Oct4 interaction with Hmgb2 regulates Akt signaling and pluripotency

Stem Cells

Volumn 31, Issue 6, 2013, Pages 1107-1120

  Campbell, Pearl A ^a,b   Rudnicki, Michael A ^a,b  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Akt; Bivalent domains; Hmgb2; Oct4; Pluripotency; Set complex

Indexed keywords

HIGH MOBILITY GROUP B2 PROTEIN; HISTONE H3; OCTAMER TRANSCRIPTION FACTOR 4; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SERINE; THREONINE; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DIFFERENTIATION; CHROMATIN; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; EPIGENETICS; GENE EXPRESSION; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SUMOYLATION;

ANIMALS; CELLS, CULTURED; CHROMATIN; DNA DAMAGE; EMBRYONIC STEM CELLS; EPIGENESIS, GENETIC; G1 PHASE; HISTONES; HMGB2 PROTEIN; MICE; OCTAMER TRANSCRIPTION FACTOR-3; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PLURIPOTENT STEM CELLS; POLYCOMB-GROUP PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTO-ONCOGENE PROTEINS C-AKT; S PHASE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84877948056     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1365     Document Type: Article

References (93)

1. Bernstein BE, Mikkelsen TS, Xie X et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006;125:315-326.
2. Guenther MG, Levine SS, Boyer LA et al. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007;130:77-88. (Pubitemid 47031323)
3. Ivanova N, Dobrin R, Lu R et al. Dissecting self-renewal in stem cells with RNA interference. Nature 2006;442:533-538. (Pubitemid 44167907)
4. Matoba R, Niwa H, Masui S et al. Dissecting Oct3/4-regulated gene networks in embryonic stem cells by expression profiling. PLoS One 2006;1:e26.
5. Boyer LA, Plath K, Zeitlinger J et al. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006;441:349-353. (Pubitemid 44050199)
6. Erhardt S, Su IH, Schneider R et al. Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development. Development 2003;130:4235-4248. (Pubitemid 37185314)
7. Squazzo SL, O'Geen H, Komashko VM et al. Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res 2006;16:890-900. (Pubitemid 43992913)
8. Walker E, Ohishi M, Davey RE et al. Prediction and testing of novel transcriptional networks regulating embryonic stem cell self-renewal and commitment. Cell Stem Cell 2007;1:71-86. (Pubitemid 46865803)
9. Ang Y-S, Tsai S-Y, Lee D-F et al. Wdr5 mediates self-renewal and reprogramming via the embryonic stem cell core transcriptional network. Cell 2011;145:183-197.
10. Arias AM, Hayward P. Filtering transcriptional noise during development: Concepts and mechanisms. Nature 2006;7:34-44. (Pubitemid 41828946)
11. Chang F, Lee JT, Navolanic PM et al. Involvement of PI3K/Akt pathway in cell cycle progression, apoptosis, and neoplastic transformation: A target for cancer chemotherapy. Leukemia 2003;17:590-603. (Pubitemid 36395654)
12. EylerCE, Foo W-C, LaFiura KM et al. Brain cancer stem cells display preferential sensitivity to akt inhibition. Stem Cells 2008;26:3027-3036.
13. Kharas MG, Okabe R, Ganis JJ et al. Constitutively active AKT depletes hematopoietic stem cells and induces leukemia in mice. Blood 2010;115:1406-1415.
14. Kimura T, Nakano T. Regulation of stem cell systems by PI3K/Akt signaling. In: Rajasekhar VK, Vemuri MC, eds. Regulatory Networks in Stem Cells. Humana Press, 2009:309-318.
15. Kimura T, Nakano T. Induction of pluripotency in primordial germ cells. Histol Histopathol 2011;26:643-650.
16. Korkaya H, Paulson A, Charafe-Jauffret E et al. Regulation of mammary stem/progenitor cells by PTEN/Akt/β-catenin signaling. PLoS Biol 2009;7:e1000121.
17. Lee J, Kanatsu-Shinohara M, Inoue K et al. Akt mediates self-renewal division of mouse spermatogonial stem cells. Development 2007;134:1853-1859. (Pubitemid 46939231)
18. Watanabe S, Umehara H, Murayama K et al. Activation of Akt signaling is sufficient to maintain pluripotency in mouse and primate embryonic stem cells. Oncogene 2006;25:2697-2707.
19. Wilson EM, Rotwein P. Selective control of skeletal muscle differentiation by Akt1. J Biol Chem 2007;282:5106-5110. (Pubitemid 47093711)
20. Hansen KH, Bracken AP, Pasini D et al. A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 2008;10:1291-1300.
21. Aoto T, Saitoh N, Sakamoto Y et al. Polycomb group protein-associated chromatin is reproduced in post-mitotic G1 phase and is required for S phase progression. J Biol Chem 2008;283:18905-18915.
22. Campbell PA, Perez-Iratxeta C, Andrade-Navarro MA et al. Oct4 targets regulatory nodes to modulate stem cell function. PLoS One 2007;2:e553.
23. Yan N, Regalado-Magdos AD, Stiggelbout B et al. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol 2010;11:1005-1013.
24. Bolstad BM, Irizarry RA, Astrand M et al. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 2003;19:185-193. (Pubitemid 36181903)
25. Thomson M, Liu SJ, Zou L-N et al. Pluripotency factors in embryonic stem cells regulate differentiation into germ layers. Cell 2011;145:875-889.
26. Doetschman TC, Eistetter H, Katz M et al. The in vitro development of blastocyst-derived embryonic stem cell lines: Formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 1985;87:27-45. (Pubitemid 15029925)
27. Shen MM, Leder P. Leukemia inhibitory factor is expressed by the preimplantation uterus and selectively blocks primitive ectoderm formation in vitro. Proc Natl Acad Sci USA 1992;89:8240-8244.
28. Burdon T, Smith A, Savatier P. Signalling, cell cycle, and pluripotency in embryonic stem cells. Trends Cell Biol 2002;12:432-438. (Pubitemid 35239952)
29. Vallier L, Touboul T, Chng Z et al. Early cell fate decisions of human embryonic stem cells and mouse epiblast stem cells are controlled by the same signalling pathways. PLoS One 2009;4:e6082.
30. Xu H, Wang W, Li C et al. WWP2 promotes degradation of transcription factor OCT4 in human embryonic stem cells. Cell Res 2009;19:561-573.
31. Searl T, Silinsky E. LY 294002 inhibits adenosine receptor activation by a mechanism independent of effects on PI-3 kinase or casein kinase II. Purinergic Signal 2005;1:389-394. (Pubitemid 43019538)
32. DeFeo-Jones D, Barnett SF, Fu S et al. Tumor cell sensitization to apoptotic stimuli by selective inhibition of specific Akt/PKB family members. Mol Cancer Ther 2005;4:271-279. (Pubitemid 40340206)
33. Therese HH, Margareta S, Boris Z. Inhibitors of the PI3-kinase/Akt pathway induce mitotic catastrophe in non-small cell lung cancer cells. Int J Cancer 2006;119:1028-1038.
34. Brumbaugh J, Hou Z, Russell JD et al. Phosphorylation regulates human OCT4. Proc Natl Acad Sci USA 2012;109:7162-7168.
35. Lin Y, Yang Y, Li W et al. Reciprocal regulation of Akt and Oct4 promotes the self-renewal and survival of embryonal carcinoma cells. Mol Cell 2012;48:627-640.
36. Sene K, Porter C, Palidwor G et al. Gene function in early mouse embryonic stem cell differentiation. BMC Genomics 2007;8:85.
37. Dailey L, Basillico C. Coevolution of HMG domains and homeodomains and the generation of transcriptional regulation by Sox/POU complexes. J Cell Physiol 2001;186:315-328. (Pubitemid 32147715)
38. 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. (Pubitemid 36999330)
39. Okumura-Nakanishi S, Saito M, Niwa H et al. Oct-3/4 and Sox2 regulate Oct-3/4 gene in embryonic stem cells. J Biol Chem 2005;280:5307-5317. (Pubitemid 40280004)
40. Chew J-L, Loh Y-H, 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. (Pubitemid 40946556)
41. Boyer LA, Lee TI, Cole MF et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005;122:1-10.
42. Ferraris L, Stewart AP, Kang J et al. Combinatorial binding of transcription factors in the pluripotency control regions of the genome. Genome Res 2011;21:1055-1064.
43. Butteroni C, De Felici M, Scholer HR et al. Phage display screening reveals an association between germline-specific transcription factor Oct-4 and multiple cellular proteins. J Mol Biol 2000;304:529-540. (Pubitemid 32006188)
44. Ringrose L, Paro R. Epigenetic regulation of cellular memory by the polycomb and trithorax group proteins. Annu Rev Genet 2004;38:413-443. (Pubitemid 40013734)
45. Zhang Q, Wang Y. HMG modifications and nuclear function. Biochim Biophys Acta 2010;1799:28-36.
46. Lieberman J, Fan Z. Nuclear war: The granzyme A-bomb. Curr Opin Immunol 2003;15:553-559. (Pubitemid 37130196)
47. Bell E, Wingate RJT, Lumsden A. Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science 1999;284:2168-2171. (Pubitemid 29297475)
48. Decoville M, Giacomello E, Leng M et al. DSP1, an HMG-like protein, is involved in the regulation of homeotic genes. Genetics 2001;157:237-244. (Pubitemid 32066310)
49. Pan G, Li J, Zhou Y et al. A negative feedback loop of transcription factors that controls stem cell pluripotency and self-renewal. FASEB J 2006;20:E1094-E1102. (Pubitemid 44943786)
50. Fung TK, Siu WY, Yam CH et al. Cyclin F is degraded during G2-M by mechanisms fundamentally different from other cyclins. J Biol Chem 2002;277:35140-35149.
51. Wrighton KH. DNA damage response: DNA takes a break with SUMO. Nat Rev Mol Cell Biol 2010;11:85-85.
52. Starita LM, Parvin JD. The multiple nuclear functions of BRCA1: Transcription, ubiquitination and DNA repair. Curr Opin Cell Biol 2003;15:345-350. (Pubitemid 36638654)
53. Shieh S-Y, Ikeda M, Taya Y et al. DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 1997;91:325-334. (Pubitemid 27467963)
54. Wei F, Scholer HR, Atchison ML. Sumoylation of Oct4 enhances its stability, DNA binding and transactivation. J Biol Chem 2007;282:21551-21560. (Pubitemid 47099909)
55. Zhang Z, Liao B, Xu M et al. Post-translational modification of POU domain transcription factor Oct-4 by SUMO-1. FASEB J 2007;21:1-10.
56. Tsuruzoe S, Ishihara K, Uchimura Y et al. Inhibition of DNA binding of Sox2 by the SUMO conjugation. Biochem Biophys Res Commun 2006;351:920-926. (Pubitemid 44715874)
57. Gill G. Something about SUMO inhibits transcription. Curr Opin Genet Dev 2005;15:536-541. (Pubitemid 41262410)
58. Bergink S, Salomons FA, Hoogstraten D et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev 2006;20:1343-1352. (Pubitemid 43727594)
59. Celeste A, Fernandez-Capetillo O, Kruhlak MJ et al. Histone, H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 2003;5:675-679. (Pubitemid 36818091)
60. Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004;432:316-323. (Pubitemid 39551659)
61. White J, Stead E, Faast R et al. Developmental activation of the Rb-E2F pathway and establishment of cell cycle-regulated cyclin-dependent kinase activity during embryonic stem cell differentiation. Mol Biol Cell 2005;16:2018-2027. (Pubitemid 40471967)
62. Sudo T, Ota Y, Kotani S et al. Activation of Cdh1-dependent APC is required for G1 cell cycle arrest and DNA damage-induced G2 checkpoint in vertebrate cells. EMBO J 2001;20:6499-6508. (Pubitemid 33078722)
63. O'Neill C. Phosphatidylinositol 3-kinase signaling in mammalian preimplantation embryo development. Reproduction 2008;136:147-156.
64. Riley JK, Carayannopoulos MO, Wyman AH et al. The PI3K/Akt pathway is present and functional in the preimplantation mouse embryo. Dev Biol 2005;284:377-386. (Pubitemid 41199813)
65. Kim J, Kim B, Kim J et al. The phosphoinositide-3-kinase/Akt pathway mediates the transient increase in Nanog expression during differentiation of F9 cells. Arch Pharm Res 2010;33:1117-1125.
66. Jeong C-H, Cho Y-Y, Kim M-O et al. Phosphorylation of Sox2 cooperates in reprogramming to pluripotent stem cells. Stem Cells 2010;28:2141-2150.
67. Bang O, Park E, Yang S et al. Overexpression of Akt inhibits NGF-induced growth arrest and neuronal differentiation of PC12 cells. J Cell Sci 2001;114:81-88. (Pubitemid 32118059)
68. Lopez-Carballo G, Moreno L, Masiá S et al. Activation of the phosphatidylinositol 3-Kinase/Akt signaling pathway by retinoic acid is required for neural differentiation of SH-SY5Y human neuroblastoma cells. J Biol Chem 2002;277:25297-25304. (Pubitemid 34951839)
69. Nakamura T, Inoue K, Ogawa S et al. Effects of Akt signaling on nuclear reprogramming. Genes Cells 2008;13:1269-1277.
70. Altomare DA, Testa JR. Perturbations of the Akt signaling pathway in human cancer. Oncogene 2005;24:7455-7464. (Pubitemid 41637985)
71. Martelli AM, Tabellini G, Bressanin D et al. The emerging multiple roles of nuclear Akt. Biochim Biophys Acta 2012;1823:2168-2178.
72. Wallin JJ, Guan J, Prior WW et al. Nuclear phospho-Akt increase predicts synergy of PI3K inhibition and doxorubicin in breast and ovarian cancer. Sci Transl Med 2010;2:48ra66.
73. Badve S, Collins NR, Bhat-Nakshatri P et al. Subcellular localization of activated AKT in estrogen receptor- and progesterone receptor-expressing breast cancers: Potential clinical implications. Am J Pathol 2010;176:2139-2149.
74. Shah A, Swain WA, Richardson D et al. Phospho-Akt expression is associated with a favorable outcome in non-small cell lung cancer. Clin Cancer Res 2005;11:2930-2936. (Pubitemid 40525195)
75. Liang J, Wan M, Zhang Y et al. Nanog and Oct4 associate with unique transcriptional repression complexes in embryonic stem cells. Nat Cell Biol 2008;10:731-739. (Pubitemid 351772939)
76. Pardo M, Lang B, Yu L et al. An expanded Oct4 interaction network: Implications for stem cell biology, development, and disease. Cell Stem Cell 2010;6:382-395.
77. van den Berg DL, Snoek T, Mullin NP et al. An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 2010;6:369-381.
78. Wang J, Rao S, Chu J et al. A protein interaction network for pluripotency of embryonic stem cells. Nature 2006;444:364-368. (Pubitemid 44764111)
79. Estanyol JM, Jaumot M, Casanovas O et al. The protein SET regulates the inhibitory effect of p21Cip1 on cyclin E-cyclin-dependent kinase 2 activity. J Biol Chem 1999;274:33161-33165. (Pubitemid 129535360)
80. Canela N, Rodriguez-Vilarrupla A, Estanyol JM et al. The SET protein regulates G2/M transition by modulating cyclin B- cyclin-dependent kinase 1 activity. J Biol Chem 2003;278:1158-1164. (Pubitemid 36790797)
81. Li M, Makkinje A, Damuni Z. The myeloid leukemia-associated protein SET is a potent inhibitor of protein phosphatase 2A. J Biol Chem 1996;271:11059-11062. (Pubitemid 26155931)
82. Kandel ES, Skeen J, Majewski N et al. Activation of Akt/protein kinase B overcomes a G2/M cell cycle checkpoint induced by DNA damage. Mol Cell Biol 2002;22:7831-7841. (Pubitemid 35217294)
83. Fernando P, Brunette S, Megeney LA. Neural stem cell differentiation is dependent upon endogenous caspase-3 activity. FASEB J 2005;19:1671-1673. (Pubitemid 41429525)
84. Fernando P, Kelly JF, Balazsi K et al. Caspase 3 activity is required for skeletal muscle differentiation. PNAS 2002;99:11025-11030. (Pubitemid 34920873)
85. Sherman MH, Bassing CH, Teitell MA. Regulation of cell differentiation by the DNA damage response. Trends Cell Biol 2011;21:312-319.
86. Fujita J, Crane AM, Souza MK et al. Caspase activity mediates the differentiation of embryonic stem cells. Cell Stem Cell 2008;2:595-601. (Pubitemid 351729216)
87. Blanpain C, Mohrin M, Sotiropoulou PA et al. DNA-damage response in tissue-specific and cancer stem cells. Cell Stem Cell 2011;8:16-29.
88. Gore A, Li Z, Fung H-L et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 2011;471:63-67.
89. Marion RM, Strati K, Li H et al. A p53-mediated DNA damage response limits reprogramming to ensure iPS cell genomic integrity. Nature 2009;460:1149-1153.
90. Hong H, Takahashi K, Ichisaka T et al. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009;460:1132-1135.
91. Kawamura T, Suzuki J, Wang YV et al. Linking the p53 tumour suppressor pathway to somatic cell reprogramming. Nature 2009;460:1140-1144.
92. Niessen HEC, Demmers JA, Voncken JW. Talking to chromatin: Post-translational modulation of polycomb group function. Epigenetics Chromatin 2009;2:10.
93. Ren X, Vincenz C, Kerppola TK. Changes in the distributions and dynamics of polycomb repressive complexes during embryonic stem cell differentiation. Mol Cell Biol 2008;28:2884-2895. (Pubitemid 351556522)