Transcriptional Networks Controlled by NKX2-1 in the Development of Forebrain GABAergic Neurons

Neuron

Volumn 91, Issue 6, 2016, Pages 1260-1275

  Sandberg, Magnus ^a   Flandin, Pierre ^a,g   Silberberg, Shanni ^a   Su Feher, Linda ^b,c   Price, James D ^a   Hu, Jia Sheng ^a   Kim, Carol ^a   Visel, Axel ^d,e,f   Nord, Alex S ^b,c   Rubenstein, John L R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^e DOE JOINT GENOME INSTITUTE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g Quanticel Pharmaceuticals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GBX1; TRANSCRIPTION FACTOR GBX2; TRANSCRIPTION FACTOR LHX6; TRANSCRIPTION FACTOR NKX2.1; UNCLASSIFIED DRUG; 4 AMINOBUTYRIC ACID RECEPTOR; CHROMATIN; GBX1 PROTEIN, MOUSE; GBX2 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; LHX6 PROTEIN, MOUSE; LIM HOMEODOMAIN PROTEIN; NERVE PROTEIN; NUCLEAR PROTEIN; POU5F1 PROTEIN, MOUSE; THYROID NUCLEAR FACTOR 1;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; FOREBRAIN; GABAERGIC SYSTEM; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; HISTONE MODIFICATION; INTERNEURON; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SUBVENTRICULAR ZONE; TRANSCRIPTION INITIATION SITE; UPREGULATION; ANIMAL; BASAL GANGLION; CHROMATIN; CYTOLOGY; E BOX ELEMENT; EPIGENETIC REPRESSION; GENE REGULATORY NETWORK; GENETICS; KNOCKOUT MOUSE; METABOLISM;

ANIMALS; BASAL GANGLIA; CHROMATIN; E-BOX ELEMENTS; EPIGENETIC REPRESSION; GABAERGIC NEURONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HOMEODOMAIN PROTEINS; INTERNEURONS; LIM-HOMEODOMAIN PROTEINS; MICE; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; OCTAMER TRANSCRIPTION FACTOR-3; TRANSCRIPTION FACTORS;

EID: 84991234843     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2016.08.020     Document Type: Article

References (49)

1. Attanasio, C., Nord, A.S., Zhu, Y., Blow, M.J., Biddie, S.C., Mendenhall, E.M., Dixon, J., Wright, C., Hosseini, R., Akiyama, J.A., et al. Tissue-specific SMARCA4 binding at active and repressed regulatory elements during embryogenesis. Genome Res. 24 (2014), 920–929.
2. Berger, M.F., Badis, G., Gehrke, A.R., Talukder, S., Philippakis, A.A., Peña-Castillo, L., Alleyne, T.M., Mnaimneh, S., Botvinnik, O.B., Chan, E.T., et al. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133 (2008), 1266–1276.
3. Bernstein, B.E., Mikkelsen, T.S., Xie, X., Kamal, M., Huebert, D.J., Cuff, J., Fry, B., Meissner, A., Wernig, M., Plath, K., et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125 (2006), 315–326.
4. Boyer, L.A., Lee, T.I., Cole, M.F., Johnstone, S.E., Levine, S.S., Zucker, J.P., Guenther, M.G., Kumar, R.M., Murray, H.L., Jenner, R.G., et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122 (2005), 947–956.
5. Briscoe, J., Pierani, A., Jessell, T.M., Ericson, J., A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101 (2000), 435–445.
6. Butt, S.J.B., Sousa, V.H., Fuccillo, M.V., Hjerling-Leffler, J., Miyoshi, G., Kimura, S., Fishell, G., The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 59 (2008), 722–732.
7. Campbell, K., Dorsal-ventral patterning in the mammalian telencephalon. Curr. Opin. Neurobiol. 13 (2003), 50–56.
8. Chen, G., Fernandez, J., Mische, S., Courey, A.J., A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev. 13 (1999), 2218–2230.
9. Chen, X., Xu, H., Yuan, P., Fang, F., Huss, M., Vega, V.B., Wong, E., Orlov, Y.L., Zhang, W., Jiang, J., et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133 (2008), 1106–1117.
10. Choi, G.B., Dong, H.-W., Murphy, A.J., Valenzuela, D.M., Yancopoulos, G.D., Swanson, L.W., Anderson, D.J., Lhx6 delineates a pathway mediating innate reproductive behaviors from the amygdala to the hypothalamus. Neuron 46 (2005), 647–660.
11. Core, L.J., Martins, A.L., Danko, C.G., Waters, C.T., Siepel, A., Lis, J.T., Analysis of nascent RNA identifies a unified architecture of initiation regions at mammalian promoters and enhancers. Nat. Genet. 46 (2014), 1311–1320.
12. Creyghton, M.P., Cheng, A.W., Welstead, G.G., Kooistra, T., Carey, B.W., Steine, E.J., Hanna, J., Lodato, M.A., Frampton, G.M., Sharp, P.A., et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. U.S.A. 107 (2010), 21931–21936.
13. De Rubeis, S., He, X., Goldberg, A.P., Poultney, C.S., Samocha, K., Cicek, A.E., Kou, Y., Liu, L., Fromer, M., Walker, S., et al. DDD Study Homozygosity Mapping Collaborative for Autism, UK10K Consortium. Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 515 (2014), 209–215.
14. Dogan, N., Wu, W., Morrissey, C.S., Chen, K.-B., Stonestrom, A., Long, M., Keller, C.A., Cheng, Y., Jain, D., Visel, A., et al. Occupancy by key transcription factors is a more accurate predictor of enhancer activity than histone modifications or chromatin accessibility. Epigenetics Chromatin, 8, 2015, 16.
15. Du, T., Xu, Q., Ocbina, P.J., Anderson, S.A., NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development 135 (2008), 1559–1567.
16. Ernst, J., Kheradpour, P., Mikkelsen, T.S., Shoresh, N., Ward, L.D., Epstein, C.B., Zhang, X., Wang, L., Issner, R., Coyne, M., et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 473 (2011), 43–49.
17. Flandin, P., Zhao, Y., Vogt, D., Jeong, J., Long, J., Potter, G., Westphal, H., Rubenstein, J.L.R., Lhx6 and Lhx8 coordinately induce neuronal expression of Shh that controls the generation of interneuron progenitors. Neuron 70 (2011), 939–950.
18. Fragkouli, A., van Wijk, N.V., Lopes, R., Kessaris, N., Pachnis, V., LIM homeodomain transcription factor-dependent specification of bipotential MGE progenitors into cholinergic and GABAergic striatal interneurons. Development 136 (2009), 3841–3851.
19. Heinz, S., Benner, C., Spann, N., Bertolino, E., Lin, Y.C., Laslo, P., Cheng, J.X., Murre, C., Singh, H., Glass, C.K., Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38 (2010), 576–589.
20. Kusakabe, T., Kawaguchi, A., Hoshi, N., Kawaguchi, R., Hoshi, S., Kimura, S., Thyroid-specific enhancer-binding protein/NKX2.1 is required for the maintenance of ordered architecture and function of the differentiated thyroid. Mol. Endocrinol. 20 (2006), 1796–1809.
21. Kwasnieski, J.C., Fiore, C., Chaudhari, H.G., Cohen, B.A., High-throughput functional testing of ENCODE segmentation predictions. Genome Res. 24 (2014), 1595–1602.
22. Lee, S.-K., Pfaff, S.L., Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 38 (2003), 731–745.
23. Li, H., Durbin, R., Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 (2009), 1754–1760.
24. Ma, Y.-C., Song, M.-R., Park, J.P., Henry Ho, H.-Y., Hu, L., Kurtev, M.V., Zieg, J., Ma, Q., Pfaff, S.L., Greenberg, M.E., Regulation of motor neuron specification by phosphorylation of neurogenin 2. Neuron 58 (2008), 65–77.
25. Madisen, L., Zwingman, T.A., Sunkin, S.M., Oh, S.W., Zariwala, H.A., Gu, H., Ng, L.L., Palmiter, R.D., Hawrylycz, M.J., Jones, A.R., et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13 (2010), 133–140.
26. Magklara, A., Yen, A., Colquitt, B.M., Clowney, E.J., Allen, W., Markenscoff-Papadimitriou, E., Evans, Z.A., Kheradpour, P., Mountoufaris, G., Carey, C., et al. An epigenetic signature for monoallelic olfactory receptor expression. Cell 145 (2011), 555–570.
27. Marín, O., Rubenstein, J.L.R., Cell migration in the forebrain. Annu. Rev. Neurosci. 26 (2003), 441–483.
28. McLean, C.Y., Bristor, D., Hiller, M., Clarke, S.L., Schaar, B.T., Lowe, C.B., Wenger, A.M., Bejerano, G., GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28 (2010), 495–501.
29. Muhr, J., Andersson, E., Persson, M., Jessell, T.M., Ericson, J., Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 104 (2001), 861–873.
30. Nord, A.S., Blow, M.J., Attanasio, C., Akiyama, J.A., Holt, A., Hosseini, R., Phouanenavong, S., Plajzer-Frick, I., Shoukry, M., Afzal, V., et al. Rapid and pervasive changes in genome-wide enhancer usage during mammalian development. Cell 155 (2013), 1521–1531.
31. Nord, A.S., Pattabiraman, K., Visel, A., Rubenstein, J.L.R., Genomic perspectives of transcriptional regulation in forebrain development. Neuron 85 (2015), 27–47.
32. Noyes, M.B., Christensen, R.G., Wakabayashi, A., Stormo, G.D., Brodsky, M.H., Wolfe, S.A., Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133 (2008), 1277–1289.
33. Patel, S.R., Bhumbra, S.S., Paknikar, R.S., Dressler, G.R., Epigenetic mechanisms of Groucho/Grg/TLE mediated transcriptional repression. Mol. Cell 45 (2012), 185–195.
34. Pekowska, A., Benoukraf, T., Zacarias-Cabeza, J., Belhocine, M., Koch, F., Holota, H., Imbert, J., Andrau, J.-C., Ferrier, P., Spicuglia, S., H3K4 tri-methylation provides an epigenetic signature of active enhancers. EMBO J. 30 (2011), 4198–4210.
35. Petryniak, M.A., Potter, G.B., Rowitch, D.H., Rubenstein, J.L.R., Dlx1 and Dlx2 control neuronal versus oligodendroglial cell fate acquisition in the developing forebrain. Neuron 55 (2007), 417–433.
36. Schaeren-Wiemers, N., Gerfin-Moser, A., A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100 (1993), 431–440.
37. Schüller, U., Heine, V.M., Mao, J., Kho, A.T., Dillon, A.K., Han, Y.-G., Huillard, E., Sun, T., Ligon, A.H., Qian, Y., et al. Acquisition of granule neuron precursor identity is a critical determinant of progenitor cell competence to form Shh-induced medulloblastoma. Cancer Cell 14 (2008), 123–134.
38. Shen, L., Shao, N., Liu, X., Nestler, E., ngs.plot: quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics, 15, 2014, 284.
39. Snyder, E.L., Watanabe, H., Magendantz, M., Hoersch, S., Chen, T.A., Wang, D.G., Crowley, D., Whittaker, C.A., Meyerson, M., Kimura, S., Jacks, T., Nkx2-1 represses a latent gastric differentiation program in lung adenocarcinoma. Mol. Cell 50 (2013), 185–199.
40. Sussel, L., Marin, O., Kimura, S., Rubenstein, J.L., Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126 (1999), 3359–3370.
41. van den Berg, D.L.C., Snoek, T., Mullin, N.P., Yates, A., Bezstarosti, K., Demmers, J., Chambers, I., Poot, R.A., An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6 (2010), 369–381.
42. Visel, A., Blow, M.J., Li, Z., Zhang, T., Akiyama, J.A., Holt, A., Plajzer-Frick, I., Shoukry, M., Wright, C., Chen, F., et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457 (2009), 854–858.
43. Visel, A., Taher, L., Girgis, H., May, D., Golonzhka, O., Hoch, R.V., McKinsey, G.L., Pattabiraman, K., Silberberg, S.N., Blow, M.J., et al. A high-resolution enhancer atlas of the developing telencephalon. Cell 152 (2013), 895–908.
44. Vogt, D., Hunt, R.F., Mandal, S., Sandberg, M., Silberberg, S.N., Nagasawa, T., Yang, Z., Baraban, S.C., Rubenstein, J.L.R., Lhx6 directly regulates Arx and CXCR7 to determine cortical interneuron fate and laminar position. Neuron 82 (2014), 350–364.
45. Vokes, S.A., Ji, H., McCuine, S., Tenzen, T., Giles, S., Zhong, S., Longabaugh, W.J.R., Davidson, E.H., Wong, W.H., McMahon, A.P., Genomic characterization of Gli-activator targets in sonic hedgehog-mediated neural patterning. Development 134 (2007), 1977–1989.
46. Watanabe, H., Francis, J.M., Woo, M.S., Etemad, B., Lin, W., Fries, D.F., Peng, S., Snyder, E.L., Tata, P.R., Izzo, F., et al. Integrated cistromic and expression analysis of amplified NKX2-1 in lung adenocarcinoma identifies LMO3 as a functional transcriptional target. Genes Dev. 27 (2013), 197–210.
47. Zhao, Y., Guo, Y.J., Tomac, A.C., Taylor, N.R., Grinberg, A., Lee, E.J., Huang, S., Westphal, H., Isolated cleft palate in mice with a targeted mutation of the LIM homeobox gene lhx8. Proc. Natl. Acad. Sci. USA 96 (1999), 15002–15006.
48. Zhao, Y., Marín, O., Hermesz, E., Powell, A., Flames, N., Palkovits, M., Rubenstein, J.L.R., Westphal, H., The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc. Natl. Acad. Sci. USA 100 (2003), 9005–9010.
49. Zhao, Y., Flandin, P., Long, J.E., Cuesta, M.D., Westphal, H., Rubenstein, J.L.R., Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J. Comp. Neurol. 510 (2008), 79–99.