Human Developmental Enhancers Conserved between Deuterostomes and Protostomes

English version České info

The identification of homologies, whether morphological, molecular, or genetic, is fundamental to our understanding of common biological principles. Homologies bridging the great divide between deuterostomes and protostomes have served as the basis for current models of animal evolution and development. It is now appreciated that these two clades share a common developmental toolkit consisting of conserved transcription factors and signaling pathways. These patterning genes sometimes show common expression patterns and genetic interactions, suggesting the existence of similar or even conserved regulatory apparatus. However, previous studies have found no regulatory sequence conserved between deuterostomes and protostomes. Here we describe the first such enhancers, which we call bilaterian conserved regulatory elements (Bicores). Bicores show conservation of sequence and gene synteny. Sequence conservation of Bicores reflects conserved patterns of transcription factor binding sites. We predict that Bicores act as response elements to signaling pathways, and we show that Bicores are developmental enhancers that drive expression of transcriptional repressors in the vertebrate central nervous system. Although the small number of identified Bicores suggests extensive rewiring of cis-regulation between the protostome and deuterostome clades, additional Bicores may be revealed as our understanding of cis-regulatory logic and sample of bilaterian genomes continue to grow.

Vyšlo v časopise: Human Developmental Enhancers Conserved between Deuterostomes and Protostomes. PLoS Genet 8(8): e32767. doi:10.1371/journal.pgen.1002852
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002852

Souhrn

Zdroje

1. DunnCWHejnolAMatusDQPangKBrowneWE 2008 Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452 745 749 doi:10.1038/nature06614

2. CarrollSB 2008 Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134 25 36 doi:10.1016/j.cell.2008.06.030

3. PeterISDavidsonEH 2011 Evolution of gene regulatory networks controlling body plan development. Cell 144 970 985 doi:10.1016/j.cell.2011.02.017

4. MastonGAEvansSKGreenMR 2006 Transcriptional regulatory elements in the human genome. Annu Rev Genomics Hum Genet 7 29 59 doi:10.1146/annurev.genom.7.080505.115623

5. BejeranoGPheasantMMakuninIStephenSKentWJ 2004 Ultraconserved elements in the human genome. Science 304 1321 1325 doi:10.1126/science.1098119

6. WoolfeAGoodsonMGoodeDKSnellPMcEwenGK 2005 Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3 e7 doi:10.1371/journal.pbio.0030007

7. PennacchioLAAhituvNMosesAMPrabhakarSNobregaMA 2006 In vivo enhancer analysis of human conserved non-coding sequences. Nature 444 499 502 doi:10.1038/nature05295

8. ViselAMinovitskySDubchakIPennacchioLA 2007 VISTA Enhancer Browser–a database of tissue-specific human enhancers. Nucleic Acids Res 35 D88 92 doi:10.1093/nar/gkl822

9. GlazovEAPheasantMMcGrawEABejeranoGMattickJS 2005 Ultraconserved elements in insect genomes: a highly conserved intronic sequence implicated in the control of homothorax mRNA splicing. Genome Res 15 800 808 doi:10.1101/gr.3545105

10. International Chicken Genome Sequencing Consortium 2004 Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432 695 716 doi:10.1038/nature03154

11. VavouriTWalterKGilksWRLehnerBElgarG 2007 Parallel evolution of conserved non-coding elements that target a common set of developmental regulatory genes from worms to humans. Genome Biol 8 R15 doi:10.1186/gb-2007-8-2-r15

12. RoyoJLMaesoIIrimiaMGaoFPeterIS 2011 Transphyletic conservation of developmental regulatory state in animal evolution. Proc Natl Acad Sci USA 108 14186 14191 doi:10.1073/pnas.1109037108

13. McLeanCYBristorDHillerMClarkeSLSchaarBT 2010 GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol 28 495 501 doi:10.1038/nbt.1630

14. HarrisRS 2007 Improved pairwise alignment of genomic DNA. The Pennsylvania State University

15. DehalPSatouYCampbellRKChapmanJDegnanB 2002 The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298 2157 2167 doi:10.1126/science.1080049

16. PutnamNHButtsTFerrierDEKFurlongRFHellstenU 2008 The amphioxus genome and the evolution of the chordate karyotype. Nature 453 1064 1071 doi:10.1038/nature06967

17. SodergrenEWeinstockGMDavidsonEHCameronRAGibbsRA 2006 The genome of the sea urchin Strongylocentrotus purpuratus. Science 314 941 952 doi:10.1126/science.1133609

18. YokotaY 2001 Id and development. Oncogene 20 8290 8298 doi:10.1038/sj.onc.1205090

19. MizutaniCMBierE 2008 EvoD/Vo: the origins of BMP signalling in the neuroectoderm. Nat Rev Genet 9 663 677 doi:10.1038/nrg2417

20. López-RoviraTChalauxEMassaguéJRosaJLVenturaF 2002 Direct binding of Smad1 and Smad4 to two distinct motifs mediates bone morphogenetic protein-specific transcriptional activation of Id1 gene. J Biol Chem 277 3176 3185 doi:10.1074/jbc.M106826200

21. KorchynskyiOten DijkeP 2002 Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 277 4883 4891 doi:10.1074/jbc.M111023200

22. ChenC-RKangYSiegelPMMassaguéJ 2002 E2F4/5 and p107 as Smad cofactors linking the TGFbeta receptor to c-myc repression. Cell 110 19 32

23. RaneyBJClineMSRosenbloomKRDreszerTRLearnedK 2011 ENCODE whole-genome data in the UCSC genome browser (2011 update). Nucleic Acids Res 39 D871 875 doi:10.1093/nar/gkq1017

24. KangYChenC-RMassaguéJ 2003 A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol Cell 11 915 926

25. PetersonKJCottonJAGehlingJGPisaniD 2008 The Ediacaran emergence of bilaterians: congruence between the genetic and the geological fossil records. Philos Trans R Soc Lond, B, Biol Sci 363 1435 1443 doi:10.1098/rstb.2007.2233

26. RauchGJLyonsDAMiddendorfIFriedlanderBAranaN 2003 Submission and Curation of Gene Expression Data. ZFIN Direct Data Submission

27. GrayPAFuHLuoPZhaoQYuJ 2004 Mouse brain organization revealed through direct genome-scale TF expression analysis. Science 306 2255 2257 doi:10.1126/science.1104935

28. Revilla-i-DomingoRMinokawaTDavidsonEH 2004 R11: a cis-regulatory node of the sea urchin embryo gene network that controls early expression of SpDelta in micromeres. Dev Biol 274 438 451 doi:10.1016/j.ydbio.2004.07.008

29. SaudemontAHaillotEMekpohFBessodesNQuirinM 2010 Ancestral regulatory circuits governing ectoderm patterning downstream of Nodal and BMP2/4 revealed by gene regulatory network analysis in an echinoderm. PLoS Genet 6 e1001259 doi:10.1371/journal.pgen.1001259

30. CheahPYMengYBYangXKimbrellDAshburnerM 1994 The Drosophila l(2)35Ba/nocA gene encodes a putative Zn finger protein involved in the development of the embryonic brain and the adult ocellar structures. Mol Cell Biol 14 1487 1499

31. RunkoAPSagerströmCG 2004 Isolation of nlz2 and characterization of essential domains in Nlz family proteins. J Biol Chem 279 11917 11925 doi:10.1074/jbc.M310076200

32. RunkoAPSagerströmCG 2003 Nlz belongs to a family of zinc-finger-containing repressors and controls segmental gene expression in the zebrafish hindbrain. Dev Biol 262 254 267

33. HoyleJTangYPWielletteELWardleFCSiveH 2004 nlz gene family is required for hindbrain patterning in the zebrafish. Dev Dyn 229 835 846 doi:10.1002/dvdy.20001

34. VlachakisNChoeSKSagerströmCG 2001 Meis3 synergizes with Pbx4 and Hoxb1b in promoting hindbrain fates in the zebrafish. Development 128 1299 1312

35. ChoeS-KVlachakisNSagerströmCG 2002 Meis family proteins are required for hindbrain development in the zebrafish. Development 129 585 595

36. RyooHDMartyTCasaresFAffolterMMannRS 1999 Regulation of Hox target genes by a DNA bound Homothorax/Hox/Extradenticle complex. Development 126 5137 5148

37. JiangYShiHLiuJ 2009 Two Hox cofactors, the Meis/Hth homolog UNC-62 and the Pbx/Exd homolog CEH-20, function together during C. elegans postembryonic mesodermal development. Dev Biol 334 535 546 doi:10.1016/j.ydbio.2009.07.034

38. PetersenCPReddienPW 2009 Wnt signaling and the polarity of the primary body axis. Cell 139 1056 1068 doi:10.1016/j.cell.2009.11.035

39. RhinnMLunKLuzMWernerMBrandM 2005 Positioning of the midbrain-hindbrain boundary organizer through global posteriorization of the neuroectoderm mediated by Wnt8 signaling. Development 132 1261 1272 doi:10.1242/dev.01685

40. McGlinnERichmanJMMetzisVTownLButterfieldNC 2008 Expression of the NET family member Zfp503 is regulated by hedgehog and BMP signaling in the limb. Dev Dyn 237 1172 1182 doi:10.1002/dvdy.21508

41. DavidsonEHCameronRARansickA 1998 Specification of cell fate in the sea urchin embryo: summary and some proposed mechanisms. Development 125 3269 3290

42. CubasPModolellJRuiz-GómezM 1994 The helix-loop-helix extramacrochaetae protein is required for proper specification of many cell types in the Drosophila embryo. Development 120 2555 2566

43. TomoyasuYNakamuraMUenoN 1998 Role of dpp signalling in prepattern formation of the dorsocentral mechanosensory organ in Drosophila melanogaster. Development 125 4215 4224

44. HollandLZ 2009 Chordate roots of the vertebrate nervous system: expanding the molecular toolkit. Nat Rev Neurosci 10 736 746 doi:10.1038/nrn2703

45. ArendtDDenesASJékelyGTessmar-RaibleK 2008 The evolution of nervous system centralization. Philos Trans R Soc Lond, B, Biol Sci 363 1523 1528 doi:10.1098/rstb.2007.2242

46. RaibleFTessmar-RaibleKOsoegawaKWinckerPJubinC 2005 Vertebrate-type intron-rich genes in the marine annelid Platynereis dumerilii. Science 310 1325 1326 doi:10.1126/science.1119089

47. PutnamNHSrivastavaMHellstenUDirksBChapmanJ 2007 Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization. Science 317 86 94 doi:10.1126/science.1139158

48. DenoeudFHenrietSMungpakdeeSAuryJ-MDa SilvaC 2010 Plasticity of animal genome architecture unmasked by rapid evolution of a pelagic tunicate. Science 330 1381 1385 doi:10.1126/science.1194167

49. McGinnisWKrumlaufR 1992 Homeobox genes and axial patterning. Cell 68 283 302

50. PasquinelliAEReinhartBJSlackFMartindaleMQKurodaMI 2000 Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408 86 89 doi:10.1038/35040556

51. ProchnikSERokhsarDSAboobakerAA 2007 Evidence for a microRNA expansion in the bilaterian ancestor. Dev Genes Evol 217 73 77 doi:10.1007/s00427-006-0116-1

52. HsuFKentWJClawsonHKuhnRMDiekhansM 2006 The UCSC Known Genes. Bioinformatics 22 1036 1046 doi:10.1093/bioinformatics/btl048

53. SiepelABejeranoGPedersenJSHinrichsASHouM 2005 Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15 1034 1050 doi:10.1101/gr.3715005

54. PruittKDTatusovaTMaglottDR 2007 NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Res 35 D61 65 doi:10.1093/nar/gkl842

55. HubbardTBarkerDBirneyECameronGChenY 2002 The Ensembl genome database project. Nucleic Acids Res 30 38 41

56. SiepelAHausslerD 2004 Computational identification of evolutionarily conserved exons. Proceedings of the eighth annual international conference on Resaerch in computational molecular biology. RECOMB '04 New York, NY, USA ACM 177 186 Available:http://doi.acm.org/10.1145/974614.974638. Accessed 22 December 2011

57. BensonDAKarsch-MizrachiILipmanDJOstellJWheelerDL 2004 GenBank: update. Nucleic Acids Res 32 D23 26 doi:10.1093/nar/gkh045

58. GerhardDSWagnerLFeingoldEAShenmenCMGrouseLH 2004 The status, quality, and expansion of the NIH full-length cDNA project: the Mammalian Gene Collection (MGC). Genome Res 14 2121 2127 doi:10.1101/gr.2596504

59. Griffiths-JonesSSainiHKvan DongenSEnrightAJ 2008 miRBase: tools for microRNA genomics. Nucleic Acids Res 36 D154 158 doi:10.1093/nar/gkm952

60. LestradeLWeberMJ 2006 snoRNA-LBME-db, a comprehensive database of human H/ACA and C/D box snoRNAs. Nucleic Acids Res 34 D158 162 doi:10.1093/nar/gkj002

61. KarroJEYanYZhengDZhangZCarrieroN 2007 Pseudogene.org: a comprehensive database and comparison platform for pseudogene annotation. Nucleic Acids Res 35 D55 60 doi:10.1093/nar/gkl851

62. AshurstJLChenC-KGilbertJGRJekoschKKeenanS 2005 The Vertebrate Genome Annotation (Vega) database. Nucleic Acids Res 33 D459 465 doi:10.1093/nar/gki135

63. PedersenJSBejeranoGSiepelARosenbloomKLindblad-TohK 2006 Identification and classification of conserved RNA secondary structures in the human genome. PLoS Comput Biol 2 e33 doi:10.1371/journal.pcbi.0020033

64. ChiaromonteFYapVBMillerW 2002 Scoring pairwise genomic sequence alignments. Pac Symp Biocomput 115 126

65. AltschulSFGishWMillerWMyersEWLipmanDJ 1990 Basic local alignment search tool. J Mol Biol 215 403 410 doi:10.1006/jmbi.1990.9999

66. BlanchetteMKentWJRiemerCElnitskiLSmitAFA 2004 Aligning multiple genomic sequences with the threaded blockset aligner. Genome Res 14 708 715 doi:10.1101/gr.1933104

67. LarkinMABlackshieldsGBrownNPChennaRMcGettiganPA 2007 Clustal W and Clustal X version 2.0. Bioinformatics 23 2947 2948 doi:10.1093/bioinformatics/btm404

68. WaterhouseAMProcterJBMartinDMAClampMBartonGJ 2009 Jalview Version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics 25 1189 1191 doi:10.1093/bioinformatics/btp033

69. CrooksGEHonGChandoniaJ-MBrennerSE 2004 WebLogo: a sequence logo generator. Genome Res 14 1188 1190 doi:10.1101/gr.849004

70. NewburgerDEBulykML 2009 UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res 37 D77 82 doi:10.1093/nar/gkn660

71. MatysVKel-MargoulisOVFrickeELiebichILandS 2006 TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34 D108 110 doi:10.1093/nar/gkj143

72. LiQRitterDYangNDongZLiH 2010 A systematic approach to identify functional motifs within vertebrate developmental enhancers. Dev Biol 337 484 495 doi:10.1016/j.ydbio.2009.10.019

73. FisherSGriceEAVintonRMBesslingSLUrasakiA 2006 Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat Protoc 1 1297 1305 doi:10.1038/nprot.2006.230

74. DiLeoneRJRussellLBKingsleyDM 1998 An extensive 3′ regulatory region controls expression of Bmp5 in specific anatomical structures of the mouse embryo. Genetics 148 401 408