning prevents impairment of passive avoidance learning and suppression of brain NGFI-A expression induced by severe hypoxia. Behavioural Brain Research, vol. 160, no. 1, pp. 107–114. https://doi.org/10.1016/j.bbr.2004.11.023 (In English)
Samoilov, M. O. (1985) Reaktsii nejronov mozga na gipoksiyu [Reactions of brain neurons to hypoxia]. Leningrad: Nauka Publ., 190 p. (In Russian)
Samoilov, M. O. (1999) Mozg i adaptatsiya: molekulyarno-kletochnye mekhanizmy [Brain and adaptation. Molecular-cellular mechanisms]. Saint Petersburg: Pavlov Institute of Physiology RAS Publ., 271 p. (In Russian)
Samoilov, M. O., Churilova, A. V., Glushchenko, T. S., Rybnikova, E. A. (2016) Osobennosti vliyaniya razlichnykh rezhimov gipobaricheskoj gipoksii na soderzhanie epigeneticheskikh faktorov v nejronakh neokorteksa krys [Effects of different modes of hypobaric hypoxia on the content of epigenetic factors in the rat in neurons of rat neocortex]. Byulleten’ eksperimental’noj biologii i meditsiny, vol. 162, no. 12, pp. 686–690. (In Russian)
Samoilov, M. O., Churilova, A. V., Glushchenko, T. S., Rybnikova, E. A. (2017) Vliyanie razlichnykh rezhimov gipobaricheskoj gipoksii na metilirovanie gistona N3 v nejronakh neokorteksa i gippokampa krys [The influence of different types of hypobaric hypoxia on histone H3 methylation in rat neocortical and hippocampal neurons]. Nejrokhimiya, vol. 34, no. 3, pp. 218–226. https://doi.org/10.7868/S102781331702011X (In Russian)
Samoilov, M., Churilova, A., Gluschenko, T. et al. (2016) Acetylation of histones in neocortex and hippocampus of rats exposed to different modes of hypobaric hypoxia: Implications for brain hypoxic injury and tolerance. Acta Histochemica, vol. 118, no. 2, pp. 80–89. https://doi.org/10.1016/j.acthis.2015.11.008 (In English)
Samoilov, M. O., Lazarevich, E. V., Semenov, D. G. et al. (2001a) Adaptivnye effekty gipoksicheskogo prekonditsionirovaniya nejronov mozga [Adaptive effects of hypoxic preconditioning in brain neurons]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 87, no. 6, pp. 714–729. (In Russian)
Samoilov, M. O., Maiorov, V. N., Bodrova, L. V., Semenov, D. G. (1982) Primenenie kontaktnoj mikroskopii v prizhiznennykh issledovaniyakh mozga [Use of contact microscopy in intravital studies of the neurons]. Tsitologiya, vol. 24, no. 1, pp. 119–123. (In Russian)
Samoilov, M. O., Mokrushin, A. A. (1997) Peptidnaya modulyatsiya sinapticheskoj plastichnosti, indutsiruemaya anoksiej [Peptide modulation of synaptic plasticity induced by anoxia]. Doklady Akademii nauk, vol. 357, no. 4, pp. 565–567. (In Russian)
Samoilov, M. O., Mokrushin, A. A. (1999) Rol’ ob’emnoj peredachi adaptogennykh signalov v formirovanii prisposobitel’nykh reaktsij mozga [The role of volume transmission of the adaptogenic signals in the formation of adaptive brain responses]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 85, no. 1, pp. 4–20. (In Russian)
Samoilov, M. O., Rybnikova, E. A. (2012) Molekulyarno-kletochnye i gormonal’nye mekhanizmy indutsirovannoj tolerantnosti mozga k ekstremal’nym faktoram sredy [Molecular-cellular and hormonal mechanisms of induced brain tolerance of extreme factors]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 98, no. 1, pp. 108–126. (In Russian)
Samoilov, M. O., Rybnikova, E. A., Churilova, A. V. (2012) Signal’nye molekulyarnye i gormonal’nye mekhanizmy formirovaniya protektivnykh effektov gipoksicheskogo prekonditsionirovaniya [Signal molecular and hormonal mechanisms of formation of the hypoxic preconditioning protective effects]. Patologicheskaya fiziologiya i eksperimental’naya terapiya — Pathological Physiology and Experimental Therapy, vol. 56, no. 3, pp. 3–10. (In Russian)
Samoilov, M. O., Rybnikova, E. A., Sitnik, N. A. et al. (2007) Preconditioning modifies the activities of mitogen-activated protein kinases and c-Jun transcription factor in rat hippocampus after severe hypobaric hypoxia. Neurochemical Journal, vol. 1, no. 3, pp. 219–226. https://doi.org/10.1134/S1819712407030087 (In English)
Samoilov, M. O., Rybnikova, E. A., Tulkova, E. I. et al. (2001b) Vliyanie gipobaricheskoj gipoksii na povedencheskie reaktsii i ekspressiyu rannikh genov v mozge krys: korrektiruyushchij effekt prekonditsioniruyushchego vozdejstviya [Hypobaric hypoxia affects rat behavior and immediate early gene expression in the brain: The corrective effect of preconditioning]. Doklady Akademii nauk, vol. 381, no. 1, pp. 136–138. (In Russian)
Samoilov, M. O., Semenov, D. G. (1978) Prizhiznennoe morfologicheskoe issledovanie kory bol’shikh polusharij mozga [Lifetime morphological study of the cerebral cortex]. In: V. N. Majorov, V. G. Lukashin, L. A. Podol’skaya et al. Prizhiznennaya mikroskopiya nejrona [Neuron lifetime microscopy]. Leningrad: Nauka Publ., pp. 58–72. (In Russian)
Samoilov, M. O., Semenov, D. G., Tyul’kova, E. I., Bolekhan, E. A. (1992) Vovlechenie vnutrikletochnykh regulyatornykh sistem v mekhanizmy vosstanovleniya aktivnosti nejronov kory golovnogo mozga posle anoksii [The involvement of intracellular regulatory systems in the mechanisms of the recovery of the neuronal activity of the cerebral cortex in anoxia]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 78, no. 6, pp. 11–17. (In Russian)
Samoilov, M. O., Semenov, D. G., Tiul’kova, E. I., Bolekhan, E. A. (1994a) Vliyanie kratkosrochnoj anoksii na mekhanizmy vnutrikletochnoj signal’noj transduktsii v kore golovnogo mozga [The effect of short-term anoxia on the mechanisms of intracellular signal transduction in the cat cerebral cortex]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 80, no. 11, pp. 37–43. (In Russian)
Samoilov, M. O., Semenov, D. G., Tiul’kova, E. I., Bolekhan, E. A. (1994b) Molekulyarno-kletochnye mekhanizmy protektiruyushchego effekta kratkosrochnoj anoksii [The molecular cellular mechanisms of the protective effect of short-term anoxia]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 80, no. 12, pp. 71–75. (In Russian)
Samoilov, M. O., Semenov, D. G., Tyulkova, E. I., Lazarevich, J. W. (1992) Early postanoxic changes of polyphosphoinositides and bound Ca2+ content in relation to neuronal activity in brain cortex. Resuscitation, vol. 23, no. 1, pp. 33–43. https://doi.org/10.1016/0300-9572(92)90160-e (In English)
Samoilov, M. O., Sitnik, N. A., Rybnikova, E. A. et al. (2005) Osobennosti ekspressii pro- i antiapopticheskikh belkov Bax i Bcl-2 v nejronakh mozga krys v otvet na tyazheluyu gipobaricheskuyu gipoksiyu: korrektiruyushchij effekt gipoksicheskogo prekonditsionirovaniya [The expression pattern of pro- and antiapoptotic proteins Bax and Bcl-2 in rat brain neurons in response to severe hypobaric hypoxia: The correcting effect of hypoxic preconditioning]. Doklady Akademii nauk, vol. 402, no. 4, pp. 563–565. (In Russian)
Semenov, D. G. (1978) Membrannyj potentsial perezhivayushchego nejrona kory golovnogo mozga [Membrane potential of the surviving neurons in the cerebral cortex]. Fiziologicheskij zhurnal SSSR im. I. M. Sechenova, vol. 64, no. 3, pp. 410–413. (In Russian)
Semenov, D. G., Samoilov, M. O., Lazarewicz, J. W. (2002) Calcium transients in the model of rapidly induced anoxic tolerance in rat cortical slices: Involvement of NMDA receptors. Neurosignals, vol. 11, no. 6, pp. 329–335. https://doi.org/10.1159/000068255 (In English)
Semenov, D. G., Samoilov, M. O., Lazarewicz, J. W. (2009) Preconditioning reduces hypoxia-evoked alterations in glutamatergic Ca2+ signaling in rat cortex. Acta Neurobiologiae Experimentalis, vol. 68, no. 2, pp. 169–179. https://doi.org/10.55782/ane-2008-1686 (In English)
Semenov, D. G., Samoilov, M. O., Zielonka, P., Lazarewicz, J. W. (2000a) Responses to reversible anoxia of intracellular free and bound Ca2+ in rat cortical slices. Resuscitation, vol. 44, no. 3, pp. 207–214. https://doi.org/10.1016/s0300-9572(00)00136-2 (In English)
Semenov, D. G., Tyul’kova, E. I., Samojlov, M. O. (1995) Vnutrikletochnye mekhanizmy glutamat- i kholinergicheskoj signal’noj transduktsii, vovlekaemye v adaptivnye reaktsii kory golovnogo mozga [Intracellular mechanisms of glutaminergic and cholinergic signal transduction in the cerebral cortex]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 81, no. 8, pp. 51–56. (In Russian)
Semenov, D. G., Tiul’kova, E. I., Samoilov, M. O., Lazarevich, E. V. (1999) Uchastie vnutrikletochnykh regulyatornykh sistem v adaptivnykh effektakh kratkosrochnoj anoksii in vitro [Involvement of the intracellular regulatory systems in the adaptive effect of short-term anoxia in vitro]. Rossijskij fiziologicheskij zhurnal im. I. M. Sechenova — Russian Journal of Physiology, vol. 85, no. 1, pp. 139–148. (In Russian)
Semenov, D., Tyul’kova, E. I., Samoilov, M. O., Lazarevich, E. V. (2000b). Involvement of intracellular regulatory systems in the adaptive effects of transient anoxia in vitro. Neuroscience and Behavioral Physiology, vol. 30, no. 3, pp. 357–363. https://doi.org/10.1007/BF02471790 (In English)
Stroev, S. A., Gluschenko, T. S., Tjulkova, E. I. et al. (2004b) Preconditioning enhances the expression of mitochondrial antioxidant thioredoxin-2 in the forebrain of rats exposed to severe hypobaric hypoxia. Journal of Neuroscience Research, vol. 78, no. 4, pp. 563–569. https://doi.org/10.1002/jnr.20282 (In English)
Stroev, S. A., Tjulkova, E. I., Gluschenko, T. S. et al. (2004a) The augmentation of brain thioredoxin-1 expression after severe hypobaric hypoxia by the preconditioning in rats. Neuroscience Letters, vol. 370, no. 2–3, pp. 224–229. https://doi.org/10.1016/j.neulet.2004.08.022 (In English)
Tyul’kova, E. I., Semenov, D. G., Samoilov, M. O. (1998) Uchastie kal’tsievoj i fosfoinozitidnoj sistem vnutrikletochnoj regulyatsii v adaptatsii nejronov srezov obonyatel’noj kory k gipoksii in vitro [The participation of calcium and phosphoinositide systems of intracellular regulation in the adaptation of neurons of sections of the olfactory cortex to hypoxia in vitro]. Byulleten’ eksperimental’noj biologii i meditsiny, vol. 125, no. 3, pp. 259–262. (In Russian)
Tiul’kova, E. I., Vataeva, L. A., Samoilov, M. O., Otellin, V. A. (2010) Mekhanizmy formirovaniya reaktsij mozga na dejstvie gipobaricheskoj gipoksii v razlichnye sroki prenatal’nogo perioda razvitiya u krys [The mechanisms of hypobaric hypoxia-induced alteration in brain development. Influence of gestational age at exposure]. Zhurnal akusherstva i zhenskikh boleznej, vol. 59, no. 4, pp. 99–110. (In Russian)
Vataeva, L. A., Tyulkova, E. I., Samoilov, M. O. (2004a) Vliyanie predvaritel’nogo vozdejstviya umerennoj gipoksii na narushenie vyrabotki i vosproizvedeniya uslovnoj reaktsii passivnogo izbeganiya, vyzyvaemye tyazheloj gipobaricheskoj gipoksiej u krys [The effect of preceding mild hypoxia on the alteration of the acquisition and retention of passive avoidance behavior caused by severe hypobaric hypoxia in rats]. Zhurnal vysshej nervnoj deyatel’nosti im. I. P. Pavlova, vol. 54, no. 6, pp. 835–841. (In Russian)
Vataeva, L. A., Tyul’kova, E. I., Samoilov, M. O. (2004b) Vliyanie tyazheloj gipoksii na emotsional’noe povedenie krys: korrektiruyushchij effekt prekonditsionirovaniya [Influence of severe hypoxia on rat emotional behavior: The modifying effect of preconditioning]. Doklady Akademii nauk, vol. 395, no. 3, pp. 415–417. (In Russian)
Vetrovoy, O. V., Rybnikova, E. A., Glushenko, T. S. et al. (2014) Umerennaya gipobaricheskaya gipoksiya v rezhime postkonditsionirovaniya povyshaet ekspressiyu HIF-1α i eritropoetina v SA1 pole gippokampa krys, perezhivshikh tyazheluyu gipoksiyu [Mild hypobaric hypoxic postconditioning increases the expression of HIF-1α and erythropoietin in the CA1 field of the hippocampus of rats that survive after severe hypoxia]. Nejrokhimiya, vol. 31, no. 2, pp. 134–139. https://doi.org/10.7868/S1027813314020137 (In Russian)
Vetrovoy, O. V., Rybnikova, E. A., Samoilov, M. O. (2017) Tserebral’nye mekhanizmy gipoksicheskogo/ishemicheskogo postkonditsionirovaniya [Cerebral mechanisms of hypoxic/ischemic postconditioning]. Biokhimiya, vol. 82, no. 3, pp. 542–551. (In Russian)
Vetrovoy, O., Sarieva, K., Galkina, O. et al. (2019) Neuroprotective mechanism of hypoxic post-conditioning involves HIF1-associated regulation of the pentose phosphate pathway activity in rat brain. Neurochemical Research, vol. 44, no. 6, pp. 1425–1436. https://doi.org/10.1007/s11064-018-2681-x (In English)
Vetrovoy, O., Sarieva, K., Lomert, E. et al (2020) Pharmacological HIF1 inhibition eliminates downregulation of the pentose phosphate pathway and prevents neuronal apoptosis in rat hippocampus caused by severe hypoxia. Journal of Molecular Neuroscience, vol. 70, no. 5, pp. 635–646. https://doi.org/10.1007/s12031-019-01469-8 (In English)
Vetrovoy, O., Stratilov, V., Nimiritsky, P. et al. (2021a) Prenatal hypoxia induces premature aging accompanied by impaired function of the glutamatergic system in rat hippocampus. Neurochemical Research, vol. 46, no. 3, pp. 550–563. https://doi.org/10.1007/s11064-020-03191-z (In English)
Vetrovoy, O., Tulkova, E., Sarieva, K. et al. (2017) Neuroprotective effect of hypobaric hypoxic postconditioning is accompanied by DNA protection and lipid peroxidation changes in rat hippocampus. Neuroscience Letters, vol. 639, pp. 49–52. https://doi.org/10.1016/j.neulet.2016.12.054 (In English)
Vetrovoy, O., Tyulkova, E., Stratilov, V. et al. (2021b) Long-term effects of prenatal severe hypoxia on central and peripheral components of the glucocorticoid system in rats. Developmental Neuroscience, vol. 42, no. 2-4, pp. 145–158. https://doi.org/10.1159/000512223 (In English)
Downloads
Published
Issue
Section
License
Copyright (c) 2025 Dmitry G. Semenov, Ekaterina I. Tyulkova, Elena A. Rybnikova
This work is licensed under a Creative Commons Attribution 4.0 International License.
The work is provided under the terms of the Public Offer and of Creative Commons public license Creative Commons Attribution 4.0 International (CC BY 4.0).
This license permits an unlimited number of users to copy and redistribute the material in any medium or format, and to remix, transform, and build upon the material for any purpose, including commercial use.
This license retains copyright for the authors but allows others to freely distribute, use, and adapt the work, on the mandatory condition that appropriate credit is given. Users must provide a correct link to the original publication in our journal, cite the authors' names, and indicate if any changes were made.
Copyright remains with the authors. The CC BY 4.0 license does not transfer rights to third parties but rather grants users prior permission for use, provided the attribution condition is met. Any use of the work will be governed by the terms of this license.
