Epigenetics of major psychosis: Progress, problems and perspectives

Trends in Genetics

Volumn 28, Issue 9, 2012, Pages 427-435

  Labrie, Viviane ^a   Pai, Shraddha ^a   Petronis, Arturas ^a  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

Author keywords

Bipolar disorder; DNA methylation; Epigenetics; Epigenome wide association study; Histone modifications; Schizophrenia

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; GLUTAMATE DECARBOXYLASE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; IMIPRAMINE; MESSENGER RNA; METHYL CPG BINDING PROTEIN 2; SEROTONIN 1 RECEPTOR; TESTIS DETERMINING FACTOR;

BIPOLAR DISORDER; BRAIN FUNCTION; COGNITION; COPY NUMBER VARIATION; CPG ISLAND; DNA FINGERPRINTING; DNA METHYLATION; DNA MODIFICATION; DNA SEQUENCE; EPHEMERAL SPECIES; EPIGENETICS; GABAERGIC TRANSMISSION; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; GENETIC ASSOCIATION; GENETIC RISK; GENETIC TRANSCRIPTION; GENOME; GENOTYPE ENVIRONMENT INTERACTION; HEREDITY; HERITABILITY; HISTONE MODIFICATION; HLA SYSTEM; HUMAN; MENTAL PATIENT; MENTAL STRESS; MONOZYGOTIC TWINS; NONHUMAN; PHENOTYPE; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSYCHOSIS; REVIEW; SCHIZOPHRENIA; SYNAPTIC TRANSMISSION;

ANIMALS; EPIGENESIS, GENETIC; GENOME; HUMANS; MUTATION; PSYCHOTIC DISORDERS;

EID: 84865159829     PISSN: 01689525     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tig.2012.04.002     Document Type: Review

References (104)

1. Collins P.Y., et al. Grand challenges in global mental health. Nature 2011, 475:27-30.
2. Sullivan P.F., et al. Schizophrenia as a complex trait: evidence from a meta-analysis of twin studies. Arch. Gen. Psychiatry 2003, 60:1187-1192.
3. Burmeister M., et al. Psychiatric genetics: progress amid controversy. Nat. Rev. Genet. 2008, 9:527-540.
4. Petronis A. Epigenetics as a unifying principle in the aetiology of complex traits and diseases. Nature 2010, 465:721-727.
5. Oh G., Petronis A. Environmental studies of schizophrenia through the prism of epigenetics. Schizophr. Bull. 2008, 34:1122-1129.
6. Cedar H., Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat. Rev. Genet. 2009, 10:295-304.
7. Gregg C., et al. High-resolution analysis of parent-of-origin allelic expression in the mouse brain. Science 2010, 329:643-648.
8. Feil R., Fraga M.F. Epigenetics and the environment: emerging patterns and implications. Nat. Rev. Genet. 2011, 13:97-109.
9. Day J.J., Sweatt J.D. Epigenetic mechanisms in cognition. Neuron 2011, 70:813-829.
10. Skene P.J., et al. Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol. Cell 2010, 37:457-468.
11. Li H., et al. Loss of activity-induced phosphorylation of MeCP2 enhances synaptogenesis, LTP and spatial memory. Nat. Neurosci. 2011, 14:1001-1008.
12. Guo J.U., et al. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat. Neurosci. 2011, 14:1345-1351.
13. Feng J., et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat. Neurosci. 2010, 13:423-430.
14. Miller C.A., et al. Cortical DNA methylation maintains remote memory. Nat. Neurosci. 2010, 13:664-666.
15. Guan Z., et al. Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 2002, 111:483-493.
16. Schaefer A., et al. Control of cognition and adaptive behavior by the GLP/G9a epigenetic suppressor complex. Neuron 2009, 64:678-691.
17. Guan J.S., et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009, 459:55-60.
18. Levenson J.M., et al. Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 2004, 279:40545-40559.
19. Alarcon J.M., et al. Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 2004, 42:947-959.
20. Cardno A.G., et al. Heritability estimates for psychotic disorders: the Maudsley twin psychosis series. Arch. Gen. Psychiatry 1999, 56:162-168.
21. Purcell S.M., et al. Common polygenic variation contributes to risk of schizophrenia and bipolar disorder. Nature 2009, 460:748-752.
22. Malhotra D., Sebat J. CNVs: harbingers of a rare variant revolution in psychiatric genetics. Cell 2012, 148:1223-1241.
23. Sheng G., et al. Differences in the circuitry-based association of copy numbers and gene expression between the hippocampi of patients with schizophrenia and the hippocampi of patients with bipolar disorder. Arch. Gen. Psychiatry 2012, 69:550-561.
24. Maher B. Personal genomes: the case of the missing heritability. Nature 2008, 456:18-21.
25. Visscher P.M., et al. Evidence-based psychiatric genetics, AKA the false dichotomy between common and rare variant hypotheses. Mol. Psychiatry 2012, 17:474-485.
26. Zuk O., et al. The mystery of missing heritability: genetic interactions create phantom heritability. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:1193-1198.
27. Daxinger L., Whitelaw E. Understanding transgenerational epigenetic inheritance via the gametes in mammals. Nat. Rev. Genet. 2012, 13:153-162.
28. Kaminsky Z.A., et al. DNA methylation profiles in monozygotic and dizygotic twins. Nat. Genet. 2009, 41:240-245.
29. Ollikainen M., et al. DNA methylation analysis of multiple tissues from newborn twins reveals both genetic and intrauterine components to variation in the human neonatal epigenome. Hum. Mol. Genet. 2010, 19:4176-4188.
30. Jirtle R.L., Skinner M.K. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 2007, 8:253-262.
31. Ushijima T., et al. Fidelity of the methylation pattern and its variation in the genome. Genome Res. 2003, 13:868-874.
32. Feinberg A.P., Irizarry R.A. Evolution in health and medicine Sackler colloquium: stochastic epigenetic variation as a driving force of development, evolutionary adaptation, and disease. Proc. Natl. Acad. Sci. U.S.A. 2010, 107(Suppl. 1):1757-1764.
33. Petronis A., et al. Schizophrenia: an epigenetic puzzle?. Schizophr. Bull. 1999, 25:639-655.
34. Petronis A. Human morbid genetics revisited: relevance of epigenetics. Trends Genet. 2001, 17:142-146.
35. Pidsley R., Mill J. Epigenetic studies of psychosis: current findings, methodological approaches, and implications for postmortem research. Biol. Psychiatry 2011, 69:146-156.
36. Grayson D.R., et al. Reelin promoter hypermethylation in schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:9341-9346.
37. Tamura Y., et al. Epigenetic aberration of the human REELIN gene in psychiatric disorders. Mol. Psychiatry 2007, 12:593-600.
38. Iwamoto K., et al. DNA methylation status of SOX10 correlates with its downregulation and oligodendrocyte dysfunction in schizophrenia. J. Neurosci. 2005, 25:5376-5381.
39. Tolosa A., et al. FOXP2 gene and language impairment in schizophrenia: association and epigenetic studies. BMC Med. Genet. 2010, 11:114.
40. Carrard A., et al. Increased DNA methylation status of the serotonin receptor 5HTR1A gene promoter in schizophrenia and bipolar disorder. J. Affect. Disord. 2011, 132:450-453.
41. Tochigi M., et al. Methylation status of the reelin promoter region in the brain of schizophrenic patients. Biol. Psychiatry 2008, 63:530-533.
42. Mill J., et al. Epigenomic profiling reveals DNA-methylation changes associated with major psychosis. Am. J. Hum. Genet. 2008, 82:696-711.
43. Kaminsky Z., et al. A multi-tissue analysis identifies HLA complex group 9 gene methylation differences in bipolar disorder. Mol. Psychiatry 2012, 17:728-740.
44. Dempster E.L., et al. Disease-associated epigenetic changes in monozygotic twins discordant for schizophrenia and bipolar disorder. Hum. Mol. Genet. 2011, 20:4786-4796.
45. Rosa A., et al. Differential methylation of the X-chromosome is a possible source of discordance for bipolar disorder female monozygotic twins. Am. J. Med. Genet. Part B: Neuropsychiatr. Genet. 2008, 147B:459-462.
46. Veldic M., et al. In psychosis, cortical interneurons overexpress DNA-methyltransferase 1. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:2152-2157.
47. Zhubi A., et al. An upregulation of DNA-methyltransferase 1 and 3a expressed in telencephalic GABAergic neurons of schizophrenia patients is also detected in peripheral blood lymphocytes. Schizophr. Res. 2009, 111:115-122.
48. Guidotti A., et al. S-adenosyl methionine and DNA methyltransferase-1 mRNA overexpression in psychosis. Neuroreport 2007, 18:57-60.
49. Kale A., et al. Reduced folic acid, vitamin B12 and docosahexaenoic acid and increased homocysteine and cortisol in never-medicated schizophrenia patients: implications for altered one-carbon metabolism. Psychiatry Res. 2010, 175:47-53.
50. Huang H.S., et al. Chromatin immunoprecipitation in postmortem brain. J. Neurosci. Methods 2006, 156:284-292.
51. Huang H.S., et al. Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1-regulated histone methylation at GABAergic gene promoters. J. Neurosci. 2007, 27:11254-11262.
52. Torrey E.F., et al. Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains. Biol. Psychiatry 2005, 57:252-260.
53. Akbarian S., et al. Chromatin alterations associated with down-regulated metabolic gene expression in the prefrontal cortex of subjects with schizophrenia. Arch. Gen. Psychiatry 2005, 62:829-840.
54. Gavin D.P., et al. 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, 34:232-237.
55. Sharma R.P., et al. Histone deactylase 1 expression is increased in the prefrontal cortex of schizophrenia subjects: analysis of the National Brain Databank microarray collection. Schizophr. Res. 2008, 98:111-117.
56. Benes F.M., et al. Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:10164-10169.
57. Callaghan R.C., et al. Methamphetamine use and schizophrenia: a population-based cohort study in California. Am. J. Psychiatry 2012, 169:389-396.
58. Beaulieu S., et al. The Canadian Network for Mood and Anxiety Treatments (CANMAT) task force recommendations for the management of patients with mood disorders and comorbid substance use disorders. Ann. Clin. Psychiatry 2012, 24:38-55.
59. LaPlant Q., et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat. Neurosci. 2010, 13:1137-1143.
60. Maze I., et al. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 2010, 327:213-216.
61. Covington H.E., et al. A role for repressive histone methylation in cocaine-induced vulnerability to stress. Neuron 2011, 71:656-670.
62. Renthal W., et al. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 2007, 56:517-529.
63. Wilkinson M.B., et al. Imipramine treatment and resiliency exhibit similar chromatin regulation in the mouse nucleus accumbens in depression models. J. Neurosci. 2009, 29:7820-7832.
64. Tsankova N.M., et al. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 2006, 9:519-525.
65. Rakyan V.K., et al. Epigenome-wide association studies for common human diseases. Nat. Rev. Genet. 2011, 12:529-541.
66. Clark S.J. Action at a distance: epigenetic silencing of large chromosomal regions in carcinogenesis. Hum. Mol. Genet. 2007, 16:R88-R95.
67. Lichtenstein P., et al. Common genetic determinants of schizophrenia and bipolar disorder in Swedish families: a population-based study. Lancet 2009, 373:234-239.
68. Xu G.L., Bestor T.H. Cytosine methylation targetted to pre-determined sequences. Nat. Genet. 1997, 17:376-378.
69. Saxe J.P., Lin H. Small noncoding RNAs in the germline. Cold Spring Harb. Perspect. Biol. 2011, 3:a002717.
70. Adli M., Bernstein B.E. Whole-genome chromatin profiling from limited numbers of cells using nano-ChIP-seq. Nat. Protoc. 2011, 6:1656-1668.
71. Weaver I.C., et al. Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:3480-3485.
72. Dolmetsch R., Geschwind D.H. The human brain in a dish: the promise of iPSC-derived neurons. Cell 2011, 145:831-834.
73. Gibbs J.R., et al. Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet. 2010, 6:e1000952.
74. Tycko B. Allele-specific DNA methylation: beyond imprinting. Hum. Mol. Genet. 2010, 19:R210-R220.
75. Pfeifer G.P. Mutagenesis at methylated CpG sequences. Curr. Top. Microbiol. Immunol. 2006, 301:259-281.
76. Chen R.Z., et al. DNA hypomethylation leads to elevated mutation rates. Nature 1998, 395:89-93.
77. Herculano-Houzel S. The human brain in numbers: a linearly scaled-up primate brain. Front. Hum. Neurosci. 2009, 3:31.
78. Li J. et al. Genomic hypomethylation in the human germline associates with structural mutability in the human genome. PLoS Genet. (in press).
79. Fuke C., et al. Age related changes in 5-methylcytosine content in human peripheral leukocytes and placentas: an HPLC-based study. Ann. Hum. Genet. 2004, 68:196-204.
80. Alisch R.S., et al. Age-associated DNA methylation in pediatric populations. Genome Res. 2012, 22:623-632.
81. Numata S., et al. DNA methylation signatures in development and aging of the human prefrontal cortex. Am. J. Hum. Genet. 2012, 90:260-272.
82. Fraga M.F., et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:10604-10609.
83. Heijmans B.T., et al. Heritable rather than age-related environmental and stochastic factors dominate variation in DNA methylation of the human IGF2/H19 locus. Hum. Mol. Genet. 2007, 16:547-554.
84. Metivier R., et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 2008, 452:45-50.
85. Masri S., Sassone-Corsi P. Plasticity and specificity of the circadian epigenome. Nat. Neurosci. 2010, 13:1324-1329.
86. Fraser P., Bickmore W. Nuclear organization of the genome and the potential for gene regulation. Nature 2007, 447:413-417.
87. Gilbert N., et al. DNA methylation affects nuclear organization, histone modifications, and linker histone binding but not chromatin compaction. J. Cell Biol. 2007, 177:401-411.
88. Mill J., et al. Epigenomic profiling reveals DNA-methylation changes associated with major psychosis. Am. J. Hum. Genet. 2008, 82:696-711.
89. Xie W., et al. Base-resolution analyses of sequence and parent-of-origin dependent DNA methylation in the mouse genome. Cell 2012, 148:816-831.
90. Kriaucionis S., Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 2009, 324:929-930.
91. Tahiliani M., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
92. Penn N.W., et al. The presence of 5-hydroxymethylcytosine in animal deoxyribonucleic acid. Biochem. J. 1972, 126:781-790.
93. Szulwach K.E., et al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat. Neurosci. 2011, 14:1607-1616.
94. Guo J.U., et al. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 2011, 145:423-434.
95. Ito S., et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 2011, 333:1300-1303.
96. Bernstein B.E., et al. The NIH Roadmap Epigenomics Mapping Consortium. Nat. Biotechnol. 2010, 28:1045-1048.
97. Lister R., et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009, 462:315-322.
98. Harris R.A., et al. Comparison of sequencing-based methods to profile DNA methylation and identification of monoallelic epigenetic modifications. Nat. Biotechnol. 2010, 28:1097-1105.
99. Koch C.M., et al. The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res. 2007, 17:691-707.
100. Petronis A., et al. Monozygotic twins exhibit numerous epigenetic differences: clues to twin discordance?. Schizophr. Bull. 2003, 29:169-178.
101. Phiel C.J., et al. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem. 2001, 276:36734-36741.
102. Sharma R.P., et al. Valproic acid and chromatin remodeling in schizophrenia and bipolar disorder: preliminary results from a clinical population. Schizophr. Res. 2006, 88:227-231.
103. Dong E., et al. Clozapine and sulpiride but not haloperidol or olanzapine activate brain DNA demethylation. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:13614-13619.
104. Ptak C., Petronis A. Epigenetics and complex disease: from etiology to new therapeutics. Annu. Rev. Pharmacol. Toxicol. 2008, 48:257-276.