Distinct Wnt-driven primitive streak-like populations reflect in vivo lineage precursors

Development (Cambridge)

Volumn 141, Issue 6, 2014, Pages 1209-1221

  Tsakiridis, Anestis ^a   Huang, Yali ^a   Blin, Guillaume ^a   Skylaki, Stavroula ^a   Wymeersch, Filip ^a   Osorno, Rodrigo ^a   Economou, Costas ^a   Karagianni, Eleni ^a   Zhao, Suling ^a   Lowell, Sally ^a   Wilson, Valerie ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Epiblast stem cells; Gastrulation; Heterogeneity; Mouse; Neuromesodermal progenitors; Primitive Streak; Wnt signalling

Indexed keywords

WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL RENEWAL; CONTROLLED STUDY; ECTODERM; ENDODERM; EPIBLAST STEM CELL; GASTRULA; IN VIVO STUDY; MESODERM; MOUSE; NONHUMAN; PRIMITIVE STREAK; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEM CELL;

EPIBLAST STEM CELLS; GASTRULATION; HETEROGENEITY; MOUSE; NEUROMESODERMAL PROGENITORS; PRIMITIVE STREAK; WNT SIGNALLING;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; GASTRULA; GASTRULATION; GERM LAYERS; MICE; MICE, TRANSGENIC; NEURAL PLATE; PLURIPOTENT STEM CELLS; PRIMITIVE STREAK; WNT SIGNALING PATHWAY;

EID: 84896843351     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.101014     Document Type: Article

References (81)

1. Acampora, D., Di Giovannantonio, L. G. and Simeone, A. (2013). Otx2 is an intrinsic determinant of the embryonic stem cell state and is required for transition to a stable epiblast stem cell condition. Development 140, 43-55.
2. 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.
3. Arnold, S. J., Stappert, J., Bauer, A., Kispert, A., Herrmann, B. G. and Kemler, R. (2000). Brachyury is a target gene of the Wnt/beta-catenin signaling pathway. Mech. Dev. 91, 249-258.
4. Baldwin, H. S., Shen, H. M., Yan, H. C., DeLisser, H. M., Chung, A., Mickanin, C., Trask, T., Kirschbaum, N. E., Newman, P. J., Albelda, S. M. et al. (1994). Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 120, 2539-2553.
5. Beddington, S. P. (1981). An autoradiographic analysis of the potency of embryonic ectoderm in the 8th day postimplantation mouse embryo. J. Embryol. Exp. Morphol. 64, 87-104.
6. Beddington, R. S. (1982). An autoradiographic analysis of tissue potency in different regions of the embryonic ectoderm during gastrulation in the mouse. J. Embryol. Exp. Morphol. 69, 265-285.
7. Beddington, R. S. (1983). Histogenetic and neoplastic potential of different regions of the mouse embryonic egg cylinder. J. Embryol. Exp. Morphol. 75, 189-204.
8. Ben-Haim, N., Lu, C., Guzman-Ayala, M., Pescatore, L., Mesnard, D., Bischofberger, M., Naef, F., Robertson, E. J. and Constam, D. B. (2006). The nodal precursor acting via activin receptors induces mesoderm by maintaining a source of its convertases and BMP4. Dev. Cell 11, 313-323.
9. Bernemann, C., Greber, B., Ko, K., Sterneckert, J., Han, D. W., Araúzo-Bravo, M. J. and Schöler, H. R. (2011). Distinct developmental ground states of epiblast stem cell lines determine different pluripotency features. Stem Cells 29, 1496-1503.
10. Blauwkamp, T. A., Nigam, S., Ardehali, R., Weissman, I. L. and Nusse, R. (2012). Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat. Commun. 3, 1070.
11. Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O. and Kemler, R. (2001). Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264.
12. Brons, I. G., Smithers, L. E., Trotter, M. W., Rugg-Gunn, P., Sun, B., Chuva de Sousa Lopes, S. M., Howlett, S. K., Clarkson, A., Ahrlund-Richter, L., Pedersen, R. A. et al. (2007). Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448, 191-195.
13. Burtscher, I. and Lickert, H. (2009). Foxa2 regulates polarity and epithelialization in the endoderm germ layer of the mouse embryo. Development 136, 1029-1038.
14. Cajal, M., Lawson, K. A., Hill, B., Moreau, A., Rao, J., Ross, A., Collignon, J. and Camus, A. (2012). Clonal and molecular analysis of the prospective anterior neural boundary in the mouse embryo. Development 139, 423-436.
15. Cambray, N. and Wilson, V. (2007). Two distinct sources for a population of maturing axial progenitors. Development 134, 2829-2840.
16. Candia, A. F., Hu, J., Crosby, J., Lalley, P. A., Noden, D., Nadeau, J. H. and Wright, C. V. (1992). Mox-1 and Mox-2 define a novel homeobox gene subfamily and are differentially expressed during early mesodermal patterning in mouse embryos. Development 116, 1123-1136.
17. Canham, M. A., Sharov, A. A., Ko, M. S. and Brickman, J. M. (2010). Functional heterogeneity of embryonic stem cells revealed through translational amplification of an early endodermal transcript. PLoS Biol. 8, e1000379.
18. Chambers, I., Silva, J., Colby, D., Nichols, J., Nijmeijer, B., Robertson, M., Vrana, J., Jones, K., Grotewold, L. and Smith, A. (2007). Nanog safeguards pluripotency and mediates germline development. Nature 450, 1230-1234.
19. Chapman, D. L., Agulnik, I., Hancock, S., Silver, L. M. and Papaioannou, V. E. (1996). Tbx6, a mouse T-Box gene implicated in paraxial mesoderm formation at gastrulation. Dev. Biol. 180, 534-542.
20. Clements, D., Taylor, H. C., Herrmann, B. G. and Stott, D. (1996). Distinct regulatory control of the Brachyury gene in axial and non-axial mesoderm suggests separation of mesoderm lineages early in mouse gastrulation. Mech. Dev. 56, 139-149.
21. Conlon, F. L., Lyons, K. M., Takaesu, N., Barth, K. S., Kispert, A., Herrmann, B. and Robertson, E. J. (1994). A primary requirement for nodal in the formation and maintenance of the primitive streak in the mouse. Development 120, 1919-1928.
22. Davies, O. R., Lin, C. Y., Radzisheuskaya, A., Zhou, X., Taube, J., Blin, G., Waterhouse, A., Smith, A. J. and Lowell, S. (2013). Tcf15 primes pluripotent cells for differentiation. Cell Rep. 3, 472-484.
23. Deschamps, J., van den Akker, E., Forlani, S., De Graaff, W., Oosterveen, T., Roelen, B. and Roelfsema, J. (1999). Initiation, establishment and maintenance of Hox gene expression patterns in the mouse. Int. J. Dev. Biol. 43, 635-650.
24. Du, P., Kibbe, W. A. and Lin, S. M. (2008). lumi: a pipeline for processing Illumina microarray. Bioinformatics 24, 1547-1548.
25. Faunes, F., Hayward, P., Descalzo, S. M., Chatterjee, S. S., Balayo, T., Trott, J., Christoforou, A., Ferrer-Vaquer, A., Hadjantonakis, A. K., Dasgupta, R. et al. (2013). A membrane-associated β-catenin/Oct4 complex correlates with groundstate pluripotency in mouse embryonic stem cells. Development 140, 1171-1183.
26. Forlani, S., Lawson, K. A. and Deschamps, J. (2003). Acquisition of Hox codes during gastrulation and axial elongation in the mouse embryo. Development 130, 3807-3819.
27. Gadue, P., Huber, T. L., Paddison, P. J. and Keller, G. M. (2006). Wnt and TGF-beta signaling are required for the induction of an in vitro model of primitive streak formation using embryonic stem cells. Proc. Natl. Acad. Sci. USA 103, 16806-16811.
28. Gamer, L. W. and Wright, C. V. (1993). Murine Cdx-4 bears striking similarities to the Drosophila caudal gene in its homeodomain sequence and early expression pattern. Mech. Dev. 43, 71-81.
29. Gilchrist, D. S., Ure, J., Hook, L. and Medvinsky, A. (2003). Labeling of hematopoietic stem and progenitor cells in novel activatable EGFP reporter mice. Genesis 36, 168-176.
30. Goulding, M., Lumsden, A. and Paquette, A. J. (1994). Regulation of Pax-3 expression in the dermomyotome and its role in muscle development. Development 120, 957-971.
31. Greber, B., Wu, G., Bernemann, C., Joo, J. Y., Han, D. W., Ko, K., Tapia, N., Sabour, D., Sterneckert, J., Tesar, P. et al. (2010). Conserved and divergent roles of FGF signaling in mouse epiblast stem cells and human embryonic stem cells. Cell Stem Cell 6, 215-226.
32. Grindley, J. C., Davidson, D. R. and Hill, R. E. (1995). The role of Pax-6 in eye and nasal development. Development 121, 1433-1442.
33. Guo, G., Yang, J., Nichols, J., Hall, J. S., Eyres, I., Mansfield, W. and Smith, A. (2009). Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 136, 1063-1069.
34. Han, D. W., Tapia, N., Joo, J. Y., Greber, B., Araúzo-Bravo, M. J., Bernemann, C., Ko, K., Wu, G., Stehling, M., Do, J. T. et al. (2010). Epiblast stem cell subpopulations represent mouse embryos of distinct pregastrulation stages. Cell 143, 617-627.
35. Hayashi, K. and Surani, M. A. (2009). Self-renewing epiblast stem cells exhibit continual delineation of germ cells with epigenetic reprogramming in vitro. Development 136, 3549-3556.
36. Hsieh, J. C., Kodjabachian, L., Rebbert, M. L., Rattner, A., Smallwood, P. M., Samos, C. H., Nusse, R., Dawid, I. B. and Nathans, J. (1999). A new secreted protein that binds to Wnt proteins and inhibits their activities. Nature 398, 431-436.
37. Huang, Y., Osorno, R., Tsakiridis, A. and Wilson, V. (2012). In Vivo differentiation potential of epiblast stem cells revealed by chimeric embryo formation. Cell Rep. 2, 1571-1578.
38. Inman, G. J., Nicolás, F. J., Callahan, J. F., Harling, J. D., Gaster, L. M., Reith, A. D., Laping, N. J. and Hill, C. S. (2002). SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol. 62, 65-74.
39. Iwafuchi-Doi, M., Matsuda, K., Murakami, K., Niwa, H., Tesar, P. J., Aruga, J., Matsuo, I. and Kondoh, H. (2012). Transcriptional regulatory networks in epiblast cells and during anterior neural plate development as modeled in epiblast stem cells. Development 139, 3926-3937.
40. Kelly, O. G., Pinson, K. I. and Skarnes, W. C. (2004). The Wnt co-receptors Lrp5 and Lrp6 are essential for gastrulation in mice. Development 131, 2803-2815.
41. Kim, H., Wu, J., Ye, S., Tai, C. I., Zhou, X., Yan, H., Li, P., Pera, M. and Ying, Q. L. (2013). Modulation of β-catenin function maintains mouse epiblast stem cell and human embryonic stem cell self-renewal. Nat. Commun. 4, 2403.
42. Kinder, S. J., Tsang, T. E., Quinlan, G. A., Hadjantonakis, A. K., Nagy, A. and Tam, P. P. (1999). The orderly allocation of mesodermal cells to the extraembryonic structures and the anteroposterior axis during gastrulation of the mouse embryo. Development 126, 4691-4701.
43. Kinder, S. J., Tsang, T. E., Wakamiya, M., Sasaki, H., Behringer, R. R., Nagy, A. and Tam, P. P. (2001). The organizer of the mouse gastrula is composed of a dynamic population of progenitor cells for the axial mesoderm. Development 128, 3623-3634.
44. Kispert, A. and Herrmann, B. G. (1994). Immunohistochemical analysis of the Brachyury protein in wild-type and mutant mouse embryos. Dev. Biol. 161, 179-193.
45. Kojima, Y., Kaufman-Francis, K., Studdert, J. B., Steiner, K. A., Power, M. D., Loebel, D. A., Jones, V., Hor, A., de Alencastro, G., Logan, G. J. et al. (2014). The transcriptional and functional properties of mouse epiblast stem cells resemble the anterior primitive streak. Cell Stem Cell 14, 107-120.
46. Kubo, A., Shinozaki, K., Shannon, J. M., Kouskoff, V., Kennedy, M., Woo, S., Fehling, H. J. and Keller, G. (2004). Development of definitive endoderm from embryonic stem cells in culture. Development 131, 1651-1662.
47. Latinkić, B. V., Umbhauer, M., Neal, K. A., Lerchner, W., Smith, J. C. and Cunliffe, V. (1997). The Xenopus Brachyury promoter is activated by FGF and low concentrations of activin and suppressed by high concentrations of activin and by paired-type homeodomain proteins. Genes Dev. 11, 3265-3276.
48. Lawson, K. A. (1999). Fate mapping the mouse embryo. Int. J. Dev. Biol. 43, 773-775.
49. Lawson, K. A., Meneses, J. J. and Pedersen, R. A. (1991). Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113, 891-911.
50. Lee, K. L., Lim, S. K., Orlov, Y. L., Yit, Y., Yang, H., Ang, L. T., Poellinger, L. and Lim, B. (2011). Graded Nodal/Activin signaling titrates conversion of quantitative phospho-Smad2 levels into qualitative embryonic stem cell fate decisions. PLoS Genet. 7, e1002130.
51. Lendahl, U., Zimmerman, L. B. and McKay, R. D. (1990). CNS stem cells express a new class of intermediate filament protein. Cell 60, 585-595.
52. Liu, P., Wakamiya, M., Shea, M. J., Albrecht, U., Behringer, R. R. and Bradley, A. (1999). Requirement for Wnt3 in vertebrate axis formation. Nat. Genet. 22, 361-365.
53. Lyashenko, N., Winter, M., Migliorini, D., Biechele, T., Moon, R. T. and Hartmann, C. (2011). Differential requirement for the dual functions of β-catenin in embryonic stem cell self-renewal and germ layer formation. Nat. Cell Biol. 13, 753-761.
54. Martin, B. L. and Kimelman, D. (2010). Brachyury establishes the embryonic mesodermal progenitor niche. Genes Dev. 24, 2778-2783.
55. Martin, B. L. and Kimelman, D. (2012). Canonical Wnt signaling dynamically controls multiple stem cell fate decisions during vertebrate body formation. Dev. Cell 22, 223-232.
56. Mohamed, O. A., Clarke, H. J. and Dufort, D. (2004). Beta-catenin signaling marks the prospective site of primitive streak formation in the mouse embryo. Dev. Dyn. 231, 416-424.
57. Morrisey, E. E., Ip, H. S., Lu, M. M. and Parmacek, M. S. (1996). GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev. Biol. 177, 309-322.
58. Murray, J. T., Campbell, D. G., Morrice, N., Auld, G. C., Shpiro, N., Marquez, R., Peggie, M., Bain, J., Bloomberg, G. B., Grahammer, F. et al. (2004). Exploitation of KESTREL to identify NDRG family members as physiological substrates for SGK1 and GSK3. Biochem. J. 384, 477-488.
59. Olivera-Martinez, I., Harada, H., Halley, P. A. and Storey, K. G. (2012). Loss of FGFdependent mesoderm identity and rise of endogenous retinoid signalling determine cessation of body axis elongation. PLoS Biol. 10, e1001415.
60. Osorno, R., Tsakiridis, A., Wong, F., Cambray, N., Economou, C., Wilkie, R., Blin, G., Scotting, P. J., Chambers, I. and Wilson, V. (2012). The developmental dismantling of pluripotency is reversed by ectopic Oct4 expression. Development 139, 2288-2298.
61. Pfister, S., Steiner, K. A. and Tam, P. P. (2007). Gene expression pattern and progression of embryogenesis in the immediate post-implantation period of mouse development. Gene Expr. Patterns 7, 558-573.
62. Radice, G. L., Rayburn, H., Matsunami, H., Knudsen, K. A., Takeichi, M. and Hynes, R. O. (1997). Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol. 181, 64-78.
63. Ring, D. B., Johnson, K. W., Henriksen, E. J., Nuss, J. M., Goff, D., Kinnick, T. R., Ma, S. T., Reeder, J. W., Samuels, I., Slabiak, T. et al. (2003). Selective glycogen synthase kinase 3 inhibitors potentiate insulin activation of glucose transport and utilization in vitro and in vivo. Diabetes 52, 588-595.
64. Rivera-Pérez, J. A. and Magnuson, T. (2005). Primitive streak formation in mice is preceded by localized activation of Brachyury and Wnt3. Dev. Biol. 288, 363-371.
65. Saga, Y., Miyagawa-Tomita, S., Takagi, A., Kitajima, S., Miyazaki, J. and Inoue, T. (1999). MesP1 is expressed in the heart precursor cells and required for the formation of a single heart tube. Development 126, 3437-3447.
66. Sasaki, H. and Hogan, B. L. (1993). Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118, 47-59.
67. Schubert, F. R., Fainsod, A., Gruenbaum, Y. and Gruss, P. (1995). Expression of the novel murine homeobox gene Sax-1 in the developing nervous system. Mech. Dev. 51, 99-114.
68. Searcy, R. D., Vincent, E. B., Liberatore, C. M. and Yutzey, K. E. (1998). A GATAdependent nkx-2.5 regulatory element activates early cardiac gene expression in transgenic mice. Development 125, 4461-4470.
69. Sefton, M., Sánchez, S. and Nieto, M. A. (1998). Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development 125, 3111-3121.
70. Smyth, G. K. (2005). Limma: linear models for microarray data. In Bioinformatics and Computational Biology Solutions Using R and Bioconductor (ed. R. Gentleman, V. Carey, S. Dudoit, R. Irizarry and W. Huber), pp. 397-420. New York, NY: Springer.
71. Sumi, T., Oki, S., Kitajima, K. and Meno, C. (2013). Epiblast ground state is controlled by canonical Wnt/β-catenin signaling in the postimplantation mouse embryo and epiblast stem cells. PLoS ONE 8, e63378.
72. Takada, S., Stark, K. L., Shea, M. J., Vassileva, G., McMahon, J. A. and McMahon, A. P. (1994). Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8, 174-189.
73. Tam, P. P. and Behringer, R. R. (1997). Mouse gastrulation: the formation of a mammalian body plan. Mech. Dev. 68, 3-25.
74. Teo, A. K., Arnold, S. J., Trotter, M. W., Brown, S., Ang, L. T., Chng, Z., Robertson, E. J., Dunn, N. R. and Vallier, L. (2011). Pluripotency factors regulate definitive endoderm specification through eomesodermin. Genes Dev. 25, 238-250.
75. Tesar, P. J., Chenoweth, J. G., Brook, F. A., Davies, T. J., Evans, E. P., Mack, D. L., Gardner, R. L. and McKay, R. D. (2007). New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448, 196-199.
76. 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.
77. Vallier, L., Mendjan, S., Brown, S., Chng, Z., Teo, A., Smithers, L. E., Trotter, M. W., Cho, C. H., Martinez, A., Rugg-Gunn, P. et al. (2009). Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development 136, 1339-1349.
78. Wilkinson, D. G., Bhatt, S. and Herrmann, B. G. (1990). Expression pattern of the mouse T gene and its role in mesoderm formation. Nature 343, 657-659.
79. Wood, H. B. and Episkopou, V. (1999). Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech. Dev. 86, 197-201.
80. Yamaguchi, T. P., Takada, S., Yoshikawa, Y., Wu, N. and McMahon, A. P. (1999). T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 13, 3185-3190.
81. 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.