EPIGENETIC CHANGES IN POST-TRAUMATIC STRESS DISORDER: POSSIBILITIES AND LIMITATIONS OF EPIGENETIC THERAPY



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Abstract

The review describes epigenetic mechanisms that may contribute to individual differences in resistance and risk of developing post-traumatic stress disorder. The review provides data on the potential use of epigenetic modifications as biomarkers of traumatic stress and factors responsible for the inheritance by offspring of the negative consequences of psychogenic trauma suffered by their parents. The possibilities and limitations of epigenetic therapy of post-traumatic and stress-related disorders are discussed.

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About the authors

Irina Olegovna Suchkova

FSBSI «Institute of Experimental Medicine»

Author for correspondence.
Email: irsuchkova@mail.ru
ORCID iD: 0000-0003-2127-0459
SPIN-code: 4155-7314
Scopus Author ID: 6602838276
ResearcherId: H-4484-2014

PhD, Cand. Sci. (Biol.), Senior Research Associate, Laboratory of Molecular cytogenetics of mammalian development, Department of Molecular genetics

Russian Federation, 197022, Saint-Petersburg, Acad. Pavlov str., 12

Eugene L'vovich Patkin

FSBSI "Institute of Experimental Medicine"

Email: elp44@mail.ru
ORCID iD: 0000-0002-6292-4167
SPIN-code: 4929-4630
Scopus Author ID: 7003713993
ResearcherId: J-7779-2013

MD, Dr. Sci. (Biol.), Professor, Head of Laboratory of Molecular Cytogenetics of Mammalian Development, Department of Molecular Genetics

Russian Federation, 197022, St. Petersburg, Acad. Pavlova str., 12

Sergey Georgievich Tsikunov

FSBSI "Institute of Experimental Medicine"

Email: secikunov@yandex.ru
ORCID iD: 0000-0002-7097-1940
SPIN-code: 7771-1940
Scopus Author ID: 6506948997
ResearcherId: E-6273-2014

MD, Dr. Sci. (Med.), Professor, Head of the Laboratory of the Psychophysiology of Emotions of Physiological Department named I.P. Pavlov

Russian Federation, 197022, Russia, Saint Petersburg, Acad. Pavlov str.,12

Henrikh Aleksandrovich Sofronov

Military Medical Academy named after. C.M. Kirov of the Ministry of Defense of the Russian Federation; FSBSI "Institute of Experimental Medicine"

Email: gasofronov@mail.ru
ORCID iD: 0000-0002-8587-1328
SPIN-code: 7334-4881
Scopus Author ID: 7003953555
ResearcherId: G-4791-2015

MD, Dr. Sci. (Med.), Professor, Academician of RAS, Head of the Laboratory of Medicinal and Environmental Toxicology of the Research Department (medical and biological research) of the Research Center; Scientific director of Federal State Budget Scientific Institution «Institute of Experimental Medicine»

Russian Federation, 194044, St. Petersburg, Acad. Lebedeva str., 6; 197022, St. Petersburg, Acad. Pavlov str., 12

References

  1. Qureshi IA, Mehler MF. Impact of nuclear organization and dynamics on epigenetic regulation in the central nervous system: implications for neurological disease states. Ann N Y Acad Sci. 2010;1204 Suppl(Suppl):E20-37. doi: 10.1111/j.1749-6632.2010.05718.x
  2. Qureshi IA, Mehler MF. Epigenetic mechanisms underlying nervous system diseases. Handb Clin Neurol. 2018;147:43-58. doi: 10.1016/b978-0-444-63233-3.00005-1
  3. Varela RB, Cararo JH, Tye SJ, et al. Contributions of epigenetic inheritance to the predisposition of major psychiatric disorders: Theoretical framework, evidence, and implications. Neurosci Biobehav Rev. 2022;135:104579. doi: 10.1016/j.neubiorev.2022.104579
  4. Sokolov PL, Chebanenko NV, Mednaya DM. Epigenetic influences and brain development. Zhurnal Nevrologii i Psikhiatrii imeni SS Korsakova. 2023;123(3):12-19. (In Russ). doi: 10.17116/jnevro202312303112
  5. Kim GS, Smith AK, Nievergelt CM, Uddin M. Neuroepigenetics of post-traumatic stress disorder. Prog Mol Biol Transl Sci. 2018;158:227-253. doi: 10.1016/bs.pmbts.2018.04.001
  6. Dyuzhikova NA, Skomorokhova EB, Vaido AI. Epigenetic mechanisms in post-stress states. Uspekhi fiziologicheskikh nauk. 2015;46(1):47-75. (In Russ.)
  7. Apraksina NK, Nemtseva PS, Avaliani TV et al. Delayed effect of vital stress on the level of genome-wide DNA methylationat different stages of the estrous cycle in female rats. Pathogenesis. 2022;22(3):65-66. (In Russ.) doi: 10.25557/2310-0435.2022.03.65-66
  8. Chou PC, Huang YC, Yu S. Mechanisms of epigenetic inheritance in post-traumatic stress disorder. Life (Basel). 2024;14(1):98. doi: 10.3390/life14010098
  9. Kringel D, Malkusch S, Lötsch J. Drugs and epigenetic molecular functions. A pharmacological data scientometric analysis. Int J Mol Sci. 2021;22(14):7250. doi: 10.3390/ijms22147250
  10. Toth M. Epigenetic neuropharmacology: Drugs affecting the epigenome in the brain. Annu Rev Pharmacol Toxicol. 2021;61:181-201. doi: 10.1146/annurev-pharmtox-030220-022920
  11. Szyf M. Prospects for the development of epigenetic drugs for CNS conditions. Nature Reviews Drug Discovery. 2015;14(7):461-474. doi: 10.1038/nrd4580
  12. Sahafnejad Z, Ramazi S, Allahverdi A. An update of epigenetic drugs for the treatment of cancers and brain diseases: A comprehensive review. Genes (Basel). 2023;14(4):873. doi: 10.3390/genes14040873
  13. Allis DCD, Caparro M-L, Jenuwein T, Reinberg D, Lachner M. Epigenetics. Second ed. Cold Springer Harbor Laboratory Press. Cold Spring Harbor; 2015:967. p.
  14. Patkin EL. Epigenetic mechanisms for primary differentiation in mammalian embryos. International Review of Cytology. 2002;216:81-129. doi: 10.1016/s0074-7696(02)16004-9
  15. Patkin EL, Sofronov GA. Environmentally-related human diseases. Epigenetic mechanisms of origin and inheritance (Ekologo-zavisimyye zabolevaniya cheloveka. Epigeneticheskiye mekhanizmy vozniknoveniya i nasledovaniya). Medical Academic Journal. 2015;15(3):7-23. (In Russ.)
  16. KM, Moguchaia EV, Rotar OP. Transgenerational inheritance: understanding the etiology of a disease. Arterial Hypertension. 2021;27(2):122-132. (In Russ.) doi: 10.18705/1607-419X-2021-27-2-122-132
  17. Barnhill JW. Posttraumatic stress disorder (PTSD). In: MSD Manual. Professional version. URL: https://www.msdmanuals.com/professional/psychiatric-disorders/anxiety-and-stressor-related-disorders/posttraumatic-stress-disorder-ptsd (accessed 14.01.2024)
  18. World Health Organization. International statistical classification of diseases and related health problems 10th Revision (ICD-10). Chapter V. Mental and behavioural disorders (F00-F99). Neurotic, stress-related and somatoform disorders (F40-F48). URL: https://icd.who.int/browse10/2019/en#/F43.0 (accessed 14.01.2024)
  19. Howie H, Rijal CM, Ressler KJ. A review of epigenetic contributions to post-traumatic stress disorder Dialogues Clin Neurosci. 2019;21(4):417-428. doi: 10.31887/DCNS.2019.21.4/kressler
  20. Dyuzhikova NA, Daev EV. Genome and stress-reaction in animals and humans. Ecological genetics. 2018;16(1):4-26. (In Russ.) doi: 10.17816/ecogen1614-26
  21. Aykac A, Kalkan R. Epigenetic approach to PTSD: In the aspects of rat models. Glob Med Genet. 2022;9(1):7-13. doi: 10.1055/s-0041-1736633
  22. Vaido AI, Dyuzhikova NA, Shiryaeva NV, Sokolova NE, Vshivtseva VV, Sawenko YN. Systemic control of the molecular, cell, and epigenetic mechanisms of long-lasting consequences of stress. Russian Journal of Genetics. 2009;45(3):298-303. doi: 10.1134/S1022795409030065
  23. Ordyan NE, Malysheva OV, Akulova VK et al. The capability to learn and expression of the insulin-like growth factor ii gene in the brain of male rat offspring of fathers subjected to action of stress factors in the “stress–restress” paradigm. Neurochemical Journal. 2020;14(2):191-196. doi: 10.1134/s1819712420020075
  24. Seckl JR. Glucocorticoids, developmental 'programming' and the risk of affective dysfunction. Prog Brain Res. 2008;167:17-34. doi: 10.1016/s0079-6123(07)67002-2
  25. Ordyan NE, Pivina SG, Akulova VK, Kholova GI. Changes in the nature of behavior and the activity of the hypophyseal-adrenocortical system in the offspring of paternal rats subjected to stress in the stress-restress paradigm before Mating. Neuroscience and Behavioral Physiology. 2021;51(4):528-534. doi: 10.1007/s11055-021-01100-7
  26. Ordjan NE, Pivina SG, Mironova VI et al. The hypothalamic-pituitary-adrenal axis activity in prenatal stressed female rats in the model of posttraumatic stress disorder. Ross Fiziol Zh im. I.M. Sechenova. 2014;100(12):1409-1420. (In Russ.)
  27. Pivina SG, Rakitskaya VV, Akulova VK, Ordyan NE. Activity of the hypothalamic-pituitary-adrenal system in prenatally stressed male rats on the experimental model of post-traumatic stress disorder. Bull Exp Biol Med. 2016;160(5):601-604. doi: 10.1007/s10517-016-3227-3
  28. Gatta E, Saudagar V, Auta J, Grayson DR, Guidotti A. Epigenetic landscape of stress surfeit disorders: Key role for DNA methylation dynamics. Int Rev Neurobiol. 2021;156:127-183. doi: 10.1016/bs.irn.2020.08.002
  29. Coelho AA, Lima-Bastos S, Gobira PH, Lisboa SF. Endocannabinoid signaling and epigenetics modifications in the neurobiology of stress-related disorders. Neuronal Signal. 2023;7(2):Ns20220034. doi: 10.1042/ns20220034
  30. Cao-Lei L, Saumier D, Fortin J, Brunet A. A narrative review of the epigenetics of post-traumatic stress disorder and post-traumatic stress disorder treatment. Front Psychiatry. 2022;13:857087. doi: 10.3389/fpsyt.2022.857087
  31. Qi P, Huang M, Ren X, Zhai Y, Qiu C, Zhu H. Identification of potential biomarkers and therapeutic targets related to post-traumatic stress disorder due to traumatic brain injury. Eur J Med Res. 2024;29(1):44. doi: 10.1186/s40001-024-01640-x
  32. Gökbuget D, Blelloch R. Epigenetic control of transcriptional regulation in pluripotency and early differentiation. Development. 2019;146(19):dev164772. doi: 10.1242/dev.164772
  33. Ambrosi C, Manzo M, Baubec T. Dynamics and context-dependent roles of DNA methylation. J Mol Biol. 2017;429(10):1459-1475. doi: 10.1016/j.jmb.2017.02.008
  34. Ooi SK, Qiu C, Bernstein E, et al. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature. 2007;448(7154):714-717. doi: 10.1038/nature05987
  35. Li H, Liu H, Zhu D, et al. Biological function molecular pathways and druggability of DNMT2/TRDMT1. Pharmacological Research. 2024;205:107222. DOI:https://doi.org/10.1016/j.phrs.2024.107222
  36. Li H, Zhu D, Yang Y, et al. Determinants of DNMT2/TRDMT1 preference for substrates tRNA and DNA during the evolution. RNA Biol. 2023;20(1):875-892. doi: 10.1080/15476286.2023.2272473
  37. Dong A, Yoder JA, Zhang X, Zhou L, Bestor TH, Cheng X. Structure of human DNMT2, an enigmatic DNA methyltransferase homolog that displays denaturant-resistant binding to DNA. Nucleic Acids Res. 2001;29(2):439-448. doi: 10.1093/nar/29.2.439
  38. Sardina JL, Collombet S, Tian TV, et al. Transcription factors drive Tet2-mediated enhancer demethylation to reprogram cell fate. Cell Stem Cell. 2018;23(5):727-741.e729. doi: 10.1016/j.stem.2018.08.016
  39. Jones PL, Veenstra GJ, Wade PA, et al. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet. 1998;19(2):187-191. doi: 10.1038/561
  40. Klose RJ, Bird AP. Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci. 2006;31(2):89-97. doi: 10.1016/j.tibs.2005.12.008
  41. Clouaire T, Stancheva I. Methyl-CpG binding proteins: specialized transcriptional repressors or structural components of chromatin? Cell Mol Life Sci. 2008;65(10):1509-1522. doi: 10.1007/s00018-008-7324-y
  42. Bahar Halpern K, Vana T, Walker MD. Paradoxical role of DNA methylation in activation of FoxA2 gene expression during endoderm development. J Biol Chem. 2014;289(34):23882-23892. doi: 10.1074/jbc.M114.573469
  43. Patkin EL. Epigenetic mechanisms of common human diseases. S-Petersburg: Nestor-Istoriya; 2008. 196 p. (In Russ.)
  44. Sutherland JE, Costa M. Epigenetics and the environment. Ann N Y Acad Sci. 2003;983:151-160. doi: 10.1111/j.1749-6632.2003.tb05970.x
  45. Patkin EL, Sofronov GA. Epigenetic changes as a common mechanism of disease, aging and chemical toxicity. S-Petersburg:Eko-Vektor. 2019. 237 p. (In Russ.)
  46. Dyuzhikova NA, Pavlova MB, Shiryaeva NV et al. Long-term post-stress changes in DNA methylation and histone H3 in the amygdala of rats with high and low nervous system excitability. In: Proceedings of the XXIII Congress of the Physiological Society named after I.P. Pavlova.Voronezh. 2017. P. 1149-1151. (In Russ.)
  47. Dyuzhikova NA. Cytogenetic and molecular-cellular mechanisms of post-stress conditions / Abstract of the dissertation for the degree of Doctor of Biological Sciences. Institute of Physiology named after. I.P. Pavlova RAS. 2016. 42 p. (In Russ.)
  48. Jawahar MC, Murgatroyd C, Harrison EL, Baune BT. Epigenetic alterations following early postnatal stress: a review on novel aetiological mechanisms of common psychiatric disorders. Clin Epigenetics. 2015;7:122. doi: 10.1186/s13148-015-0156-3
  49. Martin CA, Vorn R, Schrieber M, et al. Identification of DNA methylation changes that predict onset of post-traumatic stress disorder and depression following physical trauma. Front Neurosci. 2021;15:738347. doi: 10.3389/fnins.2021.738347
  50. Al Jowf GI, Snijders C, Rutten BPF, de Nijs L, Eijssen LMT. The molecular biology of susceptibility to post-traumatic stress disorder: Highlights of epigenetics and epigenomics. Int J Mol Sci. 2021;22(19):10743. doi: 10.3390/ijms221910743
  51. Bhattacharya S, Fontaine A, MacCallum PE, Drover J, Blundell J. Stress across generations: DNA methylation as a potential mechanism underlying intergenerational effects of stress in both post-traumatic stress disorder and pre-clinical predator stress rodent models. Front Behav Neurosci. 2019;13:113. doi: 10.3389/fnbeh.2019.00113
  52. Dyuzhikova NA, Savenko YN, Sokolova NE, Savvateeva-Popova EV, Vaido AI. Effect of prolonged emotional and pain stress on the content of methylcytosine-binding protein MeCP2 in nuclei of hippocampal neurons in rats with different excitability of the nervous system. Bulletin of Experimental Biology and Medicine. 2006;142(2):239-241. doi: 10.1007/s10517-006-0337-3
  53. Cosentino L, Witt SH, Dukal H, et al. Methyl-CpG binding protein 2 expression is associated with symptom severity in patients with PTSD in a sex-dependent manner. Transl Psychiatry. 2023;13(1):249. doi: 10.1038/s41398-023-02529-9
  54. Cosentino L, Zidda F, Dukal H, Witt SH, De Filippis B, Flor H. Low levels of methyl-CpG binding protein 2 are accompanied by an increased vulnerability to the negative outcomes of stress exposure during childhood in healthy women. Transl Psychiatry. 2022;12(1):506. doi: 10.1038/s41398-022-02259-4
  55. Dirven BCJ, Homberg JR, Kozicz T, Henckens M. Epigenetic programming of the neuroendocrine stress response by adult life stress. J Mol Endocrinol. 2017;59(1):R11-r31. doi: 10.1530/jme-17-0019
  56. Zovkic IB, Sweatt JD. Epigenetic mechanisms in learned fear: implications for PTSD. Neuropsychopharmacology. 2013;38(1):77-93. doi: 10.1038/npp.2012.79
  57. Globisch D, Münzel M, Müller M, et al. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One. 2010;5(12):e15367. doi: 10.1371/journal.pone.0015367
  58. Hack LM, Dick ALW, Provençal N. Epigenetic mechanisms involved in the effects of stress exposure: Focus on 5-hydroxymethylcytosine. Environ Epigenet. 2016;2(3):dvw016. doi: 10.1093/eep/dvw016
  59. Li S, Papale LA, Zhang Q, et al. Genome-wide alterations in hippocampal 5-hydroxymethylcytosine links plasticity genes to acute stress. Neurobiol Dis. 2016;86:99-108. doi: 10.1016/j.nbd.2015.11.010
  60. Kochmanski J, Bernstein AI. The Impact of environmental factors on 5-hydroxymethylcytosine in the brain. Curr Environ Health Rep. 2020;7(2):109-120. doi: 10.1007/s40572-020-00268-3
  61. Yehuda R, Daskalakis NP, Desarnaud F, et al. Epigenetic biomarkers as predictors and correlates of symptom improvement following psychotherapy in combat veterans with PTSD. Front Psychiatry. 2013;4:118. doi: 10.3389/fpsyt.2013.00118
  62. Rutten BPF, Vermetten E, Vinkers CH, et al. Longitudinal analyses of the DNA methylome in deployed military servicemen identify susceptibility loci for post-traumatic stress disorder. Mol Psychiatry. 2018;23(5):1145-1156. doi: 10.1038/mp.2017.120
  63. Mehta D, Bruenig D, Carrillo-Roa T, et al. Genomewide DNA methylation analysis in combat veterans reveals a novel locus for PTSD. Acta Psychiatr Scand. 2017;136(5):493-505. doi: 10.1111/acps.12778
  64. Kang JI, Kim TY, Choi JH, So HS, Kim SJ. Allele-specific DNA methylation level of FKBP5 is associated with post-traumatic stress disorder. Psychoneuroendocrinology. 2019;103:1-7. doi: 10.1016/j.psyneuen.2018.12.226
  65. Vinkers CH, Geuze E, van Rooij SH, et al. Successful treatment of post-traumatic stress disorder reverses DNA methylation marks. Mol Psychiatry. 2021;26(4):1264-1271. doi: 10.1038/s41380-019-0549-3
  66. Occean JR, Wani AH, Donglasan J, et al. DNA methylation of nuclear factor of activated T cells 1 mediates the prospective relation between exposure to different traumatic event types and post-traumatic stress disorder. Psychiatry Res. 2022;311:114510. doi: 10.1016/j.psychres.2022.114510
  67. Wen Y, Shang Y, Wang Q. Exploration of the mechanism of linoleic acid metabolism dysregulation in metabolic syndrome. Genet Res (Camb). 2022;2022:6793346. doi: 10.1155/2022/6793346
  68. Crombach A, Rukundo-Zeller AC, Vukojevic V, et al. Differential methylation of linoleic acid pathway genes is associated with PTSD symptoms - a longitudinal study with Burundian soldiers returning from a war zone. Transl Psychiatry. 2024;14(1):32. doi: 10.1038/s41398-024-02757-7
  69. Xin N, Wang DT, Zhang L, Zhou Y, Cheng Y. Early developmental stage glucocorticoid exposure causes DNA methylation and behavioral defects in adult zebrafish. Comp Biochem Physiol C Toxicol Pharmacol. 2022;256:109301. doi: 10.1016/j.cbpc.2022.109301
  70. Radtke KM, Ruf M, Gunter HM, et al. Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor. Transl Psychiatry. 2011;1(7):e21. doi: 10.1038/tp.2011.21
  71. Cordero MI, Stenz L, Moser DA, Rusconi Serpa S, Paoloni-Giacobino A, Schechter DS. The relationship of maternal and child methylation of the glucocorticoid receptor NR3C1 during early childhood and subsequent child psychopathology at school-age in the context of maternal interpersonal violence-related post-traumatic stress disorder. Front Psychiatry. 2022;13:919820. doi: 10.3389/fpsyt.2022.919820
  72. Hjort L, Rushiti F, Wang SJ, et al. Intergenerational effects of maternal post-traumatic stress disorder on offspring epigenetic patterns and cortisol levels. Epigenomics. 2021;13(12):967-980. doi: 10.2217/epi-2021-0015
  73. Klengel T, Dias BG, Ressler KJ. Models of intergenerational and transgenerational transmission of risk for psychopathology in mice. Neuropsychopharmacology. 2016;41(1):219-231. doi: 10.1038/npp.2015.249
  74. Yehuda R, Daskalakis NP, Bierer LM, et al. Holocaust exposure induced intergenerational effects on FKBP5 methylation. Biol Psychiatry. 2016;80(5):372-380. doi: 10.1016/j.biopsych.2015.08.005
  75. Fransquet PD, Hjort L, Rushiti F, et al. DNA methylation in blood cells is associated with cortisol levels in offspring of mothers who had prenatal post-traumatic stress disorder. Stress Health. 2022;38(4):755-766. doi: 10.1002/smi.3131
  76. Sharma R, Frasch MG, Zelgert C, et al. Maternal-fetal stress and DNA methylation signatures in neonatal saliva: an epigenome-wide association study. Clin Epigenetics. 2022;14(1):87. doi: 10.1186/s13148-022-01310-x
  77. Saunderson EA, Spiers H, Mifsud KR, et al. Stress-induced gene expression and behavior are controlled by DNA methylation and methyl donor availability in the dentate gyrus. Proc Natl Acad Sci U S A. 2016;113(17):4830-4835. doi: 10.1073/pnas.1524857113
  78. Vlasov I, Filatova E, Slominsky P, Shadrina M. Differential expression of Dusp1 and immediate early response genes in the hippocampus of rats, subjected to forced swim test. Sci Rep. 2023;13(1):9985. doi: 10.1038/s41598-023-36611-5
  79. Blouin AM, Sillivan SE, Joseph NF, Miller CA. The potential of epigenetics in stress-enhanced fear learning models of PTSD. Learn Mem. 2016;23(10):576-586. doi: 10.1101/lm.040485.115
  80. Chertkow-Deutsher Y, Cohen H, Klein E, Ben-Shachar D. DNA methylation in vulnerability to post-traumatic stress in rats: Evidence for the role of the post-synaptic density protein Dlgap2. Int J Neuropsychopharmacol. 2010;13(3):347-359. doi: 10.1017/s146114570999071x
  81. Bohacek J, Farinelli M, Mirante O, et al. Pathological brain plasticity and cognition in the offspring of males subjected to postnatal traumatic stress. Mol Psychiatry. 2015;20(5):621-631. doi: 10.1038/mp.2014.80
  82. Li B, Carey M, Workman JL. The role of chromatin during transcription. Cell. 2007;128(4):707-719. doi: 10.1016/j.cell.2007.01.015
  83. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21(3):381-395. doi: 10.1038/cr.2011.22
  84. Tan M, Luo H, Lee S, et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell. 2011;146(6):1016-1028. doi: 10.1016/j.cell.2011.08.008
  85. Pradeepa MM. Causal role of histone acetylations in enhancer function. Transcription. 2017;8(1):40-47. doi: 10.1080/21541264.2016.1253529
  86. Millán-Zambrano G, Burton A, Bannister AJ, Schneider R. Histone post-translational modifications - cause and consequence of genome function. Nat Rev Genet. 2022;23(9):563-580. doi: 10.1038/s41576-022-00468-7
  87. Patel AB, He Y, Radhakrishnan I. Histone acetylation and deacetylation - Mechanistic insights from structural biology. Gene. 2024;890:147798. doi: 10.1016/j.gene.2023.147798
  88. Wei S, Li C, Yin Z, et al. Histone methylation in DNA repair and clinical practice: new findings during the past 5-years. J Cancer. 2018;9(12):2072-2081. doi: 10.7150/jca.23427
  89. Husmann D, Gozani O. Histone lysine methyltransferases in biology and disease. Nat Struct Mol Biol. 2019;26(10):880-889. doi: 10.1038/s41594-019-0298-7
  90. Wang Y, Khandelwal N, Liu S, et al. KDM6B cooperates with Tau and regulates synaptic plasticity and cognition via inducing VGLUT1/2. Mol Psychiatry. 2022;27(12):5213-5226. doi: 10.1038/s41380-022-01750-0
  91. Cao X, Dang W. Chapter 15 - Histone modification changes during aging: Cause or consequence? What we have learned about epigenetic regulation of aging from model organisms. In: Epigenetics of Aging and Longevity / by editors Moskalev A, Vaiserman AM. Boston: Academic Press; 2018:309-328.
  92. Watson NA, Higgins JMG. Chapter 4 - Histone kinases and phosphatases. In: Chromatin Signaling and Diseases / be editors Binda O, Fernandez-Zapico ME. Boston:Academic Press; 2016:75-94.
  93. Cao J, Yan Q. Histone ubiquitination and deubiquitination in transcription, DNA damage response, and cancer. Front Oncol. 2012;2:26. doi: 10.3389/fonc.2012.00026
  94. Ryu HY, Hochstrasser M. Histone sumoylation and chromatin dynamics. Nucleic Acids Res. 2021;49(11):6043-6052. doi: 10.1093/nar/gkab280
  95. Li K, Wang Z. Histone crotonylation-centric gene regulation. Epigenetics Chromatin. 2021;14(1):10. doi: 10.1186/s13072-021-00385-9
  96. Cheng J, Huang M, Zhu Y, et al. SUMOylation of MeCP2 is essential for transcriptional repression and hippocampal synapse development. J Neurochem. 2014;128(6):798-806. doi: 10.1111/jnc.12523
  97. Stielow C, Stielow B, Finkernagel F, Scharfe M, Jarek M, Suske G. SUMOylation of the polycomb group protein L3MBTL2 facilitates repression of its target genes. Nucleic Acids Res. 2014;42(5):3044-3058. doi: 10.1093/nar/gkt1317
  98. Mattiroli F, Penengo L. Histone ubiquitination: An integrative signaling platform in genome stability. Trends Genet. 2021;37(6):566-581. doi: 10.1016/j.tig.2020.12.005
  99. Zhang Y, Sun Z, Jia J, et al. Overview of histone modification. Adv Exp Med Biol. 2021;1283:1-16. doi: 10.1007/978-981-15-8104-5_1
  100. Cerutti H, Casas-Mollano JA. Histone H3 phosphorylation: Universal code or lineage specific dialects? Epigenetics. 2009;4(2):71-75. doi: 10.4161/epi.4.2.7781
  101. Murakami Y. Phosphorylation of repressive histone code readers by casein kinase 2 plays diverse roles in heterochromatin regulation. J Biochem. 2019;166(1):3-6. doi: 10.1093/jb/mvz045
  102. Bahl S, Seto E. Regulation of histone deacetylase activities and functions by phosphorylation and its physiological relevance. Cell Mol Life Sci. 2021;78(2):427-445. doi: 10.1007/s00018-020-03599-4
  103. Wu G, Broniscer A, McEachron TA, et al. Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat Genet. 2012;44(3):251-253. doi: 10.1038/ng.1102
  104. Labrie V, Pai S, Petronis A. Epigenetics of major psychosis: progress, problems and perspectives. Trends Genet. 2012;28(9):427-435. doi: 10.1016/j.tig.2012.04.002
  105. Gavin DP, Rosen C, Chase K, Grayson DR, Tun N, Sharma RP. Dimethylated lysine 9 of histone 3 is elevated in schizophrenia and exhibits a divergent response to histone deacetylase inhibitors in lymphocyte cultures. J Psychiatry Neurosci. 2009;34(3):232-237.
  106. Dyuzhikova NA, Pavlova MB, Levina AS, Khlebaeva DAA, Vaido AI. Effects of prolonged emotional-pain stress on histone H3 phosphorylation in the medial prefrontal cortex and basolateral area of the amygdala in rats with genetic differences in nervous system arousability. Neuroscience and Behavioral Physiology. 2021;51(4):553-558. doi: 10.1007/s11055-021-01104-3
  107. Levina AS, Shiryaeva NV, Vaido AI, Dyuzhikova NA. Effect of NMDA receptor activity on histone H3 methylation and its asymmetry in the hippocampal pyramidal neurons of rats with different excitability thresholds under normal and stress conditions. Journal of Evolutionary Biochemistry and Physiology. 2013;49(6):615-623. doi: 10.1134/S0022093013060091
  108. Pavlova MB, Dyuzhikova NA, Shiryaeva NV, Savenko YN, Vaido AI. Effect of long-term stress on H3Ser10 histone phosphorylation in neuronal nuclei of the sensorimotor cortex and midbrain reticular formation in rats with different nervous system excitability. Bull Exp Biol Med. 2013;155(3):373-375. doi: 10.1007/s10517-013-2157-6
  109. Pavlova MB, Shiryaeva NV, Dyuzhikova NA, Vaido 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. Neurochemical Journal. 2017;11(3):229-235. doi: 10.1134/S1819712417030096
  110. Sokolova NE, Shiryaeva NV, Dyuzhikova NA, Savenko YN, Vaido AI. Effect of long-term mental and pain stress on the dynamics of H4 histone acetylation in hippocampal neurons of rats with different levels of nervous system excitability. Bull Exp Biol Med. 2006;142(3):341-343. doi: 10.1007/s10517-006-0361-3
  111. Reed B, Fang N, Mayer-Blackwell B, et al. Chromatin alterations in response to forced swimming underlie increased prodynorphin transcription. Neuroscience. 2012;220:109-118. doi: 10.1016/j.neuroscience.2012.06.006
  112. Hunter RG, McCarthy KJ, Milne TA, Pfaff DW, McEwen BS. Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proc Natl Acad Sci U S A. 2009;106(49):20912-20917. doi: 10.1073/pnas.0911143106
  113. Sanacora G, Yan Z, Popoli M. The stressed synapse 2.0: pathophysiological mechanisms in stress-related neuropsychiatric disorders. Nat Rev Neurosci. 2022;23(2):86-103. doi: 10.1038/s41583-021-00540-x
  114. Bam M, Yang X, Zhou J, et al. Evidence for epigenetic regulation of pro-inflammatory cytokines, interleukin-12 and interferon gamma, in peripheral blood mononuclear cells from PTSD patients. J Neuroimmune Pharmacol. 2016;11(1):168-181. doi: 10.1007/s11481-015-9643-8
  115. Rusconi F, Grillo B, Ponzoni L, et al. LSD1 modulates stress-evoked transcription of immediate early genes and emotional behavior. Proc Natl Acad Sci U S A. 2016;113(13):3651-3656. doi: 10.1073/pnas.1511974113
  116. Liu Y, Li M, Fan M, et al. Chromodomain Y-like protein-mediated histone crotonylation regulates stress-induced depressive behaviors. Biol Psychiatry. 2019;85(8):635-649. doi: 10.1016/j.biopsych.2018.11.025
  117. Dyuzhikova NA, Savenko YN, Mironov SV et al. Heterochromatin characteristics in hippocampal neurons of rats with different excitability of the nervous system under conditions of posttraumatic stress disorder modeling. Morfologiia. 2007;131(2):43-50. (In Russ.)
  118. Reul JM. Making memories of stressful events: a journey along epigenetic, gene transcription, and signaling pathways. Front Psychiatry. 2014;5:5. doi: 10.3389/fpsyt.2014.00005
  119. Trollope AF, Gutièrrez-Mecinas M, Mifsud KR, Collins A, Saunderson EA, Reul JM. Stress, epigenetic control of gene expression and memory formation. Exp Neurol. 2012;233(1):3-11. doi: 10.1016/j.expneurol.2011.03.022
  120. Webb WM, Sanchez RG, Perez G, et al. Dynamic association of epigenetic H3K4me3 and DNA 5hmC marks in the dorsal hippocampus and anterior cingulate cortex following reactivation of a fear memory. Neurobiol Learn Mem. 2017;142(Pt A):66-78. doi: 10.1016/j.nlm.2017.02.010
  121. Whittle N, Singewald N. HDAC inhibitors as cognitive enhancers in fear, anxiety and trauma therapy: where do we stand? Biochem Soc Trans. 2014;42(2):569-581. doi: 10.1042/bst20130233
  122. Bonomi RE, Girgenti M, Krystal JH, Cosgrove KP. A role for histone deacetylases in the biology and treatment of post-traumatic stress disorder: what do we know and where do we go from here? Complex Psychiatry. 2022;8(1-2):13-27. doi: 10.1159/000524079
  123. Sun YM, Chen YQ. Principles and innovative technologies for decrypting noncoding RNAs: from discovery and functional prediction to clinical application. J Hematol Oncol. 2020;13(1):109. doi: 10.1186/s13045-020-00945-8
  124. Peedicayil J. Chapter 15. Non-coding RNAs and psychiatric disorders. In: Epigenetics in Psychiatry (Second Edition / by ediors Peedicayil J, Grayson DR, Avramopoulos D. Academic Press; 2021:321-333.
  125. Kaikkonen MU, Lam MT, Glass CK. Non-coding RNAs as regulators of gene expression and epigenetics. Cardiovasc Res. 2011;90(3):430-440. doi: 10.1093/cvr/cvr097
  126. Wang W, Min L, Qiu X, et al. Biological function of long non-coding RNA (LncRNA) Xist. Front Cell Dev Biol. 2021;9:645647. doi: 10.3389/fcell.2021.645647
  127. Pasquinelli AE. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat Rev Genet. 2012;13(4):271-282. doi: 10.1038/nrg3162
  128. Xu JZ, Zhang JL, Zhang WG. Antisense RNA: the new favorite in genetic research. J Zhejiang Univ Sci B. 2018;19(10):739-749. doi: 10.1631/jzus.B1700594
  129. Statello L, Guo CJ, Chen LL, Huarte M. Gene regulation by long non-coding RNAs and its biological functions. Nat Rev Mol Cell Biol. 2021;22(2):96-118. doi: 10.1038/s41580-020-00315-9
  130. Nepal C, Taranta A, Hadzhiev Y, et al. Ancestrally duplicated conserved noncoding element suggests dual regulatory roles of HOTAIR in cis and trans. iScience. 2020;23(4):101008. doi: 10.1016/j.isci.2020.101008
  131. Tsai MC, Manor O, Wan Y, et al. Long noncoding RNA as modular scaffold of histone modification complexes. Science. 2010;329(5992):689-693. doi: 10.1126/science.1192002
  132. Schorderet P, Duboule D. Structural and functional differences in the long non-coding RNA hotair in mouse and human. PLoS Genet. 2011;7(5):e1002071. doi: 10.1371/journal.pgen.1002071
  133. Rosspopoff O, Cazottes E, Huret C, et al. Species-specific regulation of XIST by the JPX/FTX orthologs. Nucleic Acids Res. 2023;51(5):2177-2194. doi: 10.1093/nar/gkad029
  134. Boeren J, Gribnau J. Xist-mediated chromatin changes that establish silencing of an entire X chromosome in mammals. Curr Opin Cell Biol. 2021;70:44-50. doi: 10.1016/j.ceb.2020.11.004
  135. Patel RS, Krause-Hauch M, Kenney K, Miles S, Nakase-Richardson R, Patel NA. Long noncoding RNA VLDLR-AS1 levels in serum correlate with combat-related chronic mild traumatic brain injury and depression symptoms in US veterans. Int J Mol Sci. 2024;25(3):1473. doi: 10.3390/ijms25031473
  136. Bam M, Yang X, Ginsberg JP, et al. Long non-coding RNA LINC00926 regulates WNT10B signaling pathway thereby altering inflammatory gene expression in PTSD. Transl Psychiatry. 2022;12(1):200. doi: 10.1038/s41398-022-01971-5
  137. Zhu Z, Huang X, Du M, et al. Recent advances in the role of miRNAs in post-traumatic stress disorder and traumatic brain injury. Mol Psychiatry. 2023;28(7):2630-2644. doi: 10.1038/s41380-023-02126-8
  138. Guffanti G, Galea S, Yan L, et al. Genome-wide association study implicates a novel RNA gene, the lincRNA AC068718.1, as a risk factor for post-traumatic stress disorder in women. Psychoneuroendocrinology. 2013;38(12):3029-3038. doi: 10.1016/j.psyneuen.2013.08.014
  139. Snijders C, de Nijs L, Baker DG, et al. MicroRNAs in post-traumatic stress disorder. Curr Top Behav Neurosci. 2018;38:23-46. doi: 10.1007/7854_2017_32
  140. Wingo AP, Almli LM, Stevens JS, et al. DICER1 and microRNA regulation in post-traumatic stress disorder with comorbid depression. Nat Commun. 2015;6:10106. doi: 10.1038/ncomms10106
  141. Bam M, Yang X, Zumbrun EE, et al. Dysregulated immune system networks in war veterans with PTSD is an outcome of altered miRNA expression and DNA methylation. Sci Rep. 2016;6:31209. doi: 10.1038/srep31209
  142. Martin CG, Kim H, Yun S, et al. Circulating miRNA associated with posttraumatic stress disorder in a cohort of military combat veterans. Psychiatry Res. 2017;251:261-265. doi: 10.1016/j.psychres.2017.01.081
  143. Zhou J, Nagarkatti P, Zhong Y, et al. Dysregulation in microRNA expression is associated with alterations in immune functions in combat veterans with post-traumatic stress disorder. PLoS One. 2014;9(4):e94075. doi: 10.1371/journal.pone.0094075
  144. Jung SH, Wang Y, Kim T, et al. Molecular mechanisms of repeated social defeat-induced glucocorticoid resistance: Role of microRNA. Brain Behav Immun. 2015;44:195-206. doi: 10.1016/j.bbi.2014.09.015
  145. Schouten M, Aschrafi A, Bielefeld P, Doxakis E, Fitzsimons CP. microRNAs and the regulation of neuronal plasticity under stress conditions. Neuroscience. 2013;241:188-205. doi: 10.1016/j.neuroscience.2013.02.065
  146. Meerson A, Cacheaux L, Goosens KA, Sapolsky RM, Soreq H, Kaufer D. Changes in brain microRNAs contribute to cholinergic stress reactions. J Mol Neurosci. 2010;40(1-2):47-55. doi: 10.1007/s12031-009-9252-1
  147. Pasinetti GM, Ho L, Dooley C, Abbi B, Lange G. Select non-coding RNA in blood components provide novel clinically accessible biological surrogates for improved identification of traumatic brain injury in OEF/OIF Veterans. Am J Neurodegener Dis. 2012;1(1):88-98.
  148. Gapp K, Jawaid A, Sarkies P, et al. Implication of sperm RNAs in transgenerational inheritance of the effects of early trauma in mice. Nat Neurosci. 2014;17(5):667-669. doi: 10.1038/nn.3695
  149. Dias BG, Goodman JV, Ahluwalia R, Easton AE, Andero R, Ressler KJ. Amygdala-dependent fear memory consolidation via miR-34a and Notch signaling. Neuron. 2014;83(4):906-918. doi: 10.1016/j.neuron.2014.07.019
  150. Vetere G, Barbato C, Pezzola S, et al. Selective inhibition of miR-92 in hippocampal neurons alters contextual fear memory. Hippocampus. 2014;24(12):1458-1465. doi: 10.1002/hipo.22326
  151. Wang RY, Phang RZ, Hsu PH, Wang WH, Huang HT, Liu IY. In vivo knockdown of hippocampal miR-132 expression impairs memory acquisition of trace fear conditioning. Hippocampus. 2013;23(7):625-633. doi: 10.1002/hipo.22123
  152. Lin Q, Wei W, Coelho CM, et al. The brain-specific microRNA miR-128b regulates the formation of fear-extinction memory. Nat Neurosci. 2011;14(9):1115-1117. doi: 10.1038/nn.2891
  153. Jovasevic V, Corcoran KA, Leaderbrand K, et al. GABAergic mechanisms regulated by miR-33 encode state-dependent fear. Nat Neurosci. 2015;18(9):1265-1271. doi: 10.1038/nn.4084
  154. Balakathiresan NS, Chandran R, Bhomia M, Jia M, Li H, Maheshwari RK. Serum and amygdala microRNA signatures of posttraumatic stress: fear correlation and biomarker potential. J Psychiatr Res. 2014;57:65-73. doi: 10.1016/j.jpsychires.2014.05.020
  155. Schmidt U, Herrmann L, Hagl K, et al. Therapeutic action of fluoxetine is associated with a reduction in prefrontal cortical miR-1971 expression levels in a mouse model of posttraumatic stress disorder. Front Psychiatry. 2013;4:66. doi: 10.3389/fpsyt.2013.00066
  156. Sun P, Liu DZ, Jickling GC, Sharp FR, Yin KJ. MicroRNA-based therapeutics in central nervous system injuries. J Cereb Blood Flow Metab. 2018;38(7):1125-1148. doi: 10.1177/0271678x18773871
  157. Razin SV, Bystritskiy AA. Chromatin: packaged genome (4th edition). Moskow: BINOM. Laboratoriya znaniy. 2015. 191 p. (In Russ.)
  158. Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem. 2009;78:273-304. doi: 10.1146/annurev.biochem.77.062706.153223
  159. Hammond CM, Strømme CB, Huang H, Patel DJ, Groth A. Histone chaperone networks shaping chromatin function. Nat Rev Mol Cell Biol. 2017;18(3):141-158. doi: 10.1038/nrm.2016.159
  160. Berson A, Nativio R, Berger SL, Bonini NM. Epigenetic regulation in neurodegenerative diseases. Trends Neurosci. 2018;41(9):587-598. doi: 10.1016/j.tins.2018.05.005
  161. Rajam SM, Varghese PC, Dutta D. Histone chaperones as cardinal players in development. Front Cell Dev Biol. 2022;10:767773. doi: 10.3389/fcell.2022.767773
  162. Akishina AA, Kuvaeva EE, Vorontsova YE, Simonova OB. NAP family histone chaperones: characterization and role in ontogenesis. Russian Journal of Developmental Biology. 2020;51(6):343-355. doi: 10.1134/S1062360420060028
  163. Antontseva EV, Bondar NP. Chromatin remodeling in oligodendrogenesis. Vavilov J Genet Breeding. 2021;25(5):573-579. doi: 10.18699/VJ21.064
  164. Goodwin LR, Picketts DJ. The role of ISWI chromatin remodeling complexes in brain development and neurodevelopmental disorders. Mol Cell Neurosci. 2018;87:55-64. doi: 10.1016/j.mcn.2017.10.008
  165. Masliah-Planchon J, Bièche I, Guinebretière JM, Bourdeaut F, Delattre O. SWI/SNF chromatin remodeling and human malignancies. Annu Rev Pathol. 2015;10:145-171. doi: 10.1146/annurev-pathol-012414-040445
  166. Wang GG, Allis CD, Chi P. Chromatin remodeling and cancer, Part II: ATP-dependent chromatin remodeling. Trends Mol Med. 2007;13(9):373-380. doi: 10.1016/j.molmed.2007.07.004
  167. Larrigan S, Shah S, Fernandes A, Mattar P. Chromatin remodeling in the brain-a NuRDevelopmental odyssey. Int J Mol Sci. 2021;22(9):4768. doi: 10.3390/ijms22094768
  168. Pulice JL, Kadoch C. Composition and function of mammalian SWI/SNF chromatin remodeling complexes in human disease. Cold Spring Harb Symp Quant Biol. 2016;81:53-60. doi: 10.1101/sqb.2016.81.031021
  169. Bielawski T, Misiak B, Moustafa A, Frydecka D. Epigenetic mechanisms, trauma, and psychopathology: Targeting chromatin remodeling complexes. Rev Neurosci. 2019;30(6):595-604. doi: 10.1515/revneuro-2018-0055
  170. Cunliffe VT. The epigenetic impacts of social stress: how does social adversity become biologically embedded? Epigenomics. 2016;8(12):1653-1669. doi: 10.2217/epi-2016-0075
  171. Yuan M, Yang B, Rothschild G, et al. Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential. Signal Transduction and Targeted Therapy. 2023;8(1):309. doi: 10.1038/s41392-023-01519-z
  172. Zhang L, Li H, Hu X, Li XX, Smerin S, Ursano R. Glucocorticoid-induced p11 over-expression and chromatin remodeling: a novel molecular mechanism of traumatic stress? Med Hypotheses. 2011;76(6):774-777. doi: 10.1016/j.mehy.2011.02.015
  173. King HA, Trotter KW, Archer TK. Chromatin remodeling during glucocorticoid receptor regulated transactivation. Biochim Biophys Acta. 2012;1819(7):716-726. doi: 10.1016/j.bbagrm.2012.02.019
  174. Li X, An Z, Zhang W, Li F. Phase separation: Direct and indirect driving force for high-order chromatin organization. Genes (Basel). 2023;14(2):499. doi: 10.3390/genes14020499
  175. Ling X, Liu X, Jiang S, Fan L, Ding J. The dynamics of three-dimensional chromatin organization and phase separation in cell fate transitions and diseases. Cell Regen. 2022;11(1):42. doi: 10.1186/s13619-022-00145-4
  176. Theis A, Harrison MM. Reprogramming of three-dimensional chromatin organization in the early embryo. Curr Opin Struct Biol. 2023;81:102613. doi: 10.1016/j.sbi.2023.102613
  177. Chen X, Lin H, Li G. The influence of high-order chromatin state in the regulation of stem cell fate. Biochem Soc Trans. 2022;50(6):1809-1822. doi: 10.1042/bst20220763
  178. Vertii A. Stress as a chromatin landscape architect. Front Cell Dev Biol. 2021;9:790138. doi: 10.3389/fcell.2021.790138
  179. Gluch A, Vidakovic M, Bode J. Scaffold/matrix attachment regions (S/MARs): relevance for disease and therapy. Handb Exp Pharmacol. 2008;(186):67-103. doi: 10.1007/978-3-540-72843-6_4
  180. Podgornaya OI. Nuclear organization by satellite DNA, SAF-A/hnRNPU and matrix attachment regions. Semin Cell Dev Biol. 2022;128:61-68. doi: 10.1016/j.semcdb.2022.04.018
  181. Benham C, Kohwi-Shigematsu T, Bode J. Stress-induced duplex DNA destabilization in scaffold/matrix attachment regions. J Mol Biol. 1997;274(2):181-196. doi: 10.1006/jmbi.1997.1385
  182. Mitrentsi I, Lou J, Kerjouan A, et al. Heterochromatic repeat clustering imposes a physical barrier on homologous recombination to prevent chromosomal translocations. Mol Cell. 2022;82(11):2132-2147.e2136. doi: 10.1016/j.molcel.2022.03.033
  183. Wang B, Ji L, Bian Q. SATB1 regulates 3D genome architecture in T cells by constraining chromatin interactions surrounding CTCF-binding sites. Cell Rep. 2023;42(4):112323. doi: 10.1016/j.celrep.2023.112323
  184. Russo T, Kolisnyk B, Plessis-Belair J, et al. The SATB1-MIR22-GBA axis mediates glucocerebroside accumulation inducing a cellular senescence-like phenotype in dopaminergic neurons. Aging Cell. 2024:e14077. doi: 10.1111/acel.14077
  185. Babcock KJ, Abdolmohammadi B, Kiernan PT, et al. Interface astrogliosis in contact sport head impacts and military blast exposure. Acta Neuropathol Commun. 2022;10(1):52. doi: 10.1186/s40478-022-01358-z
  186. Broussard JI, Acion L, De Jesús-Cortés H, et al. Repeated mild traumatic brain injury produces neuroinflammation, anxiety-like behaviour and impaired spatial memory in mice. Brain Inj. 2018;32(1):113-122. doi: 10.1080/02699052.2017.1380228
  187. Ochiai H, Ohishi H, Sato Y, Kimura H. Organization of transcription and 3D genome as revealed by live-cell imaging. Curr Opin Struct Biol. 2023;81:102615. doi: 10.1016/j.sbi.2023.102615
  188. da Costa-Nunes JA, Noordermeer D. TADs: Dynamic structures to create stable regulatory functions. Curr Opin Struct Biol. 2023;81:102622. doi: 10.1016/j.sbi.2023.102622
  189. Bertero A, Rosa-Garrido M. Three-dimensional chromatin organization in cardiac development and disease. J Mol Cell Cardiol. 2021;151:89-105. doi: 10.1016/j.yjmcc.2020.11.008
  190. Won H, de la Torre-Ubieta L, Stein JL, et al. Chromosome conformation elucidates regulatory relationships in developing human brain. Nature. 2016;538(7626):523-527. doi: 10.1038/nature19847
  191. Rajarajan P, Borrman T, Liao W, et al. Neuron-specific signatures in the chromosomal connectome associated with schizophrenia risk. Science. 2018;362(6420):eaat4311. doi: 10.1126/science.aat4311
  192. Mansour M, Joseph GR, Joy GK, et al. Post-traumatic stress disorder: A narrative review of pharmacological and psychotherapeutic interventions. Cureus. 2023;15(9):e44905. doi: 10.7759/cureus.44905
  193. Cano GH, Dean J, Abreu SP, et al. Key characteristics and development of psychoceuticals: A review. Int J Mol Sci. 2022;23(24):15777. doi: 10.3390/ijms232415777
  194. Ullrich D, Mac Gillavry DW. Mini-review: A possible role for galanin in post-traumatic stress disorder. Neurosci Lett. 2021;756:135980. doi: 10.1016/j.neulet.2021.135980
  195. Miller MW. Leveraging genetics to enhance the efficacy of PTSD pharmacotherapies. Neurosci Lett. 2020;726:133562. doi: 10.1016/j.neulet.2018.04.039
  196. Rudzki S. Is PTSD an evolutionary survival adaptation initiated by unrestrained cytokine signaling and maintained by epigenetic change? Mil Med. 2022;doi: 10.1093/milmed/usac095
  197. Koweszko T, de Barbaro B, Izydorczyk B, et al. The position statement of the Working Group on the treatment of post-traumatic stress disorders in adults. Psychiatr Pol. 2023;57(4):705-727. Stanowisko grupy roboczej dotyczące terapii zaburzeń związanych ze stresem pourazowym u osób dorosłych. doi: 10.12740/pp/166172
  198. Zeifman RJ, Kettner H, Ross S, et al. Preliminary evidence for the importance of therapeutic alliance in MDMA-assisted psychotherapy for posttraumatic stress disorder. Eur J Psychotraumatol. 2024;15(1):2297536. doi: 10.1080/20008066.2023.2297536
  199. Deckel GM, Lepow LA, Guss J. "Psychedelic assisted therapy" Must not be retired. Am J Psychiatry. 2024;181(1):77-78. doi: 10.1176/appi.ajp.20230667
  200. Danböck SK, Duek O, Ben-Zion Z, et al. Effects of a dissociative drug on fronto-limbic resting-state functional connectivity in individuals with posttraumatic stress disorder: a randomized controlled pilot study. Psychopharmacology (Berl). 2024;241(2):243-252. doi: 10.1007/s00213-023-06479-4
  201. Fedotshev AI. Stress, the consequences of its influence on humans and modern non-drug methods of stress-induced states reduction. Uspekhi fiziologicheskikh nauk. 2009;40(1):77-91. (In Russ.)
  202. Tissen IY, Yakushina ND, Lebedev AA et al. Effect of SB-408124, an orexin A OX1R receptor antagonist, on the compulsive behavior and the level of anxiety after the vital stress in rats. Rev Clin Pharmd Drug Therapy. 2018;16(1):34-42. (In Russ.) doi: 10.17816/RCF16134-42
  203. Avaliani T, Apraksina N, Tsikunov S. Primeneniye vazopressina dlya korrektsii posledstviy vliyaniya psikhogennoy travmy materey na povedeniye potomstva. Eurasian Union Scientists. 2020;3(9(78)):4-10. (In Russ.) doi: 10.31618/ESU.2413-9335.2020.3.78.1013
  204. Xu Z, Li W, Sun Y, et al. Melatonin alleviates PTSD-like behaviors and restores serum GABA and cortisol levels in mice. Psychopharmacology (Berl). 2023;240(2):259-269. doi: 10.1007/s00213-023-06312-y
  205. Moskaleva PV, Shnayder NA, Dmitrenko DV, Shilkina OS, Neznanov NG, Nasyrova RF. Association of polymorphism of TPH1 and TPH2 genes with risk of psychoneurological disorders development. Uspekhi fiziologicheskikh nauk 2021; 52(2):51-60. (In Russ.) doi: 10.31857/S0301179821020077
  206. Skolariki K, Vlamos P. Exploring gene-drug interactions for personalized treatment of post-traumatic stress disorder. Front Comput Neurosci. 2023;17:1307523. doi: 10.3389/fncom.2023.1307523
  207. Gu T, Xu C, Meng X, et al. Sevoflurane preconditioning alleviates posttraumatic stress disorder-induced apoptosis in the hippocampus via the EZH2-regulated Akt/mTOR axis and improves synaptic Plasticity. J Mol Neurosci. 2023;73(4-5):225-236. doi: 10.1007/s12031-023-02114-1
  208. Klyueva NN, Avaliani TV, Apraksina NK. Lipid spectrum in rat offspring in a model of preconditioning of psychotraumatic effects. Rev Clin Pharm Drug Therapy. 2020;18(1):57-61. (In Russ.) doi: 10.17816/RCF18157-61
  209. Baranova KA, Rybnikova EA, Samoilov MO. The neurotrophin bdnf is involved in the development and prevention of stress-induced psychopathologies. Neurochem J. 2015;9(2):108-115. doi: 10.1134/S1819712415020038
  210. Ding FS, Cheng X, Zhao T, et al. Intermittent hypoxic preconditioning relieves fear and anxiety behavior in post-traumatic stress model mice. Sheng Li Xue Bao. 2019;71(4):537-546.
  211. He Q, Wang W, Xu D, et al. Potential causal association between gut microbiome and posttraumatic stress disorder. Transl Psychiatry. 2024;14(1):67. doi: 10.1038/s41398-024-02765-7
  212. Neznanov NG, Leonova LV, Rukavishnikov GV et al. Enteric microbiota as a research object in mental disorders. Uspekhi fiziologicheskikh nauk 2021;52(1):64-76. (In Russ.) doi: 10.31857/S0301179821010069
  213. Nikitina VA, Zakharova MV, Trofimov AN, et al. Neonatal exposure to bacterial lipopolysaccharide affects behavior and expression of ionotropic glutamate receptors in the hippocampus of adult rats after psychogenic Trauma. Biochemistry (Mosc). 2021;86(6):761-772. doi: 10.1134/s0006297921060134
  214. Csoka AB, Szyf M. Epigenetic side-effects of common pharmaceuticals: A potential new field in medicine and pharmacology. Medical Hypotheses. 2009;73(5):770-780. doi: 10.1016/j.mehy.2008.10.039
  215. Gladkova MG, Leidmaa E, Anderzhanova EA. Epidrugs in the therapy of central nervous system disorders: a way to drive on? Cells. 2023;12(11):1464. doi: 10.3390/cells12111464
  216. Lloyd S, Lutz PE, Bonventre C. Can you remember silence? Epigenetic memory and reversibility as a site of intervention. Bioessays. 2023;45(7):e2300019. doi: 10.1002/bies.202300019
  217. Zannas AS, Linnstaedt SD, An X, et al. Epigenetic aging and PTSD outcomes in the immediate aftermath of trauma. Psychol Med. 2023;53(15):7170-7179. doi: 10.1017/s0033291723000636
  218. Avaliani TV, Lebedev AA, Belobokova NK et al. Dopamine dependent behaviors of rat pups from mothers stressed in pregnancy. Psychopharmacol Biol Narcol. 2005;5(2):953-956. (In Russ.)
  219. Nguyen M, Roth A, Kyzar EJ, et al. Decoding the contribution of dopaminergic genes and pathways to autism spectrum disorder (ASD). Neurochem Int. 2014;66:15-26. doi: 10.1016/j.neuint.2014.01.002
  220. Santos-Toscano R, Arevalo MA, Garcia-Segura LM, Grassi D, Lagunas N. Interaction of gonadal hormones, dopaminergic system, and epigenetic regulation in the generation of sex differences in substance use disorders: A systematic review. Front Neuroendocrinol. 2023;71:101085. doi: 10.1016/j.yfrne.2023.101085
  221. Kovalenko IL, Galyamina AG, Smagin DA et al. Co-expression of glutamatergic and autismrelated genes in the hippocampus of male mice with disturbances of social behavior. Vavilov J Genetics Breeding. 2020;24(2):191-199. (In Russ.) DOI:https://doi.org/10.18699/VJ20.42-o
  222. Plekanchuk VS, Ryazanova MA. Expression of glutamate receptor genesin the hippocampus and frontal cortex in GC rat strain with genetic catatonia. Journal of Evolutionary Biochemistry and Physiology. 2021;57(1):156-163. doi: 10.1134/S0022093021010154
  223. Kovalenko AA, Zakharova MV, Nikitina VA et al. Alterations in the expression of genes that encode subunits of ionotropic glutamate receptors and the glutamate transporter in brain structures of rats after psychogenic stress. Neurochemistry (Moscow). 2018;35(2):132-139. doi: 10.7868/S102781331802005X
  224. Belokoskova SG, Stepanov II, Tsikunov SG. Agonist of V2 vasopressin receptor reduces depressive disorders in post-stroke patients. Vestnik Rossiyskoy akademii meditsinskikh nauk. 2012;67(4):40-44. (In Russ.) doi: 10.15690/vramn.v67i4.197
  225. Tyuzikov IA, Kalinchenko SY, Vorslov LO, Tishova YA. Vasopressin: non-classic effects and role in pathogenesis of age-associated diseases. Effektivnaya farmakoterapiya. 2015;26:38-50. (In Russ.)
  226. Hillemacher T, Frieling H, Luber K, et al. Epigenetic regulation and gene expression of vasopressin and atrial natriuretic peptide in alcohol withdrawal. Psychoneuroendocrinology. 2009;34(4):555-560. doi: 10.1016/j.psyneuen.2008.10.019
  227. Faustova AG. Current views on the genetic markers of post-traumatic stress disorder. Clin Psychol Special Education. 2021;10(1):61-69. (In Russ.) doi: 10.17759/cpse.2021100104
  228. Kmita H, Pinna G, Lushchak VI. Potential oxidative stress related targets of mitochondria-focused therapy of PTSD. Front Physiol. 2023;14:1266575. doi: 10.3389/fphys.2023.1266575
  229. Cristancho AG, Marsh ED. Epigenetics modifiers: Potential hub for understanding and treating neurodevelopmental disorders from hypoxic injury. J Neurodev Disord. 2020;12(1):37. doi: 10.1186/s11689-020-09344-z
  230. Rybnikova E, Nalivaeva N. Glucocorticoid-dependent mechanisms of brain tolerance to hypoxia. Int J Mol Sci. 2021;22(15):7982. doi: 10.3390/ijms22157982
  231. Abdul-Muneer PM. Nrf2 as a potential therapeutic target for traumatic brain injury. J Integr Neurosci. 2023;22(4):81. doi: 10.31083/j.jin2204081
  232. Kim YK, Amidfar M, Won E. A review on inflammatory cytokine-induced alterations of the brain as potential neural biomarkers in post-traumatic stress disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2019;91:103-112. doi: 10.1016/j.pnpbp.2018.06.008
  233. Sharrouf KA, Suchkova IO. The influence of lactoferrin on the epigenetic characteristics of mammalian cells of different types. Medical Academic Journal. 2021;21(1):85-95. doi: 10.17816/MAJ64106
  234. Suchkova IO, Sharrouf KA, Sasina LK, Dergacheva NI, Baranova TV, Patkin EL. Apo-form of recombinant human lactoferrin changes the genome-wide DNA methylation level and the chromatin compaction degree in neuroblastoma cell line IMR-32. Medical Academic Journal. 2022;22(4):77-96. (In Russ.) doi: 10.17816/MAJ112498
  235. Cardoner N, Andero R, Cano M, et al. Impact of stress on brain morphology: Insights into structural biomarkers of stress-related disorders. Curr Neuropharmacol. 2024;22(5):935-962. doi: 10.2174/1570159x21666230703091435
  236. Vialou V, Feng J, Robison AJ, Nestler EJ. Epigenetic mechanisms of depression and antidepressant action. Annu Rev Pharmacol Toxicol. 2013;53:59-87. doi: 10.1146/annurev-pharmtox-010611-134540
  237. Han J, Bichell TJ, Golden S, et al. A placebo-controlled trial of folic acid and betaine in identical twins with Angelman syndrome. Orphanet J Rare Dis. 2019;14(1):232. doi: 10.1186/s13023-019-1216-0
  238. Freilinger M, Dunkler D, Lanator I, et al. Effects of creatine supplementation in Rett syndrome: a randomized, placebo-controlled trial. J Dev Behav Pediatr. 2011;32(6):454-460. doi: 10.1097/DBP.0b013e31822177a8
  239. Jangra A, Sriram CS, Pandey S, et al. Epigenetic modifications, alcoholic brain and potential drug targets. Ann Neurosci. 2016;23(4):246-260. doi: 10.1159/000449486
  240. Schäfer A, Schomacher L, Barreto G, Döderlein G, Niehrs C. Gemcitabine functions epigenetically by inhibiting repair mediated DNA demethylation. PLoS One. 2010;5(11):e14060. doi: 10.1371/journal.pone.0014060
  241. Xu S, Jiang C, Lin R, et al. Epigenetic activation of the elongator complex sensitizes gallbladder cancer to gemcitabine therapy. J Exp Clin Cancer Res. 2021;40(1):373. doi: 10.1186/s13046-021-02186-0
  242. Zhou Z, Li HQ, Liu F. DNA methyltransferase inhibitors and their therapeutic potential. Curr Top Med Chem. 2018;18(28):2448-2457. doi: 10.2174/1568026619666181120150122
  243. Stresemann C, Lyko F. Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int J Cancer. 2008;123(1):8-13. doi: 10.1002/ijc.23607
  244. Kirsanova OV, Cherepanova NA, Gromova ES. Inhibition of C5-cytosine-DNA-methyltransferases. Biochemistry (Moscow). 2009;74(11):1175-1186. doi: 10.1134/S0006297909110017
  245. Kumanishi S, Yamanegi K, Nishiura H, et al. Epigenetic modulators hydralazine and sodium valproate act synergistically in VEGI-mediated anti-angiogenesis and VEGF interference in human osteosarcoma and vascular endothelial cells. Int J Oncol. 2019;55(1):167-178. doi: 10.3892/ijo.2019.4811
  246. Blaauboer A, van Koetsveld PM, Mustafa DAM, et al. The class I HDAC inhibitor valproic acid strongly potentiates gemcitabine efficacy in pancreatic cancer by immune system activation. Biomedicines. 2022;10(3):517. doi: 10.3390/biomedicines10030517
  247. Gao Z, Xu Z, Hung MS, et al. Procaine and procainamide inhibit the Wnt canonical pathway by promoter demethylation of WIF-1 in lung cancer cells. Oncol Rep. 2009;22(6):1479-1484. doi: 10.3892/or_00000590
  248. Franco I, Ortiz-López L, Roque-Ramírez B, Ramírez-Rodríguez GB, Lamas M. Pharmacological inhibition of DNA methyltransferase 1 promotes neuronal differentiation from rodent and human nasal olfactory stem/progenitor cell cultures. Int J Dev Neurosci. 2017;58:65-73. doi: 10.1016/j.ijdevneu.2017.01.013
  249. Detich N, Bovenzi V, Szyf M. Valproate induces replication-independent active DNA demethylation. J Biol Chem. 2003;278(30):27586-27592. doi: 10.1074/jbc.M303740200
  250. Attia SM, Ahmad SF, Nadeem A, et al. 3-Aminobenzamide alleviates elevated DNA damage and DNA methylation in a BTBR T(+)Itpr3(tf)/J mouse model of autism by enhancing repair gene expression. Pharmacol Biochem Behav. 2020;199:173057. doi: 10.1016/j.pbb.2020.173057
  251. Yastrebov DV. Atypical antipsychotics of the substituted benzamides group: tiapride, sulpiride and amisulpride. Pharmacological action and clinical use. Sotsial'naya i klinicheskaya psikhiatriya. 2015;25(3):72-79. (In Russ.)
  252. Rompala G, Nagamatsu ST, Martínez-Magaña JJ, et al. Profiling neuronal methylome and hydroxymethylome of opioid use disorder in the human orbitofrontal cortex. Nat Commun. 2023;14(1):4544. doi: 10.1038/s41467-023-40285-y
  253. Sarkar S, Deyoung T, Ressler H, Chandler W. Brain tumors: Development, drug resistance, and sensitization - an epigenetic approach. Epigenetics. 2023;18(1):2237761. doi: 10.1080/15592294.2023.2237761
  254. Lewis CR, Tafur J, Spencer S, et al. Pilot study suggests DNA methylation of the glucocorticoid receptor gene (NR3C1) is associated with MDMA-assisted therapy treatment response for severe PTSD. Front Psychiatry. 2023;14:959590. doi: 10.3389/fpsyt.2023.959590
  255. Wilker S, Vukojevic V, Schneider A, et al. Epigenetics of traumatic stress: The association of NR3C1 methylation and posttraumatic stress disorder symptom changes in response to narrative exposure therapy. Transl Psychiatry. 2023;13(1):14. doi: 10.1038/s41398-023-02316-6
  256. Schieffler DA, Matta SE. Evidence to support the use of S-adenosylmethionine for treatment of post-concussive sequelae in the military. Mil Med. 2022;187(9-10):e1182-e1192. doi: 10.1093/milmed/usab130
  257. Drakontaeidi A, Pontiki E. A review on molecular docking on HDAC isoforms: Novel tool for designing selective inhibitors. Pharmaceuticals (Basel). 2023;16(12):1639. doi: 10.3390/ph16121639
  258. Datta M, Staszewski O, Raschi E, et al. Histone deacetylases 1 and 2 regulate microglia function during development, homeostasis, and neurodegeneration in a context-dependent manner. Immunity. 2018;48(3):514-529.e516. doi: 10.1016/j.immuni.2018.02.016
  259. Legastelois R, Jeanblanc J, Vilpoux C, Bourguet E, Naassila M. Epigenetic mechanisms and alcohol use disorders: a potential therapeutic target. Biol Aujourdhui. 2017;211(1):83-91. Mécanismes épigénétiques et troubles de l’usage d’alcool : une cible thérapeutique intéressante? doi: 10.1051/jbio/2017014
  260. Kurita M, Holloway T, García-Bea A, et al. HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity. Nat Neurosci. 2012;15(9):1245-1254. doi: 10.1038/nn.3181
  261. Tanelian A, Nankova B, Hu F, Sahawneh JD, Sabban EL. Effect of acetate supplementation on traumatic stress-induced behavioral impairments in male rats. Neurobiol Stress. 2023;27:100572. doi: 10.1016/j.ynstr.2023.100572
  262. Wan SS, Pan YM, Yang WJ, Rao ZQ, Yang YN. Inhibition of EZH2 alleviates angiogenesis in a model of corneal neovascularization by blocking FoxO3a-mediated oxidative stress. Faseb j. 2020;34(8):10168-10181. doi: 10.1096/fj.201902814RRR
  263. Li D, Peng X, Hu Z, Li S, Chen J, Pan W. Small molecules targeting selected histone methyltransferases (HMTs) for cancer treatment: Current progress and novel strategies. Eur J Med Chem. 2024;264:115982. doi: 10.1016/j.ejmech.2023.115982
  264. Ravikumar Y, Koonyosying P, Srichairatanakool S, Ponpandian LN, Kumaravelu J, Srichairatanakool S. In silico molecular docking and dynamics simulation analysis of potential histone lysine methyl transferase inhibitors for managing β-thalassemia. Molecules. 2023;28(21):7266. doi: 10.3390/molecules28217266
  265. Leshem M, Schulkin J. Transgenerational effects of infantile adversity and enrichment in male and female rats. Dev Psychobiol. 2012;54(2):169-186. doi: 10.1002/dev.20592
  266. Arai JA, Li S, Hartley DM, Feig LA. Transgenerational rescue of a genetic defect in long-term potentiation and memory formation by juvenile enrichment. J Neurosci. 2009;29(5):1496-1502. doi: 10.1523/jneurosci.5057-08.2009
  267. Gapp K, Bohacek J, Grossmann J, et al. Potential of environmental enrichment to prevent transgenerational effects of paternal trauma. Neuropsychopharmacology. 2016;41(11):2749-2758. doi: 10.1038/npp.2016.87
  268. Li M, Wang X, Yang L, Jiang Y, Xie Y, Li K. Acupuncture improves learning and memory ability of posttraumatic stress disorder model rats through epigenetic regulation of microglial phosphatidylinositol 3-kinase pathway. Technol Health Care. 2023;31(S1):409-421. doi: 10.3233/thc-236035
  269. Cohen T, Shomron N. Can RNA affect memory modulation? Implications for PTSD understanding and treatment. Int J Mol Sci. 2023;24(16):12908. doi: 10.3390/ijms241612908
  270. Giridharan VV, Thandavarayan RA, Fries GR, et al. Newer insights into the role of miRNA a tiny genetic tool in psychiatric disorders: Focus on post-traumatic stress disorder. Transl Psychiatry. 2016;6(11):e954. doi: 10.1038/tp.2016.220
  271. Wang S, Tang L, Huang N, Wang H. The roles of long noncoding RNA in depression. Front Biosci (Landmark Ed). 2023;28(11):321. doi: 10.31083/j.fbl2811321
  272. Mustafin RN, Enikeeva RF, Khusnutdinova EK, Davydova YD. The role of epigenetic factors in the development of depressive disorders. Russian Journal of Genetics. 2018;54(12):1397-1409. doi: 10.1134/S1022795418120104
  273. Gupta S, Guleria RS, Szabo YZ. MicroRNAs as biomarker and novel therapeutic target for posttraumatic stress disorder in Veterans. Psychiatry Res. 2021;305:114252. doi: 10.1016/j.psychres.2021.114252
  274. Bolouki A, Rahimi M, Azarpira N, Baghban F. Integrated multi-omics analysis identifies epigenetic alteration related to neurodegeneration development in post-traumatic stress disorder patients. Psychiatr Genet. 2023;33(5):167-181. doi: 10.1097/ypg.0000000000000340
  275. Shkundin A, Halaris A. Associations of BDNF/BDNF-AS SNPs with Depression, Schizophrenia, and Bipolar Disorder. J Pers Med. 2023;13(9):1395. doi: 10.3390/jpm13091395
  276. Kleeman EA, Reisinger SN, Adithya P, et al. Paternal immune activation by Poly I:C modulates sperm noncoding RNA profiles and causes transgenerational changes in offspring behavior. Brain Behav Immun. 2024;115:258-279. doi: 10.1016/j.bbi.2023.10.005
  277. Short AK, Yeshurun S, Powell R, et al. Exercise alters mouse sperm small noncoding RNAs and induces a transgenerational modification of male offspring conditioned fear and anxiety. Transl Psychiatry. 2017;7(5):e1114. doi: 10.1038/tp.2017.82
  278. Raj P, Rauniyar S, Sapkale B. Psychedelic drugs or hallucinogens: Exploring their medicinal potential. Cureus. 2023;15(11):e48719. doi: 10.7759/cureus.48719
  279. Kargbo RB. Tryptamines and mental health: Activating the 5-HT receptor for therapeutic potential. ACS Med Chem Lett. 2023;14(10):1331-1333. doi: 10.1021/acsmedchemlett.3c00390
  280. Proskynitopoulos PJ, Bleich S, Muschler MAN, et al. Methylation of the oxytocin, oxytocin receptor, and vasopressin gene promoters in tobacco use disorder during cessation. Neuropsychobiology. 2024;83(1):28-40. doi: 10.1159/000535663
  281. Hopkins WD, Staes N, Guevara EE, Mulholland MM, Sherwood CC, Bradley BJ. Vasopressin, and not oxytocin, receptor gene methylation is associated with individual differences in receptive joint attention in chimpanzees (Pan troglodytes). Autism Res. 2023;16(4):713-722. doi: 10.1002/aur.2895
  282. Murgatroyd CA, Hicks-Nelson A, Fink A, et al. Effects of chronic social stress and maternal intranasal oxytocin and vasopressin on offspring interferon-γ and behavior. Front Endocrinol (Lausanne). 2016;7:155. doi: 10.3389/fendo.2016.00155
  283. Dannenhoffer CA, Kim EU, Saalfield J, Werner DF, Varlinskaya EI, Spear LP. Oxytocin and vasopressin modulation of social anxiety following adolescent intermittent ethanol exposure. Psychopharmacology (Berl). 2018;235(10):3065-3077. doi: 10.1007/s00213-018-5003-8
  284. Mardanpour M, Ghavidel N, Asadi S, Khodagholi F. Paternal stress in rats increased oxytocin, oxytocin receptor, and arginine vasopressin gene expression in the male offspring amygdala with no effect on their social interaction behaviors. Neuroreport. 2022;33(2):48-54. doi: 10.1097/wnr.0000000000001749
  285. Guoynes CD, Marler CA. Acute intranasal oxytocin dose enhances social preference for parents over peers in male but not female peri-adolescent California mice (Peromyscus californicus). Gen Comp Endocrinol. 2023;335:114230. doi: 10.1016/j.ygcen.2023.114230
  286. Aguirre-Vázquez A, Castorena-Torres F, Silva-Ramírez B, et al. Cell-type dependent regulation of pluripotency and chromatin remodeling genes by hydralazine. Stem Cell Res Ther. 2023;14(1):42. doi: 10.1186/s13287-023-03268-w
  287. Sapozhnikov DM, Szyf M. Enzyme-free targeted DNA demethylation using CRISPR-dCas9-based steric hindrance to identify DNA methylation marks causal to altered gene expression. Nat Protoc. 2022;17(12):2840-2881. doi: 10.1038/s41596-022-00741-3
  288. Grinkevich LN. Genome editing and regulation of gene expression using CRISPR/СAS technologies in neurobiology. Uspekhi fiziologicheskikh nauk 2021;52(3):4-23. (In Russ.) doi: 10.31857/S0301179821030024
  289. Xiao H, Xi K, Wang K, et al. Restoring the function of thalamocortical circuit through correcting thalamic Kv3.2 channelopathy normalizes fear extinction impairments in a PTSD mouse model. Adv Sci (Weinh). 2024;11(9):e2305939. doi: 10.1002/advs.202305939
  290. Liu H, Zhou T, Wang B, Li L, Ye D, Yu S. Identification and functional analysis of a potential key lncRNA involved in fat loss of cancer cachexia. J Cell Biochem. 2018;119(2):1679-1688. doi: 10.1002/jcb.26328

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