STAT3 phosphorylation at tyrosine 705 and serine 727 differentially regulates mouse esc fates

Stem Cells

Volumn 32, Issue 5, 2014, Pages 1149-1160

  Huang, Guanyi ^a   Yan, Hexin ^a,b   Ye, Shoudong ^a   Tong, Chang ^a   Ying, Qi Long ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Differentiation; Embryonic stem cell; Phosphorylation; Self renewal; STAT3

Indexed keywords

FIBROBLAST GROWTH FACTOR; LEUKEMIA INHIBITORY FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; SERINE; STAT3 PROTEIN; TYROSINE; BENZAMIDE DERIVATIVE; DIPHENYLAMINE; N (2,3 DIHYDROXYPROPOXY) 3,4 DIFLUORO 2 (2 FLUORO 4 IODOANILINO)BENZAMIDE; NESTIN; STAT3 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL PROLIFERATION; CELL RENEWAL; ECTODERM; EMBRYONIC STEM CELL; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; AMINO ACID SUBSTITUTION; ANALOGS AND DERIVATIVES; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GENETICS; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE; WESTERN BLOTTING;

AMINO ACID SUBSTITUTION; ANIMALS; BENZAMIDES; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DIPHENYLAMINE; EMBRYONIC STEM CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; LEUKEMIA INHIBITORY FACTOR; MICE, KNOCKOUT; MICE, TRANSGENIC; NESTIN; NEURONS; PHOSPHORYLATION; PLURIPOTENT STEM CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERINE; STAT3 TRANSCRIPTION FACTOR; TYROSINE;

EID: 84899032575     PISSN: 10665099     EISSN: 15494918     Source Type: Journal    
DOI: 10.1002/stem.1609     Document Type: Article

References (43)

1. Bromberg J, Darnell JE Jr,. The role of STATs in transcriptional control and their impact on cellular function. Oncogene 2000; 19: 2468-2473.
2. Decker T, Kovarik P,. Serine phosphorylation of STATs. Oncogene 2000; 19: 2628-2637.
3. Qin HR, Kim HJ, Kim JY, et al. Activation of signal transducer and activator of transcription 3 through a phosphomimetic serine 727 promotes prostate tumorigenesis independent of tyrosine 705 phosphorylation. Cancer Res 2008; 68: 7736-7741.
4. Hazan-Halevy I, Harris D, Liu Z, et al. STAT3 is constitutively phosphorylated on serine 727 residues, binds DNA, and activates transcription in CLL cells. Blood 2010; 115: 2852-2863.
5. Aggarwal BB, Kunnumakkara AB, Harikumar KB, et al. Signal transducer and activator of transcription-3, inflammation, and cancer: How intimate is the relationship? Ann N Y Acad Sci 2009; 1171: 59-76.
6. Shi X, Zhang H, Paddon H, et al. Phosphorylation of STAT3 serine-727 by cyclin-dependent kinase 1 is critical for nocodazole-induced mitotic arrest. Biochemistry 2006; 45: 5857-5867.
7. Burdon T, Smith A, Savatier P,. Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol 2002; 12: 432-438.
8. Frank DA,. STAT3 as a central mediator of neoplastic cellular transformation. Cancer Lett 2007; 251: 199-210.
9. de la Iglesia N, Konopka G, Puram SV, et al. Identification of a PTEN-regulated STAT3 brain tumor suppressor pathway. Genes Dev 2008; 22: 449-462.
10. Chapman RS, Lourenco P, Tonner E, et al. The role of Stat3 in apoptosis and mammary gland involution. Conditional deletion of Stat3. Adv Exp Med Biol 2000; 480: 129-138.
11. Chapman RS, Lourenco PC, Tonner E, et al. Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3. Genes Dev 1999; 13: 2604-2616.
12. O'Farrell AM, Liu Y, Moore KW, et al. IL-10 inhibits macrophage activation and proliferation by distinct signaling mechanisms: Evidence for Stat3-dependent and -independent pathways. EMBO J 1998; 17: 1006-1018.
13. Hutchins AP, Diez D, Takahashi Y, et al. Distinct transcriptional regulatory modules underlie STAT3's cell type-independent and cell type-specific functions. Nucl Acid Res 2013; 41: 2155-2170.
14. Niwa H, Burdon T, Chambers I, et al. Self-renewal of pluripotent embryonic stem cells is mediated via activation of STAT3. Genes Dev 1998; 12: 2048-2060.
15. Raz R, Lee CK, Cannizzaro LA, et al. Essential role of STAT3 for embryonic stem cell pluripotency. Proc Natl Acad Sci U S A 1999; 96: 2846-2851.
16. Ying QL, Wray J, Nichols J, et al. The ground state of embryonic stem cell self-renewal. Nature 2008; 453: 519-523.
17. Takeda K, Noguchi K, Shi W, et al. Targeted disruption of the mouse Stat3 gene leads to early embryonic lethality. Proc Natl Acad Sci U S A 1997; 94: 3801-3804.
18. Tong C, Huang G, Ashton C, et al. Generating gene knockout rats by homologous recombination in embryonic stem cells. Nat Protoc 2011; 6: 827-844.
19. Tompers DM, Labosky PA,. Electroporation of murine embryonic stem cells: A step-by-step guide. Stem Cells 2004; 22: 243-249.
20. Banaszynski LA, Chen LC, Maynard-Smith LA, et al. A rapid, reversible, and tunable method to regulate protein function in living cells using synthetic small molecules. Cell 2006; 126: 995-1004.
21. Miyakoshi M, Yamamoto M, Tanaka H, et al. Serine 727 phosphorylation of STAT3: An early change in mouse hepatocarcinogenesis induced by neonatal treatment with diethylnitrosamine. Mol Carcinog 2012.
22. Sakaguchi M, Oka M, Iwasaki T, et al. Role and regulation of STAT3 phosphorylation at Ser727 in melanocytes and melanoma cells. J Invest Dermatol 2012; 132: 1877-1885.
23. Gartsbein M, Alt A, Hashimoto K, et al. The role of protein kinase C delta activation and STAT3 Ser727 phosphorylation in insulin-induced keratinocyte proliferation. J Cell Sci 2006; 119: 470-481.
24. Cartwright P, McLean C, Sheppard A, et al. LIF/STAT3 controls ES cell self-renewal and pluripotency by a Myc-dependent mechanism. Development 2005; 132: 885-896.
25. Kidder BL, Yang J, Palmer S,. Stat3 and c-Myc genome-wide promoter occupancy in embryonic stem cells. Plos One 2008; 3: e3932.
26. Kim J, Woo AJ, Chu J, et al. A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 2010; 143: 313-324.
27. Bromberg JF, Wrzeszczynska MH, Devgan G, et al. Stat3 as an oncogene. Cell 1999; 98: 295-303.
28. Qin S, Zhang CL,. Role of Kruppel-like factor 4 in neurogenesis and radial neuronal migration in the developing cerebral cortex. Mol Cell Biol 2012; 32: 4297-4305.
29. Cao F, Hata R, Zhu P, et al. Conditional deletion of Stat3 promotes neurogenesis and inhibits astrogliogenesis in neural stem cells. Biochem Biophys Res Commun 2010; 394: 843-847.
30. Tsai SY, Yang LY, Wu CH, et al. Injury-induced Janus kinase/protein kinase C-dependent phosphorylation of growth-associated protein 43 and signal transducer and activator of transcription 3 for neurite growth in dorsal root ganglion. J Neurosci Res 2007; 85: 321-331.
31. Ying QL, Smith AG,. Defined conditions for neural commitment and differentiation. Methods Enzymol 2003; 365: 327-341.
32. Yang J, van Oosten AL, Theunissen TW, et al. Stat3 activation is limiting for reprogramming to ground state pluripotency. Cell Stem Cell 2010; 7: 319-328.
33. van Oosten AL, Costa Y, Smith A, et al. JAK/STAT3 signalling is sufficient and dominant over antagonistic cues for the establishment of naive pluripotency. Nat Commun 2012; 3: 817.
34. Hamazaki T, Kehoe SM, Nakano T, et al. The Grb2/Mek pathway represses Nanog in murine embryonic stem cells. Mol Cell Biol 2006; 26: 7539-7549.
35. Burdon T, Stracey C, Chambers I, et al. Suppression of SHP-2 and ERK signalling promotes self-renewal of mouse embryonic stem cells. Dev Biol 1999; 210: 30-43.
36. Foshay KM, Gallicano GI,. Regulation of Sox2 by STAT3 initiates commitment to the neural precursor cell fate. Stem Cells Dev 2008; 17: 269-278.
37. Caldenhoven E, van Dijk TB, Solari R, et al. STAT3beta, a splice variant of transcription factor STAT3, is a dominant negative regulator of transcription. J Biol Chem 1996; 271: 13221-13227.
38. Kunath T, Saba-El-Leil MK, Almousailleakh M, et al. FGF stimulation of the Erk1/2 signalling cascade triggers transition of pluripotent embryonic stem cells from self-renewal to lineage commitment. Development 2007; 134: 2895-2902.
39. Stavridis MP, Lunn JS, Collins BJ, et al. A discrete period of FGF-induced Erk1/2 signalling is required for vertebrate neural specification. Development 2007; 134: 2889-2894.
40. Kamiya D, Banno S, Sasai N, et al. Intrinsic transition of embryonic stem-cell differentiation into neural progenitors. Nature 2011; 470: 503-509.
41. Chambers I, Silva J, Colby D, et al. Nanog safeguards pluripotency and mediates germline development. Nature 2007; 450: 1230-1234.
42. Galvin-Burgess KE, Travis ED, Pierson KE, et al. TGF-beta-Superfamily Signaling Regulates Embryonic Stem Cell Heterogeneity: Self-Renewal as a Dynamic and Regulated Equilibrium. Stem Cells 2013; 31: 48-58.
43. Singh AM, Hamazaki T, Hankowski KE, et al. A heterogeneous expression pattern for Nanog in embryonic stem cells. Stem Cells 2007; 25: 2534-2542.