Brachyury, Foxa2 and the cis-Regulatory Origins of the Notochord

PLoS Genetics

Volumn 11, Issue 12, 2015, Pages

  José Edwards, Diana S ^a   Oda Ishii, Izumi ^a,b   Kugler, Jamie E ^a   Passamaneck, Yale J ^a,c   Katikala, Lavanya ^a   Nibu, Yutaka ^a   Di Gregorio, Anna ^a,d  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF HAWAII   (United States)

^d NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRACHYURY PROTEIN; FETOPROTEIN; HEPATOCYTE NUCLEAR FACTOR 3BETA; T BOX TRANSCRIPTION FACTOR;

ANIMAL; BINDING SITE; CIONA INTESTINALIS; GENE EXPRESSION REGULATION; GENETICS; GENOME; GROWTH, DEVELOPMENT AND AGING; MORPHOGENESIS; MOUSE; NOTOCHORD; REGULATORY SEQUENCE;

ANIMALS; BINDING SITES; BODY PATTERNING; CIONA INTESTINALIS; FETAL PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOME; HEPATOCYTE NUCLEAR FACTOR 3-BETA; MICE; NOTOCHORD; REGULATORY SEQUENCES, NUCLEIC ACID; T-BOX DOMAIN PROTEINS;

EID: 84953305922     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005730     Document Type: Article

References (64)

1. Howard ML, Davidson EH, Cis-regulatory control circuits in development. Dev Biol. 2004;271: 109–118. 15196954
2. Levine M, Transcriptional Enhancers in Animal Development and Evolution. Curr Biol. 2010;20: R754–R763. doi: 10.1016/j.cub.2010.06.070 20833320
3. Erokhin M, Vassetzky Y, Georgiev P, Chetverina D, Eukaryotic enhancers: common features, regulation, and participation in diseases. Cell Mol Life Sci. 2015;72: 2361–2375. doi: 10.1007/s00018-015-1871-9 25715743
4. Kleinjan D-J, Coutinho P, Cis-ruption mechanisms: disruption of cis-regulatory control as a cause of human genetic disease. Brief Funct Genomic Proteomic. 2009;8: 317–332. doi: 10.1093/bfgp/elp022 19596743
5. Mansour MR, Abraham BJ, Anders L, Berezovskaya A, Gutierrez A, Durbin AD, et al. An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element. Science. 2014;346: 1373–1377. doi: 10.1126/science.1259037 25394790
6. Melton C, Reuter JA, Spacek DV, Snyder M, Recurrent somatic mutations in regulatory regions of human cancer genomes. Nat Genet. 2015;47: 710–716. doi: 10.1038/ng.3332 26053494
7. Levine M, Cattoglio C, Tjian R, Looping Back to Leap Forward: Transcription Enters a New Era. Cell. 2014;157: 13–25. doi: 10.1016/j.cell.2014.02.009 24679523
8. Ott CJ, Blackledge NP, Kerschner JL, Leir S-H, Crawford GE, Cotton CU, et al. Intronic enhancers coordinate epithelial-specific looping of the active CFTR locus. Proc Natl Acad Sci USA. 2009;106: 19934–19939. doi: 10.1073/pnas.0900946106 19897727
9. Hnisz D, Schuijers J, Lin CY, Weintraub AS, Abraham BJ, Lee TI, et al. Convergence of Developmental and Oncogenic Signaling Pathways at Transcriptional Super-Enhancers. Mol Cell. 2015;58: 362–370. doi: 10.1016/j.molcel.2015.02.014 25801169
10. Markstein M, Markstein P, Markstein V, Levine MS, Genome-wide analysis of clustered Dorsal binding sites identifies putative target genes in the Drosophila embryo. Proc Natl Acad Sci USA. 2002;99: 763–768. 11752406
11. Poulin F, Nobrega MA, Plajzer-Frick I, Holt A, Afzal V, Rubin EM, et al. In vivo characterization of a vertebrate ultraconserved enhancer. Genomics. 2005;85: 774–781. 15885503
12. Lusk RW, Eisen MB, Evolutionary mirages: selection on binding site composition creates the illusion of conserved grammars in Drosophila enhancers. PLoS Genetics. 2010;6: e1000829. doi: 10.1371/journal.pgen.1000829 20107516
13. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, et al. In vivo enhancer analysis of human conserved non-coding sequences. Nature. 2006;444: 499–502. 17086198
14. Jiang D, Smith WC, Ascidian notochord morphogenesis. Dev Dyn. 2007;236: 1748–1757. 17497687
15. Satoh N, Tagawa K, Takahashi H, How was the notochord born? Evol Dev. 2012;14: 56–75. doi: 10.1111/j.1525-142X.2011.00522.x 23016975
16. Stemple DL, Structure and function of the notochord: an essential organ for chordate development. Development. 2005;132: 2503–2512. 15890825
17. Lawson L, Harfe B, Notochord to Nucleus Pulposus Transition. Curr Osteoporos Rep. Springer US; 2015;13: 336–341–341. doi: 10.1007/s11914-015-0284-x 26231139
18. Passamaneck YJ, Di Gregorio A, Ciona intestinalis: chordate development made simple. Dev Dyn. 2005;233: 1–19. 15765512
19. Davidson B, Christiaen L, Linking chordate gene networks to cellular behavior in ascidians. Cell. 2006;124: 247–250. 16439196
20. Delsuc F, Brinkmann H, Chourrout D, Philippe H, Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature. 2006;439: 965–968. 16495997
21. Brown CD, Johnson DS, Sidow A, Functional Architecture and Evolution of Transcriptional Elements That Drive Gene Coexpression. Science. 2007;317: 1557–1560. 17872446
22. Stolfi A, Gainous TB, Young JJ, Mori A, Levine M, Christiaen L, Early chordate origins of the vertebrate second heart field. Science. 2010;329: 565–568. doi: 10.1126/science.1190181 20671188
23. Abitua PB, Wagner E, Navarrete IA, Levine M, Identification of a rudimentary neural crest in a non-vertebrate chordate. Nature. 2012;492: 104–107. doi: 10.1038/nature11589 23135395
24. Passamaneck YJ, Katikala L, Perrone L, Dunn MP, Oda-Ishii I, Di Gregorio A, Direct activation of a notochord cis-regulatory module by Brachyury and FoxA in the ascidian Ciona intestinalis. Development. 2009;136: 3679–3689. doi: 10.1242/dev.038141 19820186
25. Kelkar YD, Strubczewski N, Hile SE, Chiaromonte F, Eckert KA, Makova KD, What Is a Microsatellite: A Computational and Experimental Definition Based upon Repeat Mutational Behavior at A/T and GT/AC Repeats. Genome Biol Evol. 2010;2: 620–635. doi: 10.1093/gbe/evq046 20668018
26. Evans AL, Faial T, Gilchrist MJ, Down T, Vallier L, Pedersen RA, et al. Genomic Targets of Brachyury (T) in Differentiating Mouse Embryonic Stem Cells. PLoS ONE. 2012;7: e33346. doi: 10.1371/journal.pone.0033346 22479388
27. Kubo A, Suzuki N, Yuan X, Nakai K, Satoh N, Imai KS, et al. Genomic cis-regulatory networks in the early Ciona intestinalis embryo. Development. 2010;137: 1613–1623. doi: 10.1242/dev.046789 20392745
28. Kispert A, Koschorz B, Herrmann BG, The T protein encoded by Brachyury is a tissue-specific transcription factor. EMBO J. 1995;14: 4763–4772. 7588606
29. Casey ES, O'Reilly MA, Conlon FL, Smith JC, The T-box transcription factor Brachyury regulates expression of eFGF through binding to a non-palindromic response element. Development. 1998;125: 3887–3894. 9729496
30. Di Gregorio A, Levine M, Regulation of Ci-tropomyosin-like, a Brachyury target gene in the ascidian, Ciona intestinalis. Development. 1999;126: 5599–5609. 10572037
31. Conlon FL, Fairclough L, Price BM, Casey ES, Smith JC, Determinants of T box protein specificity. Development. 2001;128: 3749–3758. 11585801
32. Kusch T, Storck T, Walldorf U, Reuter R, Brachyury proteins regulate target genes through modular binding sites in a cooperative fashion. Genes Dev. 2002;16: 518–529. 11850413
33. Katikala L, Aihara H, Passamaneck YJ, Gazdoiu S, José-Edwards DS, Kugler JE, et al. Functional Brachyury binding sites establish a temporal read-out of gene expression in the Ciona notochord. PLoS Biol. 2013;11: e1001697. doi: 10.1371/journal.pbio.1001697 24204212
34. José-Edwards DS, Oda-Ishii I, Nibu Y, Di Gregorio A, Tbx2/3 is an essential mediator within the Brachyury gene network during Ciona notochord development. Development. 2013;140: 2422–2433. doi: 10.1242/dev.094227 23674602
35. Imai KS, Hino K, Yagi K, Satoh N, Satou Y, Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks. Development. 2004;131: 4047–4058. 15269171
36. José-Edwards DS, Kerner P, Kugler JE, Deng W, Jiang D, Di Gregorio A, The Identification of Transcription Factors Expressed in the Notochord of Ciona intestinalis Adds New Potential Players to the Brachyury Gene Regulatory Network. Dev Dyn. 2011;240: 1793–1805. doi: 10.1002/dvdy.22656 21594950
37. Miwata K, Chiba T, Horii R, Yamada L, Kubo A, Miyamura D, et al. Systematic analysis of embryonic expression profiles of zinc finger genes in Ciona intestinalis. Dev Biol. 2006;292: 546–554. 16519883
38. Brozovic M, Martin C, Dantec C, Dauga D, Mendez M, Simion P, et al. ANISEED 2015: a digital framework for the comparative developmental biology of ascidians. Nucleic Acids Res. 2015.
39. Johnson DS, Zhou Q, Yagi K, Satoh N, Wong W, Sidow A, De novo discovery of a tissue-specific gene regulatory module in a chordate. Genome Res. 2005;15: 1315–1324. 16169925
40. Kugler JE, Gazdoiu S, Oda-Ishii I, Passamaneck YJ, Erives AJ, Di Gregorio A, Temporal regulation of the muscle gene cascade by Macho1 and Tbx6 transcription factors in Ciona intestinalis. J Cell Sci. 2010;123: 2453–2463. doi: 10.1242/jcs.066910 20592183
41. Kusakabe T, Yoshida R, Ikeda Y, Tsuda M, Computational discovery of DNA motifs associated with cell type-specific gene expression in Ciona. Dev Biol. 2004;276: 563–580. 15581886
42. Wang W, Christiaen L, Transcriptional enhancers in ascidian development. Curr Top Dev Biol. 2012;98: 147–172. doi: 10.1016/B978-0-12-386499-4.00006-9 22305162
43. Haeussler M, Jaszczyszyn Y, Christiaen L, Joly J-S, A Cis-Regulatory Signature for Chordate Anterior Neuroectodermal Genes. PLoS Genet. 2010;6: e1000912. doi: 10.1371/journal.pgen.1000912 20419150
44. Markstein M, Zinzen R, Markstein P, Yee K-P, Erives A, Stathopoulos A, et al. A regulatory code for neurogenic gene expression in the Drosophila embryo. Development. 2004;131: 2387–2394. 15128669
45. Jin H, Stojnic R, Adryan B, Ozdemir A, Stathopoulos A, Frasch M, Genome-wide screens for in vivo Tinman binding sites identify cardiac enhancers with diverse functional architectures. PLoS Genet. 2013;9: e1003195. doi: 10.1371/journal.pgen.1003195 23326246
46. Rastegar S, Hess I, Dickmeis T, Nicod JC, Ertzer R, Hadzhiev Y, et al. The words of the regulatory code are arranged in a variable manner in highly conserved enhancers. Dev Biol. 2008;318: 366–377. doi: 10.1016/j.ydbio.2008.03.034 18455719
47. Johnson DS, Davidson B, Brown CD, Smith WC, Sidow A, Noncoding regulatory sequences of Ciona exhibit strong correspondence between evolutionary constraint and functional importance. Genome Res. 2004;14: 2448–2456. 15545496
48. Kim JH, Waterman MS, Li LM, Diploid genome reconstruction of Ciona intestinalis and comparative analysis with Ciona savignyi. Genome Res. 2007;17: 1101–1110. 17567986
49. Doglio L, Goode DK, Pelleri MC, Pauls S, Frabetti F, Shimeld SM, et al. Parallel evolution of chordate cis-regulatory code for development. PLoS Genet. 2013;9: e1003904. doi: 10.1371/journal.pgen.1003904 24282393
50. Jahangiri L, Nelson AC, Wardle FC, A cis-regulatory module upstream of deltaC regulated by Ntla and Tbx16 drives expression in the tailbud, presomitic mesoderm and somites. Dev Biol. 2012;371: 110–120. doi: 10.1016/j.ydbio.2012.07.002 22877946
51. Anno C, Satou A, Fujiwara S, Transcriptional regulation of ZicL in the Ciona intestinalis embryo. Dev Genes Evol. 2006;216: 597–605. 16705435
52. Di Gregorio A, Corbo JC, Levine M, The regulation of forkhead/HNF-3beta expression in the Ciona embryo. Dev Biol. 2001;229: 31–43. 11133152
53. Dunn MP, Di Gregorio A, The evolutionarily conserved leprecan gene: its regulation by Brachyury and its role in the developing Ciona notochord. Dev Biol. 2009;328: 561–574. doi: 10.1016/j.ydbio.2009.02.007 19217895
54. Tamplin OJ, Cox BJ, Rossant J, Integrated microarray and ChIP analysis identifies multiple Foxa2 dependent target genes in the notochord. Dev Biol. 2011;360: 415–425. doi: 10.1016/j.ydbio.2011.10.002 22008794
55. Jeong Y, Epstein DJ, Distinct regulators of Shh transcription in the floor plate and notochord indicate separate origins for these tissues in the mouse node. Development. 2003;130: 3891–3902. 12835403
56. Muller F, Chang B, Albert S, Fischer N, Tora L, Strahle U, Intronic enhancers control expression of zebrafish sonic hedgehog in floor plate and notochord. Development. 1999;126: 2103–2116. 10207136
57. Yagi K, Satou Y, Satoh N, A zinc finger transcription factor, ZicL, is a direct activator of Brachyury in the notochord specification of Ciona intestinalis. Development. 2004;131: 1279–1288. 14993185
58. Alten L, Schuster-Gossler K, Eichenlaub MP, Wittbrodt B, Wittbrodt J, Gossler A, A Novel Mammal-Specific Three Partite Enhancer Element Regulates Node and Notochord-Specific Noto Expression. PLoS ONE. 2012;7: e47785. doi: 10.1371/journal.pone.0047785 23110100
59. Sawada A, Nishizaki Y, Sato H, Yada Y, Nakayama R, Yamamoto S, et al. Tead proteins activate the Foxa2 enhancer in the node in cooperation with a second factor. Development. 2005;132: 4719–4729. 16207754
60. Kugler JE, Passamaneck YJ, Feldman TG, Beh J, Regnier TW, Di Gregorio A, Evolutionary conservation of vertebrate notochord genes in the ascidian Ciona intestinalis. Genesis. 2008;46: 697–710. doi: 10.1002/dvg.20403 18802963
61. Smith RP, Riesenfeld SJ, Holloway AK, Li Q, Murphy KK, Feliciano NM, et al. A compact, in vivo screen of all 6-mers reveals drivers of tissue-specific expression and guides synthetic regulatory element design. Genome Biol. 2013;14: R72. doi: 10.1186/gb-2013-14-7-r72 23867016
62. Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, Zaret KS, Opening of Compacted Chromatin by Early Developmental Transcription Factors HNF3 (FoxA) and GATA-4. Mol Cell. 2002;9: 279–289. 11864602
63. Ikuta T, Yoshida N, Satoh N, Saiga H, Ciona intestinalis Hox gene cluster: Its dispersed structure and residual colinear expression in development. Proc Natl Acad Sci USA. 2004;101: 15118–15123. 15469921
64. Oda-Ishii I, Di Gregorio A, Lineage-Independent Mosaic Expression and Regulation of the Ciona multidom Gene in the Ancestral notochord. Dev Dyn. 2007;236: 1806–1819. 17576134