FGF/MAPK signaling sets the switching threshold of a bistable circuit controlling cell fate decisions in embryonic stem cells

Development (Cambridge)

Volumn 142, Issue 24, 2015, Pages 4205-4216

  Schröter, Christian ^a   Rué, Pau ^a   Mackenzie, Jonathan Peter ^a   Arias, Alfonso Martinez ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Cell fate decision; Dynamic systems; Embryonic stem cells; GATA factor; Live cell imaging; Preimplantation development

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; LEUKEMIA INHIBITORY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 6; TRANSCRIPTION FACTOR NANOG; BIOLOGICAL MARKER; PHOTOPROTEIN; RED FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; CELL FATE; CELL POPULATION; CELL TRACKING; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYONIC STEM CELL; FLOW CYTOMETRY; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; MOUSE; NONHUMAN; PREIMPLANTATION EMBRYO; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; BIOLOGICAL MODEL; CELL LINEAGE; CYTOLOGY; ENDODERM; GENE EXPRESSION REGULATION; GERM LAYER; METABOLISM; MOUSE EMBRYONIC STEM CELL;

ANIMALS; BIOMARKERS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; ENDODERM; FIBROBLAST GROWTH FACTORS; GATA4 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION; GERM LAYERS; LUMINESCENT PROTEINS; MAP KINASE SIGNALING SYSTEM; MICE; MODELS, BIOLOGICAL; MOUSE EMBRYONIC STEM CELLS;

EID: 84983209674     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.127530     Document Type: Article

References (42)

1. Albeck, J. G., Mills, G. B. and Brugge, J. S. (2013). Frequency-modulated pulses of ERK activity transmit quantitative proliferation signals. Mol. Cell 49, 249-261.
2. Aoki, K., Kumagai, Y., Sakurai, A., Komatsu, N., Fujita, Y., Shionyu, C. and Matsuda, M. (2013). Stochastic ERK activation induced by noise and cell-to-cell propagation regulates cell density-dependent proliferation. Mol. Cell 52, 529-540.
3. Beard, C., Hochedlinger, K., Plath, K., Wutz, A. and Jaenisch, R. (2006). Efficient method to generate single-copy transgenic mice by site-specific integration in embryonic stem cells. Genesis 44, 23-28.
4. Beddington, R. S. and Robertson, E. J. (1989). An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo. Development 105, 733-737.
5. Bessonnard, S., De Mot, L., Gonze, D., Barriol, M., Dennis, C., Goldbeter, A., Dupont, G. and Chazaud, C. (2014). Gata6, NANOG and Erk signaling control cell fate in the inner cell mass through a tristable regulatory network. Development 141, 3637-3648.
6. Bhattacharya, S., Zhang, Q. and Andersen, M. E. (2011). A deterministic map of Waddington's epigenetic landscape for cell fate specification. BMC Syst. Biol. 5, 85.
7. Boroviak, T., Loos, R., Bertone, P., Smith, A. and Nichols, J. (2014). The ability of inner-cell-mass cells to self-renew as embryonic stem cells is acquired following epiblast specification. Nat. Cell Biol. 16, 516-528.
8. 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.
9. Cherry, J. L. and Adler, F. R. (2000). How to make a biological switch. J. Theor. Biol. 203, 117-133.
10. Cho, L. T. Y., Wamaitha, S. E., Tsai, I. J., Artus, J., Sherwood, R. I., Pedersen, R. A., Hadjantonakis, A.-K. and Niakan, K. K. (2012). Conversion from mouse embryonic to extra-embryonic endoderm stem cells reveals distinct differentiation capacities of pluripotent stem cell states. Development 139, 2866-2877.
11. Dietrich, J.-E. and Hiiragi, T. (2007). Stochastic patterning in the mouse preimplantation embryo. Development 134, 4219-4231.
12. Edelstein, A., Amodaj, N., Hoover, K., Vale, R. and Stuurman, N. (2001). Computer Control of Microscopes Using μManager. Hoboken, NJ, USA: John Wiley & Sons.
13. Fawcett, T. (2006). An introduction to ROC analysis. Pattern Recognit. Lett. 27, 861-874.
14. Filipczyk, A., Gkatzis, K., Fu, J., Hoppe, P. S., Lickert, H., Anastassiadis, K. and Schroeder, T. (2013). Biallelic expression of NANOG protein in mouse embryonic stem cells. Cell Stem Cell 13, 12-13.
15. Frankenberg, S., Gerbe, F., Bessonnard, S., Belville, C., Pouchin, P., Bardot, O. and Chazaud, C. (2011). Primitive endoderm differentiates via a three-step mechanism involving NANOG and RTK signaling. Dev. Cell 21, 1005-1013.
16. Freyer, L., Schröter, C., Saiz, N., Schrode, N., Nowotschin, S., Martinez Arias, A. and Hadjantonakis, A.-K. (2015). A loss-of-function and H2B-Venus transcriptional reporter allele for Gata6 in mice. BMC Dev. Biol. 15, 38.
17. Fujikura, J., Yamato, E., Yonemura, S., Hosoda, K., Masui, S., Nakao, K., Miyazaki, J.-I. and Niwa, H. (2002). Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev. 16, 784-789.
18. Gardner, T. S., Cantor, C. R. and Collins, J. J. (2000). Construction of a genetic toggle switch in Escherichia coli. Nature 403, 339-342.
19. Grabarek, J. B., Zyzynska, K., Saiz, N., Piliszek, A., Frankenberg, S., Nichols, J., Hadjantonakis, A.-K. and Plusa, B. (2012). Differential plasticity of epiblast and primitive endoderm precursors within the ICM of the early mouse embryo. Development 139, 129-139.
20. Hamilton, W. B. and Brickman, J. M. (2014). Erk signaling suppresses embryonic stem cell self-renewal to specify endoderm. Cell Rep. 9, 2056-2070.
21. Kalmar, T., Lim, C., Hayward, P., Muñoz-Descalzo, S., Nichols, J., Garcia- Ojalvo, J. and Martinez Arias, A. (2009). Regulated fluctuations in NANOG expression mediate cell fate decisions in embryonic stem cells. PLoS Biol. 7, e1000149.
22. Kang, M., Piliszek, A., Artus, J. and Hadjantonakis, A.-K. (2012). FGF4 is required for lineage restriction and salt-and-pepper distribution of primitive endoderm factors but not their initial expression in the mouse. Development 140, 267-279.
23. Kunath, T., Saba-El-Leil, M. K., Almousailleakh, M., Wray, J., Meloche, S. and Smith, A. (2007). FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 134, 2895-2902.
24. Lander, A. D., Gokoffski, K. K.,Wan, F. Y. M., Nie, Q. and Calof, A. L. (2009). Cell lineages and the logic of proliferative control. PLoS Biol. 7, e1000015.
25. Marks, H., Kalkan, T., Menafra, R., Denissov, S., Jones, K., Hofemeister, H., Nichols, J., Kranz, A., Francis Stewart, A., Smith, A. et al. (2012). The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149, 590-604.
26. Morgani, S. M., Canham, M. A., Nichols, J., Sharov, A. A., Migueles, R. P., Ko, M. S. H. and Brickman, J. M. (2013). Totipotent embryonic stem cells arise in ground-state culture conditions. Cell Rep. 3, 1945-1957.
27. Mulvey, C. M., Schröter, C., Gatto, L., Dikicioglu, D., Fidaner, I. B., Christoforou, A., Deery, M. J., Cho, L. T. Y., Niakan, K. K., Martinez Arias, A. et al. (2015). Dynamic proteomic profiling of extra-embryonic endoderm differentiation in mouse embryonic stem cells. Stem Cells 33, 2712-2725.
28. Nichols, J., Zevnik, B., Anastassiadis, K., Niwa, H., Klewe-Nebenius, D., Chambers, I., Schöler, H. and Smith, A. (1998). Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391.
29. Nichols, J., Silva, J., Roode, M. and Smith, A. (2009). Suppression of Erk signalling promotes ground state pluripotency in the mouse embryo. Development 136, 3215-3222.
30. Ohnishi, Y., Huber, W., Tsumura, A., Kang, M., Xenopoulos, P., Kurimoto, K., Oleś, A. K., Araúzo-Bravo, M. J., Saitou, M., Hadjantonakis, A.-K., et al. (2014). Cell-to-cell expression variability followed by signal reinforcement progressively segregates early mouse lineages. Nat. Cell Biol. 16, 27-37.
31. Plahte, E., Mestl, T. and Omholt, S. W. (1995). Feedback loops, stability and multistationarity in dynamical systems. J. Biol. Syst. 3, 409-413.
32. Plusa, B., Piliszek, A., Frankenberg, S., Artus, J. and Hadjantonakis, A.-K. (2008). Distinct sequential cell behaviours direct primitive endoderm formation in the mouse blastocyst. Development 135, 3081-3091.
33. Ptashne, M. (2004). A Genetic Switch. Cold Spring Harbor: CSHL Press.
34. Rossant, J. and Tam, P. P. L. (2009). Blastocyst lineage formation, early embryonic asymmetries and axis patterning in the mouse. Development 136, 701-713.
35. Schrode, N., Saiz, N., Di Talia, S. and Hadjantonakis, A.-K. (2014). GATA6 Levels modulate primitive endoderm cell fate choice and timing in the mouse blastocyst. Dev. Cell 29, 454-467.
36. Shimosato, D., Shiki, M. and Niwa, H. (2007). Extra-embryonic endoderm cells derived from ES cells induced by GATA factors acquire the character of XEN cells. BMC Dev. Biol. 7, 80.
37. Singh, A. M., Hamazaki, T., Hankowski, K. E. and Terada, N. (2007). A heterogeneous expression pattern for NANOG in embryonic stem cells. Stem Cells 25, 2534-2542.
38. Snoussi, E. H. (1998). Necessary conditions for multistationarity and stable periodicity. J. Biol. Syst. 6, 3-9.
39. Thomas, R. (1981). On the relation between the logical structure of systems and their ability to generate multiple steady states or sustained oscillations. In Springer Series in Synergetics (ed. D. J. Dora, J. Demongeot and B. Lacolle), pp. 180-193. Berlin: Springer.
40. Wamaitha, S. E., del Valle, I., Cho, L. T. Y.,Wei, Y., Fogarty, N. M. E., Blakeley, P., Sherwood, R. I., Ji, H. and Niakan, K. K. (2015). Gata6 potently initiates reprograming of pluripotent and differentiated cells to extraembryonic endoderm stem cells. Genes Dev. 29, 1239-1255.
41. Xenopoulos, P., Kang, M., Puliafito, A., Di Talia, S. and Hadjantonakis, A.-K. (2015). Heterogeneities in NANOG expression drive stable commitment to pluripotency in the mouse blastocyst. Cell Rep. 10, 1508-1520.
42. Yamanaka, Y., Lanner, F. and Rossant, J. (2010). FGF signal-dependent segregation of primitive endoderm and epiblast in the mouse blastocyst. Development 137, 715-724.