Can we observe epigenetic effects on human brain function?

Trends in Cognitive Sciences

Volumn 19, Issue 7, 2015, Pages 366-373

  Nikolova, Yuliya S ^a   Hariri, Ahmad R ^b  

^a CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^b DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION;

BIOLOGICAL MECHANISMS; BRAIN FUNCTIONS; DNA SEQUENCE VARIATIONS; GENE METHYLATION; HUMAN BRAIN FUNCTIONS; IMAGING GENETICS; INDIVIDUAL DIFFERENCES; SEROTONIN TRANSPORTERS;

BRAIN MAPPING;

SEROTONIN TRANSPORTER;

BRAIN FUNCTION; DATA BASE; DNA SEQUENCE; EPIGENETICS; GENETIC VARIABILITY; GENOMICS; HUMAN; HUMAN GENOME; LONGITUDINAL STUDY; MEDICAL RESEARCH; MINING; REVIEW; BRAIN; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY;

BRAIN; EPIGENESIS, GENETIC; EPIGENOMICS; HUMANS; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 84937514043     PISSN: 13646613     EISSN: 1879307X     Source Type: Journal    
DOI: 10.1016/j.tics.2015.05.003     Document Type: Review

References (104)

1. Bookheimer S.Y., et al. Patterns of brain activation in people at risk for Alzheimer's disease. N. Engl. J. Med. 2000, 343:450-456.
2. Egan M.F., et al. Effect of COMT Val108/158 Met genotype on frontal lobe function and risk for schizophrenia. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:6917-6922.
3. Hariri A.R., et al. Serotonin transporter genetic variation and the response of the human amygdala. Science 2002, 297:400-403.
4. Hariri A.R. The neurobiology of individual differences in complex behavioral traits. Annu. Rev. Neurosci. 2009, 32:225-247.
5. Hariri A.R. Genetic polymorphisms: a cornerstone of translational biobehavioral research. Sci. Transl. Med. 2010, 2:18ps16.
6. Meyer-Lindenberg A., Weinberger D.R. Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat. Rev. Neurosci. 2006, 7:818-827.
7. Bartova L., et al. Is there a personalized medicine for mood disorders?. Eur. Arch. Psychiatry Clin. Neurosci. 2010, 260(Suppl. 2):S121-S126.
8. Singh I., Rose N. Biomarkers in psychiatry. Nature 2009, 460:202-207.
9. Hariri A.R., Holmes A. Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends Cogn. Sci. 2006, 10:182-191.
10. Swartz J.R., et al. A neural biomarker of psychological vulnerability to future life stress. Neuron 2015, 85:505-511.
11. Fakra E., et al. Effects of HTR1A C(-1019)G on amygdala reactivity and trait anxiety. Arch. Gen. Psychiatry 2009, 66:33-40.
12. Munafo M.R., et al. Serotonin transporter (5-HTTLPR) genotype and amygdala activation: a meta-analysis. Biol. Psychiatry 2008, 63:852-857.
13. Caspi A., et al. Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am. J. Psychiatry 2010, 167:509-527.
14. Risch N., et al. Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk of depression: a meta-analysis. JAMA 2009, 301:2462-2471.
15. Caspi A., et al. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 2003, 301:386-389.
16. Karg K., et al. The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Arch. Gen. Psychiatry 2011, 68:444-454.
17. Insel T.R., Cuthbert B.N. Medicine. Brain disorders? Precisely. Science 2015, 348:499-500.
18. Murphy S.E., et al. The effect of the serotonin transporter polymorphism (5-HTTLPR) on amygdala function: a meta-analysis. Mol. Psychiatry 2013, 18:512-520.
19. Pezawas L., et al. Evidence of biologic epistasis between BDNF and SLC6A4 and implications for depression. Mol. Psychiatry 2008, 13:709-716.
20. Drabant E.M., et al. Neural mechanisms underlying 5-HTTLPR-related sensitivity to acute stress. Am. J. Psychiatry 2012, 169:397-405.
21. Lemogne C., et al. Cognitive appraisal and life stress moderate the effects of the 5-HTTLPR polymorphism on amygdala reactivity. Hum. Brain Mapp. 2011, 32:1856-1867.
22. Bigos K.L., Weinberger D.R. Imaging genetics - days of future past. Neuroimage 2010, 53:804-809.
23. Hyde L.W., et al. Understanding risk for psychopathology through imaging gene-environment interactions. Trends Cogn. Sci. 2011, 15:417-427.
24. Jones P.A. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 2012, 13:484-492.
25. Bernstein B.E., et al. The mammalian epigenome. Cell 2007, 128:669-681.
26. Brenet F., et al. DNA methylation of the first exon is tightly linked to transcriptional silencing. PLoS ONE 2011, 6:e14524.
27. van Dongen J., et al. Epigenetic variation in monozygotic twins: a genome-wide analysis of DNA methylation in buccal cells. Genes 2014, 5:347-365.
28. 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.
29. Nikolova Y.S., et al. Beyond genotype: serotonin transporter epigenetic modification predicts human brain function. Nat. Neurosci. 2014, 17:1153-1155.
30. Wiers C.E. Methylation and the human brain: towards a new discipline of imaging epigenetics. Eur. Arch. Psychiatry Clin. Neurosci. 2012, 262:271-273.
31. Ursini G., et al. Stress-related methylation of the catechol-O-methyltransferase Val 158 allele predicts human prefrontal cognition and activity. J. Neurosci. 2011, 31:6692-6698.
32. Vukojevic V., et al. Epigenetic modification of the glucocorticoid receptor gene is linked to traumatic memory and post-traumatic stress disorder risk in genocide survivors. J. Neurosci. 2014, 34:10274-10284.
33. Weaver I.C., et al. Epigenetic programming by maternal behavior. Nat. Neurosci. 2004, 7:847-854.
34. Beach S.R., et al. Methylation at SLC6A4 is linked to family history of child abuse: an examination of the Iowa Adoptee sample. Am. J. Med. Genet. B: Neuropsychiatr. genet. 2010, 153B:710-713.
35. Kang H.J., et al. Association of SLC6A4 methylation with early adversity, characteristics and outcomes in depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 2013, 44C:23-28.
36. Alasaari J.S., et al. Environmental stress affects DNA methylation of a CpG rich promoter region of serotonin transporter gene in a nurse cohort. PLoS ONE 2012, 7:e45813.
37. Mehta D., et al. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:8302-8307.
38. Dias B.G., Ressler K.J. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat. Neurosci. 2014, 17:89-96.
39. Lee K.W., et al. Prenatal exposure to maternal cigarette smoking and DNA methylation: epigenome-wide association in a discovery sample of adolescents and replication in an independent cohort at birth through 17 years of age. Environ. Health Perspect. 2015, 123:193-199.
40. Oberlander T.F., et al. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics 2008, 3:97-106.
41. Szyf M. Nongenetic inheritance and transgenerational epigenetics. Trends Mol. Med. 2015, 21:134-144.
42. Hyman S.E. How adversity gets under the skin. Nat. Neurosci. 2009, 12:241-243.
43. McEwen B.S. Brain on stress: how the social environment gets under the skin. Proc. Natl. Acad. Sci. U.S.A. 2012, 109(Suppl. 2):17180-17185.
44. Hertzman C., Boyce T. How experience gets under the skin to create gradients in developmental health. Annu. Rev. Public Health 2010, 31:329-347.
45. Vijg J. Somatic mutations, genome mosaicism, cancer and aging. Curr. Opin. Genet. Dev. 2014, 26:141-149.
46. Davies M.N., et al. Functional annotation of the human brain methylome identifies tissue-specific epigenetic variation across brain and blood. Genome Biol. 2012, 13:R43.
47. Tylee D.S., et al. On the outside, looking in: a review and evaluation of the comparability of blood and brain '-omes'. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 2013, 162B:595-603.
48. Horvath S., et al. Aging effects on DNA methylation modules in human brain and blood tissue. Genome Biol. 2012, 13:R97.
49. Smith A.K., et al. DNA extracted from saliva for methylation studies of psychiatric traits: evidence tissue specificity and relatedness to brain. Am. J. Med. Genet. B: Neuropsychiatr. Genet. 2015, 168B:36-44.
50. Schultz W. Getting formal with dopamine and reward. Neuron 2002, 36:241-263.
51. Wang D., et al. Peripheral SLC6A4 DNA methylation is associated with in vivo measures of human brain serotonin synthesis and childhood physical aggression. PLoS ONE 2012, 7:e39501.
52. Shumay E., et al. Evidence that the methylation state of the monoamine oxidase A (MAOA) gene predicts brain activity of MAO A enzyme in healthy men. Epigenetics 2012, 7:1151-1160.
53. Farrell M.S., et al. Evaluating historical candidate genes for schizophrenia. Mol. Psychiatry 2015, 20:555-562.
54. Tabor H.K., et al. Candidate-gene approaches for studying complex genetic traits: practical considerations. Nat. Rev. Genet. 2002, 3:391-397.
55. Schumann G., et al. The IMAGEN study: reinforcement-related behaviour in normal brain function and psychopathology. Mol. Psychiatry 2010, 15:1128-1139.
56. Nikolova Y.S., et al. Beyond genotype: serotonin transporter epigenetic modification predicts human brain function. Nat. Neurosci. 2014, 17:1153-1155.
57. Roadmap Epigenomics C., et al. Integrative analysis of 111 reference human epigenomes. Nature 2015, 518:317-330.
58. Dias B.G., et al. Epigenetic mechanisms underlying learning and the inheritance of learned behaviors. Trends Neurosci. 2015, 38:96-107.
59. Nikolova Y.S., et al. Multilocus genetic profile for dopamine signaling predicts ventral striatum reactivity. Neuropsychopharmacology 2011, 36:1940-1947.
60. Szyf M. Epigenetics, DNA methylation, and chromatin modifying drugs. Annu. Rev. Pharmacol. Toxicol. 2009, 49:243-263.
61. Van Essen D.C., et al. The Human Connectome Project: a data acquisition perspective. Neuroimage 2012, 62:2222-2231.
62. Thompson P.M., et al. The ENIGMA Consortium: large-scale collaborative analyses of neuroimaging and genetic data. Brain Imaging Behav. 2014, 8:153-182.
63. Paus T. Population neuroscience: why and how. Hum. Brain Mapp. 2010, 31:891-903.
64. Barfield R.T., et al. Accounting for population stratification in DNA methylation studies. Genet. Epidemiol. 2014, 38:231-241.
65. Binder D.K., Scharfman H.E. Brain-derived neurotrophic factor. Growth Factors 2004, 22:123-131.
66. Grossman M.H., et al. Chromosomal mapping of the human catechol-O-methyltransferase gene to 22q11.1-q11.2. Genomics 1992, 12:822-825.
67. Pratt W.B., Toft D.O. Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev. 1997, 18:306-360.
68. Hotamisligil G.S., Breakefield X.O. Human monoamine oxidase A gene determines levels of enzyme activity. Am. J. Hum. Genet. 1991, 49:383-392.
69. Hollenberg S.M., et al. Primary structure and expression of a functional human glucocorticoid receptor cDNA. Nature 1985, 318:635-641.
70. Gimpl G., Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiol. Rev. 2001, 81:629-683.
71. Kumsta R., Heinrichs M. Oxytocin, stress and social behavior: neurogenetics of the human oxytocin system. Curr. Opin. Neurobiol. 2013, 23:11-16.
72. Lesch K.P., et al. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274:1527-1531.
73. Harshman S.W., et al. H1 histones: current perspectives and challenges. Nucleic Acids Res. 2013, 41:9593-9609.
74. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
75. Mercer T.R., Mattick J.S. Structure and function of long noncoding RNAs in epigenetic regulation. Nat. Struct. Mol. Biol. 2013, 20:300-307.
76. He L., Hannon G.J. MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 2004, 5:522-531.
77. Castel S.E., Martienssen R.A. RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat. Rev. Genet. 2013, 14:100-112.
78. Levenson J.M., Sweatt J.D. Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 2005, 6:108-118.
79. Sillivan S.E., et al. Neuroepigenetic regulation of pathogenic memories. Neuroepigenetics 2015, 1:28-33.
80. Saab B.J., Mansuy I.M. Neuroepigenetics of memory formation and impairment: the role of microRNAs. Neuropharmacology 2014, 80:61-69.
81. 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.
82. Belmont A. Dynamics of chromatin, proteins, and bodies within the cell nucleus. Curr. Opin. Cell Biol. 2003, 15:304-310.
83. Branco M.R., et al. Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat. Rev. Genet. 2012, 13:7-13.
84. Lister R., et al. Global epigenomic reconfiguration during mammalian brain development. Science 2013, 341:1237905.
85. Cooper D.N., Krawczak M. Cytosine methylation and the fate of CpG dinucleotides in vertebrate genomes. Hum. Genet. 1989, 83:181-188.
86. Bird A.P. CpG-rich islands and the function of DNA methylation. Nature 1986, 321:209-213.
87. Saxonov S., et al. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:1412-1417.
88. Prendergast G.C., Ziff E.B. Methylation-sensitive sequence-specific DNA binding by the c-Myc basic region. Science 1991, 251:186-189.
89. Comb M., Goodman H.M. CpG methylation inhibits proenkephalin gene expression and binding of the transcription factor AP-2. Nucleic Acids Res. 1990, 18:3975-3982.
90. Baubec T., et al. Methylation-dependent and -independent genomic targeting principles of the MBD protein family. Cell 2013, 153:480-492.
91. Smith Z.D., Meissner A. DNA methylation: roles in mammalian development. Nat. Rev. Genet. 2013, 14:204-220.
92. Gruenbaum Y., et al. Substrate and sequence specificity of a eukaryotic DNA methylase. Nature 1982, 295:620-622.
93. Okano M., et al. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 1999, 99:247-257.
94. Wu S.C., Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol. 2010, 11:607-620.
95. Jack A., et al. DNA methylation of the oxytocin receptor gene predicts neural response to ambiguous social stimuli. Front. Hum. Neurosci. 2012, 6:280.
96. Walton E., et al. MB-COMT promoter DNA methylation is associated with working-memory processing in schizophrenia patients and healthy controls. Epigenetics 2014, 9:1101-1107.
97. Puglia M.H., et al. Epigenetic modification of the oxytocin receptor gene influences the perception of anger and fear in the human brain. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:3308-3313.
98. Frodl T., et al. DNA methylation of the serotonin transporter gene (SLC6A4) is associated with brain function involved in processing emotional stimuli. J. Psychiatry Neurosci. 2015, 40:140180.
99. Ziegler C., et al. Oxytocin receptor gene methylation: converging multilevel evidence for a role in social anxiety. Neuropsychopharmacology 2015, 40:1528-1538.
100. Klengel T., et al. Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions. Nat. Neurosci. 2013, 16:33-41.
101. Dannlowski U., et al. Serotonin transporter gene methylation is associated with hippocampal gray matter volume. Hum. Brain Mapp. 2014, 35:5356-5367.
102. Choi S., et al. Association of brain-derived neurotrophic factor DNA methylation and reduced white matter integrity in the anterior corona radiata in major depression. J. Affect. Disord. 2014, 172C:74-80.
103. Booij L., et al. DNA methylation of the serotonin transporter gene in peripheral cells and stress-related changes in hippocampal volume: a study in depressed patients and healthy controls. PLoS ONE 2015, 10:e0119061.
104. Talens R.P., et al. Variation, patterns, and temporal stability of DNA methylation: considerations for epigenetic epidemiology. FASEB J. 2010, 24:3135-3144.