A model-based analysis of culture-dependent phenotypes of mESCs

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Herberg, Maria ^a   Kalkan, Tüzer ^b   Glauche, Ingmar ^a   Smith, Austin ^b   Roeder, Ingo ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 4; LEUKEMIA INHIBITORY FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; OCTAMER TRANSCRIPTION FACTOR 4; REX PROTEIN; REX1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; CULTURE MEDIUM; HOMEODOMAIN PROTEIN; LEUKEMIA INHIBITORY FACTOR; LIF PROTEIN, MOUSE; NANOG PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FRACTIONATION; CELL HETEROGENEITY; CONTROLLED STUDY; DYNAMICS; EMBRYO; FEEDBACK SYSTEM; MATHEMATICAL MODEL; MOUSE; NONHUMAN; PHENOTYPE; PLURIPOTENT STEM CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN STABILITY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SIMULATION; STEM CELL CULTURE; ANIMAL; BIOLOGICAL MODEL; CELL CULTURE; CELL PROLIFERATION; COMPUTER SIMULATION; CULTURE MEDIUM; EMBRYONIC STEM CELL; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COMPUTER SIMULATION; CULTURE MEDIA, SERUM-FREE; EMBRYONIC STEM CELLS; HOMEODOMAIN PROTEINS; LEUKEMIA INHIBITORY FACTOR; MICE; MODELS, BIOLOGICAL; PHENOTYPE; PROTEIN STABILITY; SIGNAL TRANSDUCTION;

EID: 84898619040     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0092496     Document Type: Article

References (60)

1. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells fro (Pubitemid 11050741)
2. Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proceedings of the National Academy of Sciences of the United States of America 78: 7634-7638. (Pubitemid 12186197)
3. Niwa H, Burdon T, Chambers I, Smith A (1998) Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes & Development 12: 2048-2060. (Pubitemid 28323878)
4. Burdon T, Chambers I, Stracey C, Niwa H, Smith A (1999) Signaling mechanisms regulating self-renewal and differentiation of pluripotent embryonic stem cells. Cells, tissues, organs 165: 131-143.
5. Niwa H, Ogawa K, Shimosato D, Adachi K (2009) A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells. Nature 460: 118-122.
6. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, et al. (2005) Transcriptional regulation of nanog by OCT4 and SOX2. The Journal of biological chemistry 280: 24731-24737. (Pubitemid 40934562)
7. Loh Y-H, Wu Q, Chew J-L, Vega VB, Zhang W, et al. (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nature Genetics 38: 431-440.
8. Niwa H (2007) How is pluripotency determined and maintained? Development 134: 635-646. (Pubitemid 46437906)
9. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, et al. (2005) Interaction between Oct3/4 and Cdx2 Determines Trophectoderm Differentiation. Cell 123: 917-929. (Pubitemid 41721036)
10. Ralston A, Rossant J (2005) Genetic regulation of stem cell origins in the mouse embryo. Clinical genetics 68: 106-112. (Pubitemid 40990621)
11. Gardner TS, Cantor CR, Collins JJ (2000) Construction of a genetic toggle switch in Escherichia coli. Nature 403: 339-342. (Pubitemid 30062394)
12. Huang S, Eichler G, Bar-Yam Y, Ingber DE (2005) Cell fates as high-dimensional attractor states of a complex gene regulatory network. Physical review letters 94: 128701.
13. Roeder I, Glauche I (2006) Towards an understanding of lineage specification in hematopoietic stem cells: a mathematical model for the interaction of transcription factors GATA-1 and PU.1. Journal of Theoretical Biology 241: 852-865. (Pubitemid 44080793)
14. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, et al. (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95: 379-391. (Pubitemid 28507326)
15. Niwa H, Miyazaki J, Smith AG (2000) Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nature Genetics 24: 372-376. (Pubitemid 30187435)
16. Matoba R, Niwa H, Masui S, Ohtsuka S, Carter MG, et al. (2006) Dissecting Oct3/4-Regulated Gene Networks in Embryonic Stem Cells by Expression Profiling. PLoS ONE 1: e26.
17. Hay DC, Sutherland L, Clark J, Burdon T (2004) Oct-4 knockdown induces similar patterns of endoderm and trophoblast differentiation markers in human and mouse embryonic stem cells. Stem Cells 22: 225-235. (Pubitemid 38282637)
18. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, et al. (2007) Nanog safeguards pluripotency and mediates germline development. Nature 450: 1230-1234.
19. Singh AM, Hamazaki T, Hankowski KE, Terada N (2007) A Heterogeneous Expression Pattern for Nanog in Embryonic Stem Cells. Stem Cells 25: 2534-2542. (Pubitemid 47582745)
20. Kalmar T, Goodell MA, Lim C, Hayward P, Muñz-Descalzo S, et al. (2009) Regulated Fluctuations in Nanog Expression Mediate Cell Fate Decisions in Embryonic Stem Cells. PLoS Biology 7: e1000149.
21. Silva J, Nichols J, Theunissen TW, Guo G, van Oosten AL, et al. (2009) Nanog Is the Gateway to the Pluripotent Ground State. Cell 138: 722-737.
22. Toyooka Y, Shimosato D, Murakami K, Takahashi K, Niwa H (2008) Identification and characterization of subpopulations in undifferentiated ES cell culture. Development 135: 909-918. (Pubitemid 351524145)
23. Ben-Shushan E, Thompson JR, Gudas LJ, Bergman Y (1998) Rex-1, a gene encoding a transcription factor expressed in the early embryo, is regulated via Oct-3/4 and Oct-6 binding to an octamer site and a novel protein, Rox-1, binding to an adjacent site. Molecular and Cellular Biology 18: 1866-1878. (Pubitemid 28152635)
24. Shi W, Wang H, Pan G, Geng Y, Guo Y, et al. (2006) Regulation of the pluripotency marker Rex-1 by Nanog and Sox2. The Journal of biological chemistry 281: 23319-23325. (Pubitemid 44274106)
25. Marks H, Kalkan T, Menafra R, Denissov S, Jones K, et al. (2012) The transcriptional and epigenomic foundations of ground state pluripotency. Cell 149: 590-604.
26. Wray J, Kalkan T, Smith AG (2010) The ground state of pluripotency. Biochemical Society transactions 38: 1027-1032.
27. Luo Y, Lim CL, Nichols J, Martinez-Arias A, Wernisch L (2012) Cell signalling regulates dynamics of Nanog distribution in embryonic stem cell populations. Journal of the Royal Society, Interface/the Royal Society.
28. Ying Q-L, Wray J, Nichols J, Batlle-Morera L, Doble B, et al. (2008) The ground state of embryonic stem cell self-renewal. Nature 453: 519-523. (Pubitemid 351733324)
29. Nichols J, Smith A (2009) Naive and Primed Pluripotent States. Cell Stem Cell 4: 487-492.
30. Nichols J, Smith A (2012) Pluripotency in the embryo and in culture. Cold Spring Harbor perspectives in biology 4: a008128.
31. Karwacki-Neisius V, Goke J, Osorno R, Halbritter F, Ng JH, et al. (2013) Reduced oct4 expression directs a robust pluripotent state with distinct signaling activity and increased enhancer occupancy by oct4 and nanog. Cell Stem Cell 12: 531-545.
32. Ambrosetti DC, Basilico C, Dailey L (1997) Synergistic activation of the fibroblast growth factor 4 enhancer by Sox2 and Oct-3 depends on proteinprotein interactions facilitated by a specific spatial arrangement of factor binding sites. Molecular and Cellular Biology 17: 6321-6329. (Pubitemid 27451176)
33. Kunath T, Saba-El-Leil MK, Almousailleakh M, Wray J, Meloche S, et al. (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. (Pubitemid 47386902)
34. Silva J, Smith A (2008) Capturing Pluripotency. Cell 132: 532-536. (Pubitemid 351253697)
35. Navarro P, Festuccia N, Colby D, Gagliardi A, Mullin NP, et al. (2012) OCT4/SOX2-independent Nanog autorepression modulates heterogeneous Nanog gene expression in mouse ES cells. The EMBO journal 31: 4547-4562.
36. MacArthur BD, Sevilla A, Lenz M, Muller FJ, Schuldt BM, et al. (2012) Nanog-dependent feedback loops regulate murine embryonic stem cell heterogeneity. Nature Cell Biology 14: 1139-1147.
37. Miyanari Y, Torres-Padilla ME (2012) Control of ground-state pluripotency by allelic regulation of Nanog. Nature 483: 470-473.
38. Fidalgo M, Faiola F, Pereira CF, Ding J, Saunders A, et al. (2012) Zfp281 mediates Nanog autorepression through recruitment of the NuRD complex and inhibits somatic cell reprogramming. Proceedings of the National Academy of Sciences of the United States of America 109: 16202-16207.
39. Loh KM, Lim B (2011) A precarious balance: pluripotency factors as lineage specifiers. Cell Stem Cell 8: 363-369.
40. Chickarmane V (2006) Transcriptional Dynamics of the Embryonic Stem Cell Switch. PLoS Computational Biology 9: e123.
41. Chickarmane V, Peterson C (2008) A computational model for understanding stem cell, trophectoderm and endoderm lineage determination. PLoS ONE 3: e3478.
42. Glauche I, Herberg M, Roeder I (2010) Nanog variability and pluripotency regulation of embryonic stem cells-insights from a mathematical model analysis. PLoS ONE 5: e11238.
43. Chickarmane V, Olariu V, Peterson C (2012) Probing the role of stochasticity in a model of the embryonic stem cell-heterogeneous gene expression and reprogramming efficiency. BMC systems biology 6: 98.
44. Carter MG, Stagg CA, Falco G, Yoshikawa T, Bassey UC, et al. (2008) An in situ hybridization-based screen for heterogeneously expressed genes in mouse ES cells. Gene Expression Patterns 8: 181-198.
45. Wray J, Kalkan T, Gomez-Lopez S, Eckardt D, Cook A, et al. (2011) Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nature Cell Biology 13: 838-845.
46. Chew JL, Loh YH, Zhang W, Chen X, Tam WL, et al. (2005) Reciprocal Transcriptional Regulation of Pou5f1 and Sox2 via the Oct4/Sox2 Complex in Embryonic Stem Cells. Molecular and Cellular Biology 25: 6031-6046. (Pubitemid 40946556)
47. Wang J, Levasseur DN, Orkin SH (2008) Requirement of Nanog dimerization for stem cell self-renewal and pluripotency. Proceedings of the National Academy of Sciences 105: 6326-6331. (Pubitemid 351758345)
48. Mullin Nicholas P, Yates A, Rowe Arthur J, Nijmeijer B, Colby D, et al. (2008) The pluripotency rheostat Nanog functions as a dimer. Biochemical Journal 411: 227.
49. Hamazaki T, Kehoe SM, Nakano T, Terada N (2006) The Grb2/Mek Pathway Represses Nanog in Murine Embryonic Stem Cells. Molecular and Cellular Biology 26: 7539-7549. (Pubitemid 44547704)
50. Chambers I (2003) Functional Expression Cloning of Nanog, a Pluripotency Sustaining Factor in Embryonic Stem Cells. Cell 113: 643-655. (Pubitemid 36694189)
51. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, et al. (2003) The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113: 631-642. (Pubitemid 36694188)
52. O'Shea KS (2004) Self-renewal vs. differentiation of mouse embryonic stem cells. Biology of reproduction 71: 1755-1765. (Pubitemid 39586917)
53. Hoffmann M, Chang HH, Huang S, Ingber DE, Loeffler M, et al. (2008) Noise-driven stem cell and progenitor population dynamics. PLoS ONE 3: e2922.
54. Enver T, Pera M, Peterson C, Andrews PW (2009) Stem cell states, fates, and the rules of attraction. Cell Stem Cell 4: 387-397.
55. Ying QL, Smith AG (2003) Defined conditions for neural commitment and differentiation. Methods in enzymology 365: 327-341. (Pubitemid 37531558)
56. Martello G, Sugimoto T, Diamanti E, Joshi A, Hannah R, et al. (2012) Esrrb is a pivotal target of the gsk3/tcf3 axis regulating embryonic stem cell self-renewal. Cell Stem Cell 11: 491-504.
57. Festuccia N, Osorno R, Halbritter F, Karwacki-Neisius V, Navarro P, et al. (2012) Esrrb Is a Direct Nanog Target Gene that Can Substitute for Nanog Function in Pluripotent Cells. Cell Stem Cell 11: 477-490.
58. Pan G, Li J, Zhou Y, Zheng H, Pei D (2006) A negative feedback loop of transcription factors that controls stem cell pluripotency and self-renewal. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 20: 1730-1732.
59. Zhang X, Zhang J, Wang T, Esteban MA, Pei D (2008) Esrrb activates Oct4 transcription and sustains self-renewal and pluripotency in embryonic stem cells. The Journal of biological chemistry 283: 35825-35833.
60. Zhang P, Andrianakos R, Yang Y, Liu C, Lu W (2010) Kruppel-like factor 4 (Klf4) prevents embryonic stem (ES) cell differentiation by regulating Nanog gene expression. The Journal of biological chemistry 285: 9180-9189.