Spatial genome organization and cognition

Nature Reviews Neuroscience

Volumn 17, Issue 11, 2016, Pages 681-691

  Rajarajan, Prashanth ^a   Gil, Sergio Espeso ^b,c   Brennand, Kristen J ^a   Akbarian, Schahram ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b BARCELONA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Spain)

^c UNIVERSITAT POMPEU FABRA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; SCAFFOLD PROTEIN; DNA BINDING PROTEIN; UNTRANSLATED RNA;

AUTISM; CELL ACTIVITY; CELL PLASTICITY; CHROMATIN; CHROMOSOME; COGNITION; ENHANCER REGION; GENE SEQUENCE; GENOME ANALYSIS; HUMAN; MENTAL DISEASE; ONSET AGE; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; SPATIAL ANALYSIS; ANIMAL; DNA METHYLATION; GENETICS; GENOME; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; COGNITION; DNA METHYLATION; DNA-BINDING PROTEINS; GENOME; HUMANS; NEURODEVELOPMENTAL DISORDERS; NEURONS; RNA, UNTRANSLATED;

EID: 84990201140     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn.2016.124     Document Type: Review

References (119)

1. Stamatoyannopoulos, J. A. What does our genome encode? Genome Res. 22, 1602-1611 (2012
2. Loviglio, M. N., et al. Chromosomal contacts connect loci associated with autism, BMI and head circumference phenotypes. Mol. Psychiatry http://dx. doi.org/10.1038/mp.2016.84 (2016
3. Roussos, P., et al. A role for noncoding variation in schizophrenia. Cell Rep. 9, 1417-1429 (2014
4. Lieberman-Aiden, E., et al. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293 (2009
5. Rao, S. S., et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665-1680 (2014
6. Padeken, J., & Heun, P. Nucleolus and nuclear periphery: velcro for heterochromatin. Curr. Opin. Cell Biol. 28, 54-60 (2014
7. Nasmyth, K., & Haering, C. H. Cohesin: its roles and mechanisms. Annu. Rev. Genet. 43, 525-558 (2009
8. Wendt, K. S., et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451, 796-801 (2008
9. Dowen, J. M., et al. Control of cell identity genes occurs in insulated neighborhoods in mammalian chromosomes. Cell 159, 374-387 (2014
10. Vietri Rudan, M., et al. Comparative Hi C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep. 10, 1297-1309 (2015
11. Guo, Y., et al. CRISPR inversion of CTCF sites alters genome topology and enhancer/promoter function. Cell 162, 900-910 (2015
12. Vernimmen, D., & Bickmore, W. A. The hierarchy of transcriptional activation: from enhancer to promoter. Trends Genet. 31, 696-708 (2015
13. Zhou, V. W., Goren, A., & Bernstein, B. E. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 12, 7-18 (2011
14. Ruthenburg, A. J., Allis, C. D., & Wysocka, J. Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. Mol. Cell 25, 15-30 (2007
15. Hatzis, P., & Talianidis, I. Dynamics of enhancer-promoter communication during differentiation-induced gene activation. Mol. Cell 10, 1467-1477 (2002
16. Mueller-Storm, H. P., Sogo, J. M., & Schaffner, W. An enhancer stimulates transcription in trans when attached to the promoter via a protein bridge. Cell 58, 767-777 (1989
17. Gorkin, D. U., Leung, D., & Ren, B. The 3D genome in transcriptional regulation and pluripotency. Cell Stem Cell 14, 762-775 (2014
18. Kagey, M. H., et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 467, 430-435 (2010
19. Frank, C. L., et al. Regulation of chromatin accessibility and Zic binding at enhancers in the developing cerebellum. Nat. Neurosci. 18, 647-656 (2015
20. Sanyal, A., Lajoie, B. R., Jain, G., & Dekker, J. The long-range interaction landscape of gene promoters. Nature 489, 109-113 (2012
21. Jin, F., et al. A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature 503, 290-294 (2013
22. Andersson, R., et al. An atlas of active enhancers across human cell types and tissues. Nature 507, 455-461 (2014
23. Bharadwaj, R., et al. Conserved higher-order chromatin regulates NMDA receptor gene expression and cognition. Neuron 84, 997-1008 (2014
24. Bharadwaj, R., et al. Conserved chromosome 2q31 conformations are associated with transcriptional regulation of GAD1 GABA synthesis enzyme and altered in prefrontal cortex of subjects with schizophrenia. J. Neurosci. 33, 11839-11851 (2013
25. Joo, J. Y., Schaukowitch, K., Farbiak, L., Kilaru, G., & Kim, T. K. Stimulus-specific combinatorial functionality of neuronal c fos enhancers. Nat. Neurosci. 19, 75-83 (2016
26. Shepherd, J. D., & Bear, M. F. New views of Arc, a master regulator of synaptic plasticity. Nat. Neurosci. 14, 279-284 (2011
27. Schaukowitch, K., et al. Enhancer RNA facilitates NELF release from immediate early genes. Mol. Cell 56, 29-42 (2014
28. Madabhushi, R., et al. Activity-induced DNA breaks govern the expression of neuronal early-response genes. Cell 161, 1592-1605 (2015
29. Kim, T. K., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 465, 182-187 (2010
30. Camps, J., Erdos, M. R., & Ried, T. The role of lamin B1 for the maintenance of nuclear structure and function. Nucleus 6, 8-14 (2015
31. Peric-Hupkes, D., et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol. Cell 38, 603-613 (2010
32. Yoon, K. H., et al. Olfactory receptor genes expressed in distinct lineages are sequestered in different nuclear compartments. Proc. Natl Acad. Sci. USA 112, E2403-E2409 (2015
33. Monahan, K., & Lomvardas, S. Monoallelic expression of olfactory receptors. Annu. Rev. Cell Dev. Biol. 31, 721-740 (2015
34. Boyle, M. I., Jespersgaard, C., Brondum-Nielsen, K., Bisgaard, A. M., & Tumer, Z. Cornelia De Lange syndrome. Clin. Genet. 88, 1-12 (2015
35. Yan, J., et al. Genomic duplication resulting in increased copy number of genes encoding the sister chromatid cohesion complex conveys clinical consequences distinct from Cornelia De Lange. J. Med. Genet. 46, 626-634 (2009
36. Finnsson, J., Sundblom, J., Dahl, N., Melberg, A., & Raininko, R. LMNB1 related autosomal-dominant leukodystrophy: clinical and radiological course. Ann. Neurol. 78, 412-425 (2015
37. Nolen, L. D., Boyle, S., Ansari, M., Pritchard, E., & Bickmore, W. A. Regional chromatin decompaction in Cornelia De Lange syndrome associated with NIPBL disruption can be uncoupled from cohesin and CTCF. Hum. Mol. Genet. 22, 4180-4193 (2013
38. Watson, L. A., et al. Dual effect of CTCF loss on neuroprogenitor differentiation and survival. J. Neurosci. 34, 2860-2870 (2014
39. Gregor, A., et al. De novo mutations in the genome organizer CTCF cause intellectual disability. Am. J. Hum. Genet. 93, 124-131 (2013
40. Hirayama, T., Tarusawa, E., Yoshimura, Y., Galjart, N., & Yagi, T. CTCF is required for neural development and stochastic expression of clustered Pcdh genes in neurons. Cell Rep. 2, 345-357 (2012
41. Cai, S., Lee, C. C., & Kohwi-Shigematsu, T. SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat. Genet. 38, 1278-1288 (2006
42. Britanova, O., Akopov, S., Lukyanov, S., Gruss, P., & Tarabykin, V. Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur. J. Neurosci. 21, 658-668 (2005
43. Docker, D., et al. Further delineation of the SATB2 phenotype. Eur. J. Hum. Genet. 22, 1034-1039 (2014
44. Alcamo, E. A., et al. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57, 364-377 (2008
45. Leoyklang, P., et al. Heterozygous nonsense mutation SATB2 associated with cleft palate, osteoporosis, and cognitive defects. Hum. Mutat. 28, 732-738 (2007
46. Close, J., et al. Satb1 is an activity-modulated transcription factor required for the terminal differentiation and connectivity of medial ganglionic eminence-derived cortical interneurons. J. Neurosci. 32, 17690-17705 (2012
47. Denaxa, M., et al. Maturation-promoting activity of SATB1 in MGE-derived cortical interneurons. Cell Rep. 2, 1351-1362 (2012
48. Kernohan, K. D., Vernimmen, D., Gloor, G. B., & Berube, N. G. Analysis of neonatal brain lacking ATRX or MeCP2 reveals changes in nucleosome density, CTCF binding and chromatin looping. Nucleic Acids Res. 42, 8356-8368 (2014
49. Horike, S., Cai, S., Miyano, M., Cheng, J. F., & Kohwi-Shigematsu, T. Loss of silent-chromatin looping and impaired imprinting of DLX5 in Rett syndrome. Nat. Genet. 37, 31-40 (2005
50. Schule, B., Li, H. H., Fisch-Kohl, C., Purmann, C., & Francke, U. DLX5 and DLX6 expression is biallelic and not modulated by MeCP2 deficiency. Am. J. Hum. Genet. 81, 492-506 (2007
51. Nan, X., et al. Interaction between chromatin proteins MECP2 and ATRX is disrupted by mutations that cause inherited mental retardation. Proc. Natl Acad. Sci. USA 104, 2709-2714 (2007
52. Jakovcevski, M., & Akbarian, S. Epigenetic mechanisms in neurological disease. Nat. Med. 18, 1194-1204 (2012
53. Turner, T. N., et al. Genome sequencing of autism-affected families reveals disruption of putative noncoding regulatory DNA. Am. J. Hum. Genet. 98, 58-74 (2016
54. Dekker, J., Marti-Renom, M. A., & Mirny, L. A. Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data. Nat. Rev. Genet. 14, 390-403 (2013
55. Bergeron, K. F., et al. Male-biased aganglionic megacolon in the TashT mouse line due to perturbation of silencer elements in a large gene desert of chromosome 10. PLoS Genet. 11, e1005093 (2015
56. De la Torre-Ubieta, L., Won, H., Stein, J. L., & Geschwind, D. H. Advancing the understanding of autism disease mechanisms through genetics. Nat. Med. 22, 345-361 (2016
57. Yao, P., et al. Coexpression networks identify brain region-specific enhancer RNAs in the human brain. Nat. Neurosci. 18, 1168-1174 (2015
58. Gusev, A., et al. Partitioning heritability of regulatory and cell-type-specific variants across 11 common diseases. Am. J. Hum. Genet. 95, 535-552 (2014
59. Cross-Disorder Group of the Psychiatric Genomics Consortium. Identification of risk loci with shared effects on five major psychiatric disorders: a genome-wide analysis. Lancet 381, 1371-1379, (2013
60. Nagy, C., et al. Astrocytic abnormalities and global DNA methylation patterns in depression and suicide. Mol. Psychiatry 20, 320-328 (2015
61. Jaffe, A. E., et al. Mapping DNA methylation across development, genotype and schizophrenia in the human frontal cortex. Nat. Neurosci. 19, 40-47 (2016
62. Roussos, P., et al. The relationship of common risk variants and polygenic risk for schizophrenia to sensorimotor gating. Biol. Psychiatry 79, 988-996 (2015
63. Gjoneska, E., et al. Conserved epigenomic signals in mice and humans reveal immune basis of Alzheimer's disease. Nature 518, 365-369 (2015
64. Frost, B., Bardai, F. H., & Feany, M. B. Lamin dysfunction mediates neurodegeneration in tauopathies. Curr. Biol. 26, 129-136 (2016
65. Frost, B., Hemberg, M., Lewis, J., & Feany, M. B. Tau promotes neurodegeneration through global chromatin relaxation. Nat. Neurosci. 17, 357-366 (2014
66. Psych, E. C., et al. The PsychENCODE project. Nat. Neurosci. 18, 1707-1712 (2015
67. Mitchell, A. C., et al. The genome in three dimensions: a new frontier in human brain research. Biol. Psychiatry 75, 961-969 (2014
68. Huang, H. S., et al. Prefrontal dysfunction in schizophrenia involves mixed-lineage leukemia 1 regulated histone methylation at GABAergic gene promoters. J. Neurosci. 27, 11254-11262 (2007
69. Rocco, B. R., Lewis, D. A., & Fish, K. N. Markedly lower glutamic acid decarboxylase 67 protein levels in a subset of boutons in schizophrenia. Biol. Psychiatry 79,1006-1015 (2015
70. Lewis, D. A. Inhibitory neurons in human cortical circuits: substrate for cognitive dysfunction in schizophrenia. Curr. Opin. Neurobiol. 26, 22-26 (2014
71. Shulha, H. P., et al. Human-specific histone methylation signatures at transcription start sites in prefrontal neurons. PLoS Biol. 10, e1001427 (2012
72. Talkowski, M. E., et al. Sequencing chromosomal abnormalities reveals neurodevelopmental loci that confer risk across diagnostic boundaries. Cell 149, 525-537 (2012
73. Epi, K. C., et al. De novo mutations in epileptic encephalopathies. Nature 501, 217-221 (2013
74. Hamdan, F. F., et al. De novo mutations in moderate or severe intellectual disability. PLoS Genet. 10, e1004772 (2014
75. O'Roak, B. J., et al. Exome sequencing in sporadic autism spectrum disorders identifies severe De novo mutations. Nat. Genet. 43, 585-589 (2011
76. Jiang, Y., et al. Setdb1 histone methyltransferase regulates mood-related behaviors and expression of the NMDA receptor subunit NR2B. J. Neurosci. 30, 7152-7167 (2010
77. Taubenfeld, S. M., Milekic, M. H., Monti, B., & Alberini, C. M. The consolidation of new but not reactivated memory requires hippocampal C/EBPβ. Nat. Neurosci. 4, 813-818 (2001
78. Taubenfeld, S. M., et al. Fornix-dependent induction of hippocampal CCAAT enhancer-binding protein β and d co localizes with phosphorylated cAMP response element-binding protein and accompanies long-term memory consolidation. J. Neurosci. 21, 84-91 (2001
79. Merhav, M., et al. Behavioral interference and C/EBPβ expression in the insular-cortex reveal a prolonged time period for taste memory consolidation. Learn. Mem. 13, 571-574 (2006
80. Dickel, D. E., Visel, A., & Pennacchio, L. A. Functional anatomy of distant-acting mammalian enhancers. Phil. Trans. R. Soc. B 368, 20120359 (2013
81. Stampfel, G., et al. Transcriptional regulators form diverse groups with context-dependent regulatory functions. Nature 528, 147-151 (2015
82. Valor, L. M., Viosca, J., Lopez-Atalaya, J. P., & Barco, A. Lysine acetyltransferases CBP and p300 as therapeutic targets in cognitive and neurodegenerative disorders. Curr. Pharm. Des. 19, 5051-5064 (2013
83. Tsai, L. H., & Graff, J. On the resilience of remote traumatic memories against exposure therapy-mediated attenuation. EMBO Rep. 15, 853-861 (2014
84. Schroeder, F. A., Lin, C. L., Crusio, W. E., & Akbarian, S. Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol. Psychiatry 62, 55-64 (2007
85. Covington, H. E. III, Maze, I., Vialou, V., & Nestler, E. J. Antidepressant action of HDAC inhibition in the prefrontal cortex. Neuroscience 298, 329-335 (2015
86. Maze, I., et al. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327, 213-216 (2010
87. Huang, H. S., et al. Topoisomerase inhibitors unsilence the dormant allele of Ube3a in neurons. Nature 481, 185-189 (2012
88. Day, J. J., Kennedy, A. J., & Sweatt, J. D. DNA methylation and its implications and accessibility for neuropsychiatric therapeutics. Annu. Rev. Pharmacol. Toxicol. 55, 591-611 (2015
89. Halder, R., et al. DNA methylation changes in plasticity genes accompany the formation and maintenance of memory. Nat. Neurosci. 19, 102-110 (2016
90. Zink, D., et al. Transcription-dependent spatial arrangements of CFTR and adjacent genes in human cell nuclei. J. Cell Biol. 166, 815-825 (2004
91. Pickersgill, H., et al. Characterization of the Drosophila melanogaster genome at the nuclear lamina. Nat. Genet. 38, 1005-1014 (2006
92. Krivega, I., et al. Inhibition of G9a methyltransferase stimulates fetal hemoglobin production by facilitating LCR/γ-globin looping. Blood 126, 665-672 (2015
93. Hasan, A., Mitchell, A., Schneider, A., Halene, T., & Akbarian, S. Epigenetic dysregulation in schizophrenia: molecular and clinical aspects of histone deacetylase inhibitors. Eur. Arch. Psychiatry Clin. Neurosci. 263, 273-284 (2013
94. Laganiere, J., et al. An engineered zinc finger protein activator of the endogenous glial cell line-derived neurotrophic factor gene provides functional neuroprotection in a rat model of Parkinson's disease. J. Neurosci. 30, 16469-16474 (2010
95. Heller, E. A., et al. Locus-specific epigenetic remodeling controls addiction-and depression-related behaviors. Nat. Neurosci. 17, 1720-1727 (2014
96. Hilton, I. B., et al. Epigenome editing by a CRISPR Cas9 based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol. 33, 510-517 (2015
97. Cho, S. W., Kim, S., Kim, J. M., & Kim, J. S. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat. Biotechnol. 31, 230-232 (2013
98. Cong, L., et al. Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823 (2013
99. Tai, D. J., et al. Engineering microdeletions and microduplications by targeting segmental duplications with CRISPR. Nat. Neurosci. 19, 517-522 (2016
100. Jiang, W., Bikard, D., Cox, D., Zhang, F., & Marraffini, L. A. RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat. Biotechnol. 31, 233-239 (2013
101. Maeder, M. L., et al. CRISPR RNA-guided activation of endogenous human genes. Nat. Methods 10, 977-979 (2013
102. Perez-Pinera, P., et al. RNA-guided gene activation by CRISPR Cas9 based transcription factors. Nat. Methods 10, 973-976 (2013
103. Cheng, A. W., et al. Multiplexed activation of endogenous genes by CRISPR on, an RNA-guided transcriptional activator system. Cell Res. 23, 1 163-1171 (2013
104. Larson, M. H., et al. CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat. Protoc. 8, 2180-2196 (2013
105. Hsu, P. D., Lander, E. S., & Zhang, F. Development and applications of CRISPR Cas9 for genome engineering. Cell 157, 1262-1278 (2014
106. Li, M., Suzuki, K., Kim, N. Y., Liu, G. H., & Izpisua Belmonte, J. C. A cut above the rest: targeted genome editing technologies in human pluripotent stem cells. J. Biol. Chem. 289, 4594-4599 (2014
107. Hotta, A., & Yamanaka, S. From genomics to gene therapy: induced pluripotent stem cells meet genome editing. Annu. Rev. Genet. 49, 47-70 (2015
108. Ding, Q., et al. A TALEN genome-editing system for generating human stem cell-based disease models. Cell Stem Cell 12, 238-251 (2013
109. Martinez, R. A., et al. Genome engineering of isogenic human ES cells to model autism disorders. Nucleic Acids Res. 43, e65 (2015
110. Wen, Z., et al. Synaptic dysregulation in a human iPS cell model of mental disorders. Nature 515, 414-418 (2014
111. Chen, H., et al. Modeling ALS with iPSCs reveals that mutant SOD1 misregulates neurofilament balance in motor neurons. Cell Stem Cell 14, 796-809 (2014
112. Liu, G. H., et al. Progressive degeneration of human neural stem cells caused by pathogenic LRRK2. Nature 491, 603-607 (2012
113. Soldner, F., et al. Parkinson-associated risk variant in distal enhancer of α-synuclein modulates target gene expression. Nature 533, 95-99 (2016
114. Ochiai, H., Sugawara, T., & Yamamoto, T. Simultaneous live imaging of the transcription and nuclear position of specific genes. Nucleic Acids Res. 43, e127 (2015
115. Fudenberg, G., & Mirny, L. A. Higher-order chromatin structure: bridging physics and biology. Curr. Opin. Genet. Dev. 22, 115-124 (2012
116. Rippe, K. Making contacts on a nucleic acid polymer. Trends Biochem. Sci. 26, 733-740 (2001
117. Williamson, I., et al. Spatial genome organization: contrasting views from chromosome conformation capture and fluorescence in situ hybridization. Genes Dev. 28, 2778-2791 (2014
118. Yang, J., & Corces, V. G. Chromatin insulators: a role in nuclear organization and gene expression. Adv. Cancer Res. 110, 43-76 (2011
119. Phillips-Cremins, J. E., et al. Architectural protein subclasses shape 3D organization of genomes during lineage commitment. Cell 153, 1281-1295 (2013