Epigenetic contributions on mental health, neurodevelopmental and neurodegenerative disorders

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Review Paper 01/01/2019
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Epigenetic contributions on mental health, neurodevelopmental and neurodegenerative disorders

Roushney Fatima Mukti, Shuborno Islam
Int. J. Biosci.14( 1), 38-52, January 2019.
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The significance of epigenetics for mental health and neurodevelopment to assess the contribution of gene–environment interactions to brain function is becoming increasingly clear. Epigenetic programming functions in respect to the interaction between genetics and the environment. It has the capability to make us thinking about the infraction of the prior assumption of independence between genotype and the environment. Some environmental factors such as diet, maternal behavior, psychosocial or chemical exposures have been shown to alter the progression of epigenetic programming in a significant way during the early development. Since epigenetically modified genes can be reclaimed, methylation silenced genes can be demethylated and histone complexes can be executed transcriptionally active by modification of acetylation and methylation of various histones through drugs and/or other dietary interventions, the rapidly growing field of epigenetics provides a perfect opportunity to design rationale therapeutic strategies. The widespread impact of epigenetic modifications suggests that understanding the underlying mechanisms of epigenetic contributions on mental health as well as neurodevelopmental and neurodegenerative disorders holds a great promise for us to be a rich source of more rationale and even personalized therapeutic interventions to treat these disorders in the near future. In this review, we discussed an emerging idea that epigenetic regulation may provide a mechanism by which environmental events can be encoded at the molecular level where they are recognized to influence brain function and also the future prospects of epigenetic therapies to decrease the burden of diseases by modulating epigenetic mechanisms in various ways.


Alarcon JM, Malleret G, Touzani K, Vronskaya S, Ishii S, Kandel ER, Barco A. 2004. Chromatin acetylation, memory, and LTP are impaired in CBP+/− mice: a model for the cognitive deficit in Rubinstein–Taybi syndrome and its amelioration. Neuron 42, 947–959. https://doi.org/10.1016/j.neuron.2004.05.021

Alexander Link, Francesc Balaguer, Ajay Goel. 2010. Cancer Chemoprevention by Dietary Polyphenols: Promising Role for Epigenetics. Biochemical Pharmacology. December 15, 80(12), 1771–1792. https://doi.org/10.1016/j.bcp.2010.06.036.

Anderson AN, Roncaroli F, Hodges A, Deprez M, Turkheimer FE. 2008. Chromosomal profiles of gene expression in Huntington’s disease. Brain. 131(2), 381–388. https://doi.org/10.1093/brain/awm312.

Basan A, Leucht S. 2004. Valproate for schizophrenia. Cochrane Database of Systematic Reviews (1), CD004028. https://doi.org/10.1002/14651858.CD004028.pub2.

Bekdash RA. 2018 Jan. Choline, the brain and neurodegeneration: insights from epigenetics. Frontiers in Bioscience, Landmark 23, 1113-1143, January 1, 2018. https://doi.org/10.2741/4636.

Bilang-Bleuel A, Ulbricht S, Chandramohan Y, De Carli S, Droste SK, Reul JM. 2005. Psychological stress increases histone H3 phosphorylation in adult dentate gyrus granule neurons: involvement in a glucocorticoid receptor-dependent behavioral response. European Journal of Neuroscience. 22(7), 1691–1700. https://doi.org/10.1111/j.1460-9568.2005.04358.x.

Bittel DC, Butler MG. 2005. Prader-Willi syndrome: clinical genetics, cytogenetics and molecular biology. Expert Reviews in Molecular Medicine 7(14), 1–20. https://doi.org/10.1017/S1462399405009531.

Blewitt ME, Vickaryous NK, Paldi A, Koseki H, Whitelaw E. 2006. Dynamic reprogramming of DNA methylation at an epigenetically sensitive allele in mice. PLOS Genetics. Apr; 2(4), e49. https://doi.org/10.1371/journal.pgen.0020049.

Boissonneault V, Plante I, Rivest S, Provost P. 2009. MicroRNA-298 and microRNA-328 regulate expression of mouse beta-amyloid precursor protein-converting enzyme 1. Journal of Biological Chemistry. 284(4), 1971–1981. https://doi.org/10.1074/jbc.M807530200.

Bowden CL. 2007. Spectrum of effectiveness of valproate in neuropsychiatry. Expert Review of Neurotherapeutics 7(1), 9–16. https://doi.org/10.1586/14737175.7.1.9.

Bull C, Fenech M. 2008. Genome-health nutrigenomics and nutrigenetics: nutritional requirements or ‘nutriomes’ for chromosomal stability and telomere maintenance at the individual level. Proceedings of the Nutrition Society 67(2), 146–156. https://doi.org/10.1017/S0029665108006988.

Cang S, Ma Y, Liu D. 2009. New clinical developments in histone deacetylase inhibitors for epigenetic therapy of cancer. Journal of Hematology & Oncology 2, 22. https://doi.org/10.1186/1756-8722-2-22.

Cassidy SB, Driscoll DJ. 2009. Prader-Willi syndrome. European Journal of Human Genetics 17, 3–13. https://doi.org/10.1038/ejhg.2008.165.

Chandra V, Pandav R, Dodge HH, Johnston JM, Belle SH, DeKosky ST, Ganguli M. 2001. Incidence of Alzheimer’s disease in a rural community in India: The Indo-US study. American Academy of Neurology. 57(6), 985–989. https://doi.org/10.1212/WNL.57.6.985.

Chandramohan Y, Droste SK, Arthur JS, Reul JM. 2008. The forced swimming-induced behavioural immobility response involves histone H3 phospho-acetylation and c-Fos induction in dentate gyrus granule neurons via activation of the N-methyl-D-aspartate/extracellular signal-regulated kinase/mitogen- and stress-activated kinase signaling pathway. European Journal of Neuroscience. 27(10), 2701–2713. https://doi.org/10.1111/j.1460-9568.2008.06230.x.

Chandramohan Y, Droste SK, Reul JM. 2007. Novelty stress induces phospho-acetylation of histone H3 in rat dentate gyrus granule neurons through coincident signaling via the N-methyl-D-aspartate receptor and the glucocorticoid receptor: relevance for c-fos induction. Journal of Neurochemistry. 101(3), 815–828. https://doi.org/10.1111/j.1471-4159.2006.04396.x.

Chen L, Durkin KA, Casida JE. 2006. Structural model for gamma-aminobutyric acid receptor noncompetitive antagonist binding: widely diverse structures fit the same site. Proceedings of the National Academy of Sciences of the United States of America 103(13), 5185–5190. https://doi.org/10.1073/pnas.0600370103.

Cole LM, Casida JE. 1986. Polychlorocycloalkane insecticide-induced convulsions in mice in relation to disruption of the GABA-regulated chloride ionophore. Life Sciences. 39(20), 1855–1862. https://doi.org/10.1016/0024-3205(86)90295-X.

Cooney CA. 1993. Are somatic cells inherently deficient in methylation metabolism? A proposed mechanism for DNA methylation loss, senescence and aging. Growth Development & Aging. 57(4), 261–273.

Dashwood RH, Melinda C. Myzak, Emily Ho. 2006. Dietary HDAC inhibitors: time to rethink weak ligands in cancer chemoprevention. Carcinogenesis. 27(2), 344–349. https://doi.org/10.1093/carcin/bgi253.

Dashwood RH, Ho E. 2007. Dietary histone deacetylase inhibitors: from cells to mice to man. Seminars in Cancer Biology 17(5), 363–369. https://doi.org/10.1016/j.semcancer.2007.04.001.

Dong E,  Guidotti A,  Grayson DR,  Costa E. 2007. Histone hyperacetylation induces demethylation of reelin and 67-kDa glutamic acid decarboxylase promoters. Proceedings of the National Academy of Sciences of the United States of America. 104(11), 4676–4681. https://doi.org/10.1073/pnas.0700529104.

Ducasse M, Brown MA. 2006. Epigenetic aberrations and cancer. Molecular Cancer 5, 60. https://doi.org/10.1186/1476-4598-5-60.

Faghihi MA, Modarresi F, Khalil AM, Wood DE, Sahagan BG, Morgan TE. 2008. Expression of a noncoding RNA is elevated in Alzheimer’s disease and drives rapid feed-forward regulation of beta-secretase. Nature Medicine 14, 723–730. https://doi.org/10.1038/nm1784.

Robert J. Ferrante, James K. Kubilus, Junghee Lee, Hoon Ryu, Ayshe Beesen, Birgit Zucker, Karen Smith, Neil W. Kowall, Rajiv R. Ratan, Ruth Luthi-Carter, Steven M. Hersch. 2003. Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington’s disease mice. Journal of Neuroscience. 23(28), 9418–9427. https://doi.org/10.1523/JNEUROSCI.23-28-09418.2003.

Fischer A, Sananbenesi FWang XDobbin MTsai LH. 2007. Recovery of learning and memory is associated with chromatin remodelling. Nature International Journal of Science 447, 178–182. https://doi.org/10.1038/nature05772.

Francis DD, Diorio J, Liu D, Meaney MJ. 1999. Nongenomic transmission across generations in maternal behavior and stress responses in the rat. Science 286(5442), 1155–1158. https://doi.org/10.1126/science.286.5442.1155.

Friso S, Sang-Woon Choi, Domenico Girelli, Joel B. Mason, Gregory G. Dolnikowski, Pamela J. Bagley, Oliviero Olivieri, Paul F. Jacques, Irwin H. Rosenberg, Roberto Corrocher, Jacob Selhub. 2002. A common mutation in the 5, 10-methylenetetrahydrofolate reductase gene affects genomic DNA methylation through an interaction with folate status. Proceedings of the National Academy of Sciences of the United States of America. 99(8), 5606–5611. https://doi.org/10.1073/pnas.062066299.

Gardian G, Browne SE, Choi DK, Klivenyi P, Gregorio J, Kubilus JK,  Ryu HLangley BRatan RRFerrante RJBeal MF. 2005. Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington’s disease. Journal of Biological Chemistry 280, 556–563. https://doi.org/10.1074/jbc.M410210200.

Gibbons RJ,  McDowell TLRaman SO’Rourke DMGarrick DAyyub HHiggs DR. 2000. Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nature Genetics 24, 368–371. https://doi.org/10.1038/74191.

Gomez-Pinilla, Tyagi E. 2013. Diet and cognition: interplay between cell metabolism and neuronal plasticity. Current Opinion in Clinical Nutrition and Metabolic Care. Nov; 16(6), 726­-33. https://doi.org/10.1097/MCO.0b013e328365aae3.

Grayson DR, Chen Y, Costa E, Dong E, Guidotti A, Kundakovic M, Rajiv P. Sharma. 2006. The human reelin gene: transcription factors (+), repressors (–) and the methylation switch (+/–) in schizophrenia. Pharmacology & Therapeutics 111, 272–286. https://doi.org/10.1016/j.pharmthera.2005.01.007.

Guidotti A, Dong E, Kundakovic M, Satta R, Grayson DR, Costa E. 2009. Characterization of the action of antipsychotic subtypes on valproate-induced chromatin remodeling. Trends in Pharmacological Sciences 30(2), 55–60. https://doi.org/10.1016/j.tips.2008.10.010.

Hebert SS, Horre K, Nicolai L, Bergmans B, Papadopoulou AS, Delacourte A, De Strooper B. 2009.  MicroRNA regulation of Alzheimer’s amyloid precursor protein expression. Neurobiology of Disease 33(3), 422–428. https://doi.org/10.1016/j.nbd.2008.11.009.

House SH. 2013. Transgenerational healing: Educating children in genesis of healthy children, with focus on nutrition, emotion, and epigenetic effects on brain development. Nutritional and Health. Jan; 22(1), 9-45. https://doi.org/10.1177/0260106013506666.

Huang Y, Greene E, Murray Stewart T, Goodwin AC, Baylin SB, Woster PM, Casero RA Jr. 2007. Inhibition of lysine-specific demethylase 1 by polyamine analogues results in reexpression of aberrantly silenced genes. Proceedings of the National Academy of Sciences of the United States of America. 104(19), 8023–8028. https://doi.org/10.1073/pnas.0700720104.

Hunter RG, Mccarthy KJ, Milne TA, Pfaff DW, McEwen BS. 2009. Regulation of hippocampal H3 histone methylation by acute and chronic stress. Proceedings of the National Academy of Sciences of the United States of America. 106(49), 20912–209. https://doi.org/10.1073/pnas.0911143106.

Issa JP. 2007. DNA methylation as a therapeutic target in cancer. Clinical Cancer Research. 13(6), 1634–1637. https://doi.org/10.1158/1078-0432.CCR-06-2076.

Jaenisch R, Bird A. 2003. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nature Genetics. Mar; 33 Suppl:245–254. https://doi.org/10.1038/ng1089

Jameson RR, Seidler FJ, Slotkin TA. 2007. Nonenzymatic functions of acetylcholinesterase splice variants in the developmental neurotoxicity of organophosphates: chlorpyrifos, chlorpyrifos oxon, and diazinon. Environmental Health Perspectives. 115(1), 65–70. https://doi.org/10.1289/ehp.9487.

Jones PA, Taylor SM. 1980. Cellular differentiation, cytidine analogs and DNA methylation. Cell. 20, 85–93. https://doi.org/10.1016/0092-8674(80)90237-8.

Kenet T, Froemcke R, Schreiner C, Pessah IN, Merzenich MM. 2007. Perinatal exposure to a noncoplanar polychlorinated biphenyl alters tonotopy, receptive fields, and plasticity in rat primary auditory cortex. Proceedings of the National Academy of Sciences of the United States of America. 104, 7646–51. https://doi.org/10.1073/pnas.0701944104.

Kilgore M, Miller CA, Fass DM, Hennig KM, Haggarty SJ, Sweatt JD, Rumbaugh G. 2010. Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer’s disease. Neuropsychopharmacology 35, 870–880. https://doi.org/10.1038/npp.2009.197.

Kouzarides T. 2007. Chromatin modifications and their function. Cell. 128(4), 693–705. https://doi.org/10.1016/j.cell.2007.02.005.

Kovacheva VP, Mellott TJDavison JMWagner NLopez-Coviella ISchnitzler ACBlusztajn JK. 2007. Gestational choline deficiency causes global and Igf2 gene DNA hypermethylation by up-regulation of Dnmt1 expression. Journal of Biological Chemistry. 282(43), 31777–31788. https://doi.org/10.1074/jbc.M705539200.

Lalande M, Calciano MA. 2007. Molecular epigenetics of Angelman syndrome. Cellular and Molecular Life Science 64(7-8), 947–60. https://doi.org/10.1007/s00018-007-6460-0.

Lee MG, Wynder CSchmidt DMMcCafferty DGShiekhattar R. 2006. Histone H3 lysine 4 demethylation is a target of nonselective antidepressive medications. Chemistry & Biology. 13(6), 563–567. https://doi.org/10.1016/j.chembiol.2006.05.004.

Levenson JM Roth TLLubin FDMiller CAHuang ICDesai PMalone LMSweatt JD. 2006. Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. Journal of Biological Chemistry 281, 15763–15773. https://doi.org/10.1074/jbc.M511767200.

Lin HJ, Zuo T, Chao JR, Peng Z, Asamoto LK, Yamashita SS, Huang TH. 2009. Seed in soil, with an epigenetic view. Biochimica et Biophysica Acta (BBA)-General Subjects. Sep; 1790(9), 920–924. https://doi.org/10.1016/j.bbagen.2008.12.004.

Mathers JC, Strathdee G, Relton CL. 2010. Induction of epigenetic alterations by dietary and other environmental factors. Advances in Genetics. 71, 3–39. https://doi.org/10.1016/B978-0-12-380864-6.00001-8.

McGowan PO, Sasaki A, D’alessio AC, Dymov S, Labonte B, Szyf M, Turecki G, Meaney MJ. 2009. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nature Neuroscience. 12(3), 342–348. https://doi.org/10.1038/nn.2270.

Meck WH, Williams CL. 2003. Metabolic imprinting of choline by its availability during gestation: implications for memory and attentional processing across the lifespan. Neuroscience & Biobehavioral Reviews 27(4), 385–399. https://doi.org/10.1016/S0149-7634(03)00069-1.

Metzger E, Wissmann MYin NMüller JMSchneider RPeters AHGünther TBuettner RSchüle R. 2005. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature. 437(7057), 436–439. https://doi.org/10.1038/nature04020.

Murgatroyd C, Patchev AV, Wu Y, Micale V, Bockmuhl Y, Fischer D, Holsboer F, Wotjak CT, Almeida OF, Spengler D. 2009. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nature Neuroscience 12, 1559–1566. https://doi.org/10.1038/nn.2436.

Nestler EJ, Carlezon WA, Jr. 2006. The mesolimbic dopamine reward circuit in depression. Biological Psychiatry 59(12), 1151–1159. https://doi.org/10.1016/j.biopsych.2005.09.018.

Ogryzko VV, Schiltz RL, Russanova V, Howard BH, Nakatani Y. 1996. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell. 87(5), 953–959. https://doi.org/10.1016/S0092-8674(00)82001-2.

Packer AN, Xing Y, Harper SQ, Jones L, Davidson BL. 2008. The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington’s disease. Journal of Neuroscience 28(53), 14341–14346. https://doi.org/10.1523/JNEUROSCI.2390-08.2008

Patel N, Hoang D, Miller N, Ansaloni S, Huang Q, Rogers JT, Lee JCSaunders AJ. 2008. MicroRNAs can regulate human APP levels. Molecular Neurodegeneration. 3, 10. https://doi.org/10.1186/1750-1326-3-10

Patrick O. McGowan, Michael J. Meaney, Moshe Szyf. 2008. Diet and the epigenetic (re)programming of phenotypic differences in behavior. Brain Research. October 27; 1237, 12–24. https://doi.org/10.1016/j.brainres.2008.07.074

Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, Agis-Balboa RC, Cota P, Wittnam JL, Gogol-Doering A, Opitz L, Salinas-Riester G, Dettenhofer M, Kang H, Farinelli L, Chen W, Fischer A. 2010. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328(5979), 753–756. https://doi.org/10.1126/science.1186088

Peltier J, O’neill A, Schaffer DV. 2007. PI3K/Akt and CREB regulate adult neural hippocampal progenitor proliferation and differentiation. Developmental Neurobiology 67(10), 1348–1361. https://doi.org/10.1002/dneu.20506 

Perkins DOJeffries CD, Jarskog LF, Thomson JM, Woods K, New mann MA. Parker JSJin JHammond SM, MicroRNA. 2007. Expression in the prefrontal cortex of individuals withschizophrenia and schizoaffective disorder. Genome Biology 8, R27. https://doi.org/10.1186/gb-2007-8-2-r27.

Pessah INHansen LGAlbertson TEGarner CETa TADo ZKim KHWong PW. Structure-activity relationship for noncoplanar polychlorinated biphenyl congeners toward the ryanodine receptor-Ca2+ channel complex type 1 (RyR1). Chemical Research in Toxicology. 2006 January 19(1), 92-101. https://doi.org/10.1021/tx050196m.

Picketts DJ, Higgs DRBachoo SBlake DJQuarrell OWGibbons RJ. 1996. ATRX encodes a novel member of the SNF2 family of proteins: mutations point to a common mechanism underlying the ATR-X syndrome. Human Molecular Genetics 5, 1899–1907.

Pruessner JC, Champagne F, Meaney MJ, Dagher A. 2004. Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. Journal of Neuroscience 24(11), 2825–2831. https://doi.org/10.1523/JNEUROSCI.3422-03.2004

Ross SA. 2003. Diet and DNA methylation interactions in cancer prevention. Annals of the New York Academy of Sciences. Mar; 983, 197–207. https://doi.org/10.1111/j.1749-6632.2003.tb05974.x.

Roth TL, Sweatt JD. 2009. Regulation of chromatin structure in memory formation. Current Opinion in Neurobiology 19(3), 336–342. https://doi.org/10.1016/j.conb.2009.05.011

Ryu H, Lee J, Hagerty SW, Soh BY, McAlpin SE, Cormier KA, Smith KMFerrante RJ. 2006. ESET/SETDB1 gene expression and histone H3 (K9) trimethylation in Huntington’s disease. Proceedings of the National Academy of Sciences of the United States of America. 103(50), 19176–19181. https://doi.org/10.1073/pnas.0606373103.

Samaco RC, Hogart A, LaSalle JM. 2005. Epigenetic overlap in autism-spectrum neurodevelopmental disorders: MECP2 deficiency causes reduced expression of UBE3A and GABRB3. Human Molecular Genetics 14(4), 483–492. https://doi.org/10.1093/hmg/ddi045.

Schroeder FA, Lin CLCrusio WEAkbarian S. 2007. Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biological Psychiatry 62, 55–64. https://doi.org/10.1016/j.biopsych.2006.06.036.

Schuh RA, Lein PJ, Beckles RA, Jett DA. 2002. Noncholinesterase mechanisms of chlorpyrifos neurotoxicity: altered phosphorylation of Ca2+/cAMP response element binding protein in cultured neurons. Toxicology and Applied Pharmacology. 182(2), 176–185. https://doi.org/10.1006/taap.2002.9445.

Segura-Pacheco B, Trejo-Becerril C, Perez-Cardenas E, Taja-Chayeb L, Mariscal I, Chavez A, Acuña C, Salazar AM, Lizano M, Dueñas-Gonzalez A. 2003. Reactivation of tumor suppressor genes by the cardiovascular drugs hydralazine and procainamide and their potential use in cancer therapy. Clinical Cancer Research 9(5), 1596–1603.

Sethi P, Lukiw WJ. 2009. Micro-RNA abundance and stability in human brain: specific alterations in Alzheimer’s disease temporal lobe neocortex. Neuroscience Letters 459(2), 100–104. https://doi.org/10.1016/j.neulet.2009.04.052.

Sharma RP, Grayson DR, Gavin DP. 2008. Histone deactylase 1 expression is increased in the prefrontal cortex of schizophrenia subjects: analysis of the National Brain Databank microarray collection. Schizophrenia Research 98, 111–117. https://doi.org/10.1016/j.schres.2007.09.020.

Shi Y, Lan FMatson CMulligan PWhetstine JRCole PACasero RA. 2004. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell. 119(7), 941–953. https://doi.org/10.1016/j.cell.2004.12.012.

Silveri MM, Parow AMVillafuerte RADamico KEGoren JStoll ALCohen BMRenshaw PF. 2003. S-adenosyl-L-methionine: effects on brain bioenergetic status and transverse relaxation time in healthy subjects. Biological Psychiatry 54, 833–839. https://doi.org/10.1016/S0006-3223(03)00064-7.

Simonini MV, Camargo LMDong EMaloku EVeldic MCosta EGuidotti A. 2006. The benzamide MS-275 is a potent, long-lasting brain region-selective inhibitor of histone deacetylases. Proceedings of the National Academy of Sciences of the United States of America. 103(5), 1587–1592. https://doi.org/10.1073/pnas.0510341103.

Slyshenkov VS, Anton V. Liopo1, Lech Wojtczak. 2002. Protective role of L-methionine against free radical damage of rat brain synaptosomes. Acta Biochimica Polonica. 49, 907–916.

Strous RD, Ritsner MS, Adler S, Ratner Y, Maayan R, Kotler M. 2009. Improvement of aggressive behavior and quality of life impairment following S-adenosyl-methionine (SAM-e) augmentation in schizophrenia. European Neuropsychopharmacology 19(1), 14–22. https://doi.org/10.1016/j.euroneuro.2008.08.004

Talal Jamil, Qazi Zhenzhen, Quan Asif, Mir Hong Qing. 2018. Epigenetics in Alzheimer’s disease: Perspective of DNA Methylation. Molecular Neurobiology 55(2), p 1026–1044. https://doi.org/10.1007/s12035-016-0357-6.

Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, Karuturi RK, Tan PB, Liu ET, Yu Q. 2007. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes & Development 21, 1050–1063. https://doi.org/10.1101/gad.1524107.

Thatcher KN, Peddada S, Yasui DH, Lasalle JM. 2005. Homologous pairing of 15q11–13 imprinted domains in brain is developmentally regulated but deficient in Rett and autism samples. Human Molecular Genetics 14(6), 785–97. https://doi.org/10.1093/hmg/ddi073.

Tremblay LK, Naranjo CA, Graham SJ, Herrmann N, Mayberg HS, Hevenor S, Busto UE. 2005. Functional neuroanatomical substrates of altered reward processing in major depressive disorder revealed by a dopaminergic probe. Archives of General Psychiatry 62(11), 1228–1236. https://doi.org/10.1001/archpsyc.62.11.1228.

Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ. 2006. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nature Neuroscience 9, 519–525. https://doi.org/10.1038/nn1659.

Wang WX, Rajeev BW, Stromberg AJ, Ren N, Tang G, Huang Q. 2008b. The expression of microRNA miR-107 decreases early in Alzheimer’s disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. The Journal of Neuroscience. 2008 28, 1213–1223. https://doi.org/10.1523/JNEUROSCI.5065-07.2008.

Weaver IC, Cervoni NChampagne FAD’Alessio ACSharma SSeckl JRDymov SSzyf MMeaney MJ. 2004. Epigenetic programming by maternal behavior. Nature Neuroscience 7, 847–854. https://doi.org/10.1038/nn1276.

West RL, Lee JM, Maroun LE. 1995. Hypomethylation of the amyloid precursor protein gene in the brain of an Alzheimer’s disease patient. Journal of Molecular Neuroscience 6(2), 141–146. https://doi.org/10.1007/BF02736773.

Wilkinson MB, Xiao G, Kumar A, Laplant Q, Renthal W, Sikder D, Kodadek TJ, Nestler EJ. 2009. Imipramine treatment and resiliency exhibit similar chromatin regulation in the mouse nucleus accumbens in depression models. The Journal of Neuroscience 29, 7820–7832. https://doi.org/10.1523/JNEUROSCI.0932-09.2009

Wurdinger T, Costa FF. 2007. Molecular therapy in the microRNA era. The Pharmacogenomics Journal 7, 297–304. https://doi.org/10.1038/sj.tpj.6500429

Yan L, Nass SJ, Smith D, Nelson WG, Herman JG, Davidson NE. 2003. Specific inhibition of DNMT1 by antisense oligonucleotides induces re-expression of estrogen receptor-alpha (ER) in ER-negative human breast cancer cell lines. Cancer Biology & Therapy 2, 552–556.

Zhang TY, Keown CL, Wen X, Li J, Vousden DA, Anacker C, Bhattacharyya U, Ryan R, Diorio J, O’Toole N, Lerch JP, Mukamel EA, Meaney MJ. 2018. Environmental enrichment increases transcriptional and epigenetic differentiation between mouse dorsal and ventral dentate gyrus. Nature Communications. Jan 19,  9(1), 298. https://doi.org/10.1038/s41467-017-02748-x

Zimanyi I, Pessah IN. 1991. Pharmacological characterization of the specific binding of [3H]ryanodine to rat brain microsomal membranes. Brain Research 561(2), 181–191. https://doi.org/10.1016/0006-8993(91)91594-Q