Making sense of epigenetics

International Journal of Neuropsychopharmacology

Volumn 19, Issue 11, 2016, Pages

  Schuebel, Kornel ^a   Gitik, Miri ^a   Domschke, Katharina ^b   Goldman, David ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Chromatin; DNA methylation; Eigenetics; Neuropsychiatric disorders

Indexed keywords

COCAINE; DNA; METHAMPHETAMINE; MORPHINE; PRODYNORPHIN;

BIPOLAR DISORDER; CHEMICAL MODIFICATION; CHROMATIN STRUCTURE; DEGENERATIVE DISEASE; DEPRESSION; DNA METHYLATION; DRUG ABUSE; EARLY LIFE STRESS; EPIGENETICS; GENE FUNCTION; GENE LOCUS; GENETIC REGULATION; HUMAN; LEARNING DISORDER; MEMORY DISORDER; MENTAL DISEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SCHIZOPHRENIA; STRESS; ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC EPIGENESIS; GENETIC PREDISPOSITION; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; HEREDITY; PATHOPHYSIOLOGY; PEDIGREE; PHENOTYPE; PSYCHOLOGY; RISK FACTOR;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; EPIGENESIS, GENETIC; GENE-ENVIRONMENT INTERACTION; GENETIC PREDISPOSITION TO DISEASE; HEREDITY; HUMANS; MENTAL DISORDERS; PEDIGREE; PHENOTYPE; RISK FACTORS;

EID: 84996672296     PISSN: 14611457     EISSN: 14695111     Source Type: Journal    
DOI: 10.1093/ijnp/pyw058     Document Type: Review

References (89)

1. Aguilar-Valles A, Vaissiere T, Griggs EM, Mikaelsson MA, Takacs IF, Young EJ, Rumbaugh G, Miller CA (2014) Methamphetamineassociated memory is regulated by a writer and an eraser of permissive histone methylation. Biol Psychiatry 76:57-65.
2. 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.
3. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23:185-188.
4. Andersen AM, Dogan MV, Beach SR, Philibert RA (2015) Current and future prospects for epigenetic biomarkers of substance use disorders. Genes (Basel) 6:991-1022.
5. Anderson LM, Riffle L, Wilson R, Travlos GS, Lubomirski MS, Alvord WG (2006) Preconceptional fasting of fathers alters serum glucose in offspring of mice. Nutrition 22:327-331.
6. Bale TL (2015) Epigenetic and transgenerational reprogramming of brain development. Nat Rev Neurosci 16:332-344.
7. Barton SC, Surani MA, Norris ML (1984) Role of paternal and maternal genomes in mouse development. Nature 311:374-376.
8. Bjornsson HT (2015) The Mendelian disorders of the epigenetic machinery. Genome Res 25:1473-1481.
9. Carone BR, Fauquier L, Habib N, Shea JM, Hart CE, Li R, Bock C, Li C, Gu H, Zamore PD, Meissner A, Weng Z, Hofmann HA, Friedman N, Rando OJ (2010) Paternally induced transgenerational environmental reprogramming of metabolic gene expression in mammals. Cell 143:1084-1096.
10. Castellani CA, Laufer BI, Melka MG, Diehl EJ, O'Reilly RL, Singh SM (2015) DNA methylation differences in monozygotic twin pairs discordant for schizophrenia identifies psychosis related genes and networks. BMC Med Genomics 8:17.
11. Chokroborty-Hoque A, Alberry B, Singh SM (2014) Exploring the complexity of intellectual disability in fetal alcohol spectrum disorders. Front Pediatr 2:90.
12. Cooper DW (1971) Directed genetic change model for X chromosome inactivation in eutherian mammals. Nature 230:292-294.
13. Cortijo S, Wardenaar R, Colome-Tatche M, Gilly A, Etcheverry M, Labadie K, Caillieux E, Hospital F, Aury JM, Wincker P, Roudier F, Jansen RC, Colot V, Johannes F (2014) Mapping the epigenetic basis of complex traits. Science 343:1145-1148.
14. Dash PK, Moore AN, Kobori N, Runyan JD (2007) Molecular activity underlying working memory. Learn Mem 14:554-563.
15. Davies MN, Volta M, Pidsley R, Lunnon K, Dixit A, Lovestone S, Coarfa C, Harris RA, Milosavljevic A, Troakes C, Al-Sarraj S, Dobson R, Schalkwyk LC, Mill J (2012) Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biol 13:R43.
16. Davies MN, Krause L, Bell JT, Gao F, Ward KJ, Wu H, Lu H, Liu Y, Tsai PC, Collier DA, Murphy T, Dempster E, Mill J, Consortium UKBE, Battle A, Mostafavi S, Zhu X, Henders A, Byrne E, Wray NR, Martin NG, Spector TD, Wang J (2014) Hypermethylation in the ZBTB20 gene is associated with major depressive disorder. Genome Biol 15:R56.
17. Dempster EL, Pidsley R, Schalkwyk LC, Owens S, Georgiades A, Kane F, Kalidindi S, Picchioni M, Kravariti E, Toulopoulou T, Murray RM, Mill J (2011) Disease-associated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Hum Mol Genet 20:4786-4796.
18. Dempster EL, Wong CC, Lester KJ, Burrage J, Gregory AM, Mill J, Eley TC (2014) Genome-wide methylomic analysis of monozygotic twins discordant for adolescent depression. Biol Psychiatry 76:977-983.
19. Dias BG, Ressler KJ (2014) Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci 17(1):89-96.
20. Domschke K, Tidow N, Schwarte K, Deckert J, Lesch KP, Arolt V, Zwanzger P, Baune BT (2014) Serotonin transporter gene hypomethylation predicts impaired antidepressant treatment response. Int J Neuropsychopharmacol 17:1167-1176.
21. Duclot F, Kabbaj M (2015) Epigenetic mechanisms underlying the role of brain-derived neurotrophic factor in depression and response to antidepressants. J Exp Biol 218:21-31.
22. Duncan BK, Miller JH (1980) Mutagenic deamination of cytosine residues in DNA. Nature 287:560-561.
23. Fu Y, He C (2012) Nucleic acid modifications with epigenetic significance. Curr Opin Chem Biol 16:516-524.
24. Gibbs JR, van der Brug MP, Hernandez DG, Traynor BJ, Nalls MA, Lai SL, Arepalli S, Dillman A, Rafferty IP, Troncoso J, Johnson R, Zielke HR, Ferrucci L, Longo DL, Cookson MR, Singleton AB (2010) Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet 6:e1000952.
25. Godino A, Jayanthi S, Cadet JL (2015) Epigenetic landscape of amphetamine and methamphetamine addiction in rodents. Epigenetics 10:574-580.
26. Goldman D, Oroszi G, Ducci F (2005) The genetics of addictions: uncovering the genes. Nat Rev Genet 6(7):521-532.
27. Goll MG, Bestor TH (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74:481-514.
28. Gupta-Agarwal S, Franklin AV, Deramus T, Wheelock M, Davis RL, McMahon LL, Lubin FD (2012) G9a/GLP histone lysine dimethyltransferase complex activity in the hippocampus and the entorhinal cortex is required for gene activation and silencing during memory consolidation. J Neurosci 32:5440-5453.
29. Hannon E, Spiers H, Viana J, Pidsley R, Burrage J, Murphy TM, Troakes C, Turecki G, O'Donovan MC, Schalkwyk LC, Bray NJ, Mill J (2016) Methylation QTLs in the developing brain and their enrichment in schizophrenia risk loci. Nat Neurosci 19:48-54.
30. Harlaar N, Bryan AD, Thayer RE, Karoly HC, Oien N, Hutchison KE (2014) Methylation of a CpG site near the ALDH1A2 gene is associated with loss of control over drinking and related phenotypes. Alcohol Clin Exp Res 38:713-721.
31. Holliday R (2006) Epigenetics: a historical overview. Epigenetics 1:76-80.
32. Im HI, Hollander JA, Bali P, Kenny PJ (2010) MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nat Neurosci 13:1120-1127.
33. Issidorides MR, Stefanis CN, Varsou E, Katsorchis T (1975) Altered chromatin ultrastructure in neutrophils of schizophrenics. Nature 258:612-614.
34. Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074-1080.
35. Kerimoglu C, Agis-Balboa RC, Kranz A, Stilling R, Bahari-Javan S, Benito-Garagorri E, Halder R, Burkhardt S, Stewart AF, Fischer A (2013) Histone-methyltransferase MLL2 (KMT2B) is required for memory formation in mice. J Neurosci 33:3452-3464.
36. Kleiber ML, Diehl EJ, Laufer BI, Mantha K, Chokroborty-Hoque A, Alberry B, Singh SM (2014) Long-term genomic and epigenomic dysregulation as a consequence of prenatal alcohol exposure: a model for fetal alcohol spectrum disorders. Front Genet 5:161.
37. Klengel T, Mehta D, Anacker C, Rex-Haffner M, Pruessner JC, Pariante CM, Pace TW, Mercer KB, Mayberg HS, Bradley B, Nemeroff CB, Holsboer F, Heim CM, Ressler KJ, Rein T, Binder EB (2013) Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat Neurosci 16:33-41.
38. Klengel T, Pape J, Binder EB, Mehta D (2014) The role of DNA methylation in stress-related psychiatric disorders. Neuropharmacology 80:115-132.
39. Kuratomi G, Iwamoto K, Bundo M, Kusumi I, Kato N, Iwata N, Ozaki N, Kato T (2008) Aberrant DNA methylation associated with bipolar disorder identified from discordant monozygotic twins. Mol Psychiatry 13:429-441.
40. Launay JM, Del Pino M, Chironi G, Callebert J, Peoc'h K, Megnien JL, Mallet J, Simon A, Rendu F (2009) Smoking induces longlasting effects through a monoamine-oxidase epigenetic regulation. PLoS One 4:e7959.
41. Lipsky RH (2013) Epigenetic mechanisms regulating learning and long-term memory. Int J Dev Neurosci 31:353-358.
42. Liyanage VR, Jarmasz JS, Murugeshan N, Del Bigio MR, Rastegar M, Davie JR (2014) DNA modifications: function and applications in normal and disease States. Biology (Basel) 3:670-723.
43. Lolak S, Suwannarat P, Lipsky RH (2014) Epigenetics of depression. Prog Mol Biol Transl Sci 128:103-137.
44. Lott SA, Burghardt PR, Burghardt KJ, Bly MJ, Grove TB, Ellingrod VL (2013) The influence of metabolic syndrome, physical activity and genotype on catechol-O-methyl transferase promoterregion methylation in schizophrenia. Pharmacogenomics J 13:264-271.
45. Malvaez M, McQuown SC, Rogge GA, Astarabadi M, Jacques V, Carreiro S, Rusche JR, Wood MA (2013) HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proc Natl Acad Sci U S A 110:2647-2652.
46. Martin SJ, Grimwood PD, Morris RG (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annu Rev Neurosci 23:649-711.
47. Masemola ML, van der Merwe L, Lombard Z, Viljoen D, Ramsay M (2015) Reduced DNA methylation at the PEG3 DMR and KvDMR1 loci in children exposed to alcohol in utero: a South African Fetal Alcohol Syndrome cohort study. Front Genet 6:85.
48. Maze I, Covington HE III, Dietz DM, LaPlant Q, Renthal W, Russo SJ, Mechanic M, Mouzon E, Neve RL, Haggarty SJ, Ren Y, Sampath SC, Hurd YL, Greengard P, Tarakhovsky A, Schaefer A, Nestler EJ (2010) Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327:213-216.
49. McQuown SC, Barrett RM, Matheos DP, Post RJ, Rogge GA, Alenghat T, Mullican SE, Jones S, Rusche JR, Lazar MA, Wood MA (2011) HDAC3 is a critical negative regulator of long-term memory formation. J Neurosci 31:764-774.
50. Michan S, Li Y, Chou MM, Parrella E, Ge H, Long JM, Allard JS, Lewis K, Miller M, Xu W, Mervis RF, Chen J, Guerin KI, Smith LE, McBurney MW, Sinclair DA, Baudry M, de Cabo R, Longo VD (2010) SIRT1 is essential for normal cognitive function and synaptic plasticity. J Neurosci 30:9695-9707.
51. Miller CA, Campbell SL, Sweatt JD (2008) DNA methylation and histone acetylation work in concert to regulate memory formation and synaptic plasticity. Neurobiol Learn Mem 89:599-603.
52. Morris MJ, Mahgoub M, Na ES, Pranav H, Monteggia LM (2013) Loss of histone deacetylase 2 improves working memory and accelerates extinction learning. J Neurosci 33:6401-6411.
53. Nestler EJ, Pena CJ, Kundakovic M, Mitchell A, Akbarian S (2015) Epigenetic basis of mental illness. Neuroscientist. Epub ahead of print.
54. Ng SF, Lin RC, Laybutt DR, Barres R, Owens JA, Morris MJ (2010) Chronic high-fat diet in fathers programs beta-cell dysfunction in female rat offspring. Nature 467:963-966.
55. Nohesara S, Ghadirivasfi M, Mostafavi S, Eskandari MR, Ahmadkhaniha H, Thiagalingam S, Abdolmaleky HM (2011) DNA hypomethylation of MB-COMT promoter in the DNA derived from saliva in schizophrenia and bipolar disorder. J Psychiatr Res 45:1432-1438.
56. Pastor V, Host L, Zwiller J, Bernabeu R (2011) Histone deacetylase inhibition decreases preference without affecting aversion for nicotine. J Neurochem 116:636-645.
57. Razin A, Cedar H (1984) DNA methylation in eukaryotic cells. Int Rev Cytol 92:159-185.
58. Reik W, Dean W, Walter J (2001) Epigenetic reprogramming in mammalian development. Science 293:1089-1093.
59. Renthal W, Nestler EJ (2008) Epigenetic mechanisms in drug addiction. Trends Mol Med 14:341-350.
60. Rett A (1966) [On a unusual brain atrophy syndrome in hyperammonemia in childhood]. Wien Med Wochenschr 116:723-726.
61. Roberts S, Lester KJ, Hudson JL, Rapee RM, Creswell C, Cooper PJ, Thirlwall KJ, Coleman JR, Breen G, Wong CC, Eley TC (2014) Serotonin transporter [corrected] methylation and response to cognitive behaviour therapy in children with anxiety disorders. Transl Psychiatry 4:e444.
62. Roundtree IA, He C (2016) RNA epigenetics-chemical messages for posttranscriptional gene regulation. Curr Opin Chem Biol 30:46-51.
63. Rozen R (1996) Molecular genetics of methylenetetrahydrofolate reductase deficiency. J Inherit Metab Dis 19:589-594.
64. Rudenko A, Dawlaty MM, Seo J, Cheng AW, Meng J, Le T, Faull KF, Jaenisch R, Tsai LH (2013) Tet1 is critical for neuronal activityregulated gene expression and memory extinction. Neuron 79:1109-1122.
65. Sakharkar AJ, Zhang H, Tang L, Baxstrom K, Shi G, Moonat S, Pandey SC (2014) Effects of histone deacetylase inhibitors on amygdaloid histone acetylation and neuropeptide Y expression: a role in anxiety-like and alcohol-drinking behaviours. Int J Neuropsychopharmacol 17:1207-1220.
66. Sanchis-Segura C, Jancic D, Jimenez-Minchan M, Barco A (2009) Inhibition of cAMP responsive element binding protein in striatal neurons enhances approach and avoidance responses toward morphine--and morphine withdrawal-related cues. Front Behav Neurosci 3:30.
67. Shea JM, Serra RW, Carone BR, Shulha HP, Kucukural A, Ziller MJ, Vallaster MP, Gu H, Tapper AR, Gardner PD, Meissner A, Garber M, Rando OJ (2015) Genetic and epigenetic variation, but not diet, shape the sperm methylome. Dev Cell 35:750-758.
68. Shumay E, Logan J, Volkow ND, Fowler JS (2012) Evidence that the methylation state of the monoamine oxidase A (MAOA) gene predicts brain activity of MAO A enzyme in healthy men. Epigenetics 7:1151-1160.
69. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403:41-45.
70. Sweder KS, Hanawalt PC (1993) Transcription-coupled DNA repair. Science 262:439-440.
71. Taqi MM, Bazov I, Watanabe H, Sheedy D, Harper C, Alkass K, Druid H, Wentzel P, Nyberg F, Yakovleva T, Bakalkin G (2011) Prodynorphin CpG-SNPs associated with alcohol dependence: elevated methylation in the brain of human alcoholics. Addict Biol 16:499-509.
72. Tuesta LM, Zhang Y (2014) Mechanisms of epigenetic memory and addiction. EMBO J 33:1091-1103.
73. Van Speybroeck L (2002) From epigenesis to epigenetics: the case of C. H. Waddington. Ann N Y Acad Sci 981:61-81.
74. Vecsey CG, Hawk JD, Lattal KM, Stein JM, Fabian SA, Attner MA, Cabrera SM, McDonough CB, Brindle PK, Abel T, Wood MA (2007) Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J Neurosci 27:6128-6140.
75. Waddington CH (1952) The epigenetics of birds. Cambridge: Cambridge University Press.
76. Weaver IC (2014) Integrating early life experience, gene expression, brain development, and emergent phenotypes: unraveling the thread of nature via nurture. Adv Genet 86:277-307.
77. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, Dymov S, Szyf M, Meaney MJ (2004) Epigenetic programming by maternal behavior. Nat Neurosci 7:847-854.
78. Wei Y, Mizzen CA, Cook RG, Gorovsky MA, Allis CD (1998) Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. Proc Natl Acad Sci U S A 95:7480-7484.
79. Whiteford HA, Degenhardt L, Rehm J, Baxter AJ, Ferrari AJ, Erskine HE, Charlson FJ, Norman RE, Flaxman AD, Johns N, Burstein R, Murray CJ, Vos T (2013) Global burden of disease attributable to mental and substance use disorders: findings from the Global Burden of Disease Study 2010. Lancet 382:1575-1586.
80. Wockner LF, Noble EP, Lawford BR, Young RM, Morris CP, Whitehall VL, Voisey J (2014) Genome-wide DNA methylation analysis of human brain tissue from schizophrenia patients. Transl Psychiatry 4:e339.
81. Wolffe AP, Matzke MA (1999) Epigenetics: regulation through repression. Science 286:481-486.
82. Wu C, Morris JR (2001) Genes, genetics, and epigenetics: a correspondence. Science 293:1103-1105.
83. Xu GL, Bestor TH, Bourc'his D, Hsieh CL, Tommerup N, Bugge M, Hulten M, Qu X, Russo JJ, Viegas-Pequignot E (1999) Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402:187-191.
84. Xu J, He G, Zhu J, Zhou X, St Clair D, Wang T, Xiang Y, Zhao Q, Xing Q, Liu Y, Wang L, Li Q, He L, Zhao X (2015) Prenatal nutritional deficiency reprogrammed postnatal gene expression in mammal brains: implications for schizophrenia. Int J Neuropsychopharmacol 18.
85. Xu X, Kozikowski AP, Pozzo-Miller L (2014) A selective histone deacetylase-6 inhibitor improves BDNF trafficking in hippocampal neurons from Mecp2 knockout mice: implications for Rett syndrome. Front Cell Neurosci 8:68.
86. Yasui DH, Xu H, Dunaway KW, Lasalle JM, Jin LW, Maezawa I (2013) MeCP2 modulates gene expression pathways in astrocytes. Mol Autism 4:3.
87. Yehuda R, Daskalakis NP, Bierer LM, Bader HN, Klengel T, Holsboer F, Binder EB (2015) Holocaust exposure induced intergenerational effects on FKBP5 methylation. Biol Psychiatry. Epub ahead of print. doi: 10.1016/j.biopsych.2015.08.005.
88. Yoder JA, Walsh CP, Bestor TH (1997) Cytosine methylation and the ecology of intragenomic parasites. Trends Genet 13:335-340.
89. Ziegler C, Richter J, Mahr M, Gajewska A, Schiele MA, Gehrmann A, Schmidt B, Lesch KP, Lang T, Helbig-Lang S, Pauli P, Kircher T, Reif A, Rief W, Vossbeck-Elsebusch AN, Arolt V, Wittchen HU, Hamm AO, Deckert J, Domschke K (2016) MAOA gene hypomethylation in panic disorder-reversibility of an epigenetic risk pattern by psychotherapy. Transl Psychiatry 6:e773.