Protein kinase C-induced early growth response protein-1 binding to SNAIL promoter in epithelial-mesenchymal transition of human embryonic stem cells

Stem Cells and Development

Volumn 23, Issue 18, 2014, Pages 2180-2189

  Kinehara, Masaki ^a,b   Kawamura, Suguru ^a,b   Mimura, Sumiyo ^a,b   Suga, Mika ^a   Hamada, Akiko ^a   Wakabayashi, Mari ^a   Nikawa, Hiroki ^b   Furue, Miho K ^a  

^a NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

^b HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EARLY GROWTH RESPONSE FACTOR 1; PROTEIN KINASE C; TRANSCRIPTION FACTOR SNAIL; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN BINDING; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CULTURE MEDIUM; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; GENE INDUCTION; HUMAN; HUMAN CELL; PLURIPOTENT STEM CELL; PROMOTER REGION; PROTEIN BINDING; UPREGULATION; CELL LINE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM;

CELL LINE; EARLY GROWTH RESPONSE PROTEIN 1; EMBRYONIC STEM CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HUMANS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN KINASE C; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION FACTORS;

EID: 84906991255     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2013.0424     Document Type: Article

References (57)

1. Dreesen O and AH Brivanlou. (2007). Signaling pathways in cancer and embryonic stem cells. Stem Cell Rev 3:7-17.
2. Na J, MK Furue and PW Andrews. (2010). Inhibition of ERK1/2 prevents neural and mesendodermal differentiation and promotes human embryonic stem cell self-renewal. Stem Cell Res 5:157-169.
3. Armstrong L, O Hughes, S Yung, L Hyslop, R Stewart, I Wappler, H Peters, T Walter, P Stojkovic, et al. (2006). The role of PI3K/AKT, MAPK/ERK and NFκβ signalling in the maintenance of human embryonic stem cell pluripotency and viability highlighted by transcriptional profiling and functional analysis. Hum Mol Genet 15:1894-1913.
4. Kinehara M, S Kawamura, D Tateyama, M Suga, H Matsumura, S Mimura, N Hirayama, M Hirata, K Uchio-Yamada, et al. (2013). Protein kinase C regulates human pluripotent stem cell self-renewal. PLoS One 8:e54122.
5. Feng X, J Zhang, K Smuga-Otto, S Tian, J Yu, R Stewart and JA Thomson. (2012). Protein kinase C mediated extraembryonic endoderm differentiation of human embryonic stem cells. Stem Cells 30:461-470.
6. Sato N, L Meijer, L Skaltsounis, P Greengard and AH Brivanlou. (2004). Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat Med 10:55-63.
7. Dravid G, Z Ye, H Hammond, G Chen, A Pyle, P Donovan, X Yu and L Cheng. (2005). Defining the role of Wnt/βcatenin signaling in the survival, proliferation, and selfrenewal of human embryonic stem cells. Stem Cells 23: 1489-1501.
8. Bernardo AS, T Faial, L Gardner, KK Niakan, D Ortmann, CE Senner, EM Callery, MW Trotter, M Hemberger, et al. (2011). BRACHYURY and CDX2 mediate BMP-induced differentiation of human and mouse pluripotent stem cells into embryonic and extraembryonic lineages. Cell Stem Cell 9:144-155.
9. Vallier L, D Reynolds and RA Pedersen. (2004). Nodal inhibits differentiation of human embryonic stem cells along the neuroectodermal default pathway. Dev Biol 275: 403-421.
10. Vallier L, M Alexander and RA Pedersen. (2005). Activin/nodal and FGF pathways cooperate to maintain pluripotency of human embryonic stem cells. J Cell Sci 118: 4495-4509.
11. James D, AJ Levine, D Besser and A Hemmati-Brivanlou. (2005). TGFβ/activin/nodal signaling is necessary for the maintenance of pluripotency in human embryonic stem cells. Development 132:1273-1282.
12. Pebay A, RC Wong, SM Pitson, EJ Wolvetang, GS Peh, A Filipczyk, KL Koh, I Tellis, LT Nguyen and MF Pera. (2005). Essential roles of sphingosine-1-phosphate and platelet-derived growth factor in the maintenance of human embryonic stem cells. Stem Cells 23:1541-1548.
13. Bendall SC, MH Stewart, P Menendez, D George, K Vijayaragavan, T Werbowetski-Ogilvie, V Ramos-Mejia, A Rouleau, J Yang, et al. (2007). IGF and FGF cooperatively establish the regulatory stem cell niche of pluripotent human cells in vitro. Nature 448:1015-1021.
14. Dvorak P, D Dvorakova, S Koskova, M Vodinska, M Najvirtova, D Krekac and A Hampl. (2005). Expression and potential role of fibroblast growth factor 2 and its receptors in human embryonic stem cells. Stem Cells 23:1200-1211.
15. Avery S, K Inniss and H Moore. (2006). The regulation of self-renewal in human embryonic stem cells. Stem Cells Dev 15:729-740.
16. Ding VM, PJ Boersema, LY Foong, C Preisinger, G Koh, S Natarajan, DY Lee, J Boekhorst, B Snel, et al. (2011). Tyrosine phosphorylation profiling in FGF-2 stimulated human embryonic stem cells. PLoS One 6:e17538.
17. Furue MK, J Na, JP Jackson, T Okamoto, M Jones, D Baker, R Hata, HD Moore, JD Sato and PW Andrews. (2008). Heparin promotes the growth of human embryonic stem cells in a defined serum-free medium. Proc Natl Acad Sci U S A 105:13409-13414.
18. Hoffman LM and MK Carpenter. (2005). Characterization and culture of human embryonic stem cells. Nat Biotechnol 23:699-708.
19. Amit M, MK Carpenter, MS Inokuma, CP Chiu, CP Harris, MA Waknitz, J Itskovitz-Eldor and JA Thomson. (2000). Clonally derived human embryonic stem cell lines maintain pluripotency and proliferative potential for prolonged periods of culture. Dev Biol 227:271-278.
20. Xu RH, RM Peck, DS Li, X Feng, T Ludwig and JA Thomson. (2005). Basic FGF and suppression of BMP signaling sustain undifferentiated proliferation of human ES cells. Nat Methods 2:185-190.
21. Eiselleova L, K Matulka, V Kriz, M Kunova, Z Schmidtova, J Neradil, B Tichy, D Dvorakova, S Pospisilova, A Hampl and P Dvorak. (2009). A complex role for FGF-2 in self-renewal, survival, and adhesion of human embryonic stem cells. Stem Cells 27:1847-1857.
22. Singh AM, D Reynolds, T Cliff, S Ohtsuka, AL Mattheyses, Y Sun, L Menendez, M Kulik and S Dalton. (2012). Signaling network crosstalk in human pluripotent cells: a Smad2/3-regulated switch that controls the balance between self-renewal and differentiation. Cell Stem Cell 10:312-326.
23. Downward J. (2004). PI 3-kinase, Akt and cell survival. Semin Cell Dev Biol 15:177-182.
24. Ohgushi M, M Matsumura, M Eiraku, K Murakami, T Aramaki, A Nishiyama, K Muguruma, T Nakano, H Suga, et al. (2010). Molecular pathway and cell state responsible for dissociation-induced apoptosis in human pluripotent stem cells. Cell Stem Cell 7:225-239.
25. Xu RH, X Chen, DS Li, R Li, GC Addicks, C Glennon, TP Zwaka and JA Thomson. (2002). BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat Biotechnol 20:1261-1264.
26. Pera MF, J Andrade, S Houssami, B Reubinoff, A Trounson, EG Stanley, D Ward-van Oostwaard and C Mummery. (2004). Regulation of human embryonic stem cell differentiation by BMP-2 and its antagonist noggin. J Cell Sci 117:1269-1280.
27. Li J, G Wang, C Wang, Y Zhao, H Zhang, Z Tan, Z Song, M Ding and H Deng. (2007). MEK/ERK signaling contributes to the maintenance of human embryonic stem cell self-renewal. Differentiation 75:299-307.
28. Schlessinger J. (2004). Common and distinct elements in cellular signaling via EGF and FGF receptors. Science 306:1506-1507.
29. Ding VM, L Ling, S Natarajan, MG Yap, SM Cool and AB Choo. (2010). FGF-2 modulates Wnt signaling in undifferentiated hESC and iPS cells through activated PI3-K/GSK3β signaling. J Cell Physiol 225:417-428.
30. Blauwkamp TA, S Nigam, R Ardehali, IL Weissman and R Nusse. (2012). Endogenous Wnt signalling in human embryonic stem cells generates an equilibrium of distinct lineage-specified progenitors. Nat Commun 3:1070.
31. Thiery JP, H Acloque, RY Huang and MA Nieto. (2009). Epithelial-mesenchymal transitions in development and disease. Cell 139:871-890.
32. Bolos V, H Peinado, MA Perez-Moreno, MF Fraga, M Esteller and A Cano. (2003). The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci 116:499-511.
33. Kang Y and J Massague. (2004). Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118:277-279.
34. Comijn J, G Berx, P Vermassen, K Verschueren, L van Grunsven, E Bruyneel, M Mareel, D Huylebroeck and F van Roy. (2001). The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 7:1267-1278.
35. Perez-Moreno MA, A Locascio, I Rodrigo, G Dhondt, F Portillo, MA Nieto and A Cano. (2001). A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J Biol Chem 276: 27424-27431.
36. Grooteclaes ML and SM Frisch. (2000). Evidence for a function of CtBP in epithelial gene regulation and anoikis. Oncogene 19:3823-3828.
37. Mani SA, J Yang, M Brooks, G Schwaninger, A Zhou, N Miura, JL Kutok, K Hartwell, AL Richardson and RA Weinberg. (2007). Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc Natl Acad Sci U S A 104:10069-10074.
38. Ullmann U, C Gilles, M De Rycke, H Van de Velde, K Sermon and I Liebaers. (2008). GSK-3-specific inhibitorsupplemented hESC medium prevents the epithelial-mesenchymal transition process and the up-regulation of matrix metalloproteinases in hESCs cultured in feeder-free conditions. Mol Hum Reprod 14:169-179.
39. Ullmann U, P In't Veld, C Gilles, K Sermon, M De Rycke, H Van de Velde, A Van Steirteghem and I Liebaers. (2007). Epithelial-mesenchymal transition process in human embryonic stem cells cultured in feeder-free conditions. Mol Hum Reprod 13:21-32.
40. Van Hoof D, SR Braam, W Dormeyer, D Ward-van Oostwaard, AJ Heck, J Krijgsveld and CL Mummery. (2008). Feeder-free monolayer cultures of human embryonic stem cells express an epithelial plasma membrane protein profile. Stem Cells 26:2777-2781.
41. Eastham AM, H Spencer, F Soncin, S Ritson, CL Merry, PL Stern and CM Ward. (2007). Epithelial-mesenchymal transition events during human embryonic stem cell differentiation. Cancer Res 67:11254-11262.
42. Thomson JA, J Itskovitz-Eldor, SS Shapiro, MA Waknitz, JJ Swiergiel, VS Marshall and JM Jones. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147.
43. Furue M, T Okamoto, Y Hayashi, H Okochi, M Fujimoto, Y Myoishi, T Abe, K Ohnuma, GH Sato, M Asashima and JD Sato. (2005). Leukemia inhibitory factor as an antiapoptotic mitogen for pluripotent mouse embryonic stem cells in a serum-free medium without feeder cells. In Vitro Cell Dev Biol Anim 41:19-28.
44. Kim JH, SR Lee, LH Li, HJ Park, JH Park, KY Lee, MK Kim, BA Shin and SY Choi. (2011). High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS One 6:e18556.
45. Grotegut S, D von Schweinitz, G Christofori and F Lehembre. (2006). Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J 25:3534-3545.
46. Kuo PL, YH Chen, TC Chen, KH Shen and YL Hsu. (2011). CXCL5/ENA78 increased cell migration and epithelial-to-mesenchymal transition of hormone-independent prostate cancer by early growth response-1/snail signaling pathway. J Cell Physiol 226:1224-1231.
47. Kubosaki A, Y Tomaru, M Tagami, E Arner, H Miura, T Suzuki, M Suzuki, H Suzuki and Y Hayashizaki. (2009). Genome-wide investigation of in vivo EGR-1 binding sites in monocytic differentiation. Genome Biol 10:R41.
48. Zhou BP, J Deng, W Xia, J Xu, YM Li, M Gunduz and MC Hung. (2004). Dual regulation of Snail by GSK-3β-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6:931-940.
49. Bechard M and S Dalton. (2009). Subcellular localization of glycogen synthase kinase 3β controls embryonic stem cell self-renewal. Mol Cell Biol 29:2092-2104.
50. Bechard M, R Trost, AM Singh and S Dalton. (2012). Frat is a phosphatidylinositol 3-kinase/Akt-regulated determinant of glycogen synthase kinase 3β subcellular localization in pluripotent cells. Mol Cell Biol 32:288-296.
51. Singh AM, M Bechard, K Smith and S Dalton. (2012). Reconciling the different roles of Gsk3β in "naive" and "primed" pluripotent stem cells. Cell Cycle 11:2991-2996.
52. Davidson KC, AM Adams, JM Goodson, CE McDonald, JC Potter, JD Berndt, TL Biechele, RJ Taylor and RT Moon. (2012). Wnt/β-catenin signaling promotes differentiation, not self-renewal, of human embryonic stem cells and is repressed by Oct4. Proc Natl Acad Sci U S A 109: 4485-4490.
53. Sumi T, N Tsuneyoshi, N Nakatsuji and H Suemori. (2008). Defining early lineage specification of human embryonic stem cells by the orchestrated balance of canonical Wnt/βcatenin, Activin/Nodal and BMP signaling. Development 135:2969-2979.
54. Cai L, Z Ye, BY Zhou, P Mali, C Zhou and L Cheng. (2007). Promoting human embryonic stem cell renewal or differentiation by modulating Wnt signal and culture conditions. Cell Res 17:62-72.
55. Villa-Diaz LG, C Pacut, NA Slawny, J Ding, KS O'Shea and GD Smith. (2009). Analysis of the factors that limit the ability of feeder cells to maintain the undifferentiated state of human embryonic stem cells. Stem Cells Dev 18: 641-651.
56. Kaidanovich-Beilin O and JR Woodgett. (2011). GSK-3: functional insights from cell biology and animal models. Front Mol Neurosci 4:40.
57. Cohen P and S Frame. (2001). The renaissance of GSK3. Nat Rev Mol Cell Biol 2:769-776.