Satb1 and Satb2 regulate embryonic stem cell differentiation and Nanog expression

Genes and Development

Volumn 23, Issue 22, 2009, Pages 2625-2638

  Savarese, Fabio ^a   Dávila, Amparo ^a   Nechanitzky, Robert ^a   De La Rosa Velazquez, Inti ^a   Pereira, Carlos F ^b   Engelke, Rudolf ^a   Takahashi, Keiko ^c   Jenuwein, Thomas ^a   Kohwi Shigematsu, Terumi ^c   Fisher, Amanda G ^b   Grosschedl, Rudolf ^a  

^a MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Differentiation; Embryonic stem cells; Nanog; Pluripotency; Satb1; Satb2

Indexed keywords

BINDING PROTEIN; KRUPPEL LIKE FACTOR 4; PROTEIN TBX3; SATB1 PROTEIN; SATB2 PROTEIN; TRANSCRIPTION FACTOR NANOG; UNCLASSIFIED DRUG;

ARTICLE; B LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUSION; CELL HETEROGENEITY; CHROMATIN STRUCTURE; EMBRYONIC STEM CELL; GENE CLUSTER; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENE SILENCING; HOX GENE; HUMAN; HUMAN CELL; MULTIGENE FAMILY; PLASTICITY; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

ANIMALS; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; MATRIX ATTACHMENT REGION BINDING PROTEINS; MICE; TRANSCRIPTION FACTORS;

MURINAE;

EID: 72749087503     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1815709     Document Type: Article

References (55)

1. Agrelo R, Souabni A, Novatchkova M, Haslinger C, Leeb M, Komnenovic V, Kishimoto H, Gresh L, Kohwi-Shigematsu T, Kenner L, et al. 2009. SATB1 defines the developmental context for gene silencing by Xist in lymphoma and embryonic cells. Dev Cell 16: 507-516.
2. Alvarez JD, Yasui DH, Niida H, Joh T, Loh DY, Kohwi-Shigematsu T. 2000. The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development. Genes & Dev 14: 521-535. (Pubitemid 30159772)
3. Avilion AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. 2003. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes & Dev 17: 126-140. (Pubitemid 36062514)
4. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
5. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-956. (Pubitemid 41345211)
6. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, et al. 2006. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
7. Cai S, Han HJ, Kohwi-Shigematsu T. 2003. Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat Genet 34: 42-51. (Pubitemid 36548789)
8. Cai S, Lee CC, Kohwi-Shigematsu T. 2006. SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat Genet 38: 1278-1288. (Pubitemid 44646290)
9. Chambers I. 2004. The molecular basis of pluripotency in mouse embryonic stem cells. Cloning Stem Cells 6: 386-391.
10. Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113: 643-655.
11. Chambers I, Silva J, Colby D, Nichols J, Nijmeijer B, Robertson M, Vrana J, Jones K, Grotewold L, Smith A. 2007. Nanog safeguards pluripotency and mediates germline development. Nature 450: 1230-1234.
12. Chambeyron S, Bickmore WA. 2004. Chromatin decondensation and nuclear reorganization of the HoxB locus upon induction of transcription. Genes & Dev 18: 1119-1130. (Pubitemid 38669033)
13. Daley GQ, Scadden DT. 2008. Prospects for stem cell-based therapy. Cell 132: 544-548.
14. Dobreva G, Dambacher J, Grosschedl R. 2003. SUMO modification of a novel MAR-binding protein, SATB2, modulates immunoglobulin μ gene expression. Genes & Dev 17: 3048-3061.
15. Dobreva G, Chahrour M, Dautzenberg M, Chirivella L, Kanzler B, Farinas I, Karsenty G, Grosschedl R. 2006. SATB2 is a multifunctional determinant of craniofacial patterning and osteoblast differentiation. Cell 125: 971-986.
16. Donohoe ME, Silva SS, Pinter SF, Xu N, Lee JT. 2009. The pluripotency factor Oct4 interacts with Ctcf and also controls X-chromosome pairing and counting. Nature 460: 128-132.
17. Ema M, Mori D, Niwa H, Hasegawa Y, Yamanaka Y, Hitoshi S, Mimura J, Kawabe Y, Hosoya T, Morita M, et al. 2008. Kruppel-like factor 5 is essential for blastocyst development and the normal self-renewal of mouse ESCs. Cell Stem Cell 3: 555-567.
18. Galande S, Dickinson LA, Mian IS, Sikorska M, Kohwi-Shigematsu T. 2001. SATB1 cleavage by caspase 6 disrupts PDZ domain-mediated dimerization, causing detachment from chromatin early in T-cell apoptosis. Mol Cell Biol 21: 5591-5604.
19. Graf T, Stadtfeld M. 2008. Heterogeneity of embryonic and adult stem cells. Cell Stem Cell 3: 480-483.
20. Hayashi K, Lopes SM, Tang F, Surani MA. 2008. Dynamic equilibrium and heterogeneity of mouse pluripotent stem cells with distinct functional and epigenetic states. Cell Stem Cell 3: 391-401.
21. Jaenisch R, Young R. 2008. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132: 567-582.
22. Jiang J, Chan YS, Loh YH, Cai J, Tong GQ, Lim CA, Robson P, Zhong S, Ng HH. 2008. A core Klf circuitry regulates self-renewal of embryonic stem cells. Nat Cell Biol 10: 353-360.
23. 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.
24. Kmita M, Duboule D. 2003. Organizing axes in time and space; 25 years of colinear tinkering. Science 301: 331-333. (Pubitemid 36877058)
25. Kumar PP, Purbey PK, Ravi DS, Mitra D, Galande S. 2005. Displacement of SATB1-bound histone deacetylase 1 corepressor by the human immunodeficiency virus type 1 transactivator induces expression of interleukin-2 and its receptor in T cells. Mol Cell Biol 25: 1620-1633.
26. Kumar PP, Bischof O, Purbey PK, Notani D, Urlaub H, Dejean A, Galande S. 2007. Functional interaction between PML and SATB1 regulates chromatin-loop architecture and transcription of the MHC class I locus. Nat Cell Biol 9: 45-56.
27. Levasseur DN, Wang J, Dorschner MO, Stamatoyannopoulos JA, Orkin SH. 2008. Oct4 dependence of chromatin structure within the extended Nanog locus in ES cells. Genes & Dev 22: 575-580. (Pubitemid 351342430)
28. Li E. 2002. Chromatin modification and epigenetic reprogramming in mammalian development. Nat Rev Genet 3: 662-673.
29. Li Y, McClintick J, Zhong L, Edenberg HJ, Yoder MC, Chan RJ. 2005. Murine embryonic stem cell differentiation is promoted by SOCS-3 and inhibited by the zinc finger transcription factor Klf4. Blood 105: 635-637.
30. 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.
31. Loh YH, Zhang W, Chen X, George J, Ng HH. 2007. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes & Dev 21: 2545-2557. (Pubitemid 47607666)
32. Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. 2003. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113: 631-642. (Pubitemid 36694188)
33. Murry CE, Keller G. 2008. Differentiation of embryonic stem cells to clinically relevant populations: Lessons from embryonic development. Cell 132: 661-680.
34. Navarro P, Chambers I, Karwacki-Neisius V, Chureau C, Morey C, Rougeulle C, Avner P. 2008. Molecular coupling of Xist regulation and pluripotency. Science 321: 1693-1695.
35. 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.
36. Niwa H. 2007. How is pluripotency determined and maintained? Development 134: 635-646.
37. Niwa H, Burdon T, Chambers I, Smith A. 1998. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes & Dev 12: 2048-2060.
38. 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.
39. Pan G, Thomson JA. 2007. Nanog and transcriptional networks in embryonic stem cell pluripotency. Cell Res 17: 42-49. (Pubitemid 46096423)
40. Pavan Kumar P, Purbey PK, Sinha CK, Notani D, Limaye A, Jayani RS, Galande S. 2006. Phosphorylation of SATB1, a global gene regulator, acts as a molecular switch regulating its transcriptional activity in vivo. Mol Cell 22: 231-243.
41. Pereira CF, Terranova R, Ryan NK, Santos J, Morris KJ, Cui W, Merkenschlager M, Fisher AG. 2008. Heterokaryon-based reprogramming of human B lymphocytes for pluripotency requires Oct4 but not Sox2. PLoS Genet 4: e1000170. doi: 10.1371/journal.pgen.1000170.
42. Purbey PK, Singh S, Notani D, Kumar PP, Limaye AS, Galande S. 2009. Acetylation-dependent interaction of SATB1 and CtBP1 mediates transcriptional repression by SATB1. Mol Cell Biol 29: 1321-1337.
43. Ramakrishnan M, Liu WM, DiCroce PA, Posner A, Zheng J, Kohwi-Shigematsu T, Krontiris TG. 2000. Modulated binding of SATB1, a matrix attachment region protein, to the ATrich sequence flanking the major breakpoint region of BCL2. Mol Cell Biol 20: 868-877. (Pubitemid 30044223)
44. Silva J, Chambers I, Pollard S, Smith A. 2006. Nanog promotes transfer of pluripotency after cell fusion. Nature 441: 997-1001. (Pubitemid 43980355)
45. Singh AM, Hamazaki T, Hankowski KE, Terada N. 2007. A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 25: 2534-2542.
46. Smith AG. 2001. Embryo-derived stem cells: Of mice and men. Annu Rev Cell Dev Biol 17: 435-462.
47. Spivakov M, Fisher AG. 2007. Epigenetic signatures of stem-cell identity. Nat Rev Genet 8: 263-271.
48. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
49. 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.
50. Trouillas M, Saucourt C, Duval D, Gauthereau X, Thibault C, Dembele D, Feraud O, Menager J, Rallu M, Pradier L, et al. 2008. Bcl2, a transcriptional target of p38α, is critical for neuronal commitment of mouse embryonic stem cells. Cell Death Differ 15: 1450-1459.
51. Wagner EF. 2002. Functions of AP1 (Fos/Jun) in bone development. Ann Rheum Dis 61: ii40-ii42. doi: 10.1136/ard.61. suppl-2.ii40.
52. Wutz A, Jaenisch R. 2000. A shift from reversible to irreversible X inactivation is triggered during ES cell differentiation. Mol Cell 5: 695-705.
53. Yasui D, Miyano M, Cai S, Varga-Weisz P, Kohwi-Shigematsu T. 2002. SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419: 641-645.
54. Ying QL, Nichols J, Evans EP, Smith AG. 2002. Changing potency by spontaneous fusion. Nature 416: 545-548.
55. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, et al. 2007. Induced pluripotent stem cell lines derived from human somatic cells. Science 318: 1917-1920.