Sumoylation represses nanog expression via modulating transcription factors oct4 and sox2

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Wu, Yongyan ^a   Guo, Zekun ^a   Wu, Haibo ^a   Wang, Xiaohai ^a   Yang, Lixia ^a   Shi, Xiaoyan ^a   Du, Juan ^a   Tang, Bo ^a   Li, Wenzhong ^a   Yang, Liping ^a   Zhang, Yong ^a  

^a NORTHWEST A F UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

LIGASE; OCTAMER TRANSCRIPTION FACTOR 4; PIAS2 LIGASE; PIAS3 LIGASE; PROTEIN UBC9; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; EMBRYO; MOUSE; NONHUMAN; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SUMOYLATION;

ANIMALS; BLOTTING, WESTERN; CELL LINE; HOMEODOMAIN PROTEINS; IMMUNOPRECIPITATION; MICE; NIH 3T3 CELLS; OCTAMER TRANSCRIPTION FACTOR-3; POLYMERASE CHAIN REACTION; PROTEIN BINDING; PROTEIN INHIBITORS OF ACTIVATED STAT; SOXB1 TRANSCRIPTION FACTORS; SUMOYLATION;

EID: 84862700963     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039606     Document Type: Article

References (47)

1. Martin GR, (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 78: 7634-7638.
2. Evans MJ, Kaufman MH, (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292: 154-156.
3. Chambers I, Colby D, Robertson M, Nichols J, Lee S, et al. (2003) Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113: 643-655.
4. Lavial F, Acloque H, Bertocchini F, Macleod DJ, Boast S, et al. (2007) The Oct4 homologue PouV and Nanog regulate pluripotency in chicken embryonic stem cells. Development 134: 3549-3563.
5. 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.
6. Yamaguchi S, Kimura H, Tada M, Nakatsuji N, Tada T, (2005) Nanog expression in mouse germ cell development. Gene Expr Patterns 5: 639-646.
7. 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.
8. Kerscher O, Felberbaum R, Hochstrasser M, (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22: 159-180.
9. Guo D, Li M, Zhang Y, Yang P, Eckenrode S, et al. (2004) A functional variant of SUMO4, a new I kappa B alpha modifier, is associated with type 1 diabetes. Nat Genet. 36: 837-841.
10. Okuma T, Honda R, Ichikawa G, Tsumagari N, Yasuda H, (1999) In vitro SUMO-1 modification requires two enzymatic steps, E1 and E2. Biochem Biophys Res Commun. 254: 693-698.
11. Maderböck K, Pichler A, (2010) Sumo control. Subcell Biochem (54): 158-169.
12. Johnson ES, (2004) Protein modification by SUMO. Annu Rev Biochem 73: 355-382.
13. Hay RT, (2005) SUMO: a history of modification. Mol Cell 18: 1-12.
14. Seeler JS, Bischof O, Nacerddine K, Dejean A, (2007) SUMO, the three Rs and cancer. Curr Top Microbiol Immunol 313: 49-71.
15. Tsuruzoe S, Ishihara K, Uchimura Y, Watanabe S, Sekita Y, et al. (2006) Inhibition of DNA binding of Sox2 by the SUMO conjugation. Biochem Biophys Res Commun 351: 920-926.
16. Wei F, Schöler HR, Atchison ML, (2007) SUMOylation of Oct4 enhances its stability, DNA binding, and transactivation. J Biol Chem 282: 21551-21560.
17. Zhang Z, Liao B, Xu M, Jin Y, (2007) Post-translational modification of POU domain transcription factor Oct-4 by SUMO-1. FASEB J 21: 3042-3051.
18. Kuroda T, Tada M, Kubota H, Kimura H, Hatano SY, et al. (2005) Octamer and Sox elements are required for transcriptional cis regulation of Nanog gene expression. Mol Cell Biol 25: 2475-2485.
19. Fukuda I, Ito A, Hirai G, Nishimura S, Kawasaki H, et al. (2009) Ginkgolic acid inhibits protein SUMOylation by blocking formation of the E1-SUMO intermediate. Chem Biol 16: 133-140.
20. Liu X, Liu Z, Jang SW, Ma Z, Shinmura K, et al. (2007) SUMOylation of nucleophosmin/B23 regulates its subcellular localization, mediating cell proliferation and survival. Proc Natl Acad Sci U S A 104: 9679-9684.
21. Cai Q, Robertson ES, (2010) Ubiquitin/SUMO modification regulates VHL protein stability and nucleocytoplasmic localization. PLoS One 5: e12636.
22. Wang ZX, Teh CH, Kueh JL, Lufkin T, Robson P, et al. (2007) Oct4 and Sox2 directly regulate expression of another pluripotency transcription factor, Zfp206, in embryonic stem cells. J Biol Chem 282: 12822-12830.
23. Stefanovic S, Abboud N, Désilets S, Nury D, Cowan C, et al. (2009) Interplay of Oct4 with Sox2 and Sox17: a molecular switch from stem cell pluripotency to specifying a cardiac fate. J Cell Biol 186: 665-673.
24. Hong Y, Xing X, Li S, Bi H, Yang C, et al. (2011) SUMOylation of DEC1 Protein Regulates Its Transcriptional Activity and Enhances Its Stability. PLoS ONE 6(8): e23046.
25. Woo CH, Abe J, (2010) SUMO-a post-translational modification with therapeutic potential? Curr Opin Pharmacol 10: 146-155.
26. Yang K, Moldovan GL, Vinciguerra P, Murai J, Takeda S, et al. (2011) Regulation of the Fanconi anemia pathway by a SUMO-like delivery network. Genes Dev 25: 1847-1858.
27. Nagai S, Davoodi N, Gasser SM, (2011) Nuclear organization in genome stability: SUMO connections. Cell Res 21: 474-485.
28. Chiu SY, Asai N, Costantini F, Hsu W, (2008) SUMO-specific protease 2 is essential for modulating p53-Mdm2 in development of trophoblast stem cell niches and lineages. PLoS Biol 6: e310.
29. Gupta P, Ho PC, Huq MM, Ha SG, Park SW, et al. (2008) Retinoic acid-stimulated sequential phosphorylation, PML recruitment, and SUMOylation of nuclear receptor TR2 to suppress Oct4 expression. Proc Natl Acad Sci U S A 105: 11424-11429.
30. Sánchez J, Talamillo A, Lopitz-Otsoa F, Pérez C, Hjerpe R, et al. (2010) SUMOylation modulates the activity of Spalt-like proteins during wing development in Drosophila. J Biol Chem 285: 25841-25849.
31. Du JX, McConnell BB, Yang VW, (2010) A small ubiquitin-related modifier-interacting motif functions as the transcriptional activation domain of Krüppel-like factor 4. J Biol Chem 285: 28298-28308.
32. Chickarmane V, Troein C, Nuber UA, Sauro HM, Peterson C, (2006) Transcriptional dynamics of the embryonic stem cell switch. PLoS Comput Biol 2: e123.
33. Ren J, Gao X, Jin C, Zhu M, Wang X, et al. (2009) Systematic study of protein SUMOylation: Development of a site-specific predictor of SUMOsp 2.0. Proteomics 9: 3409-3412.
34. Georges A, Benayoun BA, Marongiu M, Dipietromaria A, L'Hôte D, et al. (2011) SUMOylation of the Forkhead Transcription Factor FOXL2 Promotes Its Stabilization/Activation through Transient Recruitment to PML Bodies. PLoS ONE 6(10): e25463.
35. Hamard PJ, Boyer-Guittaut M, Camuzeaux B, Dujardin D, Hauss C, et al. (2007) SUMOylation delays the ATF7 transcription factor subcellular localization and inhibits its transcriptional activity. Nucleic Acids Res 35: 1134-1144.
36. Liu G-H, Gerace L, (2009) Sumoylation Regulates Nuclear Localization of Lipin-1α in Neuronal Cells. PLoS ONE 4(9): e7031.
37. Rodda DJ, Chew JL, Lim LH, Loh YH, Wang B, et al. (2005) Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 280: 24731-24737.
38. van den Berg DL, Snoek T, Mullin NP, Yates A, Bezstarosti K, et al. (2010) An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6: 369-381.
39. Geiss-Friedlander R, Melchior F, (2007) Concepts in sumoylation: a decade on. Nat Rev Mol Cell Biol 8: 947-956.
40. Cox B, Briscoe J, Ulloa F, (2010) SUMOylation by Pias1 Regulates the Activity of the Hedgehog Dependent Gli Transcription Factors. PLoS ONE 5(8): e11996.
41. Hyslop L, Stojkovic M, Armstrong L, Walter T, Stojkovic P, et al. (2005) Downregulation of NANOG Induces Differentiation of Human Embryonic Stem Cells to Extraembryonic Lineages. Stem Cells 23: 1035-1043.
42. Chan KK, Zhang J, Chia NY, Chan YS, Sim HS, et al. (2009) KLF4 and PBX1 directly regulate NANOG expression in human embryonic stem cells. Stem Cells. 27: 2114-2125.
43. Karantzali E, Lekakis V, Ioannou M, Hadjimichael C, Papamatheakis J, et al. (2011) Sall1 regulates embryonic stem cell differentiation in association with nanog. J Biol Chem. 286: 1037-1045.
44. Liu LB, Omata W, Kojima I, Shibata H, (2007) The SUMO conjugating enzyme Ubc9 is a regulator of GLUT4 turnover and targeting to the insulin-responsive storage compartment in 3T3-L1 adipocytes. Diabetes 56: 1977-1985.
45. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
46. La Salle S, Sun F, Zhang XD, Matunis MJ, Handel MA, (2008) Developmental control of sumoylation pathway proteins in mouse male germ cells. Developmental Biology 321: 227-237.
47. Masui S, Nakatake Y, Toyooka Y, Shimosato D, Yagi R, et al. (2007) Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 9: 625-635.