Dynamic and Differential Regulation of Stem Cell Factor FoxD3 in the Neural Crest Is Encrypted in the Genome

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The critical stem cell transcription factor FoxD3 is expressed by the premigratory and migrating neural crest, an embryonic stem cell population that forms diverse derivatives. Despite its important role in development and stem cell biology, little is known about what mediates FoxD3 activity in these cells. We have uncovered two FoxD3 enhancers, NC1 and NC2, that drive reporter expression in spatially and temporally distinct manners. Whereas NC1 activity recapitulates initial FoxD3 expression in the cranial neural crest, NC2 activity recapitulates initial FoxD3 expression at vagal/trunk levels while appearing only later in migrating cranial crest. Detailed mutational analysis, in vivo chromatin immunoprecipitation, and morpholino knock-downs reveal that transcription factors Pax7 and Msx1/2 cooperate with the neural crest specifier gene, Ets1, to bind to the cranial NC1 regulatory element. However, at vagal/trunk levels, they function together with the neural plate border gene, Zic1, which directly binds to the NC2 enhancer. These results reveal dynamic and differential regulation of FoxD3 in distinct neural crest subpopulations, suggesting that heterogeneity is encrypted at the regulatory level. Isolation of neural crest enhancers not only allows establishment of direct regulatory connections underlying neural crest formation, but also provides valuable tools for tissue specific manipulation and investigation of neural crest cell identity in amniotes.

Vyšlo v časopise: Dynamic and Differential Regulation of Stem Cell Factor FoxD3 in the Neural Crest Is Encrypted in the Genome. PLoS Genet 8(12): e32767. doi:10.1371/journal.pgen.1003142
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003142

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1. Sauka-SpenglerT, BarembaumM (2008) Gain- and loss-of-function approaches in the chick embryo. Methods Cell Biol 87: 237–256.

2. BetancurP, Bronner-FraserM, Sauka-SpenglerT (2010) Assembling neural crest regulatory circuits into a gene regulatory network. Annu Rev Cell Dev Biol 26: 581–603.

3. MeulemansD, Bronner-FraserM (2004) Gene-regulatory interactions in neural crest evolution and development. Dev Cell 7: 291–299.

4. BaschML, Bronner-FraserM, Garcia-CastroMI (2006) Specification of the neural crest occurs during gastrulation and requires Pax7. Nature 441: 218–222.

5. BetancurP, Bronner-FraserM, Sauka-SpenglerT (2010) Genomic code for Sox10 activation reveals a key regulatory enhancer for cranial neural crest. Proc Natl Acad Sci U S A 107: 3570–3575.

6. HromasR, YeH, SpinellaM, DmitrovskyE, XuD, et al. (1999) Genesis, a Winged Helix transcriptional repressor, has embryonic expression limited to the neural crest, and stimulates proliferation in vitro in a neural development model. Cell Tissue Res 297: 371–382.

7. KosR, ReedyMV, JohnsonRL, EricksonCA (2001) The winged-helix transcription factor FoxD3 is important for establishing the neural crest lineage and repressing melanogenesis in avian embryos. Development 128: 1467–1479.

8. LaboskyPA, KaestnerKH (1998) The winged helix transcription factor Hfh2 is expressed in neural crest and spinal cord during mouse development. Mech Dev 76: 185–190.

9. ListerJA, CooperC, NguyenK, ModrellM, GrantK, et al. (2006) Zebrafish Foxd3 is required for development of a subset of neural crest derivatives. Dev Biol 290: 92–104.

10. PohlBS, KnochelW (2001) Overexpression of the transcriptional repressor FoxD3 prevents neural crest formation in Xenopus embryos. Mech Dev 103: 93–106.

11. SasaiN, MizusekiK, SasaiY (2001) Requirement of FoxD3-class signaling for neural crest determination in Xenopus. Development 128: 2525–2536.

12. YamagataM, NodaM (1998) The winged-helix transcription factor CWH-3 is expressed in developing neural crest cells. Neurosci Lett 249: 33–36.

13. DottoriM, GrossMK, LaboskyP, GouldingM (2001) The winged-helix transcription factor Foxd3 suppresses interneuron differentiation and promotes neural crest cell fate. Development 128: 4127–4138.

14. Montero-BalaguerM, LangMR, SachdevSW, KnappmeyerC, StewartRA, et al. (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.

15. StewartRA, ArduiniBL, BerghmansS, GeorgeRE, KankiJP, et al. (2006) Zebrafish foxd3 is selectively required for neural crest specification, migration and survival. Dev Biol 292: 174–188.

16. ThomasAJ, EricksonCA (2009) FoxD3 regulates the lineage switch between neural crest-derived glial cells and pigment cells by repressing MITF through a non-canonical mechanism. Development 136: 1849–1858.

17. UchikawaM, IshidaY, TakemotoT, KamachiY, KondohH (2003) Functional analysis of chicken Sox2 enhancers highlights an array of diverse regulatory elements that are conserved in mammals. Dev Cell 4: 509–519.

18. ShiauCE, DasRM, StoreyKG (2011) An effective assay for high cellular resolution time-lapse imaging of sensory placode formation and morphogenesis. BMC Neurosci 12: 37.

19. ChoiHM, ChangJY, Trinh leA, PadillaJE, FraserSE, et al. (2010) Programmable in situ amplification for multiplexed imaging of mRNA expression. Nat Biotechnol 28: 1208–1212.

20. HongCS, Saint-JeannetJP (2007) The activity of Pax3 and Zic1 regulates three distinct cell fates at the neural plate border. Mol Biol Cell 18: 2192–2202.

21. Monsoro-BurqAH, WangE, HarlandR (2005) Msx1 and Pax3 cooperate to mediate FGF8 and WNT signals during Xenopus neural crest induction. Dev Cell 8: 167–178.

22. SatoT, SasaiN, SasaiY (2005) Neural crest determination by co-activation of Pax3 and Zic1 genes in Xenopus ectoderm. Development 132: 2355–2363.

23. Sauka-SpenglerT, MeulemansD, JonesM, Bronner-FraserM (2007) Ancient evolutionary origin of the neural crest gene regulatory network. Dev Cell 13: 405–420.

24. TengL, MundellNA, FristAY, WangQ, LaboskyPA (2008) Requirement for Foxd3 in the maintenance of neural crest progenitors. Development 135: 1615–1624.

25. IgnatiusMS, MooseHE, El-HodiriHM, HenionPD (2008) colgate/hdac1 Repression of foxd3 expression is required to permit mitfa-dependent melanogenesis. Dev Biol 313: 568–583.

26. RelaixF, RocancourtD, MansouriA, BuckinghamM (2004) Divergent functions of murine Pax3 and Pax7 in limb muscle development. Genes Dev 18: 1088–1105.

27. SoleimaniVD, PunchVG, KawabeY, JonesAE, PalidworGA, et al. (2012) Transcriptional dominance of Pax7 in adult myogenesis is due to high-affinity recognition of homeodomain motifs. Dev Cell 22: 1208–1220.

28. MansouriA, StoykovaA, TorresM, GrussP (1996) Dysgenesis of cephalic neural crest derivatives in Pax7−/− mutant mice. Development 122: 831–838.

29. MaczkowiakF, MateosS, WangE, RocheD, HarlandR, et al. (2010) The Pax3 and Pax7 paralogs cooperate in neural and neural crest patterning using distinct molecular mechanisms, in Xenopus laevis embryos. Dev Biol 340: 381–396.

30. OttoA, SchmidtC, PatelK (2006) Pax3 and Pax7 expression and regulation in the avian embryo. Anat Embryol (Berl) 211: 293–310.

31. LacostaAM, CanudasJ, GonzalezC, MuniesaP, SarasaM, et al. (2007) Pax7 identifies neural crest, chromatophore lineages and pigment stem cells during zebrafish development. Int J Dev Biol 51: 327–331.

32. SatokataI, MaasR (1994) Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet 6: 348–356.

33. SatokataI, MaL, OhshimaH, BeiM, WooI, et al. (2000) Msx2 deficiency in mice causes pleiotropic defects in bone growth and ectodermal organ formation. Nat Genet 24: 391–395.

34. IshiiM, HanJ, YenHY, SucovHM, ChaiY, et al. (2005) Combined deficiencies of Msx1 and Msx2 cause impaired patterning and survival of the cranial neural crest. Development 132: 4937–4950.

35. AlappatS, ZhangZY, ChenYP (2003) Msx homeobox gene family and craniofacial development. Cell Res 13: 429–442.

36. OgawaT, KapadiaH, FengJQ, RaghowR, PetersH, et al. (2006) Functional consequences of interactions between Pax9 and Msx1 genes in normal and abnormal tooth development. J Biol Chem 281: 18363–18369.

37. ZhuangF, NguyenMP, ShulerC, LiuYH (2009) Analysis of Msx1 and Msx2 transactivation function in the context of the heat shock 70 (Hspa1b) gene promoter. Biochem Biophys Res Commun 381: 241–246.

38. TheveneauE, DubandJL, AltabefM (2007) Ets-1 confers cranial features on neural crest delamination. PLoS ONE 2: e1142 doi:10.1371/journal.pone.0001142.

39. BetancurP, Sauka-SpenglerT, BronnerM (2011) A Sox10 enhancer element common to the otic placode and neural crest is activated by tissue-specific paralogs. Development 138: 3689–3698.

40. YeM, ColdrenC, LiangX, MattinaT, GoldmuntzE, et al. (2009) Deletion of ETS-1, a gene in the Jacobsen syndrome critical region, causes ventricular septal defects and abnormal ventricular morphology in mice. Hum Mol Genet 19: 648–656.

41. MeyerD, DurliatM, SenanF, WolffM, AndreM, et al. (1997) Ets-1 and Ets-2 proto-oncogenes exhibit differential and restricted expression patterns during Xenopus laevis oogenesis and embryogenesis. Int J Dev Biol 41: 607–620.

42. GaoZ, KimGH, MackinnonAC, FlaggAE, BassettB, et al. (2010) Ets1 is required for proper migration and differentiation of the cardiac neural crest. Development 137: 1543–1551.

43. TahtakranSA, SelleckMA (2003) Ets-1 expression is associated with cranial neural crest migration and vasculogenesis in the chick embryo. Gene Expr Patterns 3: 455–458.

44. HonoreSM, AybarMJ, MayorR (2003) Sox10 is required for the early development of the prospective neural crest in Xenopus embryos. Dev Biol 260: 79–96.

45. NichaneM, RenX, SouopguiJ, BellefroidEJ (2008) Hairy2 functions through both DNA-binding and non DNA-binding mechanisms at the neural plate border in Xenopus. Dev Biol 322: 368–380.

46. Perez-AlcalaS, NietoMA, BarbasJA (2004) LSox5 regulates RhoB expression in the neural tube and promotes generation of the neural crest. Development 131: 4455–4465.

47. Le Douarin N, Kalcheim C (1999) The neural crest. Cambridge: Cambridge University Press. xxiii, 445p. p.

48. BarlowAJ, WallaceAS, ThaparN, BurnsAJ (2008) Critical numbers of neural crest cells are required in the pathways from the neural tube to the foregut to ensure complete enteric nervous system formation. Development 135: 1681–1691.

49. YuJK, MeulemansD, McKeownSJ, Bronner-FraserM (2008) Insights from the amphioxus genome on the origin of vertebrate neural crest. Genome Res 18: 1127–1132.

50. McKeownSJ, LeeVM, Bronner-FraserM, NewgreenDF, FarliePG (2005) Sox10 overexpression induces neural crest-like cells from all dorsoventral levels of the neural tube but inhibits differentiation. Dev Dyn 233: 430–444.

51. AcloqueH, WilkinsonDG, NietoMA (2008) In situ hybridization analysis of chick embryos in whole-mount and tissue sections. Methods Cell Biol 87: 169–185.

52. AredeN, TavaresAT (2008) Modified whole-mount in situ hybridization protocol for the detection of transgene expression in electroporated chick embryos. PLoS ONE 3: e2638 doi:10.1371/journal.pone.0002638.

53. DenkersN, Garcia-VillalbaP, RodeschCK, NielsonKR, MauchTJ (2004) FISHing for chick genes: Triple-label whole-mount fluorescence in situ hybridization detects simultaneous and overlapping gene expression in avian embryos. Dev Dyn 229: 651–657.

54. EzinAM, FraserSE, Bronner-FraserM (2009) Fate map and morphogenesis of presumptive neural crest and dorsal neural tube. Dev Biol 330: 221–236.

55. HeckmanKL, PeaseLR (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc 2: 924–932.

56. KarafiatV, DvorakovaM, KrejciE, KralovaJ, PajerP, et al. (2005) Transcription factor c-Myb is involved in the regulation of the epithelial-mesenchymal transition in the avian neural crest. Cell Mol Life Sci 62: 2516–2525.