#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

An Otx/Nodal Regulatory Signature for Posterior Neural Development in Ascidians


The Chordate phylum groups vertebrates, tunicates (including ascidians) and cephalochordates (amphioxus). These animals share a typical body plan characterized by the presence during embryonic life of a notochord and a dorsal neural tube. Ascidians, however, took a significantly different evolutionary path from other chordates resulting in divergent morphological, embryological and genomic features. Their development is fast and stereotyped with very few cells and ascidian genomes have undergone compaction and extensive rearrangements when compared to vertebrates, but also between ascidian species. This raises the question of whether developmental mechanisms controlling typical chordate structure formation are conserved between ascidians and vertebrates. Here, we have studied the set of ascidian genes which control the formation of the posterior part of the nervous system. We uncovered original usages of the signaling molecule Nodal and the transcription factor Otx. For example, Otx, which is a specific determinant of anterior identity in most metazoans, has been co-opted for the formation of the ascidian posterior nervous system. These two factors define a regulatory signature found in enhancers of posterior neural genes in two genomically divergent ascidian species.


Vyšlo v časopise: An Otx/Nodal Regulatory Signature for Posterior Neural Development in Ascidians. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004548
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004548

Souhrn

The Chordate phylum groups vertebrates, tunicates (including ascidians) and cephalochordates (amphioxus). These animals share a typical body plan characterized by the presence during embryonic life of a notochord and a dorsal neural tube. Ascidians, however, took a significantly different evolutionary path from other chordates resulting in divergent morphological, embryological and genomic features. Their development is fast and stereotyped with very few cells and ascidian genomes have undergone compaction and extensive rearrangements when compared to vertebrates, but also between ascidian species. This raises the question of whether developmental mechanisms controlling typical chordate structure formation are conserved between ascidians and vertebrates. Here, we have studied the set of ascidian genes which control the formation of the posterior part of the nervous system. We uncovered original usages of the signaling molecule Nodal and the transcription factor Otx. For example, Otx, which is a specific determinant of anterior identity in most metazoans, has been co-opted for the formation of the ascidian posterior nervous system. These two factors define a regulatory signature found in enhancers of posterior neural genes in two genomically divergent ascidian species.


Zdroje

1. LevineAJ, BrivanlouAH (2007) Proposal of a model of mammalian neural induction. Dev Biol 308: 247–256 doi:10.1016/j.ydbio.2007.05.036

2. SternCD (2005) Neural induction: old problem, new findings, yet more questions. Development 132: 2007–2021.

3. HarlandR (2000) Neural induction. Curr Opin Genet Dev 10: 357–362.

4. AltmannCR, BrivanlouAH (2001) Neural patterning in the vertebrate embryo. Int Rev Cytol 203: 447–482.

5. NiehrsC (2004) Regionally specific induction by the Spemann–Mangold organizer. Nat Rev Genet 5: 425–434 doi:10.1038/nrg1347

6. RogersCD, MoodySA, CaseyES (2009) Neural induction and factors that stabilize a neural fate. Birth Defects Res Part C Embryo Today Rev 87: 249–262 doi:10.1002/bdrc.20157

7. HollandLZ (2009) Chordate roots of the vertebrate nervous system: expanding the molecular toolkit. Nat Rev Neurosci 10: 736–746.

8. Satoh N (2014) Developmental genomics of ascidians. Hoboken, New Jersey: John Wiley & Sons, Inc.

9. BertrandS, CamassesA, SomorjaiI, BelgacemMR, ChabrolO, et al. (2011) Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits. Proc Natl Acad Sci U S A 108: 9160–9165 doi:10.1073/pnas.1014235108

10. YuJK, SatouY, HollandND, ShinIT, KoharaY, et al. (2007) Axial patterning in cephalochordates and the evolution of the organizer. Nature 445: 613–617.

11. 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.

12. DarrasS, NishidaH (2001) The BMP/CHORDIN antagonism controls sensory pigment cell specification and differentiation in the ascidian embryo. Dev Biol 236: 271–288.

13. DavidsonEH, ErwinDH (2006) Gene regulatory networks and the evolution of animal body plans. Science 311: 796–800 doi:10.1126/science.1113832

14. LemaireP (2006) Developmental biology. How many ways to make a chordate? Science 312: 1145–1146.

15. Satoh N (1994) Developmental biology of ascidians. Cambridge: Cambridge University Press.

16. DehalP, SatouY, CampbellRK, ChapmanJ, DegnanB, et al. (2002) The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298: 2157–2167.

17. VoskoboynikA, NeffNF, SahooD, NewmanAM, PushkarevD, et al. (2013) The genome sequence of the colonial chordate, Botryllus schlosseri. eLife 2: e00569 doi:10.7554/eLife.00569

18. HollandLZ, AlbalatR, AzumiK, Benito-GutierrezE, BlowMJ, et al. (2008) The amphioxus genome illuminates vertebrate origins and cephalochordate biology. Genome Res 18: 1100–1111.

19. PutnamNH, ButtsT, FerrierDE, FurlongRF, HellstenU, et al. (2008) The amphioxus genome and the evolution of the chordate karyotype. Nature 453: 1064–1071.

20. LemaireP (2011) Evolutionary crossroads in developmental biology: the tunicates. Development 138: 2143–2152 doi:10.1242/dev.048975

21. Oda-IshiiI, BertrandV, MatsuoI, LemaireP, SaigaH (2005) Making very similar embryos with divergent genomes: conservation of regulatory mechanisms of Otx between the ascidians Halocynthia roretzi and Ciona intestinalis. Development 132: 1663–1674.

22. TakahashiH, MitaniY, SatohG, SatohN (1999) Evolutionary alterations of the minimal promoter for notochord-specific Brachyury expression in ascidian embryos. Development 126: 3725–3734.

23. ImaiKS, StolfiA, LevineM, SatouY (2009) Gene regulatory networks underlying the compartmentalization of the Ciona central nervous system. Development 136: 285–293.

24. IkutaT, SaigaH (2007) Dynamic change in the expression of developmental genes in the ascidian central nervous system: Revisit to the tripartite model and the origin of the midbrain–hindbrain boundary region. Dev Biol 312: 631–643 doi:10.1016/j.ydbio.2007.10.005

25. LemaireP, BertrandV, HudsonC (2002) Early steps in the formation of neural tissue in ascidian embryos. Dev Biol 252: 151–169.

26. MinokawaT, YagiK, MakabeKW, NishidaH (2001) Binary specification of nerve cord and notochord cell fates in ascidian embryos. Development 128: 2007–2017.

27. HudsonC, LemaireP (2001) Induction of anterior neural fates in the ascidian Ciona intestinalis. Mech Dev 100: 189–203.

28. HudsonC, DarrasS, CaillolD, YasuoH, LemaireP (2003) A conserved role for the MEK signalling pathway in neural tissue specification and posteriorisation in the invertebrate chordate, the ascidian Ciona intestinalis. Development 130: 147–159.

29. HudsonC, YasuoH (2005) Patterning across the ascidian neural plate by lateral Nodal signalling sources. Development 132: 1199–1210.

30. KhoueiryP, RothbacherU, OhtsukaY, DaianF, FrangulianE, et al. (2010) A cis-regulatory signature in ascidians and flies, independent of transcription factor binding sites. Curr Biol 20: 792–802 doi:10.1016/j.cub.2010.03.063

31. NishidaH (1987) Cell lineage analysis in ascidian embryos by intracellular injection of a tracer enzyme. III. Up to the tissue restricted stage. Dev Biol 121: 526–541.

32. PasiniA, AmielA, RothbacherU, RoureA, LemaireP, et al. (2006) Formation of the Ascidian Epidermal Sensory Neurons: Insights into the Origin of the Chordate Peripheral Nervous System. PLoS Biol 4: e225.

33. 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. Mech Dev 121: 463–474.

34. HudsonC, LotitoS, YasuoH (2007) Sequential and combinatorial inputs from Nodal, Delta2/Notch and FGF/MEK/ERK signalling pathways establish a grid-like organisation of distinct cell identities in the ascidian neural plate. Development 134: 3527–3537.

35. ImaiKS, LevineM, SatohN, SatouY (2006) Regulatory blueprint for a chordate embryo. Science 312: 1183–1187.

36. HudsonC, YasuoH (2006) A signalling relay involving Nodal and Delta ligands acts during secondary notochord induction in Ciona embryos. Development 133: 2855–2864.

37. 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.

38. Joyce TangW, ChenJS, ZellerRW (2013) Transcriptional regulation of the peripheral nervous system in Ciona intestinalis. Dev Biol 378: 183–193 doi:10.1016/j.ydbio.2013.03.016

39. RothbacherU, BertrandV, LamyC, LemaireP (2007) A combinatorial code of maternal GATA, Ets and beta-catenin-TCF transcription factors specifies and patterns the early ascidian ectoderm. Development 134: 4023–4032.

40. LamyC, RothbacherU, CaillolD, LemaireP (2006) Ci-FoxA-a is the earliest zygotic determinant of the ascidian anterior ectoderm and directly activates Ci-sFRP1/5. Development 133: 2835–2844.

41. OhtaN, SatouY (2013) Multiple signaling pathways coordinate to induce a threshold response in a chordate embryo. PLoS Genet 9: e1003818 doi:10.1371/journal.pgen.1003818

42. HaeusslerM, JaszczyszynY, ChristiaenL, JolyJS (2010) A cis-regulatory signature for chordate anterior neuroectodermal genes. PLoS Genet 6: e1000912 doi:10.1371/journal.pgen.1000912

43. SchierAF (2003) Nodal signaling in vertebrate development. Annu Rev Cell Dev Biol 19: 589–621 doi:10.1146/annurev.cellbio.19.041603.094522

44. MassaguéJ, SeoaneJ, WottonD (2005) Smad transcription factors. Genes Dev 19: 2783–2810 doi:10.1101/gad.1350705

45. GomisRR, AlarconC, HeW, WangQ, SeoaneJ, et al. (2006) A FoxO-Smad synexpression group in human keratinocytes. Proc Natl Acad Sci U A 103: 12747–12752.

46. SilvestriC, NarimatsuM, von BothI, LiuY, TanNB, et al. (2008) Genome-wide identification of Smad/Foxh1 targets reveals a role for Foxh1 in retinoic acid regulation and forebrain development. Dev Cell 14: 411–423.

47. Portales-CasamarE, ThongjueaS, KwonAT, ArenillasD, ZhaoX, et al. (2010) JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38: D105–110 doi:10.1093/nar/gkp950

48. SatouY, MinetaK, OgasawaraM, SasakuraY, ShoguchiE, et al. (2008) Improved genome assembly and evidence-based global gene model set for the chordate Ciona intestinalis: new insight into intron and operon populations. Genome Biol 9: R152.

49. FrazerKA, PachterL, PoliakovA, RubinEM, DubchakI (2004) VISTA: computational tools for comparative genomics. Nucleic Acids Res 32: W273–279 doi:10.1093/nar/gkh458

50. KuboA, SuzukiN, YuanX, NakaiK, SatohN, et al. (2010) Genomic cis-regulatory networks in the early Ciona intestinalis embryo. Development 137: 1613–1623 doi:10.1242/dev.046789

51. RoureA, RothbacherU, RobinF, KalmarE, FeroneG, et al. (2007) A multicassette Gateway vector set for high throughput and comparative analyses in ciona and vertebrate embryos. PLoS ONE 2: e916.

52. 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.

53. CarlssonP, MahlapuuM (2002) Forkhead transcription factors: key players in development and metabolism. Dev Biol 250: 1–23.

54. YagiK, SatouY, MazetF, ShimeldSM, DegnanB, et al. (2003) A genomewide survey of developmentally relevant genes in Ciona intestinalis. III. Genes for Fox, ETS, nuclear receptors and NFkappaB. Dev Genes Evol 213: 235–244.

55. WagnerE, LevineM (2012) FGF signaling establishes the anterior border of the Ciona neural tube. Dev Camb Engl 139: 2351–2359 doi:10.1242/dev.078485

56. BoylPP, SignoreM, AnninoA, BarberaJP, AcamporaD, et al. (2001) Otx genes in the development and evolution of the vertebrate brain. Int J Dev Neurosci Off J Int Soc Dev Neurosci 19: 353–363.

57. LichtneckertR, ReichertH (2005) Insights into the urbilaterian brain: conserved genetic patterning mechanisms in insect and vertebrate brain development. Heredity 94: 465–477 doi:10.1038/sj.hdy.6800664

58. WadaS, KatsuyamaY, SatoY, ItohC, SaigaH (1996) Hroth an orthodenticle-related homeobox gene of the ascidian, Halocynthia roretzi: its expression and putative roles in the axis formation during embryogenesis. Mech Dev 60: 59–71.

59. AkanumaT, NishidaH (2004) Ets-mediated brain induction in embryos of the ascidian Halocynthia roretzi. Dev Genes Evol 214: 1–9 doi:10.1007/s00427-003-0368-y

60. MiyaT, NishidaH (2003) An Ets transcription factor, HrEts, is target of FGF signaling and involved in induction of notochord, mesenchyme, and brain in ascidian embryos. Dev Biol 261: 25–38.

61. AngS-L, ConlonRA, JinO, RossantJ (1994) Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development 120: 2979–2989.

62. FeldmanB, DouganST, SchierAF, TalbotWS (2000) Nodal-related signals establish mesendodermal fate and trunk neural identity in zebrafish. Curr Biol 10: 531–534.

63. JiaS, WuD, XingC, MengA (2009) Smad2/3 activities are required for induction and patterning of the neuroectoderm in zebrafish. Dev Biol 333: 273–284 doi:10.1016/j.ydbio.2009.06.037

64. ThisseB, WrightCV, ThisseC (2000) Activin- and Nodal-related factors control antero-posterior patterning of the zebrafish embryo. Nature 403: 425–428 doi:10.1038/35000200

65. CamusA, Perea-GomezA, MoreauA, CollignonJ (2006) Absence of Nodal signaling promotes precocious neural differentiation in the mouse embryo. Dev Biol 295: 743–755 doi:10.1016/j.ydbio.2006.03.047

66. ChangC, HarlandRM (2007) Neural induction requires continued suppression of both Smad1 and Smad2 signals during gastrulation. Development 134: 3861–3872 doi:10.1242/dev.007179

67. MorokumaJ, UenoM, KawanishiH, SaigaH, NishidaH (2002) HrNodal, the ascidian nodal-related gene, is expressed in the left side of the epidermis, and lies upstream of HrPitx. Dev Genes Evol 212: 439–446.

68. HottaK, MitsuharaK, TakahashiH, InabaK, OkaK, et al. (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.

69. SatouY, YamadaL, MochizukiY, TakatoriN, KawashimaT, et al. (2002) A cDNA resource from the basal chordate Ciona intestinalis. Genesis 33: 153–154.

70. TassyO, DaugaD, DaianF, SobralD, RobinF, et al. (2010) The ANISEED database: digital representation, formalization, and elucidation of a chordate developmental program. Genome Res 20: 1459–1468 doi:10.1101/gr.108175.110

71. SatouY, KawashimaT, ShoguchiE, NakayamaA, SatohN (2005) An integrated database of the ascidian, Ciona intestinalis: towards functional genomics. Zool Sci 22: 837–843.

72. ShiW, LevineM (2008) Ephrin signaling establishes asymmetric cell fates in an endomesoderm lineage of the Ciona embryo. Development 135: 931–940.

73. MitaK, FujiwaraS (2007) Nodal regulates neural tube formation in the Ciona intestinalis embryo. Dev Genes Evol 217: 593–601.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 8
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#