Cis-regulatory architecture of a brain signaling center predates the origin of chordates

Nature Genetics

Volumn 48, Issue 5, 2016, Pages 575-580

  Yao, Yao ^a   Minor, Paul J ^b   Zhao, Ying Tao ^a   Jeong, Yongsu ^c   Pani, Ariel M ^b   King, Anna N ^a   Symmons, Orsolya ^d   Gan, Lin ^e   Cardoso, Wellington V ^f   Spitz, Fran'ois ^d   Lowe, Christopher J ^b   Epstein, Douglas J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b STANFORD UNIVERSITY   (United States)

^c Kyung Hee University   (South Korea)

^d EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^e UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^f Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; SHH PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMBRYO; ENHANCER REGION; FEMALE; FOREBRAIN; HEMICHORDATA; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLUM; PREDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; ZONA LIMITANS INTRATHALAMICA; ANIMAL; CHORDATA; EMBRYOLOGY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; CHORDATA; ENHANCER ELEMENTS, GENETIC; EVOLUTION, MOLECULAR; FEMALE; HEDGEHOG PROTEINS; MALE; MICE; MICE, TRANSGENIC; PROSENCEPHALON; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84963620474     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3542     Document Type: Article

References (55)

1. Neph S, et al. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature. 489, 83-90 (2012).
2. Rada-Iglesias A, et al. A unique chromatin signature uncovers early developmental enhancers in humans. Nature. 470, 279-283 (2011).
3. Visel A, et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature. 457, 854-858 (2009).
4. Yue F, et al. A comparative encyclopedia of DNA elements in the mouse genome. Nature. 515, 355-364 (2014).
5. Kiecker C, & Lumsden A. Hedgehog signaling from the ZLI regulates diencephalic regional identity. Nat. Neurosci. 7, 1242-1249 (2004).
6. Vieira C, & Martinez S. Sonic hedgehog from the basal plate and the zona limitans intrathalamica exhibits differential activity on diencephalic molecular regionalization and nuclear structure. Neuroscience. 143, 129-140 (2006).
7. Hébert J.M, & Fishell G. The genetics of early telencephalon patterning: some assembly required. Nat. Rev. Neurosci. 9, 678-685 (2008).
8. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29 (2000).
9. Scholpp S, & Lumsden A. Building a bridal chamber: development of the thalamus. Trends Neurosci. 33, 373-380 (2010).
10. Frazer K.A, Elnitski L, Church D.M, Dubchak I, & Hardison R.C. Cross-species sequence comparisons: a review of methods and available resources. Genome Res. 13, 1-12 (2003).
11. Arnold C.D, et al. Quantitative genome-wide enhancer activity maps for five Drosophila species show functional enhancer conservation and turnover during cis-regulatory evolution. Nat. Genet. 46, 685-692 (2014).
12. Fisher S, Grice E.A, Vinton R.M, Bessling S.L, & McCallion A.S. Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science. 312, 276-279 (2006).
13. Hare E.E, Peterson B.K, Iyer V.N, Meier R, & Eisen M.B. Sepsid even-skipped enhancers are functionally conserved in Drosophila despite lack of sequence conservation. PLoS Genet. 4, e1000106 (2008).
14. Ludwig M.Z, Bergman C, Patel N.H, & Kreitman M. Evidence for stabilizing selection in a eukaryotic enhancer element. Nature. 403, 564-567 (2000).
15. Vierstra J, et al. Mouse regulatory DNA landscapes reveal global principles of cis-regulatory evolution. Science. 346, 1007-1012 (2014).
16. Busser B.W, et al. A machine learning approach for identifying novel cell type-specific transcriptional regulators of myogenesis. PLoS Genet. 8, e1002531 (2012).
17. De Val S, et al. Combinatorial regulation of endothelial gene expression by Ets and Forkhead transcription factors. Cell. 135, 1053-1064 (2008).
18. Erives A, & Levine M. Coordinate enhancers share common organizational features in the Drosophila genome. Proc. Natl. Acad. Sci. USA. 101, 3851-3856 (2004).
19. Junion G, et al. A transcription factor collective defines cardiac cell fate and reflects lineage history. Cell. 148, 473-486 (2012).
20. Kratsios P, Stolfi A, Levine M, & Hobert O. Coordinated regulation of cholinergic motor neuron traits through a conserved terminal selector gene. Nat. Neurosci. 15, 205-214 (2012).
21. Visel A, Minovitsky S, Dubchak I, & Pennacchio L.A. VISTA Enhancer Browser-A database of tissue-specific human enhancers. Nucleic Acids Res. 35, D88-D92 (2007).
22. Epstein D.J, McMahon A.P, & Joyner A.L. Regionalization of Sonic hedgehog transcription along the anteroposterior axis of the mouse central nervous system is regulated by Hnf3-dependent and -independent mechanisms. Development. 126, 281-292 (1999).
23. Pavesi G, Mereghetti P, Mauri G, & Pesole G. Weeder Web: Discovery of Transcription Factor Binding Sites in A Set of Sequences from Co-regulated Genes. Nucleic Acids Res. 32, W199-W203 (2004).
24. Brown C.D, Johnson D.S, & Sidow A. Functional architecture and evolution of transcriptional elements that drive gene coexpression. Science. 317, 1557-1560 (2007).
25. Smith R.P, et al. Massively parallel decoding of mammalian regulatory sequences supports a flexible organizational model. Nat. Genet. 45, 1021-1028 (2013).
26. Holland P.W.H, Booth H.A.F, & Bruford E.A. Classification and nomenclature of all human homeobox genes. BMC Biol. 5, 47 (2007).
27. Acampora D, Avantaggiato V, Tuorto F, & Simeone A. Genetic control of brain morphogenesis through Otx gene dosage requirement. Development. 124, 3639-3650 (1997).
28. Sakurai Y, et al. Otx2 and Otx1 protect diencephalon and mesencephalon from caudalization into metencephalon during early brain regionalization. Dev. Biol. 347, 392-403 (2010).
29. Scholpp S, et al. Otx1l, Otx2 and Irx1b establish and position the ZLI in the diencephalon. Development. 134, 3167-3176 (2007).
30. Juraver-Geslin H.A, Gómez-Skarmeta J.L, & Durand B.C. The conserved barH-like homeobox-2 gene barhl2 acts downstream of orthodentricle-2 and together with iroquois-3 in establishment of the caudal forebrain signaling center induced by Sonic Hedgehog. Dev. Biol. 396, 107-120 (2014).
31. Fernandez-L A, et al. YAP1 is amplified and up-regulated in hedgehog-Associated medulloblastomas and mediates Sonic hedgehog-driven neural precursor proliferation. Genes Dev. 23, 2729-2741 (2009).
32. Rosenbluh J, et al. β-catenin-driven cancers require a YAP1 transcriptional complex for survival and tumorigenesis. Cell. 151, 1457-1473 (2012).
33. Jeong Y, et al. Spatial and temporal requirements for sonic hedgehog in the regulation of thalamic interneuron identity. Development. 138, 531-541 (2011).
34. Shen Y, et al. A map of the cis-regulatory sequences in the mouse genome. Nature. 488, 116-120 (2012).
35. Irimia M, et al. Conserved developmental expression of Fezf in chordates and Drosophila and the origin of the zona limitans intrathalamica (ZLI) brain organizer. Evodevo. 1, 7 (2010).
36. Pani A.M, et al. Ancient deuterostome origins of vertebrate brain signalling centres. Nature. 483, 289-294 (2012).
37. Irimia M, et al. Comparative genomics of the Hedgehog loci in chordates and the origins of Shh regulatory novelties. Sci. Rep. 2, 433 (2012).
38. Sugahara F, et al. Involvement of Hedgehog and FGF signalling in the lamprey telencephalon: evolution of regionalization and dorsoventral patterning of the vertebrate forebrain. Development. 138, 1217-1226 (2011).
39. Takatori N, Satou Y, & Satoh N. Expression of hedgehog genes in Ciona intestinalis embryos. Mech. Dev. 116, 235-238 (2002).
40. Shubin N, Tabin C, & Carroll S. Deep homology and the origins of evolutionary novelty. Nature. 457, 818-823 (2009).
41. Liu-Chittenden Y, et al. Genetic and pharmacological disruption of the TEAD-YAP complex suppresses the oncogenic activity of YAP. Genes Dev. 26, 1300-1305 (2012).
42. Zhao L, et al. Disruption of SoxB1-dependent Sonic hedgehog expression in the hypothalamus causes septo-optic dysplasia. Dev. Cell. 22, 585-596 (2012).
43. Suda Y, et al. The same enhancer regulates the earliest Emx2 expression in caudal forebrain primordium, subsequent expression in dorsal telencephalon and later expression in the cortical ventricular zone. Development. 137, 2939-2949 (2010).
44. Symmons O, et al. Functional and topological characteristics of mammalian regulatory domains. Genome Res. 24, 390-400 (2014).
45. Ruf S, et al. Large-scale analysis of the regulatory architecture of the mouse genome with a transposon-Associated sensor. Nat. Genet. 43, 379-386 (2011).
46. Ding Q, et al. BARHL2 differentially regulates the development of retinal amacrine and ganglion neurons. J. Neurosci. 29, 3992-4003 (2009).
47. Mahoney J.E, Mori M, Szymaniak A.D, Varelas X, & Cardoso W.V. The hippo pathway effector Yap controls patterning and differentiation of airway epithelial progenitors. Dev. Cell. 30, 137-150 (2014).
48. Riccomagno M.M, Martinu L, Mulheisen M, Wu D.K, & Epstein D.J. Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev. 16, 2365-2378 (2002).
49. Ran F.A, et al. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 8, 2281-2308 (2013).
50. Jeong Y, El-Jaick K, Roessler E, Muenke M, & Epstein D.J. A functional screen for sonic hedgehog regulatory elements across a 1 Mb interval identifies long-range ventral forebrain enhancers. Development. 133, 761-772 (2006).
51. Grant G.R, et al. Comparative analysis of RNA-Seq alignment algorithms and the RNA-Seq unified mapper (RUM). Bioinformatics. 27, 2518-2528 (2011).
52. Pavesi G, & Pesole G. Using Weeder for the discovery of conserved transcription factor binding sites. Curr. Protoc. Bioinformatics Chapter 2, Unit 2.11 (2006).
53. Newburger D.E, & Bulyk M.L. UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res. 37, D77-D82 (2009).
54. Sandelin A, Alkema W, Engström P, Wasserman W.W, & Lenhard B. JASPAR: an open-Access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res. 32, D91-D94 (2004).
55. Lowe C.J, et al. Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol. 4, e291 (2006).