Foxd3 suppresses NFAT-mediated differentiation to maintain self-renewal of embryonic stem cells

EMBO Reports

Volumn 15, Issue 12, 2014, Pages 1286-1296

  Zhu, Lili ^a   Zhang, Shiyue ^a,b   Jin, Ying ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

embryonic stem cells; Foxd3; NFAT

Indexed keywords

CALCINEURIN; PROTEIN; TLE4 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXD3; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTOME; UNCLASSIFIED DRUG; FORKHEAD TRANSCRIPTION FACTOR; FOXD3 PROTEIN, MOUSE; REPRESSOR PROTEIN;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL RENEWAL; CONTROLLED STUDY; COS 7 CELL LINE; EMBRYO; EMBRYONIC STEM CELL; GENE CONTROL; MICROARRAY ANALYSIS; MOUSE; MOUSE EMBRYO; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTOMICS; ANIMAL; CELL LINE; CYTOLOGY; GEL MOBILITY SHIFT ASSAY; GENETICS; METABOLISM; PHYSIOLOGY; THEORETICAL MODEL;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EMBRYONIC STEM CELLS; FORKHEAD TRANSCRIPTION FACTORS; MICE; MODELS, THEORETICAL; NFATC TRANSCRIPTION FACTORS; REPRESSOR PROTEINS;

EID: 84915828026     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201438643     Document Type: Article

References (36)

1. Evans MJ, Kaufman MH, (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154-156
2. Chambers I, Tomlinson SR, (2009) The transcriptional foundation of pluripotency. Development 136: 2311-2322
3. Jaenisch R, Young R, (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132: 567-582
4. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB, Wong E, Orlov YL, Zhang W, Jiang J, et al, (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117
5. Kim J, Chu J, Shen X, Wang J, Orkin SH, (2008) An extended transcriptional network for pluripotency of embryonic stem cells. Cell 132: 1049-1061
6. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, et al, (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38: 431-440
7. Festuccia N, Osorno R, Halbritter F, Karwacki-Neisius V, Navarro P, Colby D, Wong F, Yates A, Tomlinson SR, Chambers I, 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
8. Lu R, Yang A, Jin Y, (2011) Dual functions of T-box 3 (Tbx3) in the control of self-renewal and extraembryonic endoderm differentiation in mouse embryonic stem cells. J Biol Chem 286: 8425-8436
9. Nichols J, Zevnik B, Anastassiadis K, Niwa H, Klewe-Nebenius D, Chambers I, Scholer H, Smith A, (1998) Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95: 379-391
10. Li X, Zhu L, Yang A, Lin J, Tang F, Jin S, Wei Z, Li J, Jin Y, (2011) Calcineurin-NFAT signaling critically regulates early lineage specification in mouse embryonic stem cells and embryos. Cell Stem Cell 8: 46-58
11. Chazaud C, Yamanaka Y, Pawson T, Rossant J, (2006) Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway. Dev Cell 10: 615-624
12. Kunath T, Saba-El-Leil MK, Almousailleakh M, Wray J, Meloche S, 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
13. Carlsson P, Mahlapuu M, (2002) Forkhead transcription factors: key players in development and metabolism. Dev Biol 250: 1-23
14. Sutton J, Costa R, Klug M, Field L, Xu D, Largaespada DA, Fletcher CF, Jenkins NA, Copeland NG, Klemsz M, et al, (1996) Genesis, a winged helix transcriptional repressor with expression restricted to embryonic stem cells. J Biol Chem 271: 23126-23133
15. Hanna LA, Foreman RK, Tarasenko IA, Kessler DS, Labosky PA, (2002) Requirement for Foxd3 in maintaining pluripotent cells of the early mouse embryo. Genes Dev 16: 2650-2661
16. Liu Y, Labosky PA, (2008) Regulation of embryonic stem cell self-renewal and pluripotency by Foxd3. Stem Cells 26: 2475-2484
17. Chin ER, Olson EN, Richardson JA, Yang Q, Humphries C, Shelton JM, Wu H, Zhu W, Bassel-Duby R, Williams RS, et al, (1998) A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 12: 2499-2509
18. Graef IA, Chen F, Chen L, Kuo A, Crabtree GR, (2001) Signals transduced by Ca(2+)/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell 105: 863-875
19. Graef IA, Wang F, Charron F, Chen L, Neilson J, Tessier-Lavigne M, Crabtree GR, (2003) Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons. Cell 113: 657-670
20. Müller MR, Sasaki Y, Stevanovic I, Lamperti ED, Ghosh S, Sharma S, Gelinas C, Rossi DJ, Pipkin ME, Rajewsky K, et al, (2009) Requirement for balanced Ca/NFAT signaling in hematopoietic and embryonic development. Proc Natl Acad Sci USA 106: 7034-7039
21. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN, (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93: 215-228
22. Macian F, (2005) NFAT proteins: key regulators of T-cell development and function. Nat Rev Immunol 5: 472-484
23. Rao A, Luo C, Hogan PG, (1997) Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15: 707-747
24. Saccani S, Saccani A, Varesio L, Ghosh P, Young HA, Sica A, (1999) Divergent effects of dithiocarbamates on AP-1-containing and AP-1-less NFAT sites. Eur J Immunol 29: 1194-1201
25. Ikeda F, Nishimura R, Matsubara T, Tanaka S, Inoue J, Reddy SV, Hata K, Yamashita K, Hiraga T, Watanabe T, et al, (2004) Critical roles of c-Jun signaling in regulation of NFAT family and RANKL-regulated osteoclast differentiation. J Clin Invest 114: 475-484
26. Smith AG, Heath JK, Donaldson DD, Wong GG, Moreau J, Stahl M, Rogers D, (1988) Inhibition of pluripotential embryonic stem cell differentiation by purified polypeptides. Nature 336: 688-690
27. Chen G, Courey AJ, (2000) Groucho/TLE family proteins and transcriptional repression. Gene 249: 1-16
28. Fric J, Zelante T, Wong AY, Mertes A, Yu HB, (2012) Ricciardi-Castagnoli P NFAT control of innate immunity. Blood 120: 1380-1389
29. Macian F, Garcia-Rodriguez C, Rao A, (2000) Gene expression elicited by NFAT in the presence or absence of cooperative recruitment of Fos and Jun. EMBO J 19: 4783-4795
30. Steiner AB, Engleka MJ, Lu Q, Piwarzyk EC, Yaklichkin S, Lefebvre JL, Walters JW, Pineda-Salgado L, Labosky PA, Kessler DS, et al, (2006) FoxD3 regulation of Nodal in the Spemann organizer is essential for Xenopus dorsal mesoderm development. Development 133: 4827-4838
31. Yaklichkin S, Steiner AB, Lu Q, Kessler DS, (2007) FoxD3 and Grg4 physically interact to repress transcription and induce mesoderm in Xenopus. J Biol Chem 282: 2548-2557
32. Roose J, Molenaar M, Peterson J, Hurenkamp J, Brantjes H, Moerer P, van de Wetering M, Destree O, Clevers H, (1998) The Xenopus Wnt effector XTcf-3 interacts with Groucho-related transcriptional repressors. Nature 395: 608-612
33. Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J, (2005) Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123: 917-929
34. Li L, Sun L, Gao F, Jiang J, Yang Y, Li C, Gu J, Wei Z, Yang A, Lu R, et al, (2010) Stk40 links the pluripotency factor Oct4 to the Erk/MAPK pathway and controls extraembryonic endoderm differentiation. Proc Natl Acad Sci USA 107: 1402-1407
35. Masui S, Shimosato D, Toyooka Y, Yagi R, Takahashi K, Niwa H, (2005) An efficient system to establish multiple embryonic stem cell lines carrying an inducible expression unit. Nucleic Acids Res 33: e43
36. Yang L, Jiang Y, Wu SF, Zhou MY, Wu YL, Chen GQ, (2008) CCAAT/enhancer-binding protein alpha antagonizes transcriptional activity of hypoxia-inducible factor 1 alpha with direct protein-protein interaction. Carcinogenesis 29: 291-298