Skip to main content

Advertisement

SpringerLink
Log in

Tet Enzyme-Mediated Response in Environmental Stress and Stress-Related Psychiatric Diseases

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

Mental disorders caused by stress have become a worldwide public health problem. These mental disorders are often the results of a combination of genes and environment, in which epigenetic modifications play a crucial role. At present, the genetic and epigenetic mechanisms of mental disorders such as posttraumatic stress disorder or depression caused by environmental stress are not entirely clear. Although many epigenetic modifications affect gene regulation, the most well-known modification in eukaryotic cells is the DNA methylation of CpG islands. Stress causes changes in DNA methylation in the brain to participate in the neuronal function or mood-modulating behaviors, and these epigenetic modifications can be passed on to offspring. Ten-eleven translocation (Tet) enzymes are the 5-methylcytosine (5mC) hydroxylases of DNA, which recognize 5mC on the DNA sequence and oxidize it to 5-hydroxymethylcytosine (5hmC), 5-formylcytosine (5fC), and 5-carboxylcytosine (5caC). Tet regulates gene expression at the transcriptional level through the demethylation of DNA. This review will elaborate on the molecular mechanism and the functions of Tet enzymes in environmental stress-related disorders and discuss future research directions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data Availability

Not applicable.

References

  1. Czamara D, Neufang A, Dieterle R, Iurato S, Arloth J, Martins J, Ising M, Binder EE et al (2022) Effects of stressful life-events on DNA methylation in panic disorder and major depressive disorder. Clin Epigenetics 14:55. https://doi.org/10.1186/s13148-022-01274-y

    Article  CAS  Google Scholar 

  2. Kessler RC, Aguilar-Gaxiola S, Alonso J, Benjet C, Bromet EJ, Cardoso G, Degenhardt L, de Girolamo G et al (2017) Trauma and PTSD in the WHO World Mental Health surveys. Eur J Psychotraumatol 8:1353383. https://doi.org/10.1080/20008198.2017.1353383

    Article  Google Scholar 

  3. Gao YN, Zhang YQ, Wang H, Deng YL, Li NM (2022) A new player in depression: MiRNAs as modulators of altered synaptic plasticity. Int J Mol Sci 23:https://doi.org/10.3390/ijms23094555

  4. Li E, Zhang Y (2014) DNA methylation in mammals. Cold Spring Harb Perspect Biol 6:a019133. https://doi.org/10.1101/cshperspect.a019133

    Article  CAS  Google Scholar 

  5. Branco MR, Ficz G, Reik W (2011) Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 13:7–13. https://doi.org/10.1038/nrg3080

    Article  CAS  Google Scholar 

  6. Globisch D, Munzel M, Muller M, Michalakis S, Wagner M, Koch S, Bruckl T, Biel M et al (2010) Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One 5:e15367. https://doi.org/10.1371/journal.pone.0015367

    Article  CAS  Google Scholar 

  7. Cheng Y, Li Z, Manupipatpong S, Lin L, Li X, Xu T, Jiang YH, Shu Q et al (2018) 5-Hydroxymethylcytosine alterations in the human postmortem brains of autism spectrum disorder. Hum Mol Genet 27:2955–2964. https://doi.org/10.1093/hmg/ddy193

    Article  CAS  Google Scholar 

  8. Dong E, Gavin DP, Chen Y, Davis J (2012) Upregulation of TET1 and downregulation of APOBEC3A and APOBEC3C in the parietal cortex of psychotic patients. Transl Psychiatry 2:e159. https://doi.org/10.1038/tp.2012.86

    Article  CAS  Google Scholar 

  9. Fan BF, Hao B, Dai YD, Xue L, Shi YW, Liu L, Xuan SM, Yang N, Wang XG, Zhao H (2022) Deficiency of Tet3 in nucleus accumbens enhances fear generalization and anxiety-like behaviors in mice. Brain Pathol e13080 https://doi.org/10.1111/bpa.13080

  10. Szulwach KE, Li X, Li Y, Song CX, Wu H, Dai Q, Irier H, Upadhyay AK et al (2011) 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci 14:1607–1616. https://doi.org/10.1038/nn.2959

    Article  CAS  Google Scholar 

  11. Papale LA, Madrid A, Zhang Q, Chen K, Sak L, Keles S, Alisch RS (2022) Gene by environment interaction mouse model reveals a functional role for 5-hydroxymethylcytosine in neurodevelopmental disorders. Genome Res 32:266–279. https://doi.org/10.1101/gr.276137.121

    Article  Google Scholar 

  12. Goldberg AD, Allis CD, Bernstein E (2007) Epigenetics: a landscape takes shape. Cell 128:635–638. https://doi.org/10.1016/j.cell.2007.02.006

    Article  CAS  Google Scholar 

  13. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suner D, Cigudosa JC et al (2005) Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 102:10604–10609. https://doi.org/10.1073/pnas.0500398102

    Article  CAS  Google Scholar 

  14. Pizzagalli DA (2014) Depression, stress, and anhedonia: toward a synthesis and integrated model. Annu Rev Clin Psychol 10:393–423. https://doi.org/10.1146/annurev-clinpsy-050212-185606

    Article  Google Scholar 

  15. Torres-Berrio A, Issler O, Parise EM, Nestler EJ (2019) Unraveling the epigenetic landscape of depression: focus on early life stress. Dialogues Clin Neurosci 21:341–357. https://doi.org/10.31887/DCNS.2019.21.4/enestler

    Article  Google Scholar 

  16. Norman RE, Byambaa M, De R, Butchart A, Scott J, Vos T (2012) The long-term health consequences of child physical abuse, emotional abuse, and neglect: a systematic review and meta-analysis. PLoS Med 9:e1001349. https://doi.org/10.1371/journal.pmed.1001349

    Article  Google Scholar 

  17. Scott KM, McLaughlin KA, Smith DA, Ellis PM (2012) Childhood maltreatment and DSM-IV adult mental disorders: comparison of prospective and retrospective findings. Br J Psychiatry 200:469–475. https://doi.org/10.1192/bjp.bp.111.103267

    Article  Google Scholar 

  18. Smeeth D, Beck S, Karam EG, Pluess M (2021) The role of epigenetics in psychological resilience. Lancet Psychiatry 8:620–629. https://doi.org/10.1016/S2215-0366(20)30515-0

    Article  Google Scholar 

  19. Jaenisch R, Bird A (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(Suppl):245–254. https://doi.org/10.1038/ng1089

    Article  CAS  Google Scholar 

  20. Xie L, Korkmaz KS, Braun K, Bock J (2013) Early life stress-induced histone acetylations correlate with activation of the synaptic plasticity genes Arc and Egr1 in the mouse hippocampus. J Neurochem 125:457–464. https://doi.org/10.1111/jnc.12210

    Article  CAS  Google Scholar 

  21. Litvin Y, Turner CA, Rios MB, Maras PM, Chaudhury S, Baker MR, Blandino P Jr, Watson SJ Jr et al (2016) Fibroblast growth factor 2 alters the oxytocin receptor in a developmental model of anxiety-like behavior in male rat pups. Horm Behav 86:64–70. https://doi.org/10.1016/j.yhbeh.2016.09.009

    Article  CAS  Google Scholar 

  22. Blaze J, Asok A, Roth TL (2015) Long-term effects of early-life caregiving experiences on brain-derived neurotrophic factor histone acetylation in the adult rat mPFC. Stress 18:607–615. https://doi.org/10.3109/10253890.2015.1071790

    Article  CAS  Google Scholar 

  23. Chaudhury S, Aurbach EL, Sharma V, Blandino P Jr, Turner CA, Watson SJ, Akil H (2014) FGF2 is a target and a trigger of epigenetic mechanisms associated with differences in emotionality: partnership with H3K9me3. Proc Natl Acad Sci U S A 111:11834–11839. https://doi.org/10.1073/pnas.1411618111

    Article  CAS  Google Scholar 

  24. Uchida S, Hara K, Kobayashi A, Otsuki K, Yamagata H, Hobara T, Suzuki T, Miyata N et al (2011) Epigenetic status of Gdnf in the ventral striatum determines susceptibility and adaptation to daily stressful events. Neuron 69:359–372. https://doi.org/10.1016/j.neuron.2010.12.023

    Article  CAS  Google Scholar 

  25. Sullivan PF, Neale MC, Kendler KS (2000) Genetic epidemiology of major depression: review and meta-analysis. Am J Psychiatry 157:1552–1562. https://doi.org/10.1176/appi.ajp.157.10.1552

    Article  CAS  Google Scholar 

  26. Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, Fischer D, Holsboer F, Wotjak CT et al (2009) Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat Neurosci 12:1559–1566. https://doi.org/10.1038/nn.2436

    Article  CAS  Google Scholar 

  27. Murgatroyd C, Spengler D (2011) Epigenetic programming of the HPA axis: early life decides. Stress 14:581–589. https://doi.org/10.3109/10253890.2011.602146

    Article  CAS  Google Scholar 

  28. Klengel T, Mehta D, Anacker C, Rex-Haffner M, Pruessner JC, Pariante CM, Pace TW, Mercer KB et al (2013) Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat Neurosci 16:33–41. https://doi.org/10.1038/nn.3275

    Article  CAS  Google Scholar 

  29. Urb M, Anier K, Matsalu T, Aonurm-Helm A, Tasa G, Koppel I, Zharkovsky A, Timmusk T et al (2019) Glucocorticoid receptor stimulation resulting from early life stress affects expression of DNA methyltransferases in rat prefrontal cortex. J Mol Neurosci 68:99–110. https://doi.org/10.1007/s12031-019-01286-z

    Article  CAS  Google Scholar 

  30. Catale C, Bussone S, Lo Iacono L, Viscomi MT, Palacios D, Troisi A, Carola V (2020) Exposure to different early-life stress experiences results in differentially altered DNA methylation in the brain and immune system. Neurobiol Stress 13:100249. https://doi.org/10.1016/j.ynstr.2020.100249

    Article  CAS  Google Scholar 

  31. Li L, Wang T, Chen S, Yue Y, Xu Z, Yuan Y (2021) DNA methylations of brain-derived neurotrophic factor exon VI are associated with major depressive disorder and antidepressant-induced remission in females. J Affect Disord 295:101–107. https://doi.org/10.1016/j.jad.2021.08.016

    Article  CAS  Google Scholar 

  32. Bai M, Zhu X, Zhang Y, Zhang S, Zhang L, Xue L, Yi J, Yao S et al (2012) Abnormal hippocampal BDNF and miR-16 expression is associated with depression-like behaviors induced by stress during early life. PLoS One 7:e46921. https://doi.org/10.1371/journal.pone.0046921

    Article  CAS  Google Scholar 

  33. Zhang Y, Wang Y, Wang L, Bai M, Zhang X, Zhu X (2015) Dopamine receptor D2 and associated microRNAs are involved in stress susceptibility and resistance to escitalopram treatment. Int J Neuropsychopharmacol 18:https://doi.org/10.1093/ijnp/pyv025

  34. Umschweif G, Medrihan L, McCabe KA, Sagi Y, Greengard P (2021) Activation of the p11/SMARCA3/Neurensin-2 pathway in parvalbumin interneurons mediates the response to chronic antidepressants. Mol Psychiatry 26:3350–3362. https://doi.org/10.1038/s41380-021-01059-4

    Article  CAS  Google Scholar 

  35. Wille A, Amort T, Singewald N, Sartori SB, Lusser A (2016) Dysregulation of select ATP-dependent chromatin remodeling factors in high trait anxiety. Behav Brain Res 311:141–146. https://doi.org/10.1016/j.bbr.2016.05.036

    Article  CAS  Google Scholar 

  36. Ma C, Seong H, Liu Y, Yu X, Xu S, Li Y (2021) Ten-eleven translocation proteins (TETs): tumor suppressors or tumor enhancers? Front Biosci (Landmark Ed) 26:895–915. https://doi.org/10.52586/4996

    Article  CAS  Google Scholar 

  37. Moore LD, Le T, Fan G (2013) DNA methylation and its basic function. Neuropsychopharmacol 38:23–38. https://doi.org/10.1038/npp.2012.112

    Article  CAS  Google Scholar 

  38. Bronner C, Alhosin M, Hamiche A, Mousli M (2019) Coordinated dialogue between UHRF1 and DNMT1 to ensure faithful inheritance of methylated DNA patterns. Genes (Basel) 10:https://doi.org/10.3390/genes10010065

  39. Hermann A, Goyal R, Jeltsch A (2004) The Dnmt1 DNA-(cytosine-C5)-methyltransferase methylates DNA processively with high preference for hemimethylated target sites. J Biol Chem 279:48350–48359. https://doi.org/10.1074/jbc.M403427200

    Article  CAS  Google Scholar 

  40. Chen Z, Zhang Y (2020) Role of mammalian DNA methyltransferases in development. Annu Rev Biochem 89:135–158. https://doi.org/10.1146/annurev-biochem-103019-102815

    Article  CAS  Google Scholar 

  41. Wu X, Zhang Y (2017) TET-mediated active DNA demethylation: mechanism, function and beyond. Nat Rev Genet 18:517–534. https://doi.org/10.1038/nrg.2017.33

    Article  CAS  Google Scholar 

  42. Ehrlich M, Gama-Sosa MA, Huang LH, Midgett RM, Kuo KC, McCune RA, Gehrke C (1982) Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res 10:2709–2721. https://doi.org/10.1093/nar/10.8.2709

    Article  CAS  Google Scholar 

  43. Bayraktar G, Kreutz MR (2018) The role of activity-dependent DNA demethylation in the adult brain and in neurological disorders. Front Mol Neurosci 11:169. https://doi.org/10.3389/fnmol.2018.00169

    Article  CAS  Google Scholar 

  44. Maity S, Farrell K, Navabpour S, Narayanan SN, Jarome TJ (2021) Epigenetic mechanisms in memory and cognitive decline associated with aging and Alzheimer’s disease. Int J Mol Sci 22:https://doi.org/10.3390/ijms222212280

  45. Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA, Johnson ND, Lucero J, Huang Y et al (2013) Global epigenomic reconfiguration during mammalian brain development. Sci 341:1237905. https://doi.org/10.1126/science.1237905

    Article  CAS  Google Scholar 

  46. Siegmund KD, Connor CM, Campan M, Long TI, Weisenberger DJ, Biniszkiewicz D, Jaenisch R, Laird PW et al (2007) DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS One 2:e895. https://doi.org/10.1371/journal.pone.0000895

    Article  CAS  Google Scholar 

  47. Paoli C, Misztak P, Mazzini G, Musazzi L (2022) DNA methylation in depression and depressive-like phenotype: biomarker or target of pharmacological intervention? Curr Neuropharmacol https://doi.org/10.2174/1570159X20666220201084536

  48. Montalvo-Ortiz JL, Gelernter J, Cheng Z, Girgenti MJ, Xu K, Zhang X, Gopalan S, Zhou H et al (2022) Epigenome-wide association study of posttraumatic stress disorder identifies novel loci in U.S. military veterans. Transl Psychiatry 12:65. https://doi.org/10.1038/s41398-022-01822-3

    Article  CAS  Google Scholar 

  49. Chen D, Meng L, Pei F, Zheng Y, Leng J (2017) A review of DNA methylation in depression. J Clin Neurosci 43:39–46. https://doi.org/10.1016/j.jocn.2017.05.022

    Article  CAS  Google Scholar 

  50. Lorsbach RB, Moore J, Mathew S, Raimondi SC, Mukatira ST, Downing JR (2003) TET1, a member of a novel protein family, is fused to MLL in acute myeloid leukemia containing the t(10;11)(q22;q23). Leukemia 17:637–641. https://doi.org/10.1038/sj.leu.2402834

    Article  CAS  Google Scholar 

  51. Ono R, Taki T, Taketani T, Taniwaki M, Kobayashi H, Hayashi Y (2002) LCX, leukemia-associated protein with a CXXC domain, is fused to MLL in acute myeloid leukemia with trilineage dysplasia having t(10;11)(q22;q23). Cancer Res 62:4075–4080

    CAS  Google Scholar 

  52. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM et al (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Sci 324:930–935. https://doi.org/10.1126/science.1170116

    Article  CAS  Google Scholar 

  53. Ito S, D’Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y (2010) Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466:1129–1133. https://doi.org/10.1038/nature09303

    Article  CAS  Google Scholar 

  54. Xu Y, Wu F, Tan L, Kong L, Xiong L, Deng J, Barbera AJ, Zheng L et al (2011) Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 42:451–464. https://doi.org/10.1016/j.molcel.2011.04.005

    Article  CAS  Google Scholar 

  55. Xu Y, Xu C, Kato A, Tempel W, Abreu JG, Bian C, Hu Y, Hu D et al (2012) Tet3 CXXC domain and dioxygenase activity cooperatively regulate key genes for Xenopus eye and neural development. Cell 151:1200–1213. https://doi.org/10.1016/j.cell.2012.11.014

    Article  CAS  Google Scholar 

  56. Ko M, An J, Bandukwala HS, Chavez L, Aijo T, Pastor WA, Segal MF, Li H et al (2013) Modulation of TET2 expression and 5-methylcytosine oxidation by the CXXC domain protein IDAX. Nature 497:122–126. https://doi.org/10.1038/nature12052

    Article  CAS  Google Scholar 

  57. Ko M, An J, Pastor WA, Koralov SB, Rajewsky K, Rao A (2015) TET proteins and 5-methylcytosine oxidation in hematological cancers. Immunol Rev 263:6–21. https://doi.org/10.1111/imr.12239

    Article  CAS  Google Scholar 

  58. Guo JU, Su Y, Zhong C, Ming GL, Song H (2011) Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145:423–434. https://doi.org/10.1016/j.cell.2011.03.022

    Article  CAS  Google Scholar 

  59. Alaghband Y, Bredy TW, Wood MA (2016) The role of active DNA demethylation and Tet enzyme function in memory formation and cocaine action. Neurosci Lett 625:40–46. https://doi.org/10.1016/j.neulet.2016.01.023

    Article  CAS  Google Scholar 

  60. Dick A, Chen A (2021) The role of TET proteins in stress-induced neuroepigenetic and behavioural adaptations. Neurobiol Stress 15:100352. https://doi.org/10.1016/j.ynstr.2021.100352

    Article  CAS  Google Scholar 

  61. Szwagierczak A, Bultmann S, Schmidt CS, Spada F, Leonhardt H (2010) Sensitive enzymatic quantification of 5-hydroxymethylcytosine in genomic DNA. Nucleic Acids Res 38:e181. https://doi.org/10.1093/nar/gkq684

    Article  CAS  Google Scholar 

  62. Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi L et al (2011) The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477:606–610. https://doi.org/10.1038/nature10443

    Article  CAS  Google Scholar 

  63. Hedelin H, Edin-Liljegren A, Grenabo L, Hugosson J, Larsson P, Pettersson S (1990) E. coli and urease-induced crystallisation in urine. Scand J Urol Nephrol 24:57–61. https://doi.org/10.3109/00365599009180361

    Article  CAS  Google Scholar 

  64. Dawlaty MM, Breiling A, Le T, Raddatz G, Barrasa MI, Cheng AW, Gao Q, Powell BE et al (2013) Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev Cell 24:310–323. https://doi.org/10.1016/j.devcel.2012.12.015

    Article  CAS  Google Scholar 

  65. Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, Laiho A, Tahiliani M et al (2011) Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 8:200–213. https://doi.org/10.1016/j.stem.2011.01.008

    Article  CAS  Google Scholar 

  66. Cimmino L, Abdel-Wahab O, Levine RL, Aifantis I (2011) TET family proteins and their role in stem cell differentiation and transformation. Cell Stem Cell 9:193–204. https://doi.org/10.1016/j.stem.2011.08.007

    Article  CAS  Google Scholar 

  67. Quivoron C, Couronne L, Della Valle V, Lopez CK, Plo I, Wagner-Ballon O, Do Cruzeiro M, Delhommeau F et al (2011) TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 20:25–38. https://doi.org/10.1016/j.ccr.2011.06.003

    Article  CAS  Google Scholar 

  68. Li Z, Cai X, Cai CL, Wang J, Zhang W, Petersen BE, Yang FC, Xu M (2011) Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood 118:4509–4518. https://doi.org/10.1182/blood-2010-12-325241

    Article  CAS  Google Scholar 

  69. Dawlaty MM, Ganz K, Powell BE, Hu YC, Markoulaki S, Cheng AW, Gao Q, Kim J et al (2011) Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 9:166–175. https://doi.org/10.1016/j.stem.2011.07.010

    Article  CAS  Google Scholar 

  70. Li T, Yang D, Li J, Tang Y, Yang J, Le W (2015) Critical role of Tet3 in neural progenitor cell maintenance and terminal differentiation. Mol Neurobiol 51:142–154. https://doi.org/10.1007/s12035-014-8734-5

    Article  CAS  Google Scholar 

  71. Yamaguchi S, Shen L, Liu Y, Sendler D, Zhang Y (2013) Role of Tet1 in erasure of genomic imprinting. Nature 504:460–464. https://doi.org/10.1038/nature12805

    Article  CAS  Google Scholar 

  72. Zhang RR, Cui QY, Murai K, Lim YC, Smith ZD, Jin S, Ye P, Rosa L et al (2013) Tet1 regulates adult hippocampal neurogenesis and cognition. Cell Stem Cell 13:237–245. https://doi.org/10.1016/j.stem.2013.05.006

    Article  CAS  Google Scholar 

  73. Rudenko A, Dawlaty MM, Seo J, Cheng AW, Meng J, Le T, Faull KF, Jaenisch R et al (2013) Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron 79:1109–1122. https://doi.org/10.1016/j.neuron.2013.08.003

    Article  CAS  Google Scholar 

  74. Kumar D, Aggarwal M, Kaas GA, Lewis J, Wang J, Ross DL, Zhong C, Kennedy A et al (2015) Tet1 oxidase regulates neuronal gene transcription, active DNA hydroxy-methylation, object location memory, and threat recognition memory. Neuroepigenetics 4:12–27. https://doi.org/10.1016/j.nepig.2015.10.002

    Article  Google Scholar 

  75. Moran-Crusio K, Reavie L, Shih A, Abdel-Wahab O, Ndiaye-Lobry D, Lobry C, Figueroa ME, Vasanthakumar A et al (2011) Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell 20:11–24. https://doi.org/10.1016/j.ccr.2011.06.001

    Article  CAS  Google Scholar 

  76. Gontier G, Iyer M, Shea JM, Bieri G, Wheatley EG, Ramalho-Santos M, Villeda SA (2018) Tet2 rescues age-related regenerative decline and enhances cognitive function in the adult mouse brain. Cell Rep 22:1974–1981. https://doi.org/10.1016/j.celrep.2018.02.001

    Article  CAS  Google Scholar 

  77. Cheng Y, Sun M, Chen L, Li Y, Lin L, Yao B, Li Z, Wang Z et al (2018) Ten-eleven translocation proteins modulate the response to environmental stress in mice. Cell Rep 25(3194–3203):e3194. https://doi.org/10.1016/j.celrep.2018.11.061

    Article  CAS  Google Scholar 

  78. Zhang Q, Hu Q, Wang J, Miao Z, Li Z, Zhao Y, Wan B, Allen EG et al (2021) Stress modulates Ahi1-dependent nuclear localization of ten-eleven translocation protein 2. Hum Mol Genet 30:2149–2160. https://doi.org/10.1093/hmg/ddab179

    Article  CAS  Google Scholar 

  79. Wang L, Li MY, Qu C, Miao WY, Yin Q, Liao J, Cao HT, Huang M et al (2017) CRISPR-Cas9-mediated genome editing in one blastomere of two-cell embryos reveals a novel Tet3 function in regulating neocortical development. Cell Res 27:815–829. https://doi.org/10.1038/cr.2017.58

    Article  CAS  Google Scholar 

  80. Antunes C, Da Silva JD, Guerra-Gomes S, Alves ND, Ferreira F, Loureiro-Campos E, Branco MR, Sousa N, et al. (2020) Tet3 ablation in adult brain neurons increases anxiety-like behavior and regulates cognitive function in mice. Mol Psychiatry https://doi.org/10.1038/s41380-020-0695-7

  81. Kaas GA, Zhong C, Eason DE, Ross DL, Vachhani RV, Ming GL, King JR, Song H et al (2013) TET1 controls CNS 5-methylcytosine hydroxylation, active DNA demethylation, gene transcription, and memory formation. Neuron 79:1086–1093. https://doi.org/10.1016/j.neuron.2013.08.032

    Article  CAS  Google Scholar 

  82. Li X, Wei W, Zhao QY, Widagdo J, Baker-Andresen D, Flavell CR, D’Alessio A, Zhang Y et al (2014) Neocortical Tet3-mediated accumulation of 5-hydroxymethylcytosine promotes rapid behavioral adaptation. Proc Natl Acad Sci U S A 111:7120–7125. https://doi.org/10.1073/pnas.1318906111

    Article  CAS  Google Scholar 

  83. Mi Y, Gao X, Dai J, Ma Y, Xu L, Jin W (2015) A novel function of TET2 in CNS: sustaining neuronal survival. Int J Mol Sci 16:21846–21857. https://doi.org/10.3390/ijms160921846

    Article  CAS  Google Scholar 

  84. Jankowska AM, Szpurka H, Tiu RV, Makishima H, Afable M, Huh J, O’Keefe CL, Ganetzky R et al (2009) Loss of heterozygosity 4q24 and TET2 mutations associated with myelodysplastic/myeloproliferative neoplasms. Blood 113:6403–6410. https://doi.org/10.1182/blood-2009-02-205690

    Article  CAS  Google Scholar 

  85. Langemeijer SM, Kuiper RP, Berends M, Knops R, Aslanyan MG, Massop M, Stevens-Linders E, van Hoogen P et al (2009) Acquired mutations in TET2 are common in myelodysplastic syndromes. Nat Genet 41:838–842. https://doi.org/10.1038/ng.391

    Article  CAS  Google Scholar 

  86. Metzeler KH, Maharry K, Radmacher MD, Mrozek K, Margeson D, Becker H, Curfman J, Holland KB et al (2011) TET2 mutations improve the new European LeukemiaNet risk classification of acute myeloid leukemia: a Cancer and Leukemia Group B study. J Clin Oncol 29:1373–1381. https://doi.org/10.1200/JCO.2010.32.7742

    Article  Google Scholar 

  87. Abdel-Wahab O, Manshouri T, Patel J, Harris K, Yao J, Hedvat C, Heguy A, Bueso-Ramos C et al (2010) Genetic analysis of transforming events that convert chronic myeloproliferative neoplasms to leukemias. Cancer Res 70:447–452. https://doi.org/10.1158/0008-5472.CAN-09-3783

    Article  CAS  Google Scholar 

  88. Delhommeau F, Dupont S, Della Valle V, James C, Trannoy S, Masse A, Kosmider O, Le Couedic JP et al (2009) Mutation in TET2 in myeloid cancers. N Engl J Med 360:2289–2301. https://doi.org/10.1056/NEJMoa0810069

    Article  Google Scholar 

  89. Burgess DJ (2015) Human genetics: somatic mutations linked to future disease risk. Nat Rev Genet 16:69. https://doi.org/10.1038/nrg3889

    Article  CAS  Google Scholar 

  90. Hammen C (2005) Stress and depression. Annu Rev Clin Psychol 1:293–319. https://doi.org/10.1146/annurev.clinpsy.1.102803.143938

    Article  Google Scholar 

  91. Hattori N, Nishino K, Ko YG, Hattori N, Ohgane J, Tanaka S, Shiota K (2004) Epigenetic control of mouse Oct-4 gene expression in embryonic stem cells and trophoblast stem cells. J Biol Chem 279:17063–17069. https://doi.org/10.1074/jbc.M309002200

    Article  CAS  Google Scholar 

  92. Imamura M, Miura K, Iwabuchi K, Ichisaka T, Nakagawa M, Lee J, Kanatsu-Shinohara M, Shinohara T et al (2006) Transcriptional repression and DNA hypermethylation of a small set of ES cell marker genes in male germline stem cells. BMC Dev Biol 6:34. https://doi.org/10.1186/1471-213X-6-34

    Article  CAS  Google Scholar 

  93. Farthing CR, Ficz G, Ng RK, Chan CF, Andrews S, Dean W, Hemberger M, Reik W (2008) Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes. PLoS Genet 4:e1000116. https://doi.org/10.1371/journal.pgen.1000116

    Article  CAS  Google Scholar 

  94. Yu H, Su Y, Shin J, Zhong C, Guo JU, Weng YL, Gao F, Geschwind DH et al (2015) Tet3 regulates synaptic transmission and homeostatic plasticity via DNA oxidation and repair. Nat Neurosci 18:836–843. https://doi.org/10.1038/nn.4008

    Article  CAS  Google Scholar 

  95. Beck DB, Petracovici A, He C, Moore HW, Louie RJ, Ansar M, Douzgou S, Sithambaram S et al (2020) Delineation of a human Mendelian disorder of the DNA demethylation machinery: TET3 deficiency. Am J Hum Genet 106:234–245. https://doi.org/10.1016/j.ajhg.2019.12.007

    Article  CAS  Google Scholar 

  96. Aristizabal MJ, Anreiter I, Halldorsdottir T, Odgers CL, McDade TW, Goldenberg A, Mostafavi S, Kobor MS et al (2020) Biological embedding of experience: a primer on epigenetics. Proc Natl Acad Sci U S A 117:23261–23269. https://doi.org/10.1073/pnas.1820838116

    Article  CAS  Google Scholar 

  97. Dong E, Tueting P, Matrisciano F, Grayson DR, Guidotti A (2016) Behavioral and molecular neuroepigenetic alterations in prenatally stressed mice: relevance for the study of chromatin remodeling properties of antipsychotic drugs. Transl Psychiatry 6:e711. https://doi.org/10.1038/tp.2015.191

    Article  CAS  Google Scholar 

  98. Kremer EA, Gaur N, Lee MA, Engmann O, Bohacek J, Mansuy IM (2018) Interplay between TETs and microRNAs in the adult brain for memory formation. Sci Rep 8:1678. https://doi.org/10.1038/s41598-018-19806-z

    Article  CAS  Google Scholar 

  99. Feng J, Pena CJ, Purushothaman I, Engmann O, Walker D, Brown AN, Issler O, Doyle M et al (2017) Tet1 in nucleus accumbens opposes depression- and anxiety-like behaviors. Neuropsychopharmacol 42:1657–1669. https://doi.org/10.1038/npp.2017.6

    Article  CAS  Google Scholar 

  100. Matrisciano F, Pinna G (2021) PPAR-alpha hypermethylation in the hippocampus of mice exposed to social isolation stress is associated with enhanced neuroinflammation and aggressive behavior. Int J Mol Sci 22:https://doi.org/10.3390/ijms221910678

  101. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y et al (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Sci 333:1303–1307. https://doi.org/10.1126/science.1210944

    Article  CAS  Google Scholar 

  102. Dirven BCJ, Homberg JR, Kozicz T, Henckens M (2017) Epigenetic programming of the neuroendocrine stress response by adult life stress. J Mol Endocrinol 59:R11–R31. https://doi.org/10.1530/JME-17-0019

    Article  CAS  Google Scholar 

  103. Thomassin H, Flavin M, Espinas ML, Grange T (2001) Glucocorticoid-induced DNA demethylation and gene memory during development. EMBO J 20:1974–1983. https://doi.org/10.1093/emboj/20.8.1974

    Article  CAS  Google Scholar 

  104. Lee RS, Tamashiro KL, Yang X, Purcell RH, Harvey A, Willour VL, Huo Y, Rongione M et al (2010) Chronic corticosterone exposure increases expression and decreases deoxyribonucleic acid methylation of Fkbp5 in mice. Endocrinol 151:4332–4343. https://doi.org/10.1210/en.2010-0225

    Article  CAS  Google Scholar 

  105. Holoch D, Moazed D (2015) RNA-mediated epigenetic regulation of gene expression. Nat Rev Genet 16:71–84. https://doi.org/10.1038/nrg3863

    Article  CAS  Google Scholar 

  106. Trixl L, Lusser A (2019) The dynamic RNA modification 5-methylcytosine and its emerging role as an epitranscriptomic mark. Wiley Interdiscip Rev RNA 10:e1510. https://doi.org/10.1002/wrna.1510

    Article  CAS  Google Scholar 

  107. Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, Parker BJ, Suter CM, Preiss T (2012) Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res 40:5023–5033. https://doi.org/10.1093/nar/gks144

    Article  CAS  Google Scholar 

  108. Fu L, Guerrero CR, Zhong N, Amato NJ, Liu Y, Liu S, Cai Q, Ji D et al (2014) Tet-mediated formation of 5-hydroxymethylcytosine in RNA. J Am Chem Soc 136:11582–11585. https://doi.org/10.1021/ja505305z

    Article  CAS  Google Scholar 

  109. He C, Sidoli S, Warneford-Thomson R, Tatomer DC, Wilusz JE, Garcia BA, Bonasio R (2016) High-resolution mapping of RNA-binding regions in the nuclear proteome of embryonic stem cells. Mol Cell 64:416–430. https://doi.org/10.1016/j.molcel.2016.09.034

    Article  CAS  Google Scholar 

  110. Shen Q, Zhang Q, Shi Y, Shi Q, Jiang Y, Gu Y, Li Z, Li X et al (2018) Tet2 promotes pathogen infection-induced myelopoiesis through mRNA oxidation. Nature 554:123–127. https://doi.org/10.1038/nature25434

    Article  CAS  Google Scholar 

  111. Lan J, Rajan N, Bizet M, Penning A, Singh NK, Guallar D, Calonne E, Li Greci A et al (2020) Functional role of Tet-mediated RNA hydroxymethylcytosine in mouse ES cells and during differentiation. Nat Commun 11:4956. https://doi.org/10.1038/s41467-020-18729-6

    Article  CAS  Google Scholar 

  112. Sun Z, Xu X, He J, Murray A, Sun MA, Wei X, Wang X, McCoig E et al (2019) EGR1 recruits TET1 to shape the brain methylome during development and upon neuronal activity. Nat Commun 10:3892. https://doi.org/10.1038/s41467-019-11905-3

    Article  CAS  Google Scholar 

  113. Blaschke K, Ebata KT, Karimi MM, Zepeda-Martinez JA, Goyal P, Mahapatra S, Tam A, Laird DJ et al (2013) Vitamin C induces Tet-dependent DNA demethylation and a blastocyst-like state in ES cells. Nature 500:222–226. https://doi.org/10.1038/nature12362

    Article  CAS  Google Scholar 

  114. Li D, Xu W, Wu Q, Zheng H, Li Y (2021) Ascorbic acid intake is inversely associated with prevalence of depressive symptoms in US midlife women: a cross-sectional study. J Affect Disord 299:498–503. https://doi.org/10.1016/j.jad.2021.12.049

    Article  CAS  Google Scholar 

  115. Wang A, Luo J, Zhang T, Zhang D (2021) Dietary vitamin C and vitamin C derived from vegetables are inversely associated with the risk of depressive symptoms among the general population. Antioxidants (Basel) 10:https://doi.org/10.3390/antiox10121984

  116. Wang Y, Zhang Y (2014) Regulation of TET protein stability by calpains. Cell Rep 6:278–284. https://doi.org/10.1016/j.celrep.2013.12.031

    Article  CAS  Google Scholar 

  117. Song Z, Shen F, Zhang Z, Wu S, Zhu G (2020) Calpain inhibition ameliorates depression-like behaviors by reducing inflammation and promoting synaptic protein expression in the hippocampus. Neuropharmacol 174:108175. https://doi.org/10.1016/j.neuropharm.2020.108175

    Article  CAS  Google Scholar 

  118. Hanover JA, Krause MW, Love DC (2012) Bittersweet memories: linking metabolism to epigenetics through O-GlcNAcylation. Nat Rev Mol Cell Biol 13:312–321. https://doi.org/10.1038/nrm3334

    Article  CAS  Google Scholar 

  119. Moore M, Avula N, Jo S, Beetch M, Alejandro EU (2021) Disruption of O-linked N-acetylglucosamine signaling in placenta induces insulin sensitivity in female offspring. Int J Mol Sci 22:https://doi.org/10.3390/ijms22136918

  120. Vella P, Scelfo A, Jammula S, Chiacchiera F, Williams K, Cuomo A, Roberto A, Christensen J et al (2013) Tet proteins connect the O-linked N-acetylglucosamine transferase Ogt to chromatin in embryonic stem cells. Mol Cell 49:645–656. https://doi.org/10.1016/j.molcel.2012.12.019

    Article  CAS  Google Scholar 

  121. Chen Q, Chen Y, Bian C, Fujiki R, Yu X (2013) TET2 promotes histone O-GlcNAcylation during gene transcription. Nature 493:561–564. https://doi.org/10.1038/nature11742

    Article  CAS  Google Scholar 

  122. Deplus R, Delatte B, Schwinn MK, Defrance M, Mendez J, Murphy N, Dawson MA, Volkmar M et al (2013) TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J 32:645–655. https://doi.org/10.1038/emboj.2012.357

    Article  CAS  Google Scholar 

  123. Zhang Q, Liu X, Gao W, Li P, Hou J, Li J, Wong J (2014) Differential regulation of the ten-eleven translocation (TET) family of dioxygenases by O-linked beta-N-acetylglucosamine transferase (OGT). J Biol Chem 289:5986–5996. https://doi.org/10.1074/jbc.M113.524140

    Article  CAS  Google Scholar 

  124. Brown AS, Derkits EJ (2010) Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry 167:261–280. https://doi.org/10.1176/appi.ajp.2009.09030361

    Article  Google Scholar 

  125. Brown AS (2012) Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev Neurobiol 72:1272–1276. https://doi.org/10.1002/dneu.22024

    Article  Google Scholar 

  126. Matrisciano F, Tueting P, Dalal I, Kadriu B, Grayson DR, Davis JM, Nicoletti F, Guidotti A (2013) Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice. Neuropharmacol 68:184–194. https://doi.org/10.1016/j.neuropharm.2012.04.013

    Article  CAS  Google Scholar 

  127. Dong E, Dzitoyeva SG, Matrisciano F, Tueting P, Grayson DR, Guidotti A (2015) Brain-derived neurotrophic factor epigenetic modifications associated with schizophrenia-like phenotype induced by prenatal stress in mice. Biol Psychiatry 77:589–596. https://doi.org/10.1016/j.biopsych.2014.08.012

    Article  CAS  Google Scholar 

  128. Mill J, Petronis A (2009) Profiling DNA methylation from small amounts of genomic DNA starting material: efficient sodium bisulfite conversion and subsequent whole-genome amplification. Methods Mol Biol 507:371–381. https://doi.org/10.1007/978-1-59745-522-0_27

    Article  CAS  Google Scholar 

  129. Arion D, Unger T, Lewis DA, Levitt P, Mirnics K (2007) Molecular evidence for increased expression of genes related to immune and chaperone function in the prefrontal cortex in schizophrenia. Biol Psychiatry 62:711–721. https://doi.org/10.1016/j.biopsych.2006.12.021

    Article  CAS  Google Scholar 

  130. Jiang T, Zong L, Zhou L, Hou Y, Zhang L, Zheng X, Han H, Li S et al (2017) Variation in global DNA hydroxymethylation with age associated with schizophrenia. Psychiatry Res 257:497–500. https://doi.org/10.1016/j.psychres.2017.08.022

    Article  CAS  Google Scholar 

  131. Bin W, Zhigang M, Bo W, Xingshun X (2021) Prevention for post-traumatic stress disorder after the COVID-19 epidemic: lessons from the SARS epidemic. Stress Brain 1:1–10. https://doi.org/10.26599/SAB.2020.9060007

    Article  Google Scholar 

  132. Orsini CA, Maren S (2012) Neural and cellular mechanisms of fear and extinction memory formation. Neurosci Biobehav Rev 36:1773–1802. https://doi.org/10.1016/j.neubiorev.2011.12.014

    Article  Google Scholar 

  133. Davis M (1986) Pharmacological and anatomical analysis of fear conditioning using the fear-potentiated startle paradigm. Behav Neurosci 100:814–824. https://doi.org/10.1037//0735-7044.100.6.814

    Article  CAS  Google Scholar 

  134. Sawamura T, Klengel T, Armario A, Jovanovic T, Norrholm SD, Ressler KJ, Andero R (2016) Dexamethasone treatment leads to enhanced fear extinction and dynamic Fkbp5 regulation in amygdala. Neuropsychopharmacol 41:832–846. https://doi.org/10.1038/npp.2015.210

    Article  CAS  Google Scholar 

  135. Gilbertson MW, Shenton ME, Ciszewski A, Kasai K, Lasko NB, Orr SP, Pitman RK (2002) Smaller hippocampal volume predicts pathologic vulnerability to psychological trauma. Nat Neurosci 5:1242–1247. https://doi.org/10.1038/nn958

    Article  CAS  Google Scholar 

  136. Maletic V, Robinson M, Oakes T, Iyengar S, Ball SG, Russell J (2007) Neurobiology of depression: an integrated view of key findings. Int J Clin Pract 61:2030–2040. https://doi.org/10.1111/j.1742-1241.2007.01602.x

    Article  CAS  Google Scholar 

  137. Mengxin M, Xin C, Haitao W (2021) Animal models of stress and stress-related neurocircuits: a comprehensive review. Stress and Brain 1:108–127. https://doi.org/10.26599/SAB.2021.9060001

    Article  Google Scholar 

  138. Wang Q, Timberlake MA 2nd, Prall K, Dwivedi Y (2017) The recent progress in animal models of depression. Prog Neuropsychopharmacol Biol Psychiatry 77:99–109. https://doi.org/10.1016/j.pnpbp.2017.04.008

    Article  Google Scholar 

  139. Reszka E, Jablonska E, Lesicka M, Wieczorek E, Kapelski P, Szczepankiewicz A, Pawlak J, Dmitrzak-Weglarz M (2021) An altered global DNA methylation status in women with depression. J Psychiatr Res 137:283–289. https://doi.org/10.1016/j.jpsychires.2021.03.003

    Article  Google Scholar 

  140. Zhang HG, Wang B, Yang Y, Liu X, Wang J, Xin N, Li S, Miao Y et al (2022) Depression compromises antiviral innate immunity via the AVP-AHI1-Tyk2 axis. Cell Res 32:897–913. https://doi.org/10.1038/s41422-022-00689-9

    Article  CAS  Google Scholar 

  141. Wei X, Yu L, Zhang Y, Li X, Wu H, Jiang J, Qing Y, Miao Z et al (2021) The role of Tet2-mediated hydroxymethylation in poststroke depression. Neurosci 461:118–129. https://doi.org/10.1016/j.neuroscience.2021.02.033

    Article  CAS  Google Scholar 

  142. Tsankova N, Renthal W, Kumar A, Nestler EJ (2007) Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci 8:355–367. https://doi.org/10.1038/nrn2132

    Article  CAS  Google Scholar 

  143. Benes FM, Lim B, Matzilevich D, Walsh JP, Subburaju S, Minns M (2007) Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc Natl Acad Sci U S A 104:10164–10169. https://doi.org/10.1073/pnas.0703806104

    Article  CAS  Google Scholar 

  144. Mill J, Tang T, Kaminsky Z, Khare T, Yazdanpanah S, Bouchard L, Jia P, Assadzadeh A et al (2008) Epigenomic profiling reveals DNA-methylation changes associated with major psychosis. Am J Hum Genet 82:696–711. https://doi.org/10.1016/j.ajhg.2008.01.008

    Article  CAS  Google Scholar 

  145. Benes FM, Berretta S (2001) GABAergic interneurons: implications for understanding schizophrenia and bipolar disorder. Neuropsychopharmacol 25:1–27. https://doi.org/10.1016/S0893-133X(01)00225-1

    Article  CAS  Google Scholar 

  146. Couve A, Restituito S, Brandon JM, Charles KJ, Bawagan H, Freeman KB, Pangalos MN, Calver AR et al (2004) Marlin-1, a novel RNA-binding protein associates with GABA receptors. J Biol Chem 279:13934–13943. https://doi.org/10.1074/jbc.M311737200

    Article  CAS  Google Scholar 

  147. Coyle JT (2004) The GABA-glutamate connection in schizophrenia: which is the proximate cause? Biochem Pharmacol 68:1507–1514. https://doi.org/10.1016/j.bcp.2004.07.034

    Article  CAS  Google Scholar 

  148. Xing G, Zhang L, Russell S, Post R (2006) Reduction of dopamine-related transcription factors Nurr1 and NGFI-B in the prefrontal cortex in schizophrenia and bipolar disorders. Schizophr Res 84:36–56. https://doi.org/10.1016/j.schres.2005.11.006

    Article  Google Scholar 

  149. Van den Bergh BRH, van den Heuvel MI, Lahti M, Braeken M, de Rooij SR, Entringer S, Hoyer D, Roseboom T, Raikkonen K, King S et al (2017) Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neurosci Biobehav Rev https://doi.org/10.1016/j.neubiorev.2017.07.003

  150. Walsh K, McCormack CA, Webster R, Pinto A, Lee S, Feng T, Krakovsky HS, O’Grady SM et al (2019) Maternal prenatal stress phenotypes associate with fetal neurodevelopment and birth outcomes. Proc Natl Acad Sci U S A 116:23996–24005. https://doi.org/10.1073/pnas.1905890116

    Article  CAS  Google Scholar 

  151. Gillott A, Standen PJ (2007) Levels of anxiety and sources of stress in adults with autism. J Intellect Disabil 11:359–370. https://doi.org/10.1177/1744629507083585

    Article  Google Scholar 

  152. Rice F, Jones I, Thapar A (2007) The impact of gestational stress and prenatal growth on emotional problems in offspring: a review. Acta Psychiatr Scand 115:171–183. https://doi.org/10.1111/j.1600-0447.2006.00895.x

    Article  CAS  Google Scholar 

  153. Weinstock M (2001) Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol 65:427–451. https://doi.org/10.1016/s0301-0082(01)00018-1

    Article  CAS  Google Scholar 

  154. Scheinost D, Spann MN, McDonough L, Peterson BS, Monk C (2020) Associations between different dimensions of prenatal distress, neonatal hippocampal connectivity, and infant memory. Neuropsychopharmacol 45:1272–1279. https://doi.org/10.1038/s41386-020-0677-0

    Article  Google Scholar 

  155. Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S, Grace AA (2008) Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 31:234–242. https://doi.org/10.1016/j.tins.2008.02.005

    Article  CAS  Google Scholar 

  156. Massart R, Suderman M, Provencal N, Yi C, Bennett AJ, Suomi S, Szyf M (2014) Hydroxymethylation and DNA methylation profiles in the prefrontal cortex of the non-human primate rhesus macaque and the impact of maternal deprivation on hydroxymethylation. Neurosci 268:139–148. https://doi.org/10.1016/j.neuroscience.2014.03.021

    Article  CAS  Google Scholar 

  157. Goud Alladi C, Etain B, Bellivier F, Marie-Claire C (2018) DNA methylation as a biomarker of treatment response variability in serious mental illnesses: a systematic review focused on bipolar disorder, schizophrenia, and major depressive disorder. Int J Mol Sci 19:https://doi.org/10.3390/ijms19103026

Download references

Funding

This work was supported by Postgraduate Research & Practice Innovation Program of Jiangsu Province (KYCX21a_2974) and Chinese Scholarship Council.

Author information

Authors and Affiliations

  1. Departments of Neurology, the Second Affiliated Hospital of Soochow University, Suzhou City, 215006, China

    Meiling Xia & Xingshun Xu

  2. Department of Physiology and Biomedical Sciences, Seoul National University College of Medicine, Seoul City, 03080, Korea

    Meiling Xia & Myoung-Hwan Kim

  3. Institute of Neuroscience, Soochow University, Suzhou City, China

    Rui Yan & Xingshun Xu

  4. Jiangsu Key Laboratory of Neuropsychiatric Diseases, Soochow University, Suzhou City, China

    Xingshun Xu

Authors
  1. Meiling Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rui Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Myoung-Hwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xingshun Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

XM and YR wrote this review. XX and KMH revised the paper. All authors read and approved the final manuscript. All authors contributed to the article and approved the submitted version.

Corresponding authors

Correspondence to Myoung-Hwan Kim or Xingshun Xu.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent to Publish

Yes.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xia, M., Yan, R., Kim, MH. et al. Tet Enzyme-Mediated Response in Environmental Stress and Stress-Related Psychiatric Diseases. Mol Neurobiol 60, 1594–1608 (2023). https://doi.org/10.1007/s12035-022-03168-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-022-03168-9

Keywords

Search

Navigation