EPIGENETIC CHANGES IN POST-TRAUMATIC STRESS DISORDER: POSSIBILITIES AND LIMITATIONS OF EPIGENETIC THERAPY
- Authors: Suchkova I.O.1, Patkin E.L.2, Tsikunov S.G.2, Sofronov H.A.3,2
-
Affiliations:
- FSBSI «Institute of Experimental Medicine»
- FSBSI "Institute of Experimental Medicine"
- Military Medical Academy named after. C.M. Kirov of the Ministry of Defense of the Russian Federation
- Section: Analytical reviews
- Published: 09.07.2024
- URL: https://journals.eco-vector.com/MAJ/article/view/632018
- DOI: https://doi.org/10.17816/MAJ632018
- ID: 632018
Cite item
Full Text
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.
Full Text
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., 12Eugene 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., 12Sergey 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.,12Henrikh 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., 12References
- 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
- 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
- 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
- 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
- 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
- Dyuzhikova NA, Skomorokhova EB, Vaido AI. Epigenetic mechanisms in post-stress states. Uspekhi fiziologicheskikh nauk. 2015;46(1):47-75. (In Russ.)
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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.)
- 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
- 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)
- 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)
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.)
- 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
- 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
- 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
- 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
- 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
- Gökbuget D, Blelloch R. Epigenetic control of transcriptional regulation in pluripotency and early differentiation. Development. 2019;146(19):dev164772. doi: 10.1242/dev.164772
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Patkin EL. Epigenetic mechanisms of common human diseases. S-Petersburg: Nestor-Istoriya; 2008. 196 p. (In Russ.)
- 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
- 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.)
- 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.)
- 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.)
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Zovkic IB, Sweatt JD. Epigenetic mechanisms in learned fear: implications for PTSD. Neuropsychopharmacology. 2013;38(1):77-93. doi: 10.1038/npp.2012.79
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21(3):381-395. doi: 10.1038/cr.2011.22
- 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
- Pradeepa MM. Causal role of histone acetylations in enhancer function. Transcription. 2017;8(1):40-47. doi: 10.1080/21541264.2016.1253529
- 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
- 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
- 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
- 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
- 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
- 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.
- 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.
- 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
- Ryu HY, Hochstrasser M. Histone sumoylation and chromatin dynamics. Nucleic Acids Res. 2021;49(11):6043-6052. doi: 10.1093/nar/gkab280
- Li K, Wang Z. Histone crotonylation-centric gene regulation. Epigenetics Chromatin. 2021;14(1):10. doi: 10.1186/s13072-021-00385-9
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.)
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Razin SV, Bystritskiy AA. Chromatin: packaged genome (4th edition). Moskow: BINOM. Laboratoriya znaniy. 2015. 191 p. (In Russ.)
- 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
- 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
- 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
- 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
- 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
- Antontseva EV, Bondar NP. Chromatin remodeling in oligodendrogenesis. Vavilov J Genet Breeding. 2021;25(5):573-579. doi: 10.18699/VJ21.064
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Vertii A. Stress as a chromatin landscape architect. Front Cell Dev Biol. 2021;9:790138. doi: 10.3389/fcell.2021.790138
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Miller MW. Leveraging genetics to enhance the efficacy of PTSD pharmacotherapies. Neurosci Lett. 2020;726:133562. doi: 10.1016/j.neulet.2018.04.039
- 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
- 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
- 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
- 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
- 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
- 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.)
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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.)
- 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
- 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
- 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
- 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
- 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
- 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
- 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.)
- 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
- 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
- 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
- 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
- Rybnikova E, Nalivaeva N. Glucocorticoid-dependent mechanisms of brain tolerance to hypoxia. Int J Mol Sci. 2021;22(15):7982. doi: 10.3390/ijms22157982
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Kirsanova OV, Cherepanova NA, Gromova ES. Inhibition of C5-cytosine-DNA-methyltransferases. Biochemistry (Moscow). 2009;74(11):1175-1186. doi: 10.1134/S0006297909110017
- 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
- 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
- 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
- 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
- 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
- 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
- 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.)
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Raj P, Rauniyar S, Sapkale B. Psychedelic drugs or hallucinogens: Exploring their medicinal potential. Cureus. 2023;15(11):e48719. doi: 10.7759/cureus.48719
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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