A -Regulatory Signature for Chordate Anterior Neuroectodermal Genes

English version České info

One of the striking findings of comparative developmental genetics was that expression patterns of core transcription factors are extraordinarily conserved in bilaterians. However, it remains unclear whether cis-regulatory elements of their target genes also exhibit common signatures associated with conserved embryonic fields. To address this question, we focused on genes that are active in the anterior neuroectoderm and non-neural ectoderm of the ascidian Ciona intestinalis. Following the dissection of a prototypic anterior placodal enhancer, we searched all genomic conserved non-coding elements for duplicated motifs around genes showing anterior neuroectodermal expression. Strikingly, we identified an over-represented pentamer motif corresponding to the binding site of the homeodomain protein OTX, which plays a pivotal role in the anterior development of all bilaterian species. Using an in vivo reporter gene assay, we observed that 10 of 23 candidate cis-regulatory elements containing duplicated OTX motifs are active in the anterior neuroectoderm, thus showing that this cis-regulatory signature is predictive of neuroectodermal enhancers. These results show that a common cis-regulatory signature corresponding to K50-Paired homeodomain transcription factors is found in non-coding sequences flanking anterior neuroectodermal genes in chordate embryos. Thus, field-specific selector genes impose architectural constraints in the form of combinations of short tags on their target enhancers. This could account for the strong evolutionary conservation of the regulatory elements controlling field-specific selector genes responsible for body plan formation.

Vyšlo v časopise: A -Regulatory Signature for Chordate Anterior Neuroectodermal Genes. PLoS Genet 6(4): e32767. doi:10.1371/journal.pgen.1000912
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1000912

Souhrn

Zdroje

1. Garcia-BellidoA

1975 Genetic control of wing disc development in Drosophila. Ciba Found Symp 0 161 182

2. HobertO

2008 Regulatory logic of neuronal diversity: terminal selector genes and selector motifs. Proc Natl Acad Sci U S A 105 20067 20071

3. BlackshawS

FraioliRE

FurukawaT

CepkoCL

2001 Comprehensive analysis of photoreceptor gene expression and the identification of candidate retinal disease genes. Cell 107 579 589

4. ChenS

WangQL

NieZ

SunH

LennonG

1997 Crx, a novel Otx-like paired-homeodomain protein, binds to and transactivates photoreceptor cell-specific genes. Neuron 19 1017 1030

5. HsiauTH

DiaconuC

MyersCA

LeeJ

CepkoCL

2007 The cis-regulatory logic of the mammalian photoreceptor transcriptional network. PLoS ONE 2 e643 doi:10.1371/journal.pone.0000643

6. AlonU

2007 Network motifs: theory and experimental approaches. Nat Rev Genet 8 450 461

7. KoikeC

NishidaA

UenoS

SaitoH

SanukiR

2007 Functional roles of Otx2 transcription factor in postnatal mouse retinal development. Mol Cell Biol 27 8318 8329

8. NishidaA

FurukawaA

KoikeC

TanoY

AizawaS

2003 Otx2 homeobox gene controls retinal photoreceptor cell fate and pineal gland development. Nat Neurosci 6 1255 1263

9. RanadeSS

Yang-ZhouD

KongSW

McDonaldEC

CookTA

2008 Analysis of the Otd-dependent transcriptome supports the evolutionary conservation of CRX/OTX/OTD functions in flies and vertebrates. Dev Biol 315 521 534

10. TahayatoA

SonnevilleR

PichaudF

WernetMF

PapatsenkoD

2003 Otd/Crx, a dual regulator for the specification of ommatidia subtypes in the Drosophila retina. Dev Cell 5 391 402

11. McDonaldJA

FujiokaM

OddenJP

JaynesJB

DoeCQ

2003 Specification of motoneuron fate in Drosophila: integration of positive and negative transcription factor inputs by a minimal eve enhancer. J Neurobiol 57 193 203

12. WenickAS

HobertO

2004 Genomic cis-regulatory architecture and trans-acting regulators of a single interneuron-specific gene battery in C. elegans. Dev Cell 6 757 770

13. HongJW

HendrixDA

PapatsenkoD

LevineMS

2008 How the Dorsal gradient works: insights from postgenome technologies. Proc Natl Acad Sci U S A 105 20072 20076

14. ZinzenRP

CandeJ

RonshaugenM

PapatsenkoD

LevineM

2006 Evolution of the ventral midline in insect embryos. Dev Cell 11 895 902

15. DenesAS

JekelyG

SteinmetzPR

RaibleF

SnymanH

2007 Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129 277 288

16. ChioriR

JagerM

DenkerE

WinckerP

Da SilvaC

2009 Are Hox genes ancestrally involved in axial patterning? Evidence from the hydrozoan Clytia hemisphaerica (Cnidaria). PLoS ONE 4 e4231 doi:10.1371/journal.pone.0004231

17. DavidsonE

2006 The regulatory genome San Diego Academic

18. LoweCJ

WuM

SalicA

EvansL

LanderE

2003 Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 113 853 865

19. BruceAE

ShanklandM

1998 Expression of the head gene Lox22-Otx in the leech Helobdella and the origin of the bilaterian body plan. Developmental biology 201 101 112

20. HudsonC

LemaireP

2001 Induction of anterior neural fates in the ascidian Ciona intestinalis. Mechanisms of development 100 189 203

21. WilliamsN

HollandP

1996 Old head on young shoulders. Nature 383 490 490

22. SchlosserG

2006 Induction and specification of cranial placodes. Developmental Biology 294 303 351

23. AcamporaD

MazanS

LallemandY

AvantaggiatoV

MauryM

1995 Forebrain and midbrain regions are deleted in Otx2−/− mutants due to a defective anterior neuroectoderm specification during gastrulation. Development (Cambridge, England) 121 3279 3290

24. AcamporaD

GulisanoM

BroccoliV

SimeoneA

2001 Otx genes in brain morphogenesis. Progress in neurobiology 64 69 95

25. BergerMF

BadisG

GehrkeAR

TalukderS

PhilippakisAA

2008 Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133 1266 1276

26. NoyesMB

ChristensenRG

WakabayashiA

StormoGD

BrodskyMH

2008 Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell 133 1277 1289

27. HanesSD

BrentR

1991 A genetic model for interaction of the homeodomain recognition helix with DNA. Science (New York, NY) 251 426 430

28. AcamporaD

AvantaggiatoV

TuortoF

BaroneP

PereraM

1999 Differential transcriptional control as the major molecular event in generating Otx1−/− and Otx2−/− divergent phenotypes. Development (Cambridge, England) 126 1417 1426

29. AcamporaD

AvantaggiatoV

TuortoF

BaroneP

ReichertH

1998 Murine Otx1 and Drosophila otd genes share conserved genetic functions required in invertebrate and vertebrate brain development. Development (Cambridge, England) 125 1691 1702

30. AdachiY

NagaoT

SaigaH

Furukubo-TokunagaK

2001 Cross-phylum regulatory potential of the ascidian Otx gene in brain development in Drosophila melanogaster. Dev Genes Evol 211 269 280

31. WadaH

SaigaH

SatohN

HollandPW

1998 Tripartite organization of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax-2/5/8, Hox and Otx genes. Development 125 1113 1122

32. SatohN

LevineM

2005 Surfing with the tunicates into the post-genome era. Genes Dev 19 2407 2411

33. ImaiKS

HinoK

YagiK

SatohN

SatouY

2004 Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks. Development 131 4047 4058

34. SatouY

TakatoriN

YamadaL

MochizukiY

HamaguchiM

2001 Gene expression profiles in Ciona intestinalis tailbud embryos. Development 128 2893 2904

35. TassyO

DaianF

HudsonC

BertrandV

LemaireP

2006 A quantitative approach to the study of cell shapes and interactions during early chordate embryogenesis. Curr Biol 16 345 358

36. ChristiaenL

BourratF

JolyJS

2005 A modular cis-regulatory system controls isoform-specific pitx expression in ascidian stomodaeum. Dev Biol 277 557 566

37. BoormanCJ

ShimeldSM

2002 Pitx homeobox genes in Ciona and amphioxus show left-right asymmetry is a conserved chordate character and define the ascidian adenohypophysis. Evol Dev 4 354 365

38. ChristiaenL

BurighelP

SmithWC

VernierP

BourratF

2002 Pitx genes in Tunicates provide new molecular insight into the evolutionary origin of pituitary. Gene 287 107 113

39. BertrandV

HudsonC

CaillolD

PopoviciC

LemaireP

2003 Neural tissue in ascidian embryos is induced by FGF9/16/20, acting via a combination of maternal GATA and Ets transcription factors. Cell 115 615 627

40. BryneJC

ValenE

TangMH

MarstrandT

WintherO

2008 JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Res 36 D102 106

41. MatysV

FrickeE

GeffersR

GosslingE

HaubrockM

2003 TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31 374 378

42. LebrechtD

FoehrM

SmithE

LopesFJ

Vanario-AlonsoCE

2005 Bicoid cooperative DNA binding is critical for embryonic patterning in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 102 13176 13181

43. ArnoneMI

DavidsonEH

1997 The hardwiring of development: organization and function of genomic regulatory systems. Development 124 1851 1864

44. FuD

ZhaoC

MaJ

2003 Enhancer sequences influence the role of the amino-terminal domain of bicoid in transcription. Molecular and cellular biology 23 4439 4448

45. MaX

YuanD

DiepoldK

ScarboroughT

MaJ

1996 The Drosophila morphogenetic protein Bicoid binds DNA cooperatively. Development 122 1195 1206

46. HareEE

PetersonBK

EisenMB

2008 A careful look at binding site reorganization in the even-skipped enhancers of Drosophila and sepsids. PLoS Genet 4 e1000268 doi:10.1371/journal.pgen.1000268

47. OndekB

GlossL

HerrW

1988 The SV40 enhancer contains two distinct levels of organization. Nature 333 40 45

48. FriedmanAM

FischmannTO

SteitzTA

1995 Crystal structure of lac repressor core tetramer and its implications for DNA looping. Science 268 1721 1727

49. WadaS

SudouN

SaigaH

2004 Roles of Hroth, the ascidian otx gene, in the differentiation of the brain (sensory vesicle) and anterior trunk epidermis in the larval development of Halocynthia roretzi. Mechanisms of development 121 463 474

50. DufourHD

ChettouhZ

DeytsC

de RosaR

GoridisC

2006 Precraniate origin of cranial motoneurons. Proc Natl Acad Sci U S A 103 8727 8732

51. ImaiKS

SatohN

SatouY

2002 Region specific gene expressions in the central nervous system of the ascidian embryo. Mech Dev 119 Suppl 1 S275 277

52. PennacchioL

AhituvN

MosesA

PrabhakarS

NobregaM

2006 In vivo enhancer analysis of human conserved non-coding sequences. Nature

53. WoolfeA

GoodsonM

GoodeDK

SnellP

McEwenGK

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

54. KentWJ

BaertschR

HinrichsA

MillerW

HausslerD

2003 Evolution's cauldron: duplication, deletion, and rearrangement in the mouse and human genomes. Proc Natl Acad Sci U S A 100 11484 11489

55. Yoseph BarashGB

FriedmanNir

Moret OGaBME, ed. Algorithms in Bioinformatics, First International Workshop, WABI 2001, Aarhus, Denmark, August 28–31, 2001, Proceedings. Lecture Notes in Computer Science; 2001 2001; Aarhus, Denmark Springer 278 293

56. CorboJC

LevineM

ZellerRW

1997 Characterization of a notochord-specific enhancer from the Brachyury promoter region of the ascidian, Ciona intestinalis. Development 124 589 602

57. HarafujiN

KeysDN

LevineM

2002 Genome-wide identification of tissue-specific enhancers in the Ciona tadpole. Proc Natl Acad Sci U S A 99 6802 6805

58. PhilippakisA

BusserB

GisselbrechtS

HeF

EstradaB

2006 Expression-Guided In Silico Evaluation of Candidate Cis Regulatory Codes for Drosophila Muscle Founder Cells. PLoS Comput Biol 2 e53 doi:10.1371/journal.pcbi.0020053

59. HalfonMS

GradY

ChurchGM

MichelsonAM

2002 Computation-based discovery of related transcriptional regulatory modules and motifs using an experimentally validated combinatorial model. Genome Res 12 1019 1028

60. ChristiaenL

JaszczyszynY

KerfantM

KanoS

ThermesV

2007 Evolutionary modification of mouth position in deuterostomes. Semin Cell Dev Biol 18 502 511

61. HottaK

MitsuharaK

TakahashiH

InabaK

OkaK

2007 A web-based interactive developmental table for the ascidian Ciona intestinalis, including 3D real-image embryo reconstructions: I. From fertilized egg to hatching larva. Dev Dyn 236 1790 1805

62. NewburgerDE

BulykML

2009 UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res 37 D77 82

63. RoureA

RothbacherU

RobinF

KalmarE

FeroneG

2007 A multicassette Gateway vector set for high throughput and comparative analyses in ciona and vertebrate embryos. PLoS ONE 2 e916 doi:10.1371/journal.pone.0000916