AKT/GSK-3β regulates stability and transcription of snail which is crucial for bFGF-induced epithelial-mesenchymal transition of prostate cancer cells

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 10, 2014, Pages 3096-3105

  Liu, Zong Cai ^a   Wang, Hong Sheng ^a   Zhang, Ge ^a   Liu, Hao ^b   Chen, Xiao Hui ^a   Zhang, Fan ^a   Chen, Dan Yang ^a   Cai, Shao Hui ^c   Du, Jun ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b GUANGZHOU MEDICAL UNIVERSITY   (China)

^c JINAN UNIVERSITY   (China)

Author keywords

Basic fibroblast growth factor; Epithelial mesenchymal transition; Invasion; Prostate cancer; Snail

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN KINASE B; TRANSCRIPTION FACTOR SNAIL;

ARTICLE; BIOASSAY; CELL INVASION ASSAY; CELL MIGRATION ASSAY; CELL MOTILITY; CONTROLLED STUDY; ENZYME REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; MALE; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROSTATE CANCER CELL LINE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STABILITY; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SNAIL GENE; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; WOUND HEALING; WOUND HEALING SCRATCH ASSAY;

BASIC FIBROBLAST GROWTH FACTOR; EPITHELIAL-MESENCHYMAL TRANSITION; INVASION; PROSTATE CANCER; SNAIL;

CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; FIBROBLAST GROWTH FACTOR 2; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MALE; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84907863195     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.07.018     Document Type: Article

References (50)

1. V.D. Acevedo, R.D. Gangula, K.W. Freeman, R. Li, Y. Zhang, F. Wang, G.E. Ayala, L.E. Peterson, M. Ittmann, and D.M. Spencer Inducible FGFR-1 activation leads to irreversible prostate adenocarcinoma and an epithelial-to-mesenchymal transition Cancer Cell 12 2007 559 571
2. A. Albini, and R. Benelli The chemoinvasion assay: a method to assess tumor and endothelial cell invasion and its modulation Nat. Protoc. 2 2007 504 511
3. G. Argast, J. Krueger, S. Thomson, I. Sujka-Kwok, K. Carey, S. Silva, M. O'Connor, P. Mercado, I. Mulford, G.D. Young, R. Sennello, R. Wild, J. Pachter, J.C. Kan, J. Haley, M. Rosenfeld-Franklin, and D. Epstein Inducible expression of TGFβ, Snail and Zeb1 recapitulates EMT in vitro and in vivo in a NSCLC model Clin. Exp. Metastasis 28 2011 593 614
4. R.E. Bachelder, S.-O. Yoon, C. Franci, A.G. de Herreros, and A.M. Mercurio Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition J. Cell Biol. 168 2005 29 33
5. M.J. Barbera, I. Puig, D. Dominguez, S. Julien-Grille, S. Guaita-Esteruelas, S. Peiro, J. Baulida, C. Franci, S. Dedhar, L. Larue, and A. Garcia de Herreros Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells Oncogene 23 2004 7345 7354
6. M. Brandl, B. Seidler, F. Haller, J. Adamski, R.M. Schmid, D. Saur, and G. Schneider IKKα controls canonical TGFβ-SMAD signaling to regulate genes expressing SNAIL and SLUG during EMT in Panc1 cells J. Cell Sci. 123 2010 4231 4239
7. K.-C. Chen, C.-Y. Chen, C.-J. Lin, T.-Y. Yang, T.-H. Chen, L.-C. Wu, and C.-C. Wu Luteolin attenuates TGF-β1-induced epithelial-mesenchymal transition of lung cancer cells by interfering in the PI3K/Akt-NF-κB-Snail pathway Life Sci. 93 2013 924 933
8. J. Chen, G. Chen, Z. Yan, Y. Guo, M. Yu, L. Feng, Z. Jiang, W. Guo, and W. Tian TGF-β1 and FGF2 stimulate the epithelial-mesenchymal transition of HERS cells through a MEK-dependent mechanism J. Cell. Physiol. 229 2014 1647 1659
9. C. Dong, Y. Wu, J. Yao, Y. Wang, Y. Yu, P.G. Rychahou, B.M. Evers, and B.P. Zhou G9a interacts with Snail and is critical for Snail-mediated E-cadherin repression in human breast cancer J. Clin. Invest. 122 2012 1469 1486
10. J.-C. Cheng, C. Klausen, and P.C.K. Leung Hydrogen peroxide mediates EGF-induced down-regulation of E-cadherin expression via p38 MAPK and Snail in human ovarian cancer cells Mol. Endocrinol. 24 2010 1569 1580
11. G. Christofori New signals from the invasive front Nature 441 2006 444 450
12. M.-C. Delfini, M. De La Celle, J. Gros, O. Serralbo, I. Marics, M. Seux, M. Scaal, and C. Marcelle The timing of emergence of muscle progenitors is controlled by an FGF/ERK/SNAIL1 pathway Dev. Biol. 333 2009 229 237
13. R. Fang, G. Zhang, Q. Guo, F. Ning, H. Wang, S. Cai, and J. Du Nodal promotes aggressive phenotype via Snail-mediated epithelial-mesenchymal transition in murine melanoma Cancer Lett. 333 2013 66 75
14. V. Flati, L.I. Pastore, A.W. Griffioen, S. Satijn, E. Toniato, I. D'Alimonte, E. Laglia, P. Marchetti, A. Gulino, and S. Martinotti Endothelial cell anergy is mediated by bFGF through the sustained activation of p38-MAPK and NF-kappaB inhibition Int. J. Immunopathol. Pharmacol. 19 2006 761 773
15. D. Giri, F. Ropiquet, and M. Ittmann Alterations in expression of basic fibroblast growth factor (FGF) 2 and its receptor FGFR-1 in human prostate cancer Clin. Cancer Res. 5 1999 1063 1071
16. D. Gospodarowicz Purification of a fibroblast growth factor from bovine pituitary J. Biol. Chem. 2515 1975
17. D. Hanahan, and Robert A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
18. G.-M. Jiang, H.-S. Wang, F. Zhang, K.-S. Zhang, Z.-C. Liu, R. Fang, H. Wang, S.-H. Cai, and J. Du Histone deacetylase inhibitor induction of epithelial-mesenchymal transitions via up-regulation of Snail facilitates cancer progression Biochim. Biophys. Acta (BBA) - Mol. Cell Res. 1833 2013 663 671
19. K.M. Hardy, T.A. Yatskievych, J.H. Konieczka, A.S. Bobbs, P.B. Masuko, and K. Masaru FGF signalling through RAS/MAPK and PI3K pathways regulates cell movement and gene expression in the chicken primitive streak without affecting E-cadherin expression BMC Dev. Biol. 11 2011
20. M. Katoh, and M. Katoh Cross-talk of WNT and FGF signaling pathways at GSK3ß to regulate ß-catenin and SNAIL signaling cascades Cancer Biol. Ther. 5 2006 1059 1064
21. L.A. Kingsley, P.G.J. Fournier, J.M. Chirgwin, and T.A. Guise Molecular biology of bone metastasis Mol. Cancer Ther. 6 2007 2609 2617
22. B. Kwabi-Addo, M. Ozen, and M. Ittmann The role of fibroblast growth factors and their receptors in prostate cancer Endocr. Relat. Cancer 11 2004 709 724
23. P. Mak, I. Leav, B. Pursell, D. Bae, X. Yang, C.A. Taglienti, L.M. Gouvin, V.M. Sharma, and A.M. Mercurio ERβ impedes prostate cancer EMT by destabilizing HIF-1α and inhibiting VEGF-mediated snail nuclear localization: implications for gleason grading Cancer Cell 17 2010 319 332
24. V. Masola, G. Gambaro, E. Tibaldi, A.M. Brunati, A. Gastaldello, A. D'Angelo, M. Onisto, and A. Lupo Heparanase and syndecan-1 interplay orchestrates fibroblast growth factor-2-induced epithelial-mesenchymal transition in renal tubular cells J. Biol. Chem. 287 2012 1478 1488
25. E. Matuszak, and N. Kyprianou Androgen regulation of epithelial- mesenchymal transition in prostate tumorigenesis Expert. Rev. Endocrinol. Metab. 6 2011
26. M.E. Kaighn, K.S. Naarayan, Y. Ohnuki, J.F. Lechner, and L.W. Jones Establishment and characterization of a human prostatic carcinoma cell line (PC-3) Invest. Urol. 17 1979 16 23
27. L.A. Megeney, R.L.S. Perry, J.E. Lecouter, and M.A. Rudnicki bFGF and LIF signaling activates STAT3 in proliferating myoblasts Dev. Genet. 19 1996 139 145
28. Z. Michael, and G.N. Eric Biomarkers for epithelial-mesenchymal transitions J. Clin. Invest. 119 2009 1429 1437
29. J.T. Nauseef, and M.D. Henry Epithelial-to-mesenchymal transition in prostate cancer: paradigm or puzzle? Nat. Rev. Urol. 8 2011 428 439
30. M.A. Nieto The snail superfamily of zinc-finger transcription factors Nat. Rev. Mol. Cell Biol. 3 2002 155 166
31. S. Nomura, H. Yoshitomi, S. Takano, T. Shida, S. Kobayashi, M. Ohtsuka, F. Kimura, H. Shimizu, H. Yoshidome, A. Kato, and M. Miyazaki FGF10/FGFR2 signal induces cell migration and invasion in pancreatic cancer Br. J. Cancer 99 2008 305 313
32. M. Okada-Ban, J.P. Thiery, and J. Jouanneau Fibroblast growth factor-2 Int. J. Biochem. Cell Biol. 32 2000 263 267
33. D. Olmeda, M. Jorda, H. Peinado, A. Fabra, and A. Cano Snail silencing effectively suppresses tumour growth and invasiveness Oncogene 26 2006 1862 1874
34. M. Papetti, J. Shujath, K.N. Riley, and I.M. Herman FGF-2 antagonizes the TGF-β1-mediated induction of pericyte α-smooth muscle actin expression: a role for Myf-5 and Smad-mediated signaling pathways Invest. Ophthalmol. Vis. Sci. 44 2003 4994 5005
35. H. Peinado, D. Olmeda, and A. Cano Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat. Rev. Cancer 7 2007 415 428
36. Y.L. Pon, H.Y. Zhou, A.N.Y. Cheung, H.Y.S. Ngan, and A.S.T. Wong p70 S6 kinase promotes epithelial to mesenchymal transition through snail induction in ovarian cancer cells Cancer Res. 68 2008 6524 6532
37. K. Sakuma, M. Aoki, and R. Kannagi Transcription factors c-Myc and CDX2 mediate E-selectin ligand expression in colon cancer cells undergoing EGF/bFGF-induced epithelial-mesenchymal transition Proc. Natl. Acad. Sci. 109 2012 7776 7781
38. E. Schreiber, K. Harshman, I. Kemler, U. Malipiero, W. Schaffner, and A. Fontana Astrocytes and glioblastoma cells express novel octamer-DNA binding proteins distinct from the ubiquitous Oct-1 and B cell type Oct-2 proteins Nucleic Acids Res. 18 1990 5495 5503
39. R. Siegel, C. DeSantis, K. Virgo, K. Stein, A. Mariotto, T. Smith, D. Cooper, T. Gansler, C. Lerro, S. Fedewa, C. Lin, C. Leach, R.S. Cannady, H. Cho, S. Scoppa, M. Hachey, R. Kirch, A. Jemal, and E. Ward Cancer treatment and survivorship statistics, 2012 CA Cancer J. Clin. 62 2012 220 241
40. F. Strutz, M. Zeisberg, F.N. Ziyadeh, C.-Q. Yang, R. Kalluri, G.A. Muller, and E.G. Neilson Role of basic fibroblast growth factor-2 in epithelial-mesenchymal transformation Kidney Int. 61 2002 1714 1728
41. R.S. Taichman, R.D. Loberg, R. Mehra, and K.J. Pienta The evolving biology and treatment of prostate cancer J. Clin. Invest. 117 2007 2351 2361
42. E. Tomaskovic-Crook, E. Thompson, and J. Thiery Epithelial to mesenchymal transition and breast cancer Breast Cancer Res. 11 2009 213
43. N. Turner, and R. Grose Fibroblast growth factor signalling: from development to cancer Nat. Rev. Cancer 10 2010 116 129
44. H. Wang, R. Fang, X.-F. Wang, F. Zhang, D.-Y. Chen, B. Zhou, H.-S. Wang, S.-H. Cai, and J. Du Stabilization of Snail through AKT/GSK-3β signaling pathway is required for TNF-α-induced epithelial-mesenchymal transition in prostate cancer PC3 cells Eur. J. Pharmacol. 714 2013 48 55
45. H. Wang, H.-S. Wang, B.-H. Zhou, C.-L. Li, F. Zhang, X.-F. Wang, G. Zhang, X.-Z. Bu, S.-H. Cai, and J. Du Epithelial-mesenchymal transition (EMT) induced by TNF-α requires AKT/GSK-3β-mediated stabilization of snail in colorectal cancer PLoS ONE 8 2013 e56664
46. Y. Wu, J. Deng, P.G. Rychahou, S. Qiu, B.M. Evers, and B.P. Zhou Stabilization of Snail by NF-kB is required for inflammation-induced cell migration and invasion Cancer Cell 15 2009 416 428
47. A. Yadav, B. Kumar, J. Datta, T.N. Teknos, and P. Kumar IL-6 promotes head and neck tumor metastasis by inducing epithelial-mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway Mol. Cancer Res. 9 2011 1658 1667
48. W. Yifan, S. Jian, C. Kequn, Y. Xuhua, and P.Z. Binhua The role of Snail in EMT and tumorigenesis Curr. Cancer Drug Targets 13 2013 963 972
49. X. Zhang, O.A. Ibrahimi, S.K. Olsen, H. Umemori, M. Mohammadi, and D.M. Ornitz Receptor specificity of the fibroblast growth factor family: the complete mammalian FGF family J. Biol. Chem. 281 2006 15694 15700
50. B.P. Zhou, J. Deng, W. Xia, J. Xu, Y.M. Li, M. Gunduz, and M.-C. Hung Dual regulation of Snail by GSK-3[beta]-mediated phosphorylation in control of epithelial-mesenchymal transition Nat. Cell Biol. 6 2004 931 940