Wnt/β-catenin and FGF signalling direct the specification and maintenance of a neuromesodermal axial progenitor in ensembles of mouse embryonic stem cells

Development (Cambridge)

Volumn 141, Issue 22, 2014, Pages 4243-4253

  Turner, David A ^a   Hayward, Penelope C ^a   Baillie Johnson, Peter ^a   Rué, Pau ^a   Broome, Rebecca ^a   Faunes, Fernando ^a   Arias, Alfonso Martinez ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Mesodermal; Morphogenesis; Neural; Stem cells; Wnt signalling

Indexed keywords

BETA CATENIN; FIBROBLAST GROWTH FACTOR; WNT PROTEIN;

ADHERENT CELL; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL POPULATION; EMBRYONIC STEM CELL; GENE EXPRESSION; MOUSE; NEUROMESODERMAL AXIAL PRECURSOR; NONHUMAN; SIGNAL TRANSDUCTION; SINGLE CELL ANALYSIS; STEM CELL; WNT SIGNALING PATHWAY; ANIMAL; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; CULTURE TECHNIQUE; EMBRYO INDUCTION; EMBRYOLOGY; FLOW CYTOMETRY; FLUORESCENCE; GENE EXPRESSION REGULATION; MESODERM; MORPHOGENESIS; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TIME LAPSE IMAGING;

ANIMALS; CELL CULTURE TECHNIQUES; CELL LINEAGE; CENTRAL NERVOUS SYSTEM; EMBRYONIC INDUCTION; FIBROBLAST GROWTH FACTORS; FLOW CYTOMETRY; FLUORESCENCE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MESODERM; MICE; MORPHOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION; SINGLE-CELL ANALYSIS; TIME-LAPSE IMAGING; WNT SIGNALING PATHWAY;

EID: 84908398512     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.112979     Document Type: Article

References (79)

1. Abranches, E., Silva, M., Pradier, L., Schulz, H., Hummel, O., Henrique, D. and Bekman, E. (2009). Neural differentiation of embryonic stem cells in vitro: a road map to neurogenesis in the embryo. PLoS ONE 4, e6286.
2. Andoniadou, C. L. and Martinez-Barbera, J. P. (2013). Developmental mechanisms directing early anterior forebrain specification in vertebrates. Cell. Mol. Life Sci. 70, 3739-3752.
3. Ang, S.-L. and Rossant, J. (1994). HNF-3 beta is essential for node and notochord formation in mouse development. Cell 78, 561-574.
4. Ang, S. L., Wierda, A., Wong, D., Stevens, K. A., Cascio, S., Rossant, J. and Zaret, K. S. (1993). The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119, 1301-1315.
5. Arnold, S. J. and Robertson, E. J. (2009). Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat. Rev. Mol. Cell Biol. 10, 91-103.
6. Aulehla, A. and Pourquie, O. (2010). Signaling gradients during paraxial mesoderm development. Cold Spring Harb. Perspect. Biol. 2, a000869.
7. Aulehla, A., Wiegraebe, W., Baubet, V., Wahl, M. B., Deng, C., Taketo, M., Lewandoski, M. and Pourquié, O. (2008). A beta-catenin gradient links the clock and wavefront systems in mouse embryo segmentation. Nat. Cell Biol. 10, 186-193.
8. Baillie-Johnson, P., van den Brink, S. C., Balayo, T., Turner, D. A. and Martinez Arias, A. (2014). Generation of aggregates of mouse ES cells that show symmetry breaking, polarisation and emergent collective behaviour in vitro. Biorxiv.
9. Brown, J. M. and Storey, K. G. (2000). A region of the vertebrate neural plate in which neighbouring cells can adopt neural or epidermal fates. Curr. Biol. 10, 869-872.
10. Cambray, N. and Wilson, V. (2002). Axial progenitors with extensive potency are localised to the mouse chordoneural hinge. Development 129, 4855-4866.
11. Cambray, N. and Wilson, V. (2007). Two distinct sources for a population of maturing axial progenitors. Development 134, 2829-2840.
12. Davidson, B. P., Kinder, S. J., Steiner, K., Schoenwolf, G. C. and Tam, P. P. L. (1999). Impact of node ablation on the morphogenesis of the body axis and the lateral asymmetry of the mouse embryo during early organogenesis. Dev. Biol. 211, 11-26.
13. De Robertis, E. M. (2009). Spemann’s organizer and the self-regulation of embryonic fields. Mech. Dev. 126, 925-941.
14. De Robertis, E. M., Larraín, J., Oelgeschläger, M. and Wessely, O. (2000). The establishment of Spemann’s organizer and patterning of the vertebrate embryo. Nat. Rev. Genet. 1, 171-181.
15. De Robertis, E. M., Wessely, O., Oelgeschlager, M., Brizuela, B., Pera, E., Larrain, J., Abreu, J. and Bachiller, D. (2001). Molecular mechanisms of cell-cell signaling by the Spemann-Mangold organizer. Int. J. Dev. Biol. 45, 189-197.
16. Delfino-Machin, M., Lunn, J. S., Breitkreuz, D. N., Akai, J. and Storey, K. G. (2005). Specification and maintenance of the spinal cord stem zone. Development 132, 4273-4283.
17. Dunty, W. C., Jr., Biris, K. K., Chalamalasetty, R. B., Taketo, M. M., Lewandoski, M. and Yamaguchi, T. P. (2008). Wnt3a/beta-catenin signaling controls posterior body development by coordinating mesoderm formation and segmentation. Development 135, 85-94.
18. Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., Wataya, T., Nishiyama, A., Muguruma, K. and Sasai, Y. (2008). Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519-532.
19. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., Sekiguchi, K., Adachi, T. and Sasai, Y. (2011). Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56.
20. Faunes, F., Hayward, P., Muñoz-Descalzo, S., Chatterjee, S. S., Balayo, T., Trott, J., Christophorou, A., Ferrer-Vaquer, A., Hadjantonakis, A.-K., DasGupta, R. et al. (2013). A membrane-associated β-catenin/Oct4 complex correlates with ground-state pluripotency in mouse embryonic stem cells. Development 140, 1171-1183.
21. Gadue, P., Huber, T. L., Nostro, M. C., Kattman, S. and Keller, G. M. (2005). Germ layer induction from embryonic stem cells. Exp. Hematol. 33, 955-964.
22. Gouti, M., Tsakiridis, A., Wymeersch, F. J., Huang, Y., Kleinjung, J. et al. (2014). In Vitro Generation of Neuromesodermal Progenitors Reveals Distinct Roles for Wnt Signalling in the Specification of Spinal Cord and Paraxial MesodermIdentity. PLoS Biol. 12(8), e1001937.
23. Graham, V., Khudyakov, J., Ellis, P. and Pevny, L. (2003). SOX2 functions to maintain neural progenitor identity. Neuron 39, 749-765.
24. Hamburger, V. (2001). Induction of embryonic primordia by implantation of organizers from a different species. Int. J. Dev. Biol. 45, 13-38.
25. Hemmati-Brivanlou, A. and Melton, D. (1997a). Vertebrate embryonic cells will become nerve cells unless told otherwise. Cell 88, 13-17.
26. Hemmati-Brivanlou, A. and Melton, D. (1997b). Vertebrate neural induction. Annu. Rev. Neurosci. 20, 43-60.
27. Hu, G. and Wade, P. A. (2012). NuRD and pluripotency: a complex balancing act. Cell Stem Cell 10, 497-503.
28. Kaji, K., Caballero, I. M., MacLeod, R., Nichols, J., Wilson, V. A. and Hendrich, B. (2006). The NuRD component Mbd3 is required for pluripotency of embryonic stem cells. Nat. Cell Biol. 8, 285-292.
29. Kamachi, Y. and Kondoh, H. (2013). Sox proteins: regulators of cell fate specification and differentiation. Development 140, 4129-4144.
30. Kamachi, Y., Iwafuchi, M., Okuda, Y., Takemoto, T., Uchikawa, M. and Kondoh, H. (2009). Evolution of non-coding regulatory sequences involved in the developmental process: reflection of differential employment of paralogous genes as highlighted by Sox2 and group B1 Sox genes. Proc. Jpn. Acad. B Phys. Biol. Sci. 85, 55-68.
31. Kiecker, C. and Niehrs, C. (2001). A morphogen gradient of Wnt/beta-catenin signalling regulates anteroposterior neural patterning in Xenopus. Development 128, 4189-4201.
32. Kim, W.-Y., Wang, X., Wu, Y., Doble, B.W., Patel, S., Woodgett, J. R. and Snider, W. D. (2009). GSK-3 is a master regulator of neural progenitor homeostasis. Nat. Neurosci. 12, 1390-1397.
33. Klingensmith, J., Ang, S.-L., Bachiller, D. and Rossant, J. (1999). Neural induction and patterning in the mouse in the absence of the node and its derivatives. Dev. Biol. 216, 535-549.
34. Kondoh, H. and Takemoto, T. (2012). Axial stem cells deriving both posterior neural and mesodermal tissues during gastrulation. Curr. Opin. Genet. Dev. 22, 374-380.
35. Lancaster, M. A., Renner, M., Martin, C.-A., Wenzel, D., Bicknell, L. S., Hurles, M. E., Homfray, T., Penninger, J. M., Jackson, A. P. and Knoblich, J. A. (2013). Cerebral organoids model human brain development and microcephaly. Nature 501, 373-379.
36. Mangold, O. (1933). Über die Induktionsfä higkeit der verschiedenen Bezirke der Neurula von Urodelen. Naturwissenschaften 21, 761-766.
37. Martinez Arias, A. and Brickman, J. M. (2011). Gene expression heterogeneities in embryonic stem cell populations: origin and function. Curr. Opin. Cell Biol. 23, 650-656.
38. Mathis, L. and Nicolas, J. F. (2000). Different clonal dispersion in the rostral and caudal mouse central nervous system. Development 127, 1277-1290.
39. Mathis, L., Kulesa, P. M. and Fraser, S. E. (2001). FGF receptor signalling is required to maintain neural progenitors during Hensen’s node progression. Nat. Cell Biol. 3, 559-566.
40. Mazzoni, E. O., Mahony, S., Peljto, M., Patel, T., Thornton, S. R., McCuine, S., Reeder, C., Boyer, L. A., Young, R. A., Gifford, D. K. et al. (2013). Saltatory remodeling of Hox chromatin in response to rostrocaudal patterning signals. Nat. Neurosci. 16, 1191-1198.
41. Munoz Descalzo, S., Rue, P., Faunes, F., Hayward, P., Jakt, L. M., Balayo, T., Garcia-Ojalvo, J. and Martinez Arias, A. (2013). A competitive protein interaction network buffers Oct4-mediated differentiation to promote pluripotency in embryonic stem cells. Mol. Syst. Biol. 9, 694.
42. Nieuwkoop, P. and Nigtevecht, G. V. (1954). Neural activation and transformation in explants of competent ectoderm under the influence of fragments of anterior notochord in Urodeles. J. Embryol. Exp. Morphol. 2, 175-193.
43. Nieuwkoop, P. D., Boterenbrood, E. C., Kremer, A., Bloesma, F. F. S. N., Hoessels, E. L. M. J., Meyer, G. and Verheyen, F. J. (1952). Activation and organisation of the central nervous system in amphibians. J. Exp. Zool. 120, 1-108.
44. Nordström, U., Jessell, T. M. and Edlund, T. (2002). Progressive induction of caudal neural character by graded Wnt signaling. Nat. Neurosci. 5, 525-532.
45. Nordström, U., Maier, E., Jessell, T. M. and Edlund, T. (2006). An early role for WNT signaling in specifying neural patterns of Cdx and Hox gene expression and motor neuron subtype identity. PLoS Biol. 4, e252.
46. Nowotschin, S., Ferrer-Vaquer, A., Concepcion, D., Papaioannou, V. E. and Hadjantonakis, A.-K. (2012). Interaction of Wnt3a, Msgn1 and Tbx6 in neural versus paraxial mesoderm lineage commitment and paraxial mesoderm differentiation in the mouse embryo. Dev. Biol. 367, 1-14.
47. Otero, J. J., Fu, W., Kan, L., Cuadra, A. E. and Kessler, J. A. (2004). Beta-catenin signaling is required for neural differentiation of embryonic stem cells. Development 131, 3545-3557.
48. Pevny, L. H., Sockanathan, S., Placzek, M. and Lovell-Badge, R. (1998). A role for SOX1 in neural determination. Development 125, 1967-1978.
49. Rossant, J. and Tam, P. P. L. (2009). Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701-713.
50. Roszko, I., Faure, P. and Mathis, L. (2007). Stemcell growth becomes predominant while neural plate progenitor pool decreases during spinal cord elongation. Dev. Biol. 304, 232-245.
51. Sasai, Y. (2013). Next-generation regenerative medicine: organogenesis from stem cells in 3D culture. Cell Stem Cell 12, 520-530.
52. Sasai, Y., Eiraku, M. and Suga, H. (2012). In vitro organogenesis in three dimensions: self-organising stem cells. Development 139, 4111-4121.
53. Saxén, L. and Toivonen, S. (1961). The two-gradient hypothesis in primary induction: the combined effect of two types of inducers mixed in different ratios. J. Embryol. Exp. Morph. 9, 514-533.
54. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676-682.
55. Shyh-Chang, N. and Daley, G. Q. (2013). Lin28: primal regulator of growth and metabolism in stem cells. Cell Stem Cell 12, 395-406.
56. Slawny, N. A. and O’Shea, K. S. (2011). Dynamic changes in Wnt signaling are required for neuronal differentiation of mouse embryonic stem cells. Mol. Cell. Neurosci. 48, 205-216.
57. Spemann, H. and Mangold, H. (1924). Über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. Arch. Mikrosk. Anat. Entwicklungsmechanick 100, 599-638.
58. Stern, C. D. (2005). Neural induction: old problem, new findings, yet more questions. Development 132, 2007-2021.
59. Stern, C. D., Charite, J., Deschamps, J., Duboule, D., Durston, A. J., Kmita, M., Nicolas, J.-F., Palmeirim, I., Smith, J. C. and Wolpert, L. (2006). Head-tail patterning of the vertebrate embryo: one, two or many unresolved problems? Int. J. Dev. Biol. 50, 3-15.
60. Sterneckert, J., Stehling, M., Bernemann, C., Araúzo-Bravo, M. J., Greber, B., Gentile, L., Ortmeier, C., Sinn, M., Wu, G., Ruau, D. et al. (2010). Neural induction intermediates exhibit distinct roles of Fgf signaling. Stem Cells 28, 1772-1781.
61. Storey, K. G., Goriely, A., Sargent, C. M., Brown, J. M., Burns, H. D., Abud, H. M. and Heath, J. K. (1998). Early posterior neural tissue is induced by FGF in the chick embryo. Development 125, 473-484.
62. Takemoto, T., Uchikawa, M., Kamachi, Y. and Kondoh, H. (2006). Convergence of Wnt and FGF signals in the genesis of posterior neural plate through activation of the Sox2 enhancer N-1. Development 133, 297-306.
63. Takemoto, T., Uchikawa, M., Yoshida, M., Bell, D. M., Lovell-Badge, R., Papaioannou, V. E. and Kondoh, H. (2011). Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 470, 394-398.
64. Thomson, M., Liu, S. J., Zou, L.-N., Smith, Z., Meissner, A. and Ramanathan, S. (2011). Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 145, 875-889.
65. Tsakiridis, A., Huang, Y., Blin, G., Skylaki, S., Wymeersch, F., Osorno, R., Economou, C., Karagianni, E., Zhao, S., Lowell, S. et al. (2014). Distinct Wntdriven primitive streak-like populations reflect in vivo lineage precursors. Development 141, 1209-1221.
66. Turner, D. A., Rué, P., Mackenzie, J. P., Davies, E. and Martinez Arias, A. (2014a). Brachyury cooperates with Wnt/β-Catenin signalling to elicit primitivestreak- like behaviour in differentiating mouse ES cells. BMC Biol. 12, 63.
67. Turner, D. A., Trott, J., Hayward, P., Rue, P. and Martinez Arias, A. (2014b). An interplay between extracellular signalling and the dynamics of the exit from pluripotency drives cell fate decisions in mouse ES cells. Biol. Open 3, 614-626.
68. Tzouanacou, E., Wegener, A., Wymeersch, F. J., Wilson, V. and Nicolas, J.-F. (2009). Redefining the progression of lineage segregations during mammalian embryogenesis by clonal analysis. Dev. Cell 17, 365-376.
69. van den Brink, S. C., Baillie-Johnson, P., Balayo, T., Hadjantonakis, A.-K., Nowotschin, S., Turner, D. A. and Martinez Arias, A. (2014). Symmetry breaking, germ layer specification and axial organisation in aggregates of mouse embryonic stem cells. Development 141, 4231-4242.
70. van de Ven, C., Bialecka, M., Neijts, R., Young, T., Rowland, J. E., Stringer, E. J., Van Rooijen, C., Meijlink, F., Novoa, A., Freund, J.-N. et al. (2011). Concerted involvement of Cdx/Hox genes and Wnt signaling in morphogenesis of the caudal neural tube and cloacal derivatives from the posterior growth zone. Development 138, 3451-3462.
71. Viswanathan, S. R. and Daley, G. Q. (2010). Lin28: A microRNA regulator with a macro role. Cell 140, 445-449.
72. Watanabe, K., Kamiya, D., Nishiyama, A., Katayama, T., Nozaki, S., Kawasaki, H., Watanabe, Y., Mizuseki, K. and Sasai, Y. (2005). Directed differentiation of telencephalic precursors from embryonic stem cells. Nat. Neurosci. 8, 288-296.
73. Wataya, T., Ando, S., Muguruma, K., Ikeda, H., Watanabe, K., Eiraku, M., Kawada, M., Takahashi, J., Hashimoto, N. and Sasai, Y. (2008). Minimization of exogenous signals in ES cell culture induces rostral hypothalamic differentiation. Proc. Natl. Acad. Sci. USA 105, 11796-11801.
74. Weinstein, D. C., Ruiz i Altaba, A., Chen, W. S., Hoodless, P., Prezioso, V. R., Jessell, T. M. and Darnell, J. E., Jr. (1994). The winged-helix transcription factor HNF-3 beta is required for notochord development in the mouse embryo. Cell 78, 575-588.
75. Wills, A. E., Choi, V. M., Bennett, M. J., Khokha, M. K. and Harland, R. M. (2010). BMP antagonists and FGF signaling contribute to different domains of the neural plate in Xenopus. Dev. Biol. 337, 335-350.
76. Wilson, V., Olivera-Martinez, I. and Storey, K. G. (2009). Stem cells, signals and vertebrate body axis extension. Development 136, 1591-1604.
77. Ying, Q.-L., Stavridis, M., Griffiths, D., Li, M. and Smith, A. (2003). Conversion of embryonic stem cells into neuroectodermal precursors in adherent monoculture. Nat. Biotechnol. 21, 183-186.
78. Zechner, D., Fujita, Y., Hülsken, J., Müller, T., Walther, I., Taketo, M. M., Crenshaw, E. B., III, Birchmeier, W. and Birchmeier, C. (2003). Beta-Catenin signals regulate cell growth and the balance between progenitor cell expansion and differentiation in the nervous system. Dev. Biol. 258, 406-418.
79. Zhao, T., Zhou, X., Szabó, N., Leitges, M. and Alvarez-Bolado, G. (2007). Foxb1- driven Cre expression in somites and the neuroepithelium of diencephalon, brainstem, and spinal cord. Genesis 45, 781-787.