Genome and stress-reaction in animals and humans

Cover Page

Cite item

Full Text

Abstract

Current data on the effects of stress at the level of the cell genomes of the central nervous system and peripheral organs in animals are discussed. Regulatory and structural genomic changes in the cells of the central nervous system under stress are considered as a mechanism for regulating the functions of the brain and peripheral organs that form the organism manifestations of stress. Based on the Yu.Ya. Kerkis and M.E. Lobashev point of view, we consider stress as a special physiological state of the nervous system, affecting the work and integrity of the genome in target cells in animals, and thus playing a major role in microevolutionary transformations.

About the authors

Natalya A. Dyuzhikova

Pavlov Institute of Physiology of the RAS

Author for correspondence.
Email: dyuzhikova@mail.ru
SPIN-code: 6206-3889

PhD, ScD, Head of the Lab of Genetics of Higher Nervous Activity

Russian Federation, Saint Petersburg

Eugene V. Daev

Saint Petersburg State University

Email: mouse_gene@mail.ru

PhD, ScD, Professor, Department of Genetics and Biotechnology

Russian Federation, Saint Petersburg

References

  1. Cannon WB. The wisdom of the body. New York: W.W. Norton & Co; 1932.
  2. Селье Г. Очерки об адаптационном синдроме. – М.: МЕДГИЗ, 1960. [Sel’e G. The Story of the Adaptation Syndrome. Moscow: MEDGIZ; 1960. (In Russ.)]
  3. Лобашев М.Е., Пономаренко В.В., Полянская Г.Г., Цапыгина Р.И. О роли нервной системы в регуляции генетических и цитогенетических процессов // Журнал эволюционной биохимии и физиологии. – 1973. – Т. 9. – № 4. – С. 398–405. [Lobashev ME, Ponomarenko VV, Polyanskaya GG, Tsapygina RI. The role of the nervous system in the regulation of genetic and cytogenetic processes. Zh Evol Biokhim Fiziol. 1973;9(4):398-405. (In Russ.)]
  4. Лопатина Н.Г., Смирнова Г.П., Пономаренко В.В. Гипотеза нервной регуляции процесса реализации наследственной информации // Проблемы высшей нервной деятельности и нейрофизиологии / Под ред. Н.Ф. Суворова. – Л., 1975. – С. 107–121. [Lopatina NG, Smirnova GP, Ponomarenko VV. Hypothesis of nervous regulation of the hereditary information rea lization process. In: Problems of higher nervous acti vity and neurophysiology. Ed by N.F. Suvorov. Leningrad; 1975. P. 107-121. (In Russ.)]
  5. Пономаренко В.В. О некоторых молекулярных и системных аспектах генетического контроля поведения // Труды ХI съезда Физиологического общества им. И.П. Павлова. – Л., 1970. – С. 97–101. [Ponomarenko VV. Some molecular and systemic aspects of genetic control of behavior. In: Proceedings of the XI Congress of the I.P. Pavlov Physiological Society. Leningrad; 1970. P. 97-101. (In Russ.)]
  6. Savvateeva-Popova EV, Dyuzhikova NA. Stress and genome lability: Drosophyla and Rat genetic models. In: Proceedings of the International Norway-Russian Startup PHAsE Seminar “Physiological mechanisms of humans and animals in the processes of adaptation to environmental changes”. Saint Petersburg; 2017. P. 18-19.
  7. Kaushik M, Kaushik S, Roy K, et al. A bouquet of DNA structures: Emerging diversity. Biochem Biophys Rep. 2016;5:388-395. doi: 10.1016/j.bbrep.2016.01.013.
  8. Brazda V, Laister RC, Jagelska EB, Arrowsmith C. Cruciform structures are a common DNA feature important for regulating biological processes. BMC Mol Biol. 2011;12:33. doi: 10.1186/1471-2199-12-33.
  9. Григорьян Г.А., Гуляева Н.В. Стресс-реактивность и стресс-устойчивость в патогенезе депрессивных расстройств: роль эпигенетических механизмов // Журнал высшей нервной деятельности им. И.П. Павлова. – 2015. – Т. 65. – № 1. – С. 19–32. [Grigor’yan GA, Gulyaeva NV. Stress Reactivity and Stress-Resilience in the Pathogenesis of Depressive Disorders: Involvement of Epigenetic Mechanisms. Zh Vyssh Nerv Deiat Im IP Pavlova. 2015;65(1):19-32. (In Russ.)]
  10. Cholewa-Waclaw J, Bird A, von Schimmelmann M, et al. The Role of Epigenetic Mechanisms in the Regulation of Gene Expression in the Nervous System. Journal Neurosci. 2016;36(45):11427-11434. doi: 10.1523/JNEUROSCI.2492-16.2016.
  11. Sweatt JD, Tamminga CA. An epigenomics approach to individual differences and its translation to neuropsychiatric conditions. Dialogues Clin Neurosci. 2016;18(3):289-298. PMC5067146.
  12. Griffiths BB, Hunter RG. Neuroepigenetics of stress. Neuroscience. 2014;275:420-435. doi: 10.1016/j.neuroscience.2014.06.041.
  13. McEwen BS, Bowles NP, Gray JD, et al. Mechanisms of stress in the brain. Nat Neurosci. 2015;18(10):1353-1363. doi: 10.1038/nn.4086.
  14. McEwen BS, Nasca C, Gray JD. Stress Effects on Neuronal Structure: Hippocampus, Amygdala, and Prefrontal Cortex. Neuropsychopharmacology. 2016;41(1):3-23. doi: 10.1038/npp.2015.171.
  15. Hunter RG, Gagnidze K, McEwen BS, Pfaff DW. Stress and the dynamic genome: Steroids, epigenetics, and the transposome. Proc Natl Acad Sci USA. 2015;112(22):6828-6833. doi: 10.1073/pnas.1411260111.
  16. Zannas AS, West AE. Epigenetics and the regulation of stress vulnerability and resilience. Neuroscience. 2014;264:157-170. doi: 10.1016/j.neuroscience.2013.12.003.
  17. Jankord R, Zhang R, Flak JN, et al. Stress activation of IL-6 neurons in the hypothalamus. Am J Physiol Regul Integr Comp Physiol. 2010;299(1):R343-351. doi: 10.1152/ajpregu.00131.2010.
  18. Mantella RC, Vollmer RR, Rinaman L, et al. Enhanced corticosterone concentrations and attenuated Fos expression in the medial amygdala of female oxytocin knockout mice exposed to psychogenic stress. Am J Physiol Regul Integr Comp Physiol. 2004;287(6): R1494-1504. doi: 10.1152/ajpregu.00387.2004.
  19. Sterrenburg L, Gaszner B, Boerrigter J, et al. Sex-dependent and differential responses to acute restraint stress of corticotropin-releasing factor-producing neurons in the rat paraventricular nucleus, central amygdala, and bed nucleus of the stria terminalis. J Neurosci Res. 2012;90(1):179-192. doi: 10.1002/jnr.22737.
  20. Yuen EY, Wei J, Yan Z. Molecular and Epigenetic Mechanisms for the Complex Effects of Stress on Synaptic Physiology and Cognitive Functions. Int J Neuropsychopharmacol. 2017;20(11):948-955. doi: 10.1093/ijnp/pyx052.
  21. Явич М.П., Рожицкая И.И., Голубева Л.Ю., Меерсон Ф.З. Эффекты операционного стресса на синтез ДНК в клетках печени и мозга // Вопросы медицинской химии. – 1990. – Т. 36. – № 5. – С. 8–11. [Yavich MP, Rozhitskaya II, Golubeva LY, Meerson FZ. Effects of operational stress on DNA synthesis in liver and brain cells. Vopr Med Khim. 1990;36(5):8-11. (In Russ.)]
  22. Autelitano DJ. Stress-induced stimulation of pituitary POMC gene expression is associated with activation of transcription factor AP-1 in hypothalamus and pituitary. Brain Res Bull. 1998;45(1):75-82. doi: 10.1016/S0361-9230(97)00303-1.
  23. Forsberg K, Aalling N, Wortwein G, et al. Dynamic regulation of cerebral DNA repair genes by psychological stress. Mutat Res Genet Toxicol Environ Mutagen. 2015;778:37-43. doi: 10.1016/j.mrgentox.2014.12.003.
  24. Fukudo S, Abe K, Hongo M, et al. Brain-gut induction of heat shock protein (HSP) 70 mRNA by psychophysiological stress in rats. Brain Res. 1997;757(1): 146-148. doi: 10.1016/S0006-8993(97)00179-0.
  25. Irwin LN. Gene expression in the hippocampus of behaviorally stimulated rats: analysis by DNA microarray. Brain Res Mol Brain Res. 2001;96(1-2):163-169. doi: 10.1016/S0169-328X(01)00269-8.
  26. Le Greves P, Sharma HS, Westman J, et al. Acute heat stress induces edema and nitric oxide synthase upregulation and down-regulates mRNA levels of the NMDAR1, NMDAR2A and NMDAR2B subunits in the rat hippocampus. In: James HE, Marschall LF, Raulen HJ, et al, editors. Brain Edema X. Acta Neurochirurgica Supplements. Vol 70. Vienna: Springer; 1997. doi: 10.1007/978-3-7091-6837-0_85.
  27. Senba E, Ueyama T. Stress-induced expression of immediate early genes in the brain and peripheral organs of the rat. Neurosci Res. 1997;29(3):183-207. doi: 10.1016/S0168-0102(97)00095-3.
  28. Stam R, Bruijnzeel AW, Wiegant VM. Long-lasting stress sensitisation. Eur J Pharmacol. 2000;405(1-3): 217-224. doi: 10.1016/S0014-2999(00)00555-0.
  29. Vellucci SV, Parrott RF. Vasopressin and oxytocin gene expression in the porcine forebrain under basal conditions and following acute stress. Neuropeptides. 1997;31(5):431-438. doi: 10.1016/S0143-4179(97)90036-6.
  30. Yamanishi K, Doe N, Sumida M, et al. Hepatocyte nuclear factor 4 alpha is a key factor related to depression and physiological homeostasis in the mouse brain. PloS One. 2015;10(3):e0119021. doi: 10.1371/journal.pone.0119021.
  31. Zhao J, Qi XR, Gao SF, et al. Different stress-related gene expression in depression and suicide. J Psychiatr Res. 2015;68:176-185. doi: 10.1016/j.jpsychires.2015.06.010.
  32. Stankiewicz AM, Goscik J, Majewska A, et al. The Effect of Acute and Chronic Social Stress on the Hippocampal Transcriptome in Mice. PloS One. 2015;10(11): e0142195. doi: 10.1371/journal.pone.0142195.
  33. Provencal N, Binder EB. The effects of early life stress on the epigenome: From the womb to adulthood and even before. Exp Neurol. 2015;268:10-20. doi: 10.1016/j.expneurol.2014.09.001.
  34. McGowan PO, Sasaki A, D’Alessio AC, et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009;12(3):342-348. doi: 10.1038/nn.2270.
  35. McGowan PO, Hope TA, Meck WH, et al. Impaired social recognition memory in recombination activating gene 1-deficient mice. Brain Res. 2011;1383:187-195. doi: 10.1016/j.brainres.2011.02.054.
  36. Berger SL, Kouzarides T, Shiekhattar R, Shilatifard A. An operational definition of epigenetics. Genes Dev. 2009;23(7):781-783. doi: 10.1101/gad.1787609.
  37. Rudenko A, Tsai LH. Epigenetic modifications in the nervous system and their impact upon cognitive impairments. Neuropharmacology. 2014;80:70-82. doi: 10.1016/j.neuropharm.2014.01.043.
  38. Houston I, Peter CJ, Mitchell A, et al. Epigenetics in the human brain. Neuropsychopharmacology. 2013;38(1):183-197. doi: 10.1038/npp.2012.78.
  39. Graff J, Mansuy IM. Epigenetic codes in cognition and behaviour. Behav Brain Res. 2008;192(1):70-87. doi: 10.1016/j.bbr.2008.01.021.
  40. Akbarian S, Beeri MS, Haroutunian V. Epigenetic determinants of healthy and diseased brain aging and cognition. JAMA Neurol. 2013;70(6):711-718. doi: 10.1001/jamaneurol.2013.1459.
  41. Graff J, Kim D, Dobbin MM, Tsai LH. Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiol Rev. 2011;91(2):603-649. doi: 10.1152/physrev.00012.2010.
  42. Dalton VS, Kolshus E, McLoughlin DM. Epigenetics and depression: return of the repressed. J Affect Disord. 2014;155:1-12. doi: 10.1016/j.jad.2013. 10.028.
  43. Miller CA, Sweatt JD. Covalent modification of DNA regulates memory formation. Neuron. 2007;53(6):857-869. doi: 10.1016/j.neuron.2007.02.022.
  44. Pena CJ, Bagot RC, Labonte B, Nestler EJ. Epigenetic signaling in psychiatric disorders. J Mol Biol. 2014;426(20):3389-3412. doi: 10.1016/j.jmb.2014.03.016.
  45. Tsankova NM, Berton O, Renthal W, et al. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci. 2006;9(4):519-525. doi: 10.1038/nn1659.
  46. Bagot RC, Labonte B, Pena CJ, Nestler EJ. Epigenetic signaling in psychiatric disorders: stress and depression. Dialogues Clin Neurosci. 2014;16(3):281-295.
  47. Bartlett AA, Singh R, Hunter RG. Anxiety and Epigenetics. Adv Exp Med Biol. 2017;978:145-166. doi: 10.1007/978-3-319-53889-1_8.
  48. Sweatt JD, Tamminga CA. An epigenomics approach to individual differences and its translation to neuropsychiatric conditions. Dialogues Clin Neurosci. 2016;18(3):289-298.
  49. Zannas AS, Provencal N, Binder EB. Epigenetics of Posttraumatic Stress Disorder: Current Evidence, Challenges, and Future Directions. Biol Psychiatry. 2015;78(5):327-335. doi: 10.1016/j.biopsych.2015.04.003.
  50. Mehler MF. Epigenetic principles and mechanisms underlying nervous system functions in health and disease. Prog Neurobiol. 2008;86(4):305-341. doi: 10.1016/j.pneurobio.2008.10.001.
  51. Ricq EL, Hooker JM, Haggarty SJ. Toward development of epigenetic drugs for central nervous system disorders: Modulating neuroplasticity via H3K4 methylation. Psychiatry Clin Neurosci. 2016;70(12):536-550. doi: 10.1111/pcn.12426.
  52. Karsli-Ceppioglu S. Epigenetic Mechanisms in Psychiatric Diseases and Epigenetic Therapy. Drug Dev Res. 2016;77(7):407-413. doi: 10.1002/ddr.21340.
  53. Strahl BD, Allis CD. The language of covalent histone modifications. Nature. 2000;403(6765):41-45. doi: 10.1038/47412.
  54. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693-705. doi: 10.1016/j.cell.2007.02.005.
  55. Chakravarty S, Pathak SS, Maitra S, et al. Epigenetic regulatory mechanisms in stress-induced behavior. Int Rev Neurobiol. 2014;115:117-154. doi: 10.1016/B978-0-12-801311-3.00004-4.
  56. Дюжикова Н.А., Скоморохова Е.Б., Вайдо А.И. Эпигенетические механизмы формирования пост стрессорных состояний // Успехи физиологических наук. – 2015. – Т. 46. – № 1. – С. 47–75. [Dyuzhikova NA, Skomorokhova EB, Vaydo AI. Epigenetic Mechanisms in Post-Stress States. Usp Fiziol Nauk. 2015;46(1):47-75. (In Russ.)]
  57. Parkel S, Lopez-Atalaya JP, Barco A. Histone H3 lysine methylation in cognition and intellectual disability disorders. Learn Mem. 2013;20(10):570-579. doi: 10.1101/lm.029363.112.
  58. Berger SL. Histone modifications in transcriptional regulation. Curr Opin Genet Dev. 2002;12(2):142-8. doi: 10.1016/S0959-437X(02)00279-4.
  59. Jarome TJ, Lubin FD. Histone lysine methylation: critical regulator of memory and behavior. Rev Neurosci. 2013;24(4):375-387. doi: 10.1515/revneuro-2013-0008.
  60. Sun H, Kennedy PJ, Nestler EJ. Epigenetics of the depressed brain: role of histone acetylation and methylation. Neuropsychopharmacology. 2013;38(1):124-37. doi: 10.1038/npp.2012.73.
  61. Stankiewicz AM, Swiergiel AH, Lisowski P. Epigenetics of stress adaptations in the brain. Brain Res Bull. 2013;98:76-92. doi: 10.1016/j.brainresbull.2013.07.003.
  62. Chandramohan Y, Droste SK, Arthur JS, Reul JM. The forced swimming-induced behavioural immobility response involves histone H3 phospho-acetylation and c-Fos induction in dentate gyrus granule neurons via activation of the N-methyl-D-aspartate/extracellular signal-regulated kinase/mitogen- and stress-activated kinase signalling pathway. Eur J Neurosci. 2008;27(10):2701-2713. doi: 10.1111/j.1460-9568.2008.06230.x.
  63. Chandramohan Y, Droste SK, Reul JM. Novelty stress induces phospho-acetylation of histone H3 in rat dentate gyrus granule neurons through coincident signalling via the N-methyl-D-aspartate receptor and the glucocorticoid receptor: relevance for c-fos induction. J Neurochem. 2007;101(3):815-828. doi: 10.1111/j.1471-4159.2006.04396.x.
  64. Covington HE, Vialou VF, LaPlant Q, et al. Hippocampal-dependent antidepressant-like activity of histone deacetylase inhibition. Neurosci Lett. 2011;493(3):122-126. doi: 10.1016/j.neulet.2011.02.022.
  65. Hunter RG, McCarthy KJ, Milne TA, et al. Re gulation of hippocampal H3 histone methylation by acute and chronic stress. Proc Natl Acad Sci USA. 2009;106(49): 20912-17. doi: 10.1073/pnas. 0911143106.
  66. Ferland CL, Schrader LA. Regulation of histone acetylation in the hippocampus of chronically stressed rats: a potential role of sirtuins. Neuroscience. 2011;174: 104-14. doi: 10.1016/j.neuroscience.2010.10.077.
  67. Hinwood M, Tynan RJ, Day TA, Walker FR. Repeated social defeat selectively increases deltaFosB expression and histone H3 acetylation in the infralimbic medial prefrontal cortex. Cereb Cortex. 2011;21(2):262-271. doi: 10.1093/cercor/bhq080.
  68. Hollis F, Wang H, Dietz D, et al. The effects of repeated social defeat on long-term depressive-like behavior and short-term histone modifications in the hippocampus in male Sprague-Dawley rats. Psychopharmacology (Berl). 2010;211(1):69-77. doi: 10.1007/s00213-010-1869-9.
  69. Hollis F, Duclot F, Gunjan A, Kabbaj M. Individual differences in the effect of social defeat on anhedonia and histone acetylation in the rat hippocampus. Horm Behav. 2011;59(3):331-337. doi: 10.1016/j.yhbeh.2010.09.005.
  70. Covington HE, Maze I, LaPlant QC, et al. Antidepressant actions of histone deacetylase inhibitors. The J Neurosci. 2009;29(37):11451-11460. doi: 10.1523/JNEUROSCI.1758-09.2009.
  71. Wilkinson MB, Xiao G, Kumar A, et al. Imipramine treatment and resiliency exhibit similar chromatin regulation in the mouse nucleus accumbens in depression models. J Neurosci. 2009;29(24):7820-7832. doi: 10.1523/JNEUROSCI.0932-09.2009.
  72. Ferland CL, Harris EP, Lam M, Schrader LA. Facilitation of the HPA axis to a novel acute stress following chronic stress exposure modulates histone acetylation and the ERK/MAPK pathway in the dentate gyrus of male rats. Endocrinology. 2014;155(8):2942-2952. doi: 10.1210/en.2013-1918.
  73. Bilang-Bleuel A, Ulbricht S, Chandramohan Y, et al. Psychological stress increases histone H3 phosphorylation in adult dentate gyrus granule neurons: involvement in a glucocorticoid receptor-dependent behavioural response. Eur J Neurosci. 2005;22(7):1691-1700. doi: 10.1111/j.1460-9568.2005.04358.x.
  74. Lee KK, Workman JL. Histone acetyltransferase complexes: one size doesn’t fit all. Nat Rev Mol Cell Biol. 2007;8(4):284-295. doi: 10.1038/nrm2145.
  75. Choi JK, Howe LJ. Histone acetylation: truth of consequences? Biochem Cell Biol. 2009;87(1):139-150. doi: 10.1139/O08-112.
  76. Morris MJ, Karra AS, Monteggia LM. Histone deacetylases govern cellular mechanisms underlying behavioral and synaptic plasticity in the developing and adult brain. Behav Pharmacol. 2010;21(5-6):409-419. doi: 10.1097/FBP.0b013e32833c20c0.
  77. Uchida S, Hara K, Kobayashi A, et al. Epigenetic status of Gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron. 2011;69(2):359-72. doi: 10.1016/j.neuron.2010.12.023.
  78. Sterrenburg L, Gaszner B, Boerrigter J, et al. Chronic stress induces sex-specific alterations in methylation and expression of corticotropin-releasing factor gene in the rat. PloS One. 2011;6(11):e28128. doi: 10.1371/journal.pone.0028128.
  79. Renthal W, Maze I, Krishnan V, et al. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron. 2007;56(3):517-529. doi: 10.1016/j.neuron.2007.09.032.
  80. Han A, Sung YB, Chung SY, Kwon MS. Possible additional antidepressant-like mechanism of sodium butyrate: targeting the hippocampus. Neuropharmacology. 2014;81:292-302. doi: 10.1016/j.neuropharm.2014.02.017.
  81. Grayson DR, Kundakovic M, Sharma RP. Is there a future for histone deacetylase inhibitors in the pharmacotherapy of psychiatric disorders? Mol Pharmacol. 2010;77(2):126-135. doi: 10.1124/mol.109. 061333.
  82. Lin H, Geng X, Dang W, et al. Molecular mechanisms associated with the antidepressant effects of the class I histone deacetylase inhibitor MS-275 in the rat ventrolateral orbital cortex. Brain Res. 2012;1447:119-125. doi: 10.1016/j.brainres.2012.01.053.
  83. Zhao Y, Xing B, Dang YH, et al. Microinjection of valproic acid into the ventrolateral orbital cortex enhances stress-related memory formation. PloS One. 2013;8(1): e52698. doi: 10.1371/journal.pone.0052698.
  84. Covington HE, Maze I, Sun H, et al. A role for repressive histone methylation in cocaine-induced vulnerability to stress. Neuron. 2011;71(4):656-670. doi: 10.1016/j.neuron.2011.06.007.
  85. Tsankova NM, Kumar A, Nestler EJ. Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J Neurosci. 2004;24(24):5603-5610. doi: 10.1523/JNEUROSCI.0589-04.2004.
  86. Tsuji M, Miyagawa K, Takeda H. Epigenetic regulation of resistance to emotional stress: possible involvement of 5-HT1A receptor-mediated histone acetylation. J Pharmacol Sci. 2014;125(4):347-354. doi: 10.1254/jphs.14R07CP.
  87. Wang A, Nie W, Li H, et al. Epigenetic upregulation of corticotrophin-releasing hormone mediates postnatal maternal separation-induced memory deficiency. PloS One. 2014;9(4):e94394. doi: 10.1371/journal.pone.0094394.
  88. Chen J, Evans AN, Liu Y, et al. Maternal deprivation in rats is associated with corticotrophin-releasing hormone (CRH) promoter hypomethylation and enhances CRH transcriptional responses to stress in adulthood. J Neuroendocrinol. 2012;24(7):1055-1064. doi: 10.1111/j.1365-2826.2012.02306.x.
  89. Xu L, Sun Y, Gao L, et al. Prenatal restraint stress is associated with demethylation of corticotrophin releasing hormone (CRH) promoter and enhances CRH transcriptional responses to stress in adolescent rats. Neurochem Res. 2014;39(7):1193-1198. doi: 10.1007/s11064-014-1296-0.
  90. Roth TL, Sweatt JD. Annual Research Review: Epigenetic mechanisms and environmental shaping of the brain during sensitive periods of development. J Child Psychol Psychiatry. 2011;52(4):398-408. doi: 10.1111/j.1469-7610.2010.02282.x.
  91. Weaver IC, Cervoni N, Champagne FA, et al. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7(8):847-854. doi: 10.1038/nn1276.
  92. Murgatroyd C, Spengler D. Epigenetic programming of the HPA axis: early life decides. Stress. 2011;14(6):581-589. doi: 10.3109/10253890.2011.602146.
  93. Roth TL, Zoladz PR, Sweatt JD, Diamond DM. Epigenetic modification of hippocampal Bdnf DNA in adult rats in an animal model of post-traumatic stress disorder. J Psychiatr Res. 2011;45(7):919-926. doi: 10.1016/j.jpsychires.2011.01.013.
  94. Fuchikami M, Morinobu S, Kurata A, et al. Single immobilization stress differentially alters the expression profile of transcripts of the brain-derived neurotrophic factor (BDNF) gene and histone acetylation at its promoters in the rat hippocampus. Int J Neuropsychopharmacol. 2009;12(1):73-82. doi: 10.1017/S1461145708008997.
  95. Babenko O, Kovalchuk I, Metz GA. Stress-induced perinatal and transgenerational epigenetic programming of brain development and mental health. Neurosci Biobehav Rev. 2015;48:70-91. doi: 10.1016/j.neubiorev.2014.11.013.
  96. Provencal N, Binder EB. The neurobiological effects of stress as contributors to psychiatric disorders: focus on epigenetics. Curr Opin Neurobiol. 2015;30:31-37. doi: 10.1016/j.conb.2014.08.007.
  97. Bale TL. Epigenetic and transgenerational reprogramming of brain development. Nat Rev Neurosci. 2015;16(6):332-344. doi: 10.1038/nrn3818.
  98. Дюжикова Н.А., Ширяева Н.В., Вайдо А.И., и др. Пролиферативная активность и особенности структурно-функциональной организации хромосом в клетках развивающегося мозга в связи с генетически детерминированной возбудимостью нервной системы у крыс // Российский физиологический журнал им. И.М. Сеченова. – 1999. – Т. 85. – № 1. – С. 93–98. [Dyuzhikova NA, Shiryaeva NV, Vaydo AI, et al. Proliferative activity and structure-functional organization of chromosomes in cells from the developing brain in respect to genetically determined excitability of the rat nervous system. Russian Journal of Physiology. 1999;85(1):93-98. (In Russ.)]
  99. Дюжикова Н.А., Вайдо А.И., Лопатина Н.Г., и др. Влияние пренатального эмоционально-болевого стресса на состояние интерфазного хроматина в нейронах развивающегося мозга крыс с различной возбудимостью нервной системы // Цитология. – 2000. – Т. 42. – № 8. – С. 785–786. [Dyuzhikova NA, Vaydo AI, Lopatina NG, et al. A short-term emotional-painful stress and the state of interphase chromatin of developing brain neurons in rat lines differing in their nervous system excitability. Tsitologiia. 2000;42(8):772-786. (In Russ.)]
  100. Дюжикова Н.А., Ширяева Н.В., Павлова М.Б., Вайдо А.И. Долгосрочное влияние пренатального стресса на характеристики нейронов гиппокампа крыс, различающихся по возбудимости нервной системы // Бюллетень экспериментальной биологии и медицины. – 2011. – Т. 152. – № 11. – С. 499–501. [Dyuzhikova NA, Shiryaeva NV, Pavlova MB, Vaydo AI. Long-term effect of prenatal stress on the characteristics of hippocampal neurons in rats that differ in the excitability of the nervous system. Biull Eksp Biol Med. 2011;152(11):499-501. (In Russ.)]
  101. Zhang K, Qu S, Chang S, et al. An overview of posttraumatic stress disorder genetic studies by analyzing and integrating genetic data into genetic database PTSDgene. Neurosci Biobehav Rev. 2017;83:647-656. doi: 10.1016/j.neubiorev. 2017.08.021.
  102. Klengel T, Binder EB. Epigenetics of Stress-Related Psychiatric Disorders and Gene x Environment Interactions. Neuron. 2015;86(6):1343-1357. doi: 10.1016/j.neuron.2015.05.036.
  103. Лопатина Н.Г., Пономаренко В.В. Исследование генетических основ высшей нервной деятельности // Физиология поведения. Нейробиологические закономерности / Под ред. А.С. Батуева. – Л., 1987. – С. 9–59. [Lopatina NG, Ponomarenko VV. Study of the genetic basis of higher nervous activity. In: Physiology of behavior. Neurobiological regularities. Ed by A.S. Batuev. Leningrad; 1987. P. 9-59. (In Russ.)]
  104. Вайдо А.И., Дюжикова Н.А., Ширяева Н.В., и др. Системный контроль молекулярно-клеточных и эпигенетических механизмов долгосрочных последствий стресса // Генетика. – 2009. – Т. 45. – № 3. – С. 342–348. [Vaydo AI, Dyuzhikova NA, Shiryaeva NV, et al. Systemic control of the molecular, cell, and epigenetic mechanisms of long-lasting consequences of stress. Genetika. 2009;45(3): 342-348. (In Russ.)]
  105. Ширяева Н.В., Вайдо А.И., Лопатина Н.Г. Влияние невротизации спустя длительные сроки после ее окончания на поведение крыс, различающихся по возбудимости нервной системы // Журнал высшей нервной деятельности. – 1996. – Т. 46. – № 1. – С. 157–162. [Shiryaeva NV, Vaydo AI, Lopatina NG. The influence of neurologization after long periods after its termination on the behavior of rats differing in the excitability of the nervous system. Zhurnal vysshey nervnoy deyatel’nosti. 1996;46(1):157-162. (In Russ.)]
  106. Павлова М.Б., Ширяева Н.В., Дюжикова Н.А., Вайдо А.И. Влияние длительного эмоционально-болевого стресса на метилирование гистона Н3 в клетках гиппокампа и амигдалы крыс с различной возбудимостью нервной системы // Нейрохимия. – 2017. – Т. 34. – № 3. – С. 227–234. [Pavlova MB, Shiryaeva NV, Dyuzhikova NA, Vaydo AI. The Influence of the Long-Term Emotional Pain Stress on the Methylation of Histone H3 in the Cells of the Hippocampus and Amygdala of Rats with Different Excitability of the Nervous System. Neirokhimiia. 2017;34(3):227-234. (In Russ.)]
  107. Соколова Н.Е., Ширяева Н.В., Дюжикова Н.А., и др. Влияние длительного эмоционально-болевого стресса на динамику ацетилирования гистона Н4 в нейронах гиппокампа крыс с разным уровнем возбудимости нервной системы // Бюллетень экс периментальной биологии и медицины. – 2006. – Т. 142. – № 9. – С. 313–315. [Sokolova NE, Shiryaeva NV, Dyuzhikova NA, et al. The influence of prolonged emotional pain stress on the dynamics of histone H4 acetylation in hippocampal neurons in rats with different levels of excitability of the nervous system. Biull Eksp Biol Med. 2006;142(9):313-315. (In Russ.)]
  108. Дюжикова Н.А., Савенко Ю.Н., Соколова Н.Е., и др. Влияние длительного эмоционально-болевого стресса на содержание метилцитозинсвязывающего белка МеСР2 в ядрах нейронов гиппокампа крыс с различным уровнем возбудимости нервной системы // Бюллетень экспериментальной биологии и медицины. – 2006. – Т. 142. – № 8. – С. 205–207. [Dyuzhikova NA, Savenko YN, Sokolova NE, et al. The effect of prolonged emotional pain stress on the content of methylcytosin-binding protein MeCP2 in the nuclei of hippocampal neurons in rats with different levels of excitability of the nervous system. Biull Eksp Biol Med. 2006;142(8):205-207. (In Russ.)]
  109. Nesbitt AM, McCurdy RD, Bryant SM, Alter MD. Total levels of hippocampal histone acetylation predict normal variability in mouse behavior. PloS One. 2014;9(5):e94224. doi: 10.1371/journal.pone.0094224.
  110. Heinzelmann M, Gill J. Epigenetic Mechanisms Shape the Biological Response to Trauma and Risk for PTSD: A Critical Review. Nurs Res Pract. 2013;2013:417010. doi: 10.1155/2013/417010.
  111. Raabe FJ, Spengler D. Epigenetic Risk Factors in PTSD and Depression. Front Psychiatry. 2013;4:80. doi: 10.3389/fpsyt.2013.00080.
  112. Grafodatskaya D, Chung BH, Butcher DT, et al. Multilocus loss of DNA methylation in individuals with mutations in the histone H3 lysine 4 demethylase KDM5C. BMC Med Genomics. 2013;6:1. doi: 10.1186/1755-8794-6-1.
  113. Zhang Y, Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev. 2001;15(18):2343-2360. doi: 10.1101/gad.927301.
  114. Fischle W, Wang Y, Allis CD. Histone and chromatin cross-talk. Curr Opin Cell Biol. 2003;15(2):172-183. doi: 10.1016/s0955-0674(03)00013-9.
  115. Полторацкий В.П., Подгорная О.И. Роль сателлитной ДНК в пространственной организации хроматина в интерфазном ядре // Цитология. – 1992. – Т. 34. – № 2. – С. 3–10. [Poltorackiy VP, Podgornaya OI. The role of satellite DNA in the spatial organization of chromatin in the interphase nucleus. Cell and tissue biology. 1992;34(2):3-10. (In Russ.)]
  116. Ayyanathan K, Lechner MS, Bell P, et al. Regulated recruitment of HP1 to a euchromatic gene induces mitotically heritable, epigenetic gene silencing: a mammalian cell culture model of gene variegation. Genes Dev. 2003;17(15):1855-1869. doi: 10.1101/gad.1102803.
  117. Кузнецова Т.В., Баранов В.С. Прицентромерный гетерохроматин как главный режиссер программы индивидуального развития // Генетика человека и патология / Под ред. В.П. Пузырева. — Томск, 2011. – С. 59–63. [Kuznetsova TV, Baranov VS. Pricentromeric heterochromatin as the main director of the individual development program. In: Human Genetics and Pathology. Ed by V.P. Puzyrev. Tomsk; 2011. P. 59-63. (In Russ.)]
  118. Takizawa T, Meshorer E. Chromatin and nuclear architecture in the nervous system. Trends Neurosci. 2008;31(7):343-352. doi: 10.1016/j.tins.2008.03.005.
  119. Chan RKW, Peto CA, Sawchenko PE. Fine structure and plasticity of barosensitive neurons in the nucleus of solitary tract. The J Comp Neurol. 2000;422(3):338-351. doi: 10.1002/1096-9861(20000703)422:3<338:: aid-cne2>3.0.co;2-2.
  120. Отеллин В.А., Неокесарийский А. А., Коржевский Д. Э. Изменения структуры ядер нейронов неокортекса в условиях дефицита серотонина и катехоламинов // Цитология. – 1998. – Т. 40. – № 4. – С. 256–259. [Otellin VA, Neokesariyskiy AA, Korzhevskiy DE. Changes in the structure of the nucleus of neocortical neurons during deficiency of serotonin and catecholamines. Cell and tissue biology. 1998;40(4):256-259. (In Russ.)]
  121. Komitowski D, Muto S, Weiss J, et al. Structural changes in nuclear chromatin in rat pituitary after chronic stress of low intensity. Anat Rec. 1988;220(2):125-131. doi: 10.1002/ar.1092200203.
  122. Garcia-Segura LM, Berciano MT, Lafarga M. Nuclear compartmentalization in transcriptionally activated hypothalamic neurons. Biol Cell. 1993;77(2): 143-154. doi: 10.1016/s0248-4900(05)80182-0.
  123. Yu L, Tzeng W-Y, Liu M-Y. The effects of male and female companions in reversing the stressor-decreased cell proliferation and neurogenesis. In: Proceedings of the 19-th International Conference on Neuroscience and Biological Psychiatry “Stress and behavior”; May 16-19; Saint Petersburg.
  124. Koyama S, Soini HA, Foley J, et al. Stimulation of cell proliferation in the subventricular zone by synthetic murine pheromones. Front Behav Neurosci. 2013;7:101. doi: 10.3389/fnbeh.2013.00101.
  125. Akhmanova A, Verkerk T, Langeveld A, et al. Characterisation of transcriptionally active and inactive chromatin domains in neurons. J Cell Sci. 2000;113 Pt 24:4463-4474.
  126. Дюжикова Н.А., Савенко Ю.Н., Миронов С.В., и др. Характеристики гетерохроматина в нейронах гиппокампа крыс линий с различной возбудимостью нервной системы в условиях моделирования посттравматического стрессового расстройства // Морфология. – 2007. – Т. 131. – № 2. – C. 43–50. [Dyuzhikova NA, Savenko YN, Mironov SV, et al. He terochromatin characteristics in hippocampal neurons of rats with different excitability of the nervous system under conditions of posttraumatic stress disorder modeling. Morphology. 2007;131(2):43-50. (In Russ.)]
  127. Litt MD, Simpson M, Recillas-Targa F, et al. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 2001;20(9):2224-2235. doi: 10.1093/emboj/20.9.2224.
  128. Litt MD, Simpson M, Gaszner M, et al. Correlation between histone lysine methylation and deve lopmental changes at the chicken beta-globin locus. Science. 2001;293(5539):2453-2455. doi: 10.1126/science.1064413.
  129. Noma K, Allis CD, Grewal SI. Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries. Science. 2001;293(5532):1150-1155. doi: 10.1126/science. 1064150.
  130. Hall IM, Shankaranarayana GD, Noma K, et al. Establishment and maintenance of a heterochromatin domain. Science. 2002;297(5590):2232-2237. doi: 10.1126/science.1076466.
  131. Rinaldi A, Vincenti S, De Vito F, et al. Stress induces region specific alterations in microRNAs expression in mice. Behav Brain Res. 2010;208(1):265-269. doi: 10.1016/j.bbr.2009.11.012.
  132. Andolina D, Di Segni M, Bisicchia E, et al. Effects of lack of microRNA-34 on the neural circuitry underlying the stress response and anxiety. Neuropharmacology. 2016;107:305-316. doi: 10.1016/j.neuropharm.2016.03.044.
  133. Haramati S, Navon I, Issler O, et al. MicroRNA as repressors of stress-induced anxiety: the case of amygdalar miR-34. J Neurosci. 2011;31(40):14191-203. doi: 10.1523/JNEUROSCI.1673-11.2011.
  134. Mannironi C, Biundo A, Rajendran S, et al. miR-135a Regulates Synaptic Transmission and Anxiety-Like Behavior in Amygdala. Mol Neurobiol. 2018;55(4): 3301-3315. doi: 10.1007/s12035-017-0564-9.
  135. Li C, Liu Y, Liu D, et al. Dynamic Alterations of miR-34c Expression in the Hypothalamus of Male Rats after Early Adolescent Traumatic Stress. Neural Plast. 2016;2016:5249893. doi: 10.1155/2016/ 5249893.
  136. Zhou R, Yuan P, Wang Y, et al. Evidence for selective microRNAs and their effectors as common long-term targets for the actions of mood stabilizers. Neuropsychopharmacology. 2009;34(6):1395-1405. doi: 10.1038/npp.2008.131.
  137. Uchida S, Hara K, Kobayashi A, et al. Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents. J Neurosci. 2010;30(45):15007-15018. doi: 10.1523/JNEUROSCI.1436-10.2010.
  138. Olejniczak M, Kotowska-Zimmer A, Krzyzosiak W. Stress-induced changes in miRNA biogenesis and functioning. Cell Mol Life Sci. 2018;75(2):177-191. doi: 10.1007/s00018-017-2591-0.
  139. Kim AH, Reimers M, Maher B, et al. MicroRNA expression profiling in the prefrontal cortex of individuals affected with schizophrenia and bipolar disorders. Schizophr Res. 2010;124(1-3):183-191. doi: 10.1016/j.schres.2010.07.002.
  140. Rong H, Liu TB, Yang KJ, et al. MicroRNA-134 plasma levels before and after treatment for bipolar mania. J Psychiatr Res. 2011;45(1):92-95. doi: 10.1016/j.jpsychires.2010.04.028.
  141. Xu Y, Liu H, Li F, et al. A polymorphism in the microRNA-30e precursor associated with major depressive disorder risk and P300 waveform. J Affect Disord. 2010;127(1-3):332-6. doi: 10.1016/j.jad.2010.05.019.
  142. Rodgers AB, Morgan CP, Leu NA, Bale TL. Transgenerational epigenetic programming via sperm microRNA recapitulates effects of paternal stress. Proc Natl Acad Sci USA. 2015;112(44):13699-13704. doi: 10.1073/pnas.1508347112.
  143. Nestler EJ. Transgenerational Epigenetic Contributions to Stress Responses: Fact or Fiction? PLoS Biol. 2016;14(3):e1002426. doi: 10.1371/journal.pbio.1002426.
  144. Rodgers AB, Bale TL. Germ Cell Origins of Posttraumatic Stress Disorder Risk: The Transgenerational Impact of Parental Stress Experience. Biol Psychiatry. 2015;78(5):307-314. doi: 10.1016/j.biopsych.2015.03.018.
  145. Qureshi IA, Mattick JS, Mehler MF. Long non-coding RNAs in nervous system function and disease. Brain Res. 2010;1338:20-35. doi: 10.1016/j.brainres.2010.03.110.
  146. Huang X, Luo YL, Mao YS, Ji JL. The link between long noncoding RNAs and depression. Prog Neuropsychopharmacol Biol Psychiatry. 2017;73:73-78. doi: 10.1016/j.pnpbp.2016.06.004.
  147. Ni X, Liao Y, Li L, et al. Therapeutic role of long non-coding RNA TCONS_00019174 in depressive disorders is dependent on Wnt/beta-catenin signaling pathway. J Integr Neurosci. 2017. doi: 10.3233/JIN-170052.
  148. Baudry A, Mouillet-Richard S, Schneider B, et al. miR-16 targets the serotonin transporter: a new facet for adaptive responses to antidepressants. Science. 2010;329(5998):1537-1541. doi: 10.1126/science.1193692.
  149. Gao J, Wang WY, Mao YW, et al. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature. 2010;466(7310):1105-1109. doi: 10.1038/nature09271.
  150. Libert S, Pointer K, Bell EL, et al. SIRT1 activates MAO-A in the brain to mediate anxiety and exploratory drive. Cell. 2011;147(7):1459-1472. doi: 10.1016/j.cell.2011.10.054.
  151. Pezer Z, Brajkovic J, Feliciello I, Ugarkovc D. Satellite DNA-mediated effects on genome regulation. Genome Dyn. 2012;7:153-169. doi: 10.1159/000337116.
  152. Пузырев В.П., Степанов В.А. Патологическая анатомия генома человека. – Новосибирск: Наука, 1997. [Puzyrev VP, Stepanov VA. Pathological anatomy of the human genome. Novosibirsk: Nauka; 1997. (In Russ.)]
  153. McClintock B. The significance of responses of the genome to challenge. Science. 1984;226(4676): 792-801.
  154. Reilly MT, Faulkner GJ, Dubnau J, et al. The role of transposable elements in health and diseases of the central nervous system. J Neurosci. 2013;33(45):17577-17586. doi: 10.1523/JNEUROSCI.3369-13.2013.
  155. Чересиз С.В., Юрченко Н.Н., Иванников А.В., Захаров И.К. Мобильные элементы и стресс // Информационный вестник ВОГиС. – 2008. – Т. 12. – № 1–2. – С. 216–241. [Cheresiz SV, Yurchenko NN, Ivannikov AV, Zakharov IK. Elements and stress. Informatsionnyi vestnikVOGiS. 2008;12(1-2):216-41. (In Russ.)]
  156. Muotri AR, Marchetto MC, Coufal NG, Gage FH. The necessary junk: new functions for transposable elements. Hum Mol Genet. 2007;16 Spec No. 2: R159-167. doi: 10.1093/hmg/ddm196.
  157. Muotri AR, Zhao C, Marchetto MC, Gage FH. Environmental influence on L1 retrotransposons in the adult hippocampus. Hippocampus. 2009;19(10):1002-1007. doi: 10.1002/hipo.20564.
  158. Lapp HE, Hunter RG. The dynamic genome: transposons and environmental adaptation in the nervous system. Epigenomics. 2016;8(2):237-249. doi: 10.2217/epi.15.107.
  159. Vijg J, Uitterlinden AG. A search for DNA alterations in the aging mammalian genome: An experimental strategy. Mech Ageing Dev. 1987;41(1-2):47-63. doi: 10.1016/0047-6374(87)90053-4.
  160. Паткин Е.Л., Вайдо А.И., Кустова М.Е., и др. Однонитевые разрывы ДНК в отдельных клетках мозга различных линий крыс в норме и при стрессорном воздействии // Цитология. – 2001. – Т. 43. – № 3. – С. 269–272. [Patkin EL, Vaydo AI, Kustova ME, et al. Single strand breaks of DNA in separate brain cells of different rat lines in normal and under stress conditions. Cell and tissue biology. 2001;43(3):269-272. (In Russ.)]
  161. Love S, Barber R, Wilcock GK. Apoptosis and expression of DNA repair proteins in ischaemic brain injury in man. NeuroReport. 1998;9(6):955-959. doi: 10.1097/00001756-199804200-00001.
  162. Lai H. Single-and double-strand DNA breaks in rat brain cells after acute exposure to radiofrequency electromagnetic radiation. Intl J Radiat Biol. 2009;69(4):513-21. doi: 10.1080/095530096145814.
  163. Consiglio AR, Ramos AL, Henriques JA, Picada JN. DNA brain damage after stress in rats. Prog Neuropsychopharmacol Biol Psychiatry. 2010;34(4):652-656. doi: 10.1016/j.pnpbp.2010.03.004.
  164. Suberbielle E, Sanchez PE, Kravitz AV, et al. Physiologic brain activity causes DNA double-strand breaks in neurons, with exacerbation by amyloid-beta. Nat Neurosci. 2013;16(5):613-621. doi: 10.1038/nn.3356.
  165. Madabhushi R, Gao F, Pfenning AR, et al. Activity-Induced DNA Breaks Govern the Expression of Neuronal Early-Response Genes. Cell. 2015;161(7): 1592-1605. doi: 10.1016/j.cell.2015.05.032.
  166. Watson LA, Tsai LH. In the loop: how chromatin topology links genome structure to function in mechanisms underlying learning and memory. Curr Opin Neurobiol. 2017;43:48-55. doi: 10.1016/j.conb.2016.12.002.
  167. McEwen BS, Gianaros PJ. Stress- and allostasis-induced brain plasticity. Annu Rev Med. 2011;62:431-45. doi: 10.1146/annurev-med-052209-100430.
  168. Iourov IY, Vorsanova SG, Yurov YB. Somatic genome variations in health and disease. Curr Genomics. 2010;11(6):387-396. doi: 10.2174/138920210793176065.
  169. Iourov IY, Vorsanova SG, Yurov YB. Molecular cytogenetics and cytogenomics of brain diseases. Curr Genomics. 2008;9(7):452-465. doi: 10.2174/138920208786241216.
  170. Iourov IY, Vorsanova SG, Liehr T, Yurov YB. Aneuploidy in the normal, Alzheimer’s disease and ataxia-telangiectasia brain: differential expression and pathological meaning. Neurobiol Dis. 2009;34(2):212-220. doi: 10.1016/j.nbd.2009.01.003.
  171. Owusu-Ansah E, Perrimon N. Stress signaling between organs in metazoa. Annu Rev Cell Dev Biol. 2015;31:497-522. doi: 10.1146/annurev-cellbio-100814-125523.
  172. Mehta D, Klengel T, Conneely KN, et al. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Proc Natl Acad Sci U S A. 2013;110(20):8302-8307. doi: 10.1073/pnas.1217750110.
  173. Snyder-Mackler N, Somel M, Tung J. Shared signatures of social stress and aging in peripheral blood mononuclear cell gene expression profiles. Aging Cell. 2014;13(5):954-957. doi: 10.1111/acel.12239.
  174. Tung J, Barreiro LB, Johnson ZP, et al. Social environment is associated with gene regulatory variation in the rhesus macaque immune system. Proc Natl Acad Sci USA. 2012;109(17):6490-6495. doi: 10.1073/pnas.1202734109.
  175. Даев Е.В., Дукельская А.В. Феромональная индукция мейотических нарушений в сперматоцитах I как механизм угнетения репродуктивной функции самцов у домовой мыши // Цитология. – 2005. – Т. 47. – № 6. – С. 505–509. [Daev EV, Dukel’skaya AV. Induction of meiotic disturbances in spermatocytes I by pheromones as an inhibiting mechanism of male reproductive function in house mice. Cell and tissue biology. 2005;47(6):505-509. (In Russ.)]
  176. Hoffmann AA, Hercus MJ. Environmental Stress as an Evolutionary Force. BioScience. 2000;50(3):217. doi: 10.1641/0006-3568(2000)050[0217:esaaef] 2.3.co;2.
  177. Цапыгина Р.И. Изучение роли центральной нерв ной системы в регуляции цитогенетических процессов условно-рефлекторным методом: Дис. … канд. биол. наук. – Л., 1972. [Capygina RI. A study of the role of the central nervous system in the regulation of cytogenetic processes by the conditioned reflex method. [dissertation] Leningrad; 1972. (In Russ.)]
  178. Керкис Ю.Я., Скорова С.В. О факторах, контролирующих интенсивность спонтанного мутационного процесса // Информационный бюллетень научного совета по проблемам радиобиологии. – 1977. – № 20. – С. 51–52. [Kerkis YY, Skorova SV. On the factors controlling the intensity of the spontaneous mutational process. Informatsionnyy byulleten’ nauchnogo soveta po problemam radiobiologii. 1977;(20):51-52. (In Russ.)]
  179. Бородин П.М., Беляев Д.К. Влияние стресса на частоту кроссинговера во 2-й хромосоме домовой мыши // Доклады АН СССР. – 1980. – Т. 253. – № 3. – С. 727–729. [Borodin PM, Belyaev DK. Effect of stress on the frequency of crossing-over in the 2nd chromosome of a house mouse. Doklady AN SSSR. 1980;253(3):727-729. (In Russ.)]
  180. Бородин П.М., Беляев Д.К. Влияние эмоцио нального стресса на частоту рекомбинаций в 1-й хромосоме домовой мыши // Докл. АН СССР. – 1986. – Т. 286. – № 3. – С. 726–728. [Borodin PM, Belyaev DK. The influence of emotional stress on the frequency of recombinations in the 1st chromosome of a house mouse. Doklady AN SSSR. 1986;286(3):726-728. (In Russ.)]
  181. Середенин С.Б., Дурнев А.Д., Ведерникова А.А. Влияние эмоционального стресса на частоту хромосомных аберраций в клетках костного мозга мышей // Бюллетень экспериментальной биологии и медицины. – 1980. – Т. 90. – № 7. – С. 91–92. [Seredenin SB, Durnev AD, Vedernikova A.A. Effect of emotional stress on the frequency of chromosome aberrations in the bone marrow cells of mice. Biull Eksp Biol Med. 1980;90(7):91-92. (In Russ.)]
  182. Ингель Ф.И., Геворкян Н.М., Ильюшина Н.А., и др. Длительный психоэмоциональный стресс как индуктор мутаций у млекопитающих и модификатор мутагенеза // Бюллетень экспериментальной биологии и медицины. – 1993. – Т. 116. – № 9. – С. 307–309. [Ingel’ FI, Gevorkyan NM, Il’yushina NA, et al. Long emotional stress as an inducer of mutations in mammals and modifier mutagenesis. Biull Eksp Biol Med. 1993;116(9):307-309. (In Russ.)]
  183. Ингель Ф.И., Хусаинова ШН., Легостаева Т.Б., и др. Стресс у человека. Генетические аспекты // Жизнь без опасностей. Здоровье. Профилактика. Долголетие. – 2012. – Т. 7. – № 1. – С. 58–71. [Ingel’ FI, Husainova SN, Legostaeva TB, et al. Stress in humans. Genetic aspects. Zhizn’ bez opasnostey. Zdorov’e. Profilaktika. Dolgoletie. 2012;7(1):58-71. (In Russ.)]
  184. Dimitroglou E, Zafiropoulou M, Messini-Nikolaki N, et al. DNA damage in a human population affected by chronic psychogenic stress. Int J Hyg Environ Health. 2003;206(1):39-44. doi: 10.1078/1438-4639-00187.
  185. Nersesyan AK, Boffetta P, Sarkisyan TF, et al. Chromosome aberrations in lymphocytes of persons exposed to an earthquake in Armenia. Scand J Work Environ Health. 2001;27(2):120-124.
  186. Дюжикова Н.А., Быковская Н.В., Вайдо А.И., и др. Частота хромосомных нарушений, индуцированных однократным стрессорным воздействием у крыс, селектированных по возбудимости нервной системы // Генетика. – 1996. – Т. 32. – № 6. – С. 851–853. [Dyuzhikova NA, Bykovskaya NV, Vaydo AI, et al. Rate of chromosomal aberrations induced by short-term stress in rats selected for excitability of the nervous system. Genetika. 1996;32(6):851-853. (In Russ.)]
  187. Быковская Н.В., Дюжикова Н.А., Вайдо А.И., и др. Частота хромосомных аберраций, индуцированных стрессорным воздействием и циклофосфаном в клетках костного мозга крыс, селектированных по порогу возбудимости нервной системы // Генетика. – 1994. – Т. 30. – № 9. – С. 1224–1228. [Bykovskaya NV, Dyuzhikova NA, Vaydo AI, et al. The frequency of chromosomal aberrations induced by stress and cyclophosphamide in bone marrow cells of rats selected for the excitability threshold of the nervous system. Genetika. 1994;30(9):1224-1228. (In Russ.)]
  188. Керкис Ю.Я. Физиологические изменения в клетке как причина мутационного процесса // Успехи современной биологии. – 1940. – Т. 13. – № 1. – С. 143–159. [Kerkis YY. Physiological changes in the cell as the cause of the mutation process. Advances in modern biology. 1940;13(1):143-159. (In Russ.)]
  189. Керкис Ю.Я., Осетрова Т.Л., Логвинова В.В., и др. Генетические и физиологические (гуморальные) факторы, контролирующие индуцированный и спонтанный мутационный процесс у млекопитающих // Проблемы теоретической и прикладной генетики. – Новосибирск, 1973. – С. 75–93. [Kerkis YY, Osetrova TL, Logvinova VV, et al. Genetic and physiological (humoral) factors controlling the induced and spontaneous mutational process in mammals. In: Problems of theoretical and applied genetics. Novosibirsk; 1973. P. 75-93. (In Russ.)]
  190. Лобашев М.Е. Физиологическая (паранекротическая) гипотеза мутационного процесса // Вестник Ленинградского университета. – 1947. – № 8. – С. 10–29. [Lobashev ME. The physiological (paranecrotic) hypothesis of the mutational process. Vestnik Leningradskogo universiteta. 1947;(8): 10-29. (In Russ.)]
  191. Fischman HK, Pero RW, Kelly DD. Psychoge nic Stress Induces Chromosomal and Dna Damage. Int J Neurosci. 2010;84(1-4):219-227. doi: 10.3109/00207459608987267.
  192. Fischman HK, Kelly DD. Chromosomes and Stress. Int J Neurosci. 2009;99(1-4):201-219. doi: 10.3109/00207459908994325.
  193. Ингель Ф.И., Ревазова Ю.А. Модификация эмоциональным стрессом мутагенных эффектов ксенобиотиков у животных и человека // Исследования по генетике. – 1999. – № 12. – С. 86–103. [Ingel’ FI, Revazova YA. Modification of emotional stress by mutagenic effects of xenobiotics in animals and humans. Issledovaniya po genetike. 1999;(12):86-103. (In Russ.)]
  194. Горюнов И.П., Бородин П.М. Влияние эмоционального стресса на частоту мейотических нарушений у самцов мышей // Генетика. – 1986. – Т. 22. – № 6. – С. 119–121. [Goryunov IP, Borodin PM. The influence of emotional stress on the frequency of meiotic disorders in male mice. Genetika. 1986;22(6):119-121. (In Russ.)]
  195. Даев Е.В. Действие экзогенных метаболитов на цитогенетические характеристики сперматогенеза и репродуктивную функцию самцов домовой мыши: Дис. … канд. биол. наук. – Л., 1983. [Daev EV. The effect of exogenous metabolites on the cytogenetic characteristics of spermatogenesis and the reproductive function of male house mouse. [dissertation] Leningrad; 1983. (In Russ.)]
  196. Даев Е.В. Феромональный контроль генетических процессов: исследования на домовой мыши (Mus musculus L.) // Генетика. – 1994. – Т. 30. – № 8. – С. 1105–1112. [Daev EV. Pheromonal regulation of genetic processes: research on the house mouse (Mus musculus L.). Russ J Genet. 1994;30(8):1105-1112. (In Russ.)]
  197. Daev EV. Stress, chemocommunication, and the physiological hypothesis of mutation. Russ J Genet. 2007;43(10):1082-1092. doi: 10.1134/s102279540710002x.
  198. Даев Е.В. Генетические эффекты ольфакторного стресса: исследования на домовой мыши. – Saarbrucken: Lambert Academic Publishing, 2011. [Daev EV. Genetic effects of olfactory stress: studies on a house mouse. Saarbrucken: Lambert Academic Publishing; 2011. (In Russ.)]
  199. Daev EV, Petrova MV, Onopa LS, et al. DNA damage in bone marrow cells of mouse males in vivo after exposure to the pheromone: Comet assay. Russ J Genet. 2017;53(10):1105-1112. doi: 10.1134/s1022795417100027.
  200. Daev EV, Vorob’ev KV, Shustova TI, et al. Genotype-specific changes in functional parameters of immunocompetent cells in laboratory male mice under conditions of pheromoneal stress. Russ J Genet. 2000;36(8):872-876.
  201. Glinin TS, Romaschenko AV, Shubina VA, et al. Pheromone-induced genome instability is associated with negative fMRI response in mouse main olfactory bulb. In: Proceedings of the 23rd International “Stress and Behavior” Neuroscience and Biopsychiatry Conference; 2016 May 16-19; Saint Petersburg.
  202. Бородин П.М. Стресс и генетическая изменчивость // Генетика. – 1987. – Т. 23. – № 6. – С. 1003–1010. [Borodin PM. Stress and genetic variability. Genetika. 1987;23(6):1003-1010. (In Russ.)]
  203. Середенин C.B., Дурнев А.Д. Фармакологическая защита генома. – М.: ВИНИТИ, 1992. [Seredenin CV, Durnev AD. Pharmacological protection of the genome. Moscow: VINITI; 1992. (In Russ.)]
  204. Васильев В.К., Меерсон Ф.З. Повреждение и репаративный синтез ДНК различных органов крыс, вызванные эмоционально-болевым стрессом // Вопросы медицинской химии. – 1984. – Т. 30. – № 2. – C. 112–114. [Vasil’ev VK, Meerson FZ. Damage and reparative synthesis of DNA of various organs of rats caused by emotional and painful stress. Vopr Med Khim. 1984;30(2):112-114. (In Russ.)]
  205. Гуляева Н.В., Дупин А.М., Левшина И.П., и др. Карнозин предотвращает активацию свободнорадикального окисления липидов при стрессе // Бюллетень экспериментальной биологии и медицины. – 1989. – Т. 107. – № 2. – С. 144–147. [Gulyaeva NV, Dupin AM, Levshina IP, et al. Carnosine prevents the activation of free radical lipid oxidation under stress. Biull Eksp Biol Med. 1989;107(2):144-147. (In Russ.)]
  206. Даев Е.В. Генетические последствия ольфакторных стрессов у мышей: Дис. … д-ра биол. наук. – СПб., 2006. [Daev EV. Genetic consequences of olfactory stress in mice. [dissertation] Saint Petersburg; 2006. (In Russ.)]
  207. Maksymchuk O, Chashchyn M. The impact of psychogenic stressors on oxidative stress markers and patterns of CYP2E1 expression in mice liver. Pathophysiology. 2012;19(3):215-219. doi: 10.1016/j.pathophys.2012.07.002.
  208. Mejia-Carmona GE, Gosselink KL, de la Rosa LA, et al. Evaluation of antioxidant enzymes in response to predator odor stress in prefrontal cortex and amygdala. Neurochem J. 2014;8(2):125-128. doi: 10.1134/s181971241402007x.
  209. Zannas AS, Wiechmann T, Gassen NC, Binder EB. Gene-Stress-Epigenetic Regulation of FKBP5: Clinical and Translational Implications. Neuropsychopharmacology. 2016;41(1):261-274. doi: 10.1038/npp.2015.235.
  210. Kress C, Thomassin H, Grange T. Active cytosine demethylation triggered by a nuclear receptor involves DNA strand breaks. Proc Natl Acad Sci USA. 2006;103(30):11112-7. doi: 10.1073/pnas.0601793103.
  211. McKinnon PJ. Maintaining genome stability in the nervous system. Nat Neurosci. 2013;16(11):1523-1529. doi: 10.1038/nn.3537.
  212. Um JH, Brown AL, Singh SK, et al. Metabolic sensor AMPK directly phosphorylates RAG1 protein and regulates V(D)J recombination. Proc Natl Acad Sci U S A. 2013;110(24):9873-9878. doi: 10.1073/pnas.1307928110.
  213. Weinstock DM, Jasin M. Alternative Pathways for the Repair of RAG-Induced DNA Breaks. Mol Cell Biol. 2005;26(1):131-139. doi: 10.1128/mcb.26.1.131-139.2006.
  214. Weaver ICG, Korgan AC, Lee K, et al. Stress and the Emerging Roles of Chromatin Remodeling in Signal Integration and Stable Transmission of Reversible Phenotypes. Front Behav Neurosci. 2017;11:41. doi: 10.3389/fnbeh.2017.00041.
  215. Zhuk AS, Stepchenkova EI, Dukel’skaya AV, et al. The Role of Metabolic Activation of Promutagens in the Genome Destabilization under Pheromonal Stress in the House Mouse (Mus musculus). Russ J Genet. 2011;47(10):1209-14. doi: 10.1134/S102279541110019X.
  216. Беляев Д.К. Дестабилизирующий отбор как фактор изменчивости при доместикации животных // Природа. – 1979. – № 2. – С. 36–45. [Belyaev DK. Destabilizing selection as a factor of variability in the domestication of animals. Priroda. 1979;(2):36-45. (In Russ.)]
  217. Belyaev DK. Stress as a factor of genetic variation and the problem of destabilizing selection. Folia Biol (Praha). 1983;29(2):177-187.
  218. Маркель А.Л. Стресс и эволюция // Информационный вестник ВОГиС. – 2008. – Т. 12. – № 1–2. – С. 206–215. [Markel’ AL. Stress and Evolution. Informatsionnyi vestnik VOGiS. 2008;12(1-2):206-215. (In Russ.)]
  219. Опольский А.Ф. Влияние гипоталамуса на мутагенез в соматических клетках животных // Сборник тезисов конференции «Чувствительность организмов к мутагенным факторам и возникновение мутаций»; Вильнюс. 1982. – Вильнюс: Из-во Вильнюсского госуниверситета, 1982. – С. 20–21. [Opol’skiy AF. The influence of the hypothalamus on mutagenesis in somatic cells of animals. In: Procee dings of the conference “Sensitivity of organisms to mutagenic factors and occurrence of mutations”; Vilnius, 1982. Vilnius: Izdatel’stvo Vil’nyusskogo gosuniversiteta; 1982. P. 20-21. (In Russ.)]
  220. Nevo E. Evolution under environmental stress at macro- and microscales. Genome Biol Evol. 2011;3:1039-1052. doi: 10.1093/gbe/evr052.
  221. Foster PL. Stress-induced mutagenesis in bacteria. Crit Rev Biochem Mol Biol. 2007;42(5):373-397. doi: 10.1080/10409230701648494.
  222. Startek M, Le Rouzic A, Capy P, et al. Genomic parasites or symbionts? Modeling the effects of environmental pressure on transposition activity in asexual populations. Theor Popul Biol. 2013;90:145-151. doi: 10.1016/j.tpb.2013.07.004.
  223. Craddock EM. Profuse evolutionary diversification and speciation on volcanic islands: transposon instability and amplification bursts explain the genetic paradox. Biol Direct. 2016;11:44. doi: 10.1186/s13062-016-0146-1.
  224. Даев Е.В., Суринов Б.П., Дукельская А.В. Влияние постстрессорных хемосигналов на клетки иммунокомпетентных органов у лабораторных мышей трех инбредных линий // Экологическая генетика. – 2008. – Т. 6. – № 1. – С. 27–33. [Daev EV, Surinov BP, Dukelskaya AV. Post-stress chemosignals affect cells from immunocompetent organs in laboratory mice of three inbred strains. Ecological Gene tics. 2008;6(1):27-33. (In Russ.)]
  225. Daev EV. The central nervous system of mammals acts as a mutagenic/anti-mutagenic factor: role in microevolution. In: Korogodina VL, Mothersill C, Inge-Vechtomov SG, Seymour C, editors. Genetics, Evolution and Radiation. Cham: Springer; 2017. P. 487-495. doi: 10.1007/978-3-319-48838-7_39.
  226. Nesse RM, Young EA. Evolutionary Origins and Functions of the Stress Response. In: Fink G, editor. Encyclopedia of stress. Vol. 2. Academic Press/Elsevier; 2000. P. 76-84.
  227. Nagy C, Vaillancourt K, Turecki G. A role for activity-dependent epigenetics in the development and treatment of major depressive disorder. Genes Brain Behav. 2017. doi: 10.1111/gbb.12446.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Scheme of current view on stress development in animals taking into account systemic control of genetic processes at the cell genome level: PFC – prefrontal cortex; CRH – corticotropin-releasing hormone; GABA – γ-aminobutyric acid; GFs – growth factors; DA – dopamine; NE – norepinephrine; 5-HT – serotonin; NFkB – nuclear factor kappa-B; MAPK – mitogen-activated protein kinase; JAK/STAT – Janus Kinase/Signal Transducers and Activators of Transcription

Download (341KB)
Indexing metadata

Copyright (c) 2018 Dyuzhikova N.A., Daev E.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
 


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies