Woodland, Hugh R. and Zorn, Aaron M.. (2008) The core endodermal gene network of vertebrates : combining developmental precision with evolutionary flexibility. BioEssays, Volume 30 (Number 8). pp. 757-765. ISSN 0265-9247

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Abstract

Embryonic development combines paradoxical properties: it has great precision, it is usually conducted at breakneck speed and it is flexible on relatively short evolutionary time scales, particularly at early stages. While these features appear mutually exclusive, we consider how they may be reconciled by the properties of key early regulatory networks. We illustrate these ideas with the network that controls development of endoderm progenitors. We argue that this network enables precision because of its intrinsic stability, self propagation and dependence on signalling. The network enables high developmental speed because it is rapidly established by maternal inputs at multiple points. In turn these properties confer flexibility on an evolutionary time scale because they can be initiated in many ways, while buffering essential progenitor cell populations against changes in their embryonic environment on both evolutionary and developmental time scales. Although stable, these networks must be capable of rapid dissolution as cell differentiation progresses. While we focus on the core early endodermal network of vertebrates, we argue that these properties are likely to be general in early embryonic stem cell populations, such as mammalian ES cells.

Item Type:	Journal Article
Subjects:	Q Science > QD Chemistry Q Science > QH Natural history > QH301 Biology Q Science > QH Natural history > QH426 Genetics
Divisions:	Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH):	Developmental biology, Gene regulatory networks, Vertebrates -- Evolution
Journal or Publication Title:	BioEssays
Publisher:	John Wiley & Sons Ltd.
ISSN:	0265-9247
Date:	August 2008
Volume:	Volume 30
Number:	Number 8
Number of Pages:	9
Page Range:	pp. 757-765
Identification Number:	10.1002/bies.20785
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	National Institutes of Health (U.S.) (NIH), Wellcome Trust (London, England)
Grant number:	HD42572 (NIH)
References:	1. Slack JMW, Holland PWH, Graham CF. 1993. The zootype and the phylotypic stage. Nature 361:490–492. 2. Dietrich JE, Hiiragi T. 2007. Stochastic patterning in the mouse preimplantation embryo. Development 134:4219–4231. 3. Zhang J, Houston DW, King ML, Payne C, Wylie C, Heasman J. 1998. The role of maternal VegT in establishing the primary germ layers in Xenopus embryos. Cell 94:515–524. 4. Yasuo H, Lemaire P. 1999. A two-step model for the fate determination of presumptive endodermal blastomeres in Xenopus embryos. Curr Biol 9: 869–879. 5. Xanthos JB, Kofron M, Wylie C, Heasman J. 2001. Maternal VegT is the initiator of a molecular network specifying endoderm in Xenopus laevis. Development 128:167–180. 6. Clements D, Friday RV, Woodland HR. 1999. Mode of action of VegT in mesoderm and endoderm formation. Development 126:4903– 4911. 7. Nath K, Elinson RP. 2007. RNA of AmVegT, the axolotl orthologue of the Xenopus meso-endodermal determinant, is not localized in the oocyte. Gene Expr Patterns 7:197–201. 8. Griffin KJP, Amacher SL, Kimmel CB, Kimelman D. 1998. Molecular identification of spadetail: regulation of zebrafish trunk and tail mesoderm formation by T-box genes. Development 125:3379–3388. 9. Ruvinsky I, Silver LM, Ho RK. 1998. Characterization of the zebrafish tbx16 gene and evolution of the vertebrate T-box family. Dev Genes Evol 208:94–99. 10. Bjornson CRR, Griffin KJR, Farr GH, Terashima A, Himeda C et al. 2005. Eomesodermin is a localized maternal determinant required for endoderm induction in zebrafish. Dev Cell 9:523–533. 11. Gore AV, Maegawa S, Cheong A, Gilligan PC, Weinberg ES, Sampath K. 2005. The zebrafish dorsal axis is apparent at the four-cell stage. Nature 438:1030–1035. 12. Bennett JT, Joubin K, Cheng S, Aanstad P, Herwig R et al. 2007. Nodal signaling activates differentiation genes during zebrafish gastrulation. Dev Biol 304:525–540. 13. Hagos EG, Fan X, Dougan ST. 2007. The role of maternal activin-like signals in zebrafish embryos. Dev Biol 309:245–258. 14. Gore AV, Cheong A, Gilligan PC, Sampath K. 2007. Gore et al. reply. Nature 450:E2–E4. 15. Pei W, Williams PH, Clark MD, Stemple DL, Feldman B. 2007. Environmental and genetic modifiers of squint penetrance during zebrafish embryogenesis. Dev Biol 308:368–378. 16. Zorn AM, Wells JM. 2007. Molecular basis of vertebrate endoderm development. Int Rev Cytol 259:49–111. 17. Arnold SJ, Hofmann UK, Bikoff EK, Robertson EJ. 2008. Pivotal roles for eomesodermin during axis formation, epithelium-to-mesenchyme transition and endoderm specification in the mouse. Development 135:501– 511. 18. Clements D, Rex M, Woodland HR. 2001. Initiation and early patterning of the endoderm. Interntl Rev Cytol 203:383–446. 19. Stainier DYR. 2002. A glimpse into the molecular entrails of endoderm formation. Genes Dev 16:893–907. 20. Sinner D, Kirilenko P, Rankin S, Wei E, Howard L* et al. 2006. Global analysis of the transcriptional network controlling Xenopus endoderm formation. Development 133:1955–1966. 21. Howard L, Rex M, Clements D, Woodland HR. 2007. Regulation of the Xenopus Xsox17b1 promoter by co-operating VegT and Sox17 sites. Dev Biol 310:402–415. 22. Schier AF. 2003. Nodal signaling in vertebrate development. Annu Rev Cell Dev Biol 19:589–621. 23. Toyoizumi R, Ogasawara T, Takeuchi S, Mogi K. 2005. Xenopus nodal related-1 is indispensable only for left-right axis determination. Int J Dev Biol 49:923–938. 24. Lunde K, Belting HG, Driever W. 2004. Zebrafish pou5f1/pou2, homolog of mammalian Oct4, functions in the endoderm specification cascade. Curr Biol 14:48–55. 25. Reim G, Mizoguchi T, Stainier DY, Kikuchi Y, Brand M. 2004. The POU domain protein Spg (Pou2/Oct4) is essential for endoderm formation in cooperation with the HMG domain protein Casanova. Dev Cell 6:91– 101. 26. Perea Gomez A, Shawlot W, Sasaki H, Behringer RR, Ang SL. 1999. HNF3b and Lim1 interact in the visceral endoderm to regulate primitive streak formation and anterior-posterior polarity in the mouse embryo. Development 126:4499–4511. 27. Kimura-Yoshida C, Tian E, Nakano H, Amazaki S, Shimokawa K et al. 2007. Crucial roles of Foxa2 in mouse anterior-posterior axis polarization via regulation of anterior visceral endoderm-specific genes. Proc Natl Acad Sci USA 104:5919–5924. 28. Ryan K, Garrett N, Mitchell A, Gurdon JB. 1996. Eomesodermin, a key early gene in Xenopus mesoderm differentiation. Cell 87:989–1000. 29. Sinner D, Rankin S, Lee M, Zorn AM. 2004. Sox17 and b-catenin cooperate to regulate the transcription of endodermal genes. Development 131:3069–3080. 30. Afouda BA, Ciau-Uitz A, Patient R. 2005. GATA4, 5 and 6 mediate TGFb maintenance of endodermal gene expression in Xenopus embryos. Development 132:763–774. 31. Davidson EH. The regulatory genome: gene regulatory networks in development and evolution Burlington, MA; San Diego: Academic Press; 2006. xi, 289 p. p. 32. Kirschner M, Gerhart J. 1998. Evolvability. Proc Natl Acad Sci USA 95:8420–8427. 33. Muller GB. 2007. Evo-devo: extending the evolutionary synthesis. Nat Rev Genet 8:943–949. 34. Hudson C, Clements D, Friday RV, Stott D, Woodland HR. 1997. Xsox17a and -b mediate endoderm formation in Xenopus. Cell 91:397–405. 35. Zorn AM, Mason J. 2001. Gene expression in the embryonic Xenopus liver. Mech Dev 103:153–157. 36. Gurdon JB, Lemaire P, Kato K. 1993. Community effects and related phenomena in development. Cell 75:831–834. 37. Clements D, Woodland HR. 2003. VegT induces endoderm by a selflimiting mechanism and by changing the competence of cells to respond to TGF-b signals. Dev Biol 258:454–463. 38. Clements D, Woodland HR. 2000. Changes in embryonic cell fate produced by expression of an endodermal transcription factor, Xsox17. Mech Dev 99:65–70. 39. Mir A, Kofron M, Zorn AM, Bajzer M, Haque M et al. 2007. Foxl1e activates ectoderm formation and controls cell position in the Xenopus blastula. Development 134:779–788. 40. Wardle FC, Smith JC. 2004. Refinement of gene expression patterns in the early Xenopus embryo. Development 131:4687–4696. 41. Wylie CC, Snape A, Heasman J, Smith JC. 1987. Vegetal pole cells and commitment to form endoderm in Xenopus laevis. Dev Biol 119:496– 502. 42. Germain S, Howell M, Esslemont GM, Hill CS. 2000. Homeodomain and winged-helix transcription factors recruit activated Smads to distinct promoter elements via a common Smad interaction motif. Genes Dev 14:435–451. 43. Cha SW, Hwang YS, Chae JP, Lee SY, Lee HS et al. 2004. Inhibition of FGF signaling causes expansion of the endoderm in Xenopus. Biochem Biophys Res Commun 315:100–106. 44. Liu F, van den Broek O, Destree O, Hoppler S. 2005. Distinct roles for Xenopus Tcf/Lef genes in mediating specific responses to Wnt/betacatenin signalling in mesoderm development. Development 132:5375– 5385. 45. Sinner D, Kordich JJ, Spence JR, Opoka R, Rankin S et al. 2007. Sox17 and Sox4 Differentially Regulate beta-catenin/T-cell factor activity and proliferation of colon carcinoma cells. Mol Cell Biol 27:7802–7815. 46. Love JJ, Li XA, Case DA, Giese K, Grosschedl R, Wright PE. 1995. Structural basis for DNA bending by the architectural transcription factor Lef-1. Nature: 376:791–795. 47. Furumatsu T, Tsuda M, Yoshida K, Taniguchi N, Ito T et al. 2005. Sox9 and p300 cooperatively regulate chromatin-mediated transcription. J. Biol Chem 280:35203–35208. 48. Ober EA, Field HA, Stainier DY. 2003. From endoderm formation to liver and pancreas development in zebrafish. Mech Dev 120:5–18. 49. Poulain M, Lepage T. 2002. Mezzo, a paired-like homeobox protein is an immediate target of Nodal signalling and regulates endoderm specification in zebrafish. Development 129:4901–4914. 50. Kikuchi Y, Trinh LA, Reiter JF, Alexander J, Yelon D, Stainier DYR. 2000. The zebrafish bonnie and clyde gene encodes a Mix family homeodomain protein that regulates the generation of endodermal precursors. Genes Dev 14:1279–1289. 51. Dufort D, Schwartz L, Harpal K, Rossant J. 1998. The transcription factor HNF3 beta is required in visceral endoderm for normal primitive streak morphogenesis. Development 125:3015–3025. 52. Hart AH, Hartley L, Sourris K, Stadler ES, Li R et al. 2002. Mixl1 is required for axial mesendoderm morphogenesis and patterning in the murine embryo. Development 129:3597–3608. 53. Kanai-Azuma M, Kanai Y, Gad JM, Tajima Y, Taya C et al. 2002. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129:2367–2379. 54. Zhao RO, Watt AJ, Li JX, Luebke-Wheeler J, Morrisey EE, Duncan SA. 2005. GATA6 is essential for embryonic development of the liver but dispensable for early heart formation. Mol Cell Biol 25:2622–2631. 55. Futaki S, Hayashi Y, Emoto T, Weber CN, Sekiguchi K. 2004. Sox7 plays crucial roles in parietal endoderm differentiation in F9 embryonal carcinoma cells through regulating Gata-4 and Gata-6 expression. Mol Cell Biol 24:10492–10503. 56. Nath K, Boorech JL, Beckham YM, Burns MM, Elinson RP. 2005. Status of RNAs, localized in Xenopus laevis oocytes, in the frogs Rana pipiens and Eleutherodactylus coqui. J. Exp Zool 304B:28–39. 57. Kirschner M, Gerhart J. The plausibility of life: resolving Darwin’s dilemma New Haven: Yale University Press; 2005. xiii, 314 p. 58. Momose T, Houliston E. 2007. Two oppositely localised frizzled RNAs as axis determinants in a Cnidarian embryo. PLoS Biol 5:889–899. 59. Hyde CE, Old RW. 2000. Regulation of the early expression of the Xenopus nodal-related 1 gene, Xnr1. Development 127:1221–1229. 60. Xanthos JB, Kofron M, Tao QH, Schaible K, Wylie C, Heasman J. 2002. The roles of three signaling pathways in the formation and function of the Spemann Organizer. Development 129:4027–4043. 61. Ben-Haim N, Lu C, Guzman-Ayala M, Pescatore L, Mesnard D et al. 2006. The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev Cell 11:313–323. 62. Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W. 2000. Requirement for beta-catenin in anterior-posterior axis formation in mice. J. Cell Biol 148:567–578. 63. Marikawa Y. 2006. Wnt/beta-catenin signaling and body plan formation in mouse embryos. Semin Cell Dev Biol 17:175–184. 64. Meinhardt H. Models of biological pattern formation: From elementary steps to the organization of embryonic axes. Multiscale Modeling of Developmental Systems. Volume 81, Current Topics in Developmental Biology; 2008. p 1–63. 65. Wernig M, Meissner A, Foreman R, Brambrink T, Ku M et al. 2007. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448:318–324. 66. Okita K, Ichisaka T, Yamanaka S. 2007. Generation of germlinecompetent induced pluripotent stem cells. Nature 448:313–317. 67. Meissner A, Wernig M, Jaenisch R. 2007. Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat Biotechnol 25:1177–1181. 68. Wilkins AS. 1995. Moving up the Hierarchy—a Hypothesis on the Evolution of a Genetic Sex Determination Pathway. Bioessays 17:71– 77. 69. Kubo A, Shinozaki K, Shannon JM, Kouskoff V, Kennedy M et al. 2004. Development of definitive endoderm from embryonic stem cells in culture. Development 131:1651–1662. 70. D’Amour KA, Agulnick AD, Eliazer S, Kelly OG, Kroon E, Baetge EE. 2005. Efficient differentiation of human embryonic stem cells to definitive endoderm. Nature Biotech 23:1534–1541. 71. Yasunaga M, Tada S, Nishikawa ST, Nakano Y, Okada M. et al. 2005. Induction and monitoring of definitive and visceral endoderm differentiation of mouse ES cells. Nature Biotech 23:1542–1550. 72. Tada S, Era T, Furusawa C, Sakurai H, Nishikawa S. et al. 2005. Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 132:4363–4374. 73. Wolpert L. Principles of development Oxford; New York: Oxford University Press; 2007. xxiii, 551 p.
URI:	http://wrap.warwick.ac.uk/id/eprint/29599

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