From trans to cis: Transcriptional regulatory networks in neocortical development

Trends in Genetics

Volumn 31, Issue 2, 2015, Pages 77-87

  Shibata, Mikihito ^a   Gulden, Forrest O ^a   Sestan, Nenad ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Chromatin; Cis regulatory element; Disease; Epigenetics; Gene expression; Neuron; Transcription factor

Indexed keywords

CIS ACTING ELEMENT; TRANSCRIPTION FACTOR;

BRAIN CORTEX; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; GENE EXPRESSION; GENE REGULATORY NETWORK; HUMAN; MENTAL DISEASE; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; REVIEW; ANIMAL; CELL MOTION; CYTOLOGY; EMBRYOLOGY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; GLIA; METABOLISM; NEOCORTEX; NERVE CELL; NERVE CELL NETWORK; REGULATORY SEQUENCE;

ANIMALS; CELL DIFFERENTIATION; CELL MOVEMENT; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HUMANS; MENTAL DISORDERS; NEOCORTEX; NERVE NET; NERVOUS SYSTEM DISEASES; NEUROGENESIS; NEUROGLIA; NEURONS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSCRIPTION, GENETIC;

EID: 84921714149     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2014.12.004     Document Type: Review

References (136)

1. Levine M., Davidson E.H. Gene regulatory networks for development. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:4936-4942.
2. Lee T.I., Young R.A. Transcriptional regulation and its misregulation in disease. Cell 2013, 152:1237-1251.
3. Spitz F., Duboule D. Global control regions and regulatory landscapes in vertebrate development and evolution. Adv. Genet. 2008, 61:175-205.
4. Vaquerizas J.M., et al. A census of human transcription factors: function, expression and evolution. Nat. Rev. Genet. 2009, 10:252-263.
5. Spitz F., Furlong E.E. Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 2012, 13:613-626.
6. Pennacchio L.A., et al. Enhancers: five essential questions. Nat. Rev. Genet. 2013, 14:288-295.
7. Barski A., et al. High-resolution profiling of histone methylations in the human genome. Cell 2007, 129:823-837.
8. Hardison R.C., Taylor J. Genomic approaches towards finding cis-regulatory modules in animals. Nat. Rev. Genet. 2012, 13:469-483.
9. Wittkopp P.J., Kalay G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 2012, 13:59-69.
10. Nord A.S., et al. Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell 2013, 155:1521-1531.
11. Son E.Y., Crabtree G.R. The role of BAF (mSWI/SNF) complexes in mammalian neural development. Am. J. Med. Genet. C: Semin. Med. Genet. 2014, 166C:333-349.
12. Maurano M.T., et al. Systematic localization of common disease-associated variation in regulatory DNA. Science 2012, 337:1190-1195.
13. Babu M.M., et al. Structure and evolution of transcriptional regulatory networks. Curr. Opin. Struct. Biol. 2004, 14:283-291.
14. Florio M., Huttner W.B. Neural progenitors, neurogenesis and the evolution of the neocortex. Development 2014, 141:2182-2194.
15. Lui J.H., et al. Development and evolution of the human neocortex. Cell 2011, 146:18-36.
16. Hill R.S., Walsh C.A. Molecular insights into human brain evolution. Nature 2005, 437:64-67.
17. Rubenstein J.L. Annual Research Review: Development of the cerebral cortex: implications for neurodevelopmental disorders. J. Child Psychol. Psychiatry 2011, 52:339-355.
18. Kwan K.Y., et al. Transcriptional co-regulation of neuronal migration and laminar identity in the neocortex. Development 2012, 139:1535-1546.
19. Greig L.C., et al. Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 2013, 14:755-769.
20. Leone D.P., et al. The determination of projection neuron identity in the developing cerebral cortex. Curr. Opin. Neurobiol. 2008, 18:28-35.
21. Wonders C.P., Anderson S.A. The origin and specification of cortical interneurons. Nat. Rev. Neurosci. 2006, 7:687-696.
22. Kepecs A., Fishell G. Interneuron cell types are fit to function. Nature 2014, 505:318-326.
23. Han W., et al. TBR1 directly represses Fezf2 to control the laminar origin and development of the corticospinal tract. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:3041-3306.
24. Gallo V., Deneen B. Glial development: the crossroads of regeneration and repair in the CNS. Neuron 2014, 83:283-308.
25. Yoshida M., et al. Emx1 and Emx2 functions in development of dorsal telencephalon. Development 1997, 124:101-111.
26. Hanashima C., et al. Brain factor-1 controls the proliferation and differentiation of neocortical progenitor cells through independent mechanisms. J. Neurosci. 2002, 22:6526-6536.
27. Chou S.J., O'Leary D.D. Role for Lhx2 in corticogenesis through regulation of progenitor differentiation. Mol. Cell. Neurosci. 2013, 56:1-9.
28. Imayoshi I., et al. Essential roles of Notch signaling in maintenance of neural stem cells in developing and adult brains. J. Neurosci. 2010, 30:3489-3498.
29. Quinn J.C., et al. Pax6 controls cerebral cortical cell number by regulating exit from the cell cycle and specifies cortical cell identity by a cell autonomous mechanism. Dev. Biol. 2007, 302:50-65.
30. Yun K., et al. Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 2004, 131:5441-5448.
31. Schuurmans C., et al. Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways. EMBO J. 2004, 23:2892-2902.
32. Guo C., et al. Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron 2013, 80:1167-1174.
33. Pinto L., et al. AP2gamma regulates basal progenitor fate in a region- and layer-specific manner in the developing cortex. Nat. Neurosci. 2009, 12:1229-1237.
34. Sugitani Y., et al. Brn-1 and Brn-2 share crucial roles in the production and positioning of mouse neocortical neurons. Genes Dev. 2002, 16:1760-1765.
35. Cubelos B., et al. Cux-1 and Cux-2 control the development of Reelin expressing cortical interneurons. Dev. Neurobiol. 2008, 68:917-925.
36. Sessa A., et al. Tbr2 directs conversion of radial glia into basal precursors and guides neuronal amplification by indirect neurogenesis in the developing neocortex. Neuron 2008, 60:56-69.
37. Farkas L.M., et al. Insulinoma-associated 1 has a panneurogenic role and promotes the generation and expansion of basal progenitors in the developing mouse neocortex. Neuron 2008, 60:40-55.
38. Britz O., et al. A role for proneural genes in the maturation of cortical progenitor cells. Cereb. Cortex 2006, 16(Suppl. 1):138-151.
39. Scardigli R., et al. Direct and concentration-dependent regulation of the proneural gene Neurogenin2 by Pax6. Development 2003, 130:3269-3281.
40. Sansom S.N., et al. The level of the transcription factor Pax6 is essential for controlling the balance between neural stem cell self-renewal and neurogenesis. PLoS Genet. 2009, 5:e1000511.
41. Shimizu T., et al. Zinc finger genes Fezf1 and Fezf2 control neuronal differentiation by repressing Hes5 expression in the forebrain. Development 2010, 137:1875-1885.
42. Tuoc T.C., et al. Chromatin regulation by BAF170 controls cerebral cortical size and thickness. Dev. Cell 2013, 25:256-269.
43. Ninkovic J., et al. The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network. Cell Stem Cell 2013, 13:403-418.
44. Nowakowski T.J., et al. MicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:7056-7061.
45. Shibata M., et al. MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J. Neurosci. 2011, 31:3407-3422.
46. Takizawa T., et al. DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev. Cell 2001, 1:749-758.
47. Sun Y., et al. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 2001, 104:365-376.
48. Namihira M., et al. Committed neuronal precursors confer astrocytic potential on residual neural precursor cells. Dev. Cell 2009, 16:245-255.
49. Li H., et al. Two-tier transcriptional control of oligodendrocyte differentiation. Curr. Opin. Neurobiol. 2009, 19:479-485.
50. Rowitch D.H., Kriegstein A.R. Developmental genetics of vertebrate glial-cell specification. Nature 2010, 468:214-222.
51. Petryniak M.A., et al. Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron 2007, 55:417-433.
52. Silbereis J.C., et al. Olig1 function is required to repress dlx1/2 and interneuron production in Mammalian brain. Neuron 2014, 81:574-587.
53. Hand R., et al. Phosphorylation of Neurogenin2 specifies the migration properties and the dendritic morphology of pyramidal neurons in the neocortex. Neuron 2005, 48:45-62.
54. Kwan K.Y., et al. SOX5 postmitotically regulates migration, postmigratory differentiation, and projections of subplate and deep-layer neocortical neurons. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:16021-21606.
55. McEvilly R.J., et al. Transcriptional regulation of cortical neuron migration by POU domain factors. Science 2002, 295:1528-1532.
56. Nakamura K., et al. In vivo function of Rnd2 in the development of neocortical pyramidal neurons. Neurosci. Res. 2006, 54:149-153.
57. Heng J.I., et al. Neurogenin 2 controls cortical neuron migration through regulation of Rnd2. Nature 2008, 455:114-118.
58. Heng J.I., et al. The zinc finger transcription factor RP58 negatively regulates Rnd2 for the control of neuronal migration during cerebral cortical development. Cereb. Cortex 2013, Published online October 1, 2013. http://dx.doi.org/10.1093/cercor/bht277.
59. Ohtaka-Maruyama C., et al. RP58 regulates the multipolar-bipolar transition of newborn neurons in the developing cerebral cortex. Cell Rep. 2013, 3:458-471.
60. Ohtaka-Maruyama C., et al. The 5'-flanking region of the RP58 coding sequence shows prominent promoter activity in multipolar cells in the subventricular zone during corticogenesis. Neuroscience 2012, 201:67-84.
61. Xiang C., et al. RP58/ZNF238 directly modulates proneurogenic gene levels and is required for neuronal differentiation and brain expansion. Cell Death Differ. 2012, 19:692-702.
62. Alcamo E.A., et al. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 2008, 57:364-377.
63. Britanova O., et al. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 2008, 57:378-392.
64. Hevner R.F., et al. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 2001, 29:353-366.
65. Bedogni F., et al. Tbr1 regulates regional and laminar identity of postmitotic neurons in developing neocortex. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:13129-13134.
66. Molyneaux B.J., et al. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 2005, 47:817-831.
67. Chen B., et al. Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17184-17189.
68. Chen J.G., et al. Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:17792-17797.
69. Shim S., et al. Cis-regulatory control of corticospinal system development and evolution. Nature 2012, 486:74-79.
70. Srinivasan K., et al. A network of genetic repression and derepression specifies projection fates in the developing neocortex. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:19071-19078.
71. Lai T., et al. SOX5 controls the sequential generation of distinct corticofugal neuron subtypes. Neuron 2008, 57:232-247.
72. Arlotta P., et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 2005, 45:207-221.
73. McKenna W.L., et al. Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J. Neurosci. 2011, 31:549-564.
74. Tashiro K., et al. A mammalian conserved element derived from SINE displays enhancer properties recapitulating Satb2 expression in early-born callosal projection neurons. PLoS ONE 2011, 6:e28497.
75. Toma K., et al. The timing of upper-layer neurogenesis is conferred by sequential derepression and negative feedback from deep-layer neurons. J. Neurosci. 2014, 34:13259-13276.
76. Sparmann A., van Lohuizen M. Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer 2006, 6:846-856.
77. Kadoch C., et al. Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet. 2013, 45:592-601.
78. Buttner N., et al. Af9/Mllt3 interferes with Tbr1 expression through epigenetic modification of histone H3K79 during development of the cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:7042-7047.
79. Gyorgy A.B., et al. SATB2 interacts with chromatin-remodeling molecules in differentiating cortical neurons. Eur. J. Neurosci. 2008, 27:865-873.
80. Yu Y., et al. Olig2 targets chromatin remodelers to enhancers to initiate oligodendrocyte differentiation. Cell 2013, 152:248-261.
81. Namihira M., Nakashima K. Mechanisms of astrocytogenesis in the mammalian brain. Curr. Opin. Neurobiol. 2013, 23:921-927.
82. Azim E., et al. SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat. Neurosci. 2009, 12:1238-1247.
83. Batista-Brito R., et al. The cell-intrinsic requirement of Sox6 for cortical interneuron development. Neuron 2009, 63:466-481.
84. Ghanem N., et al. Distinct cis-regulatory elements from the Dlx1/Dlx2 locus mark different progenitor cell populations in the ganglionic eminences and different subtypes of adult cortical interneurons. J. Neurosci. 2007, 27:5012-5022.
85. Malik A.N., et al. Genome-wide identification and characterization of functional neuronal activity-dependent enhancers. Nat. Neurosci. 2014, 17:1330-1339.
86. West A.E., Greenberg M.E. Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb. Perspect. Biol. 2011, 3:a005744.
87. Pruunsild P., et al. Identification of cis-elements and transcription factors regulating neuronal activity-dependent transcription of human BDNF gene. J. Neurosci. 2011, 31:3295-3308.
88. Kim T.K., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
89. Clark A.G., et al. Inferring nonneutral evolution from human-chimp-mouse orthologous gene trios. Science 2003, 302:1960-1963.
90. Nielsen R., et al. A scan for positively selected genes in the genomes of humans and chimpanzees. PLoS Biol. 2005, 3:e170.
91. Bustamante C.D., et al. Natural selection on protein-coding genes in the human genome. Nature 2005, 437:1153-1157.
92. McLean C.Y., et al. Human-specific loss of regulatory DNA and the evolution of human-specific traits. Nature 2011, 471:216-219.
93. Prabhakar S., et al. Accelerated evolution of conserved noncoding sequences in humans. Science 2006, 314:786.
94. King M.C., Wilson A.C. Evolution at two levels in humans and chimpanzees. Science 1975, 188:107-116.
95. Haygood R., et al. Promoter regions of many neural- and nutrition-related genes have experienced positive selection during human evolution. Nat. Genet. 2007, 39:1140-1144.
96. Visel A., et al. A high-resolution enhancer atlas of the developing telencephalon. Cell 2013, 152:895-908.
97. Pattabiraman K., et al. Transcriptional regulation of enhancers active in protodomains of the developing cerebral cortex. Neuron 2014, 82:989-1003.
98. Kwan K.Y., et al. Species-dependent posttranscriptional regulation of NOS1 by FMRP in the developing cerebral cortex. Cell 2012, 149:899-911.
99. Iossifov I., et al. The contribution of de novo coding mutations to autism spectrum disorder. Nature 2014, 515:216-221.
100. Talkowski M.E., et al. Sequencing chromosomal abnormalities reveals neurodevelopmental loci that confer risk across diagnostic boundaries. Cell 2012, 149:525-537.
101. Rosenfeld J.A., et al. Small deletions of SATB2 cause some of the clinical features of the 2q33.1 microdeletion syndrome. PLoS ONE 2009, 4:e6568.
102. Lamb A.N., et al. Haploinsufficiency of SOX5 at 12p12.1 is associated with developmental delays with prominent language delay, behavior problems, and mild dysmorphic features. Hum. Mutat. 2012, 33:728-740.
103. Sanders S.J., et al. De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature 2012, 485:237-241.
104. Willsey A.J., et al. Coexpression networks implicate human midfetal deep cortical projection neurons in the pathogenesis of autism. Cell 2013, 155:997-1007.
105. Kang H.J., et al. Spatio-temporal transcriptome of the human brain. Nature 2011, 478:483-489.
106. Colantuoni C., et al. Temporal dynamics and genetic control of transcription in the human prefrontal cortex. Nature 2011, 478:519-523.
107. Ramasamy A., et al. Genetic variability in the regulation of gene expression in ten regions of the human brain. Nat. Neurosci. 2014, 17:1418-1428.
108. Genome-wide association study identifies five new schizophrenia loci. Nat. Genet. 2011, 43:969-976. Schizophrenia Psychiatric Genome-Wide Association Study.
109. Vernot B., et al. Personal and population genomics of human regulatory variation. Genome Res. 2012, 22:1689-1697.
110. Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4. Nat. Genet. 2011, 43:977-983. Psychiatric GWAS Consortium Bipolar Disorder Working Group.
111. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 2007, 447:661-678. Wellcome Trust Case Control Consortium.
112. Hnisz D., et al. Super-enhancers in the control of cell identity and disease. Cell 2013, 155:934-947.
113. Shulha H.P., et al. Human-specific histone methylation signatures at transcription start sites in prefrontal neurons. PLoS Biol. 2012, 10:e1001427.
114. Heintzman N.D., et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007, 39:311-318.
115. Wang X., Hayes J.J. Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Mol. Cell. Biol. 2008, 28:227-236.
116. Johnson D.S., et al. Genome-wide mapping of in vivo protein-DNA interactions. Science 2007, 316:1497-1502.
117. Lee T.I., et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 2006, 125:301-313.
118. Wendt K.S., et al. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 2008, 451:796-801.
119. Whyte W.A., et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 2013, 153:307-319.
120. Consortium E.P., et al. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447:799-816.
121. Yue F., et al. A comparative encyclopedia of DNA elements in the mouse genome. Nature 2014, 515:355-364.
122. Cahoy J.D., et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J. Neurosci. 2008, 28:264-278.
123. Cheung I., et al. Developmental regulation and individual differences of neuronal H3K4me3 epigenomes in the prefrontal cortex. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:8824-8829.
124. Lovatt D., et al. Transcriptome in vivo analysis (TIVA) of spatially defined single cells in live tissue. Nat. Methods 2014, 11:190-196.
125. Miller J.A., et al. Transcriptional landscape of the prenatal human brain. Nature 2014, 508:199-206.
126. Johnson M.B., et al. Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 2009, 62:494-509.
127. Pletikos M., et al. Temporal specification and bilaterality of human neocortical topographic gene expression. Neuron 2014, 81:321-332.
128. Wenger A.M., et al. The enhancer landscape during early neocortical development reveals patterns of dense regulation and co-option. PLoS Genet. 2013, 9:e1003728.
129. Visel A., et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
130. Vermunt M.W., et al. Large-scale identification of coregulated enhancer networks in the adult human brain. Cell Rep. 2014, 9:767-779.
131. Fullwood M.J., et al. Next-generation DNA sequencing of paired-end tags (PET) for transcriptome and genome analyses. Genome Res. 2009, 19:521-532.
132. Zhang J., et al. ChIA-PET analysis of transcriptional chromatin interactions. Methods 2012, 58:289-299.
133. Kieffer-Kwon K.R., et al. Interactome maps of mouse gene regulatory domains reveal basic principles of transcriptional regulation. Cell 2013, 155:1507-1520.
134. Melnikov A., et al. Systematic dissection and optimization of inducible enhancers in human cells using a massively parallel reporter assay. Nat. Biotechnol. 2012, 30:271-277.
135. Wang H., et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 2013, 153:910-918.
136. Cong L., et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.