Sox transcription factors require selective interactions with oct4 and specific transactivation functions to mediate reprogramming

Stem Cells

Volumn 31, Issue 12, 2013, Pages 2632-2646

  Aksoy, Irene ^a   Jauch, Ralf ^a,b   Eras, Volker ^a   Chng, Wen Bin Alfred ^a   Chen, Jiaxuan ^a   Divakar, Ushashree ^a   Ng, Calista Keow Leng ^a,c   Kolatkar, Prasanna R ^a,d,e   Stanton, Lawrence W ^a,c,d  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

^b GUANGZHOU INSTITUTES OF BIOMEDICINE AND HEALTH   (China)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^d NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^e HAMAD BIN KHALIFA UNIVERSITY   (Qatar)

Author keywords

C terminal transactivation domain; High mobility group domain; Induced pluripotent stem cells; LIF STAT3 pathway; Reprogramming; Sox transcription factors; Wnt b catenin pathway

Indexed keywords

BETA CATENIN; GLUTAMIC ACID; LYSINE; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SOX; TRANSCRIPTION FACTOR SOX11; TRANSCRIPTION FACTOR SOX12; TRANSCRIPTION FACTOR SOX13; TRANSCRIPTION FACTOR SOX17; TRANSCRIPTION FACTOR SOX18; TRANSCRIPTION FACTOR SOX4; TRANSCRIPTION FACTOR SOX5; TRANSCRIPTION FACTOR SOX6; TRANSCRIPTION FACTOR SOX7; TRANSCRIPTION FACTOR SOX8; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG; ALKALINE PHOSPHATASE; HIGH MOBILITY GROUP B PROTEIN; POU5F1 PROTEIN, HUMAN; POU5F1 PROTEIN, MOUSE; SOX17 PROTEIN, HUMAN; SOX17 PROTEIN, MOUSE; SOX7 PROTEIN, HUMAN; SOX7 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; DNA BINDING; EMBRYONIC STEM CELL; FIBROBLAST; GENE FUNCTION; GENE MUTATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; TRANSACTIVATION; ANIMAL; CULTURE TECHNIQUE; GENETICS; METABOLISM; NUCLEAR REPROGRAMMING; PHYSIOLOGY; POINT MUTATION; SCID MOUSE; TRANSCRIPTION INITIATION; TRANSPLANTATION;

ALKALINE PHOSPHATASE; ANIMALS; BETA CATENIN; CELL CULTURE TECHNIQUES; CELLULAR REPROGRAMMING; HMGB PROTEINS; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, SCID; OCTAMER TRANSCRIPTION FACTOR-3; POINT MUTATION; SOXF TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 84890476828     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1522     Document Type: Article

References (73)

1. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676.
2. Feng B, Jiang J, Kraus P et al. Reprogramming of fibroblasts into induced pluripotent stem cells with orphan nuclear receptor Esrrb. Nat Cell Biol 2009;11:197-203.
3. Huangfu D, Maehr R, Guo W et al. Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 2008;26:795-797.
4. Nakagawa M, Koyanagi M, Tanabe K et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 2008;26:101-106.
5. Wernig M, Meissner A, Cassady JP et al. c-Myc is dispensable for direct reprogramming of mouse fibroblasts. Cell Stem Cell 2008;2:10-12.
6. Aksoy I, Stanton LW. Pluripotency-regulating networks provide basis for reprogramming. Curr Mol Med 2013;13:695-706.
7. Huangfu D, Osafune K, Maehr R et al. Induction of pluripotent stem cells from primary human fibroblasts with only Oct4 and Sox2. Nat Biotechnol 2008;26:1269-1275.
8. Yu J, Vodyanik MA, Smuga-Otto K et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318:1917-1920.
9. Bowles J, Schepers G, Koopman P. Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators. Dev Biol 2000;227:239-255.
10. Herr W, Sturm RA, Clerc RG et al. The POU domain: A large conserved region in the mammalian pit-1, oct-1, oct-2, and Caenorhabditis elegans unc-86 gene products. Genes Dev 1988;2:1513-1516.
11. Ryan AK, Rosenfeld MG. POU domain family values: Flexibility, partnerships, and developmental codes. Genes Dev 1997;11:1207-1225.
12. Wegner M. From head to toes: The multiple facets of Sox proteins. Nucleic Acids Res 1999;27:1409-1420.
13. Aksoy I, Jauch R, Chen J et al. Oct4 switches partnering from Sox2 to Sox17 to reinterpret the enhancer code and specify endoderm. EMBO J 2013;32:938-953.
14. Avilion AA, Nicolis SK, Pevny LH et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003; 17:126-140.
15. Boyer LA, Lee TI, Cole MF et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005;122:947-956.
16. Kamachi Y, Uchikawa M, Kondoh H. Pairing SOX off: With partners in the regulation of embryonic development. Trends Genet 2000;16: 182-187.
17. Kamachi Y, Uchikawa M, Tanouchi A et al. Pax6 and SOX2 form a co-DNA-binding partner complex that regulates initiation of lens development. Genes Dev 2001;15:1272-1286.
18. Kanai-Azuma M, Kanai Y, Gad JM et al. Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 2002;129:2367-2379.
19. Kuhlbrodt K, Herbarth B, Sock E et al. Cooperative function of POU proteins and SOX proteins in glial cells. J Biol Chem 1998;273: 16050-16057.
20. Kuhlbrodt K, Herbarth B, Sock E et al. Sox10, a novel transcriptional modulator in glial cells. J Neurosci 1998;18:237-250.
21. Loh YH, Wu Q, Chew JL et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006;38:431-440.
22. Stefanovic S, Abboud N, Desilets S et al. Interplay of Oct4 with Sox2 and Sox17: A molecular switch from stem cell pluripotency to specifying a cardiac fate. J Cell Biol 2009;186:665-673.
23. Lovell-Badge R. The early history of the Sox genes. Int J Biochem Cell Biol 2010;42:378-380.
24. Kiefer JC. Back to basics: Sox genes. Dev Dyn 2007;236:2356-2366.
25. Lefebvre V, Dumitriu B, Penzo-Mendez A et al. Control of cell fate and differentiation by Sry-related high-mobility-group box (Sox) transcription factors. Int J Biochem Cell Biol 2007;39:2195-2214.
26. Badis G, Berger MF, Philippakis AA et al. Diversity and complexity in DNA recognition by transcription factors. Science 2009;324:1720-1723.
27. van de Wetering M, Oosterwegel M, van Norren K et al. Sox-4, an Sry-like HMG box protein, is a transcriptional activator in lymphocytes. EMBO J 1993;12:3847-3854.
28. Jauch R, Ng CK, Narasimhan K et al. Crystal structure of the Sox4 HMG/DNA complex suggests a mechanism for the positional interdependence in DNA recognition. Biochem J 2012;443:39-47.
29. Palasingam P, Jauch R, Ng CK et al. The structure of Sox17 bound to DNA reveals a conserved bending topology but selective protein interaction platforms. J Mol Biol 2009;388:619-630.
30. Remenyi A, Lins K, Nissen LJ et al. Crystal structure of a POU/ HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev 2003;17:2048-2059.
31. Werner MH, Huth JR, Gronenborn AM et al. Molecular basis of human 46X,Y sex reversal revealed from the three-dimensional solution structure of the human SRY-DNA complex. Cell 1995;81:705-714.
32. Ambrosetti DC, Basilico C, Dailey L. Synergistic activation of the fibroblast growth factor 4 enhancer by Sox2 and Oct-3 depends on protein-protein interactions facilitated by a specific spatial arrangement of factor binding sites. Mol Cell Biol 1997;17:6321-6329.
33. Wilson M, Koopman P. Matching SOX: Partner proteins and cofactors of the SOX family of transcriptional regulators. Curr Opin Genet Dev 2002;12:441-446.
34. Chew JL, Loh YH, Zhang W et al. Reciprocal transcriptional regulation of Pou5f1 and Sox2 via the Oct4/Sox2 complex in embryonic stem cells. Mol Cell Biol 2005;25:6031-6046.
35. Kuroda T, Tada M, Kubota H et al. Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol 2005;25:2475-2485.
36. Nichols J, Zevnik B, Anastassiadis K et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 1998;95:379-391.
37. Rodda DJ, Chew JL, Lim LH et al. Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 2005;280:24731-24737.
38. Tanaka S, Kamachi Y, Tanouchi A et al. Interplay of SOX and POU factors in regulation of the Nestin gene in neural primordial cells. Mol Cell Biol 2004;24:8834-8846.
39. Jauch R, Aksoy I, Hutchins AP et al. Conversion of Sox17 into a pluripotency reprogramming factor by reengineering its association with Oct4 on DNA. Stem Cells 2011;29:940-951.
40. Ng CK, Li NX, Chee S et al. Deciphering the Sox-Oct partner code by quantitative cooperativity measurements. Nucleic Acids Res 2012; 40:4933-4941.
41. Sinner D, Kordich JJ, Spence JR et al. Sox17 and Sox4 differentially regulate beta-catenin/T-cell factor activity and proliferation of colon carcinoma cells. Mol Cell Biol 2007;27:7802-7815.
42. van Amerongen R, Nusse R. Towards an integrated view of Wnt signaling in development. Development 2009;136:3205-3214.
43. Liu X, Luo M, Xie W et al. Sox17 modulates Wnt3A/beta-cateninmediated transcriptional activation of the Lef-1 promoter. Am J Physiol Lung Cell Mol Physiol 2010;299:L694-710.
44. Sinner D, Rankin S, Lee M et al. Sox17 and beta-catenin cooperate to regulate the transcription of endodermal genes. Development 2004; 131:3069-3080.
45. Huang SM, Mishina YM, Liu S et al. Tankyrase inhibition stabilizes axin and antagonizes Wnt signalling. Nature 2009;461:614-620.
46. Zhang X, Peterson KA, Liu XS et al. Gene regulatory networks mediating canonical Wnt signal directed control of pluripotency and differentiation in embryo stem cells. Stem Cells 2013 [Epub ahead of print].
47. Cole MF, Johnstone SE, Newman JJ et al. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev 2008;22:746-755.
48. Kopp JL, Ormsbee BD, Desler M et al. Small increases in the level of Sox2 trigger the differentiation of mouse embryonic stem cells. Stem Cells 2008;26:903-911.
49. Aksoy I, Sakabedoyan C, Bourillot PY et al. Self-renewal of murine embryonic stem cells is supported by the serine/threonine kinases Pim- 1 and Pim-3. Stem Cells 2007;25:2996-3004.
50. Schulz H, Kolde R, Adler P et al. The FunGenES database: A genomics resource for mouse embryonic stem cell differentiation. Plos One 2009;4:e6804.
51. Bourillot PY, Aksoy I, Schreiber V et al. Novel STAT3 target genes exert distinct roles in the inhibition of mesoderm and endoderm differentiation in cooperation with Nanog. Stem Cells 2009;27:1760-1771.
52. Tai CI, Ying QL. Gbx2, a LIF/Stat3 target, promotes reprogramming to and retention of the pluripotent ground state. J Cell Sci 2013;126: 1093-1098.
53. Zhang P, Andrianakos R, Yang Y et al. Kruppel-like factor 4 (Klf4) prevents embryonic stem (ES) cell differentiation by regulating Nanog gene expression. J Biol Chem 2010;285:9180-9189.
54. Chambers I. The molecular basis of pluripotency in mouse embryonic stem cells. Cloning Stem Cells 2004;6:386-391.
55. Nishimoto M, Fukushima A, Okuda A et al. The gene for the embryonic stem cell coactivator UTF1 carries a regulatory element which selectively interacts with a complex composed of Oct-3/4 and Sox-2. Mol Cell Biol 1999;19:5453-5465.
56. Yuan H, Corbi N, Basilico C et al. Developmental-specific activity of the FGF-4 enhancer requires the synergistic action of Sox2 and Oct-3. Genes Dev 1995;9:2635-2645.
57. Mirny LA, Gelfand MS. Using orthologous and paralogous proteins to identify specificity determining residues. Genome Biol 2002;3: Preprint0002.
58. Frum T, Halbisen MA, Wang C et al. Oct4 cell-Autonomously promotes primitive endoderm development in the mouse blastocyst. Dev Cell 2013;25:610-622.
59. Qu XB, Pan J, Zhang C et al. Sox17 facilitates the differentiation of mouse embryonic stem cells into primitive and definitive endoderm in vitro. Dev Growth Differ 2008;50:585-593.
60. Seguin CA, Draper JS, Nagy A et al. Establishment of endoderm progenitors by SOX transcription factor expression in human embryonic stem cells. Cell Stem Cell 2008;3:182-195.
61. Kamachi Y, Cheah KS, Kondoh H. Mechanism of regulatory target selection by the SOX high-mobility-group domain proteins as revealed by comparison of SOX1/2/3 and SOX9. Mol Cell Biol 1999;19:107-120.
62. Muraro MJ, Kempe H, Verschure PJ. Concise review: The dynamics of induced pluripotency and its behavior captured in gene network motifs. Stem Cells 2013;31:838-848.
63. Ogawa K, Nishinakamura R, Iwamatsu Y et al. Synergistic action of Wnt and LIF in maintaining pluripotency of mouse ES cells. Biochem Biophys Res Commun 2006;343:159-166.
64. Hao J, Li TG, Qi X et al. WNT/beta-catenin pathway up-regulates Stat3 and converges on LIF to prevent differentiation of mouse embryonic stem cells. Dev Biol 2006;290:81-91.
65. Takash W, Canizares J, Bonneaud N et al. SOX7 transcription factor: Sequence, chromosomal localisation, expression, transactivation and interference with Wnt signalling. Nucleic Acids Res 2001;29:4274-4283.
66. Francois M, Koopman P, Beltrame M. SoxF genes: Key players in the development of the cardio-vascular system. Int J Biochem Cell Biol 2009;42:445-448.
67. Sakamoto Y, Hara K, Kanai-Azuma M et al. Redundant roles of Sox17 and Sox18 in early cardiovascular development of mouse embryos. Biochem Biophys Res Commun 2007;360:539-544.
68. Niakan KK, Ji H, Maehr R et al. Sox17 promotes differentiation in mouse embryonic stem cells by directly regulating extraembryonic gene expression and indirectly antagonizing self-renewal. Genes Dev 2010;24:312-326.
69. Francois M, Caprini A, Hosking B et al. Sox18 induces development of the lymphatic vasculature in mice. Nature 2008;456:643-647.
70. Sun N, Panetta NJ, Gupta DM et al. Feeder-free derivation of induced pluripotent stem cells from adult human adipose stem cells. Proc Natl Acad Sci USA 2009;106:15720-157.
71. Zhang Y, Liu T, Meyer CA et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008;9:R137.
72. Quinlan AR, Hall IM. BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 2010;26:841-842.
73. Kraus P, Leong G, Tan V et al. A more cost effective and rapid high percentage germ-line transmitting chimeric mouse generation procedure via microinjection of 2-cell, 4-cell, and 8-cell embryos with ES and iPS cells. Genesis 2010;48:394-399.