Snail regulated by PKC/GSK-3β pathway is crucial for EGF-induced epithelial-mesenchymal transition (EMT) of cancer cells

Cell and Tissue Research

Volumn 358, Issue 2, 2014, Pages 491-502

  Liu, Zong cai ^a   Chen, Xiao hui ^a   Song, Hai xing ^b   Wang, Hong sheng ^a   Zhang, Ge ^a   Wang, Hao ^a   Chen, Dan yang ^a   Fang, Rui ^a   Liu, Hao ^a   Cai, Shao hui ^c   Du, Jun ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b CHENGDU MEDICAL COLLEGE   (China)

^c JINAN UNIVERSITY   (China)

Author keywords

Cancer cells; Epidermal growth factor (EGF); Epithelial mesenchymal transition (EMT); Snail

Indexed keywords

EPIDERMAL GROWTH FACTOR; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; PROTEIN KINASE C; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

CELL MOTION; CELL NUCLEUS; DRUG EFFECTS; ENZYMOLOGY; EPITHELIAL MESENCHYMAL TRANSITION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; NEOPLASM; PATHOLOGY; PROTEIN STABILITY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR CELL LINE; TUMOR INVASION; UPREGULATION;

CELL LINE, TUMOR; CELL MOVEMENT; CELL NUCLEUS; EPIDERMAL GROWTH FACTOR; EPITHELIAL-MESENCHYMAL TRANSITION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; NEOPLASM INVASIVENESS; NEOPLASMS; PROTEIN KINASE C; PROTEIN STABILITY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; UP-REGULATION;

EID: 84932102495     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-014-1953-2     Document Type: Article

References (51)

1. Ackland ML, Newgreen DF, Fridman M, Waltham MC, Arvanitis A, Minichiello J, Price JT, Thompson EW (2003) Epidermal growth factor-induced epithelio-mesenchymal transition in human breast carcinoma cells. Lab Invest 83:435–448
2. Argast G, Krueger J, Thomson S, Sujka-Kwok I, Carey K, Silva S, O’Connor M, Mercado P, Mulford I, Young GD, Sennello R, Wild R, Pachter J, Kan JC, Haley J, Rosenfeld-Franklin M, Epstein D (2011) Inducible expression of TGFβ, snail and Zeb1 recapitulates EMT in vitro and in vivo in a NSCLC model. Clin Exp Metastasis 28:593–614
3. Bachelder RE, Yoon S-O, Franci C, de Herreros AG, Mercurio AM (2005) Glycogen synthase kinase-3 is an endogenous inhibitor of snail transcription: implications for the epithelial–mesenchymal transition. J Cell Biol 168:29–33
4. Barbera MJ, Puig I, Dominguez D, Julien-Grille S, Guaita-Esteruelas S, Peiro S, Baulida J, Franci C, Dedhar S, Larue L, Garcia de Herreros A (2004) Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells. Oncogene 23:7345–7354
5. Chen KC, Chen CY, Lin CJ, Yang TY, Chen TH, Wu LC, Wu CC (2013) Luteolin attenuates TGF-β1-induced epithelial–mesenchymal transition of lung cancer cells by interfering in the PI3K/Akt–NF-κB–snail pathway. Life Sci 93:924–933
6. Christofori G (2006) New signals from the invasive front. Nature 441:444–450
7. Connor P, Talavera F, Kang J-S, Burke J, Roberts J, Menon KMJ (1997) Epidermal growth factor activates protein kinase C in the human endometrial cancer cell line HEC-1-a. Gynecol Oncol 67:46–50
8. Cross DAE, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785–789
9. De Craene B, van Roy F, Berx G (2005) Unraveling signalling cascades for the Snail family of transcription factors. Cell Signal 17:535–547
10. Doble BW, Woodgett JR (2003) GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 116:1175–1186
11. Dong C, Wu Y, Yao J, Wang Y, Yu Y, Rychahou PG, Evers BM, Zhou BP (2012) G9a interacts with snail and is critical for snail-mediated E-cadherin repression in human breast cancer. J Clin Invest 122:1469–1486
12. Fang R, Zhang G, Guo Q, Ning F, Wang H, Cai S, Du J (2013) Nodal promotes aggressive phenotype via snail-mediated epithelial–mesenchymal transition in murine melanoma. Cancer Lett 333:66–75
13. Fang X, Yu SX, Lu Y, Bast RC, Woodgett JR, Mills GB (2000) Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc Natl Acad Sci 97:11960–11965
14. Goode N, Hughes K, Woodgett JR, Parker PJ (1992) Differential regulation of glycogen synthase kinase-3 beta by protein kinase C isotypes. J Biol Chem 267:16878–16882
15. Goswami S, Sahai E, Wyckoff JB, Cammer M, Cox D, Pixley FJ, Stanley ER, Segall JE, Condeelis JS (2005) Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop. Cancer Res 65:5278–5283. doi:10.1158/0008-5472.can-04-1853
16. Gould CM, Newton AC (2008) The life and death of protein kinase C. Curr Drug Targets 9:614–625
17. Ha GH, Kim JL, Breuer EK (2013) TACC3 is essential for EGF-mediated EMT in cervical cancer. PLoS One 8:e70353
18. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144:646–674
19. Hung JJ, Yang MH, Hsu HS, Hsu WH, Liu JS, Wu KJ (2009) Prognostic significance of hypoxia-inducible factor-1α, TWIST1 and Snail expression in resectable non-small cell lung cancer. Thorax 64:1082–1089
20. 2+/PKC and MAPKs. J Cell Biochem 99:1677–1687
21. Lee MY, Chou CY, Tang MJ, Shen MR (2008) Epithelial-mesenchymal transition in cervical cancer: correlation with tumor progression, epidermal growth factor receptor overexpression, and snail up-regulation. Clin Cancer Res 14:4743–4750
22. Lo H-W, Hsu S-C, Xia W, Cao X, Shih J-Y, Wei Y, Abbruzzese JL, Hortobagyi GN, Hung M-C (2007) Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Cancer Res 67:9066–9076
23. Logullo AF, Nonogaki S, Pasini FS, Osório CA, Soares FA, Brentani MM (2010) Concomitant expression of epithelial-mesenchymal transition biomarkers in breast ductal carcinoma: association with progression. Oncol Rep 23:313–320
24. Lu X, Kang Y (2009) Epidermal growth factor signalling and bone metastasis. Br J Cancer 102:457–461
25. Mak P, Leav I, Pursell B, Bae D, Yang X, Taglienti CA, Gouvin LM, Sharma VM, Mercurio AM (2010) ERβ impedes prostate cancer EMT by destabilizing HIF-1α and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell 17:319–332
26. Mendelsohn J, Baselga J (2000) The EGF receptor family as targets for cancer therapy. Oncogene 19:6550–6556
27. Nieto MA (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3:155–166
28. Olmeda D, Jorda M, Peinado H, Fabra A, Cano A (2006) Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene 26:1862–1874
29. Peinado H, Olmeda D, Cano A (2007) Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 7:415–428
30. Pon YL, Zhou HY, Cheung ANY, Ngan HYS, Wong AST (2008) p70 S6 kinase promotes epithelial to mesenchymal transition through snail induction in ovarian cancer cells. Cancer Res 68:6524–6532
31. Saito Y, Vandenheede JR, Cohen P (1994) The mechanism by which epidermal growth factor inhibits glycogen synthase kinase 3 in A431 cells. Biochem J 303:27–31
32. Salomon DS, Brandt R, Ciardiello F, Normanno N (1995) Epidermal growth factor-related peptides and their receptors in human malignancies. Crit Rev Oncol Hematol 19:183–232
33. Schreiber E, Harshman K, Kemler I, Malipiero U, Schaffner W, Fontana A (1990) 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 18:5495–5503
34. Shinojima N, Tada K, Shiraishi S, Kamiryo T, Kochi M, Nakamura H, Makino K, Saya H, Hirano H, Kuratsu J, Oka K, Ishimaru Y, Ushio Y (2003) Prognostic value of epidermal growth factor receptor in patients with glioblastoma multiforme. Cancer Res 63:6962–6970
35. Smith BN, Odero-Marah VA (2012) The role of snail in prostate cancer. Cell Adhes Migr 6:433–441
36. Stewart JR, O’Brian CA (2005) Protein kinase C-α mediates epidermal growth factor receptor transactivation in human prostate cancer cells. Mol Cancer Ther 4:726–732
37. Tomaskovic-Crook E, Thompson E, Thiery J (2009) Epithelial to mesenchymal transition and breast cancer. Breast Cancer Res 11:213
38. Tortora G, Damiano V, Bianco C, Baldassarre G, Bianco AR, Lanfrancone L, Pelicci PG, Ciardiello F (1997) The RIalpha subunit of protein kinase A (PKA) binds to Grb2 and allows PKA interaction with the activated EGF-receptor. Oncogene 14:923–928
39. Vergara D, Valente CM, Tinelli A, Siciliano C, Lorusso V, Acierno R, Giovinazzo G, Santino A, Storelli C, Maffia M (2011) Resveratrol inhibits the epidermal growth factor-induced epithelial mesenchymal transition in MCF-7 cells. Cancer Lett 310:1–8
40. Wang H, Wang H-S, Zhou B-H, Li C-L, Zhang F, Wang X-F, Zhang G, Bu X-Z, Cai S-H, Du J (2013) Epithelial–mesenchymal transition (EMT) induced by TNF-α requires AKT/GSK-3β-mediated stabilization of snail in colorectal cancer. PLoS One 8:e56664
41. Wang Y, Lin Z, Sun L, Fan S, Huang Z, Zhang D, Yang Z, Li J, Chen W (2013a) Akt/Ezrin Tyr353/NF-κB pathway regulates EGF-induced EMT and metastasis in tongue squamous cell carcinoma. Br J Cancer 110:695–705
42. Wang Y, Shi J, Chai K, Ying X, Zhou BP (2013b) The role of snail in EMT and tumorigenesis. Curr Cancer Drug Targets 13:963–972
43. Wen YC, Chen WY, Lee WJ, Yang SF, Lee LM, Chien MH (2014) Snail as a potential marker for predicting the recurrence of prostate cancer in patients at stage T2 after radical prostatectomy. Clin Chim Acta 431:169–173
44. Wu Y, Zhou BP (2010) Snail: more than EMT. Cell Adhes Migr 4:199–203
45. Wu Y, Deng J, Rychahou PG, Qiu S, Evers BM, Zhou BP (2009) Stabilization of snail by NF-kB is required for inflammation-induced cell migration and invasion. Cancer Cell 15:416–428
46. Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, Segall JE, Pollard JW, Condeelis J (2007) Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res 67:2649–2656
47. Xue C, Plieth D, Venkov C, Xu C, Neilson EG (2003) The gatekeeper effect of epithelial-mesenchymal transition regulates the frequency of breast cancer metastasis. Cancer Res 63:3386–3394
48. Yarden Y (2001) The EGFR family and its ligands in human cancer: signalling mechanisms and therapeutic opportunities. Eur J Cancer 37 Suppl 4:S3–S8
49. Zeisberg M, Neilson EG (2009) Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 119:1429–1437
50. Zhou BP, Deng J, Xia W, Xu J, Li YM, Gunduz M, Hung M-C (2004) Dual regulation of snail by GSK-3 [beta]-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6:931–940
51. Zuo JH, Zhu W, Li MY, Li XH, Yi H, Zeng GQ, Wan XX, He QY, Li JH, Qu JQ, Chen Y, Xiao ZQ (2011) Activation of EGFR promotes squamous carcinoma SCC10A cell migration and invasion via inducing EMT-like phenotype change and MMP-9-mediated degradation of E-cadherin. J Cell Biochem 112:2508–2517