Identification of Early Requirements for Preplacodal Ectoderm and Sensory Organ Development

English version České info

Preplacodal ectoderm arises near the end of gastrulation as a narrow band of cells surrounding the anterior neural plate. This domain later resolves into discrete cranial placodes that, together with neural crest, produce paired sensory structures of the head. Unlike the better-characterized neural crest, little is known about early regulation of preplacodal development. Classical models of ectodermal patterning posit that preplacodal identity is specified by readout of a discrete level of Bmp signaling along a DV gradient. More recent studies indicate that Bmp-antagonists are critical for promoting preplacodal development. However, it is unclear whether Bmp-antagonists establish the proper level of Bmp signaling within a morphogen gradient or, alternatively, block Bmp altogether. To begin addressing these issues, we treated zebrafish embryos with a pharmacological inhibitor of Bmp, sometimes combined with heat shock-induction of Chordin and dominant-negative Bmp receptor, to fully block Bmp signaling at various developmental stages. We find that preplacodal development occurs in two phases with opposing Bmp requirements. Initially, Bmp is required before gastrulation to co-induce four transcription factors, Tfap2a, Tfap2c, Foxi1, and Gata3, which establish preplacodal competence throughout the nonneural ectoderm. Subsequently, Bmp must be fully blocked in late gastrulation by dorsally expressed Bmp-antagonists, together with dorsally expressed Fgf and Pdgf, to specify preplacodal identity within competent cells abutting the neural plate. Localized ventral misexpression of Fgf8 and Chordin can activate ectopic preplacodal development anywhere within the zone of competence, whereas dorsal misexpression of one or more competence factors can activate ectopic preplacodal development in the neural plate. Conversely, morpholino-knockdown of competence factors specifically ablates preplacodal development. Our work supports a relatively simple two-step model that traces regulation of preplacodal development to late blastula stage, resolves two distinct phases of Bmp dependence, and identifies the main factors required for preplacodal competence and specification.

Vyšlo v časopise: Identification of Early Requirements for Preplacodal Ectoderm and Sensory Organ Development. PLoS Genet 6(9): e32767. doi:10.1371/journal.pgen.1001133
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1001133

Souhrn

Zdroje

1. BakerCVH

Bronner-FraserM

2000 Vertebrate cranial placodes I. Embryonic induction. Dev Biol 232 1 61

2. SchlosserG

2006 Induction and specification of cranial placodes. Dev Biol 294 303 351

3. StreitA

2007 The preplacodal region: an ectodermal domain with multipotential progenitors that contribute to sense organs and cranial sensory ganglia. Int J Dev Biol 51 447 461

4. BrugmannSA

MoodySA

2005 Induction and specification of the vertebrate ectodermal placodes: precursors of the cranial sensory organs. Biol Cell 97 303 319

5. AkimenkoMA

EkkerM

WegnerJ

LinW

WesterfieldM

1994 Combinatorial expression of three zebrafish genes related to Distal-less: part of a homeobox gene code for the head. J Neurosci 14 3475 3486

6. SahlyI

AndermannP

PetitC

1999 The zebrafish eya1 gene and its expression pattern during embryogenesis. Dev Genes Evol 209 399 410

7. KobayashiM

OsanaiH

KawakamiK

YamamotoM

2000 Expression of three zebrafish Six4 genes in the cranial sensory placodes and the developing somites. Mech Dev 9 151 155

8. KishimotoY

LeeKH

ZonL

HammerschmidtM

Schulte-MerkerS

1997 The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development 124 4457 4466

9. NeaveB

HolderN

PatientR

1997 A graded response to BMP-4 spatially coordinates patterning of the mesoderm and ectoderm in the zebrafish. Mech Dev 62 183 195

10. WilsonPA

LagnaG

SuzukiA

Hemmati-BrivanlouA

1997 Concentration-dependent patterning of the Xenopus ectoderm by BMP4 and its signal transducer Smad1. Development 124 3177 3184

11. MarchantL

LinkerC

RuizP

GuerreroN

MayorR

1998 The inductive properties of mesoderm suggest that the neural crest cells are specified by a BMP gradient. Dev Biol 198 319 329

12. NguyenVH

SchmidB

TroutJ

ConnorsSA

EkkerM

1998 Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2b/swirl pathway of genes. Dev Biol 199 93 110

13. BarthKA

KishimotoY

RohrKB

SeydlerC

Schulte-MerkerS

1999 Bmp activity establishes a gradient of positional information throughout the entire neural plate. Development 126 4977 4987

14. ReversadeB

De RobertisEM

2005 Regulation of ADMP and BMP2/4/7 at opposite embryonic poles generates a self-regulating morphogenetic field. Cell 123 1147 1160

15. TuckerJA

MintzerKA

MullinsMC

2008 The BMP signaling gradient patterns dorsoventral tissues in a temporally progressive manner along the anteroposterior axis. Dev Cell 14 108 119

16. EsterbergR

FritzA

2008 dlx3b/4b are required for the formation of preplacodal region and otic placode through modulation of Bmp activity. Dev Biol 325 189 199

17. KwonHJ

RileyBB

2009 Mesendodermal signals required for otic induction: Bmp-antagonists cooperate with Fgf and can facilitate formation of ectopic otic tissue. Dev Dyn 238 1582 1594

18. BrugmannSA

PandurPD

KenyonKL

PignoniF

MoodySA

2004 Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor. Development 131 5871 5881

19. GlavicA

HonoréMS

FeijóoCG

BastidasF

AllendeML

2004 Role of BMP signaling and the homeoprotein Iroquois in the specification of the cranial placodal field. Dev Biol 272 89 103

20. AhrensK

SchlosserG

2005 Tissues and signals involved in the induction of placodal Six1 expression in Xenopus laevis. Dev Biol 288 40 59

21. LitsiouA

HansonS

StreitA

2005 A balance of FGF, BMP and WNT signalling positions the future placode territory in the head. Development 132 4051 4062

22. BaschML

Bronner-FraserM

Barcía-CastroMI

2006 Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441 218 222

23. WodaJM

PastagiaJ

MercolaM

ArtingerKB

2003 Dlx proteins position the neural plate border and determine adjacent cell fates. Development 130 331 342

24. NeaveB

RodawayA

WilsonSW

PatientR

HolderN

1995 Expression of zebrafish GATA 3 (gta3) during gastrulation and neurulation suggests a role in the specification of cell fate. Mech Dev 51 169 182

25. ShengG

SternCD

1999 Gata2 and Gata3: novel markers for early embryonic polarity and for non-neural ectoderm in the chick embryo. Mech Dev 87 213 219

26. KarisA

PataI

van DoorninckJH

GrosveldF

de ZeeuwCI

2001 Transcription factor GATA-3 alters pathway selection of olivochochlear neurons and affects morphogenesis of the ear. J Comp Neurol 429 615 630

27. SolomonKS

KudohT

DawidIB

FritzA

2003 Zebrafish foxi1 mediates otic placode formation and jaw development. Development 130 929 940

28. LeeSA

ShenEL

FiserA

SaliA

GuoS

2003 The zebrafish forkhead transcription factor Foxi1 specified epibranchial placode-derived sensory neurons. Development 130 2669 2679

29. LiW

CornellRA

2007 Redundant activities of Tfap2a and Tfap2c are required for neural crest induction and development of other non-neural ectoderm derivatives in zebrafish embryos. Dev Biol 304 338 354

30. KelshRN

DuttonK

MedlinJ

WisenJS

2000 Expression of zebrafish fkd6 in neural crest-derived glia. Mech Dev 93 161 164

31. Montero-BalaguerM

LangMR

Weiss SachdevS

KnappmeyerC

StewartRA

2006 The mother superior mutation ablates foxd3 activity in neural crest progenitor cells and depletes neural crest derivatives in zebrafish. Dev Dyn 235 3199 3212

32. YuPB

HongCC

SachidanandanC

BabittJL

DengDY

2008 Dorsomorphin inhibits Bmp signals required for embryogenesis and iron metabolism. Nature Chem Biol 4 33 41

33. MullinsMC

HammerschmidtM

KaneDA

OdenthalJ

BrandM

1996 Genes establishing dorsoventral pattern formation in the zebrafish embryo: the ventral specifying genes. Development 123 81 93

34. YabeT

ShimizuT

MuraokaO

BaeYK

HirataT

2003 Ogon/Secreted Frizzled functions as a negative feedback regulator of Bmp signaling. Development 130 2705 2716

35. HoffmanTL

JavierAL

CampeauSA

KnightRD

SchillingTF

2007 Tfap2 transcription factors in zebrafish neural crest development and ectodermal evolution. J Exp Zool 308B 679 691

36. KraussS

JohansenT

KorzhV

FjoseA

1991 Expression of the zebrafish paired box genes pax[zf-b] during early neurogenesis. Development 113 1193 1206

37. KollmarR

NakamuraSK

KapplerJA

HudspethAJ

2001 Expression and phylogeny of claudins in vertebrate primordia. Proc Natl Acad Sci 98 10196 10201

38. KajiT

ArtingerKB

2004 dlx3b and dlx4b function in development of Rohon-Beard sensory neurons and trigeminal placode in the zebrafish neurula. Dev Biol 276 523 540

39. DuttaS

DietrichJE

AspöckG

BurdineRD

SchierA

2005 pitx3 defines an equivalence domain for lens and anterior pituitary placode. Development 132 1579 1590

40. KnautH

BladerP

SträhleU

SchierAF

2005 Assembly of trigeminal sensory ganglia by chemokine signaling. Neuron 47 653 666

41. SwindellEC

ZilinskiCA

HashimotoR

ShahR

LaneME

2008 Regulation and function of foxe3 during early zebrafish development. Genesis 46 177 183

42. MiyasakaN

KnautH

YoshiharaY

2007 Cxcl12/Cxcr4b chemokine signaling is required for placode assembly and sensory axon pathfinding in the zebrafish olfactory system. Development 134 2459 2468

43. NikaidoM

DoiK

ShimizuT

HibiM

KikuchiY

2007 Initial specification of the epibranchial placode in zebrafish embryos depends on the fibroblast growth factor signal. Dev Dyn 236 564 571

44. SunSK

DeeCT

TripathiVB

RengifoA

HirstCS

2007 Epibranchial and otic placodes are induced by a common Fgf signal, but their subsequent development is independent. Dev Biol 303 675 686

45. PyatiUJ

WebbAE

KimelmanD

2005 transgenic zebrafish reveal stage-specific roles for Bmp signaling in ventral and posterior mesoderm development. Development 132 2333 2343

46. BakkersJ

HildM

KramerC

Furutani-SeikiM

HammerschmidtM

2002 Zebrafish ΔMp63 is a direct target of Bmp signaling and encodes a transcriptional repressor blocking neural specification in the ventral ectoderm. Dev Cell 2 617 627

47. LeeH

KimelmanD

2002 A dominant-negative form of p63 is required for epidermal proliferation in zebrafish. Dev Cell 2 607 616

48. PhillipsBT

KwonHY

MeltonC

HoughtlingP

FritzA

2006 Zebrafish msxB, msxC and msxE function together to refine the neural-nonneural border and regulate cranial placodes and neural crest development. Dev Biol 294 376 390

49. ShojiW

YeeCS

KuwadaJY

1998 Zebrafish Semaphorin Z1a collapses specific growth cones and alters their pathway in vivo. Development 125 1275 1283

50. HansS

ChristisonJ

LiuD

WesterfieldM

2007 Fgf-dependent otic induction requires competence provided by Foxi1 and Dlx3b. BMC Dev Biol 7 5

51. SolomonKS

KwakSJ

FritzA

2004 Genetic interactions underlying otic placode induction and formation. Dev Dyn 230 419 433

52. LégerS

BrandM

2002 Fgf8 and Fgf3 are required for zebrafish ear placode induction, maintenance and inner ear patterning. Mech Dev 119 91 108

53. LiuD

ChuH

MavesL

YanYL

MorcosPA

2003 Fgf3 and Fgf8 dependent and independent transcription factors are required for otic placode specification. Development 130 2213 2224

54. LiuL

KorzhV

BablsubramaniyanNV

EkkerM

GeR

2002 Platelet-derived growth factor A (pdgf-a) expression during zebrafish embryonic development. Dev Genes Evol 212 298 301

55. MonteraJA

KilianB

ChanJ

BaylissPE

HeisenbergCP

2003 Phosphoinositide 3-kinase is required for process outgrowth and cell polarization of gastrulating mesendodermal cells. Curr Biol 13 1279 1289

56. KudohT

ConchaML

HouartC

DawidIB

WilsonSW

2004 Combinatorial Fgf and Bmp signalling patterns the gastrula ectoderm into prospective neural and epidermal domains. Development 131 3581 3592

57. PhillipsBT

BoldingK

RileyBB

2001 Zebrafish fgf3 and fgf8 encode redundant functions required for otic placode induction. Dev Biol 235 351 365

58. McCabeKL

Bronner-FraserM

2008 Essential role for PDGF signaling in ophthalmic trigeminal placode induction. Development 135 186301874

59. PattheyC

GunhagaL

EdlundT

2008 Early development of the central and peripheral nervous systems is coordinated by Wnt and Bmp signals. PLoS ONE 3 31625 doi:10.1371/journal.pone.0001625

60. PattheyC

GunhagaL

EdlundT

2009 Wnt-regulated temporal control of BMP exposure directs the choice between neural plate border and epidermal fate. Development 136 73 83

61. YamJ

XuL

CrawfordG

WangZ

BurgessSM

2006 The forkhead transcription factor Foxi1 remains bound to condensed mitotic chromosomes and stably remodels chromatin structure. Mol Cell Biol 26 155 168

62. KimmelCB

BallardWW

KimmelSR

UlmannB

SchillingTF

1995 Stages of embryonic development of the zebrafish. Dev Dyn 203 253 310

63. SidiS

SandaT

KennedyRD

HagenAT

JetteCA

2008 Chk1 suppresses a caspase-2 apoptotic response to DNA damage that bypasses p53, Bcl2, and Caspase-3. Cell 133 864 877