Epithelial-Mesenchymal Transition (EMT) Induced by TNF-α Requires AKT/GSK-3β-Mediated Stabilization of Snail in Colorectal Cancer

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Wang, Hao ^a   Wang, Hong Sheng ^a   Zhou, Bin Hua ^a   Li, Cui Lin ^a   Zhang, Fan ^a   Wang, Xian Feng ^a   Zhang, Ge ^a   Bu, Xian Zhang ^a   Cai, Shao Hui ^b   Du, Jun ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b JINAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRONECTIN; GLYCOGEN SYNTHASE KINASE 3BETA; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; PROTEIN KINASE B; PROTEIN ZO1; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR ZEB1; TUMOR NECROSIS FACTOR ALPHA; UVOMORULIN;

ARTICLE; CANCER INVASION; CELL ASSAY; CELL INVASION; CELL MIGRATION; COLORECTAL CANCER; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REPRESSION; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; METASTASIS; MOLECULAR PATHOLOGY; NUCLEAR LOCALIZATION SIGNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; UBIQUITINATION; UPREGULATION;

CACO-2 CELLS; CELL MOVEMENT; COLORECTAL NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE KNOCKDOWN TECHNIQUES; GLYCOGEN SYNTHASE KINASE 3; HCT116 CELLS; HUMANS; PROTEIN BINDING; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-AKT; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA; UBIQUITINATION;

EID: 84874217880     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056664     Document Type: Article

References (50)

1. Coussens LM, Werb Z, (2002) Inflammation and cancer. Nature 420: 860-867.
2. Shacter E, Weitzman SA, (2002) Chronic inflammation and cancer. Oncology-New York 16: 217-226.
3. Wu Y, Zhou BP, (2009) Inflammation a driving force speeds cancer metastasis. Cell Cycle 8: 3267-3273.
4. Condeelis J, Pollard JW, (2006) Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 124: 263-266.
5. Burke F, Relf M, Negus R, Balkwill F, (1996) A cytokine profile of normal and malignant ovary. Cytokine 8: 578-585.
6. van Kempen L, Ruiter DJ, van Muijen GNP, Coussens LM, (2003) The tumor microenvironment: a critical determinant of neoplastic evolution. European Journal of Cell Biology 82: 539-548.
7. Balkwill F, (2009) Tumour necrosis factor and cancer. Nature Reviews Cancer 9: 361-371.
8. Thiery JP, Acloque H, Huang RYJ, Nieto MA, (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
9. Kalluri R, Weinberg RA, (2009) The basics of epithelial-mesenchymal transition. Journal of Clinical Investigation 119: 1420-1428.
10. Wu YD, Zhou BHP, (2010) Snail more than EMT. Cell Adhesion & Migration 4: 199-203.
11. Christofori G, (2006) New signals from the invasive front. Nature 441: 444-450.
12. Barrallo-Gimeno A, Nieto MA, (2005) The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132: 3151-3161.
13. Thiery JP, Sleeman JP, (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nature Reviews Molecular Cell Biology 7: 131-142.
14. Peinado H, Olmeda D, Cano A, (2007) Snail, ZEB and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nature Reviews Cancer 7: 415-428.
15. Nieto MA, (2002) The snail superfamily of zinc-finger transcription factors. Nature Reviews Molecular Cell Biology 3: 155-166.
16. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, et al. (2000) The transcription factor Snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nature Cell Biology 2: 84-89.
17. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, et al. (2000) The transcription factor Snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nature Cell Biology 2: 76-83.
18. Dong CF, Wu YD, Yao J, Wang YF, Yu YH, et al. (2012) G9a interacts with Snail and is critical for Snail-mediated E-cadherin repression in human breast cancer. Journal of Clinical Investigation 122: 1469-1486.
19. 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 Research 68: 6524-6532.
20. Olmeda D, Jorda M, Peinado H, Fabra A, Cano A, (2007) Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene 26: 1862-1874.
21. Blanco MJ, Moreno-Bueno G, Sarrio D, Locascio A, Cano A, et al. (2002) Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 21: 3241-3246.
22. Cheng CW, Wu PE, Yu JC, Huang CS, Yue CT, et al. (2001) Mechanisms of inactivation of E-cadherin in breast carcinoma: modification of the two-hit hypothesis of tumor suppressor gene. Oncogene 20: 3814-3823.
23. Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, et al. (2005) The transcriptional repressor snail promotes mammary tumor recurrence. Cancer Cell 8: 197-209.
24. Zhou BHP, Deng J, Xia WY, Xu JH, Li YM, et al. (2004) Dual regulation of Snail by GSK-3 beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nature Cell Biology 6: 931-940.
25. Mak P, Leav I, Pursell B, Bae D, Yang XF, et al. (2010) ER beta impedes prostate cancer EMT by destabilizing HIF-1 alpha and inhibiting VEGF-mediated Snail nuclear localization: Implications for Gleason Grading. Cancer Cell 17: 319-332.
26. Xiong H, Hong J, Du W, Lin YW, Ren LL, et al. (2012) Roles of STAT3 and ZEB1 proteins in E-cadherin down-regulation and human colorectal cancer epithelial-mesenchymal transition. Journal of Biological Chemistry 287: 5819-5832.
27. Voulgari A, Pintzas A, (2009) Epithelial-mesenchymal transition in cancer metastasis: Mechanisms, markers and strategies to overcome drug resistance in the clinic. Biochimica Et Biophysica Acta-Reviews on Cancer 1796: 75-90.
28. Vandromme M, GauthierRouviere C, Lamb N, Fernandez A, (1996) Regulation of transcription factor localization: fine-tuning of gene expression. Trends in Biochemical Sciences 21: 59-64.
29. Bachelder RE, Yoon SO, 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. Journal of Cell Biology 168: 29-33.
30. Dominguez D, Montserrat-Sentis B, Virgos-Soler A, Guaita S, Grueso J, et al. (2003) Phosphorylation regulates the subcellular location and activity of the snail transcriptional repressor. Molecular and Cellular Biology 23: 5078-5089.
31. Choo MK, Sakurai H, Koizumi K, Saiki I, (2005) Stimulation of cultured colon 26 cells with TNF-alpha promotes lung metastasis through the extracellular signal-regulated kinase pathway. Cancer Letters 230: 47-56.
32. Szlosarek P, Charles KA, Balkwill FR, (2006) Tumour necrosis factor-alpha as a tumour promoter. European Journal of Cancer 42: 745-750.
33. Csiszar A, Szentes T, Haraszti B, Balazs A, Petranyi GG, et al. (2004) The pattern of cytokine gene expression in human colorectal carcinoma. Pathology & Oncology Research 10: 109-116.
34. Grimm M, Lazariotou M, Kircher S, Hofelmayr A, Germer CT, et al. (2011) Tumor necrosis factor-alpha is associated with positive lymph node status in patients with recurrence of colorectal cancer-indications for anti-TNF-alpha agents in cancer treatment. Cellular Oncology 34: 315-326.
35. Logullo AF, Nonogaki S, Pasini FS, Osorio C, Soares FA, et al. (2010) Concomitant expression of epithelial-mesenchymal transition biomarkers in breast ductal carcinoma: Association with progression. Oncology Reports 23: 313-320.
36. Xue CS, Plieth D, Venkov C, Xu C, Neilson EG, (2003) The gatekeeper effect of epithelial-mesenchymal transition regulates the frequency of breast cancer metastasis. Cancer Research 63: 3386-3394.
37. Sheehan KM, Gulmann C, Eichler GS, Weinstein JN, Barrett HL, et al. (2008) Signal pathway pro. ling of epithelial and stromal compartments of colonic carcinoma reveals epithelial-mesenchymal transition. Oncogene 27: 323-331.
38. Fan XJ, Wan XB, Yang ZL, Fu XH, Huang Y, et al. (2012) Snail promotes lymph node metastasis and Twist enhances tumor deposit formation through epithelial-mesenchymal transition in colorectal cancer. Human Pathology. DOI:10.1016/j.humpath.2012.03.029.
39. Li CW, Xia WY, Huo LF, Lim SO, Wu Y, et al. (2012) Epithelial-mesenchymal transition induced by TNF-alpha requires NF-kappa B-mediated transcriptional upregulation of Twist1. Cancer Research 72: 1290-1300.
40. Storci G, Sansone P, Mari S, D'Uva G, Tavolari S, et al. (2010) TNFalpha up-regulates Slug via the NF-kappaB/HIF1alpha axis, which imparts breast cancer cells with a stem cell-like phenotype. Journal of Cellular Physiology 225: 682-691.
41. De Craene B, van Roy F, Berx G, (2005) Unraveling signalling cascades for the Snail family of transcription factors. Cellular Signalling 17: 535-547.
42. Karin M, Greten FR, (2005) NF kappa B: linking inflammation and immunity to cancer development and progression. Nature Reviews Immunology 5: 749-759.
43. Wu Y, Deng J, Rychahou PG, Qiu SM, Evers BM, et al. (2009) Stabilization of Snail by NF-kappa B is required for inflammation-induced cell migration and invasion. Cancer Cell 15: 416-428.
44. Grille SJ, Bellacosa A, Upson J, Klein-Szanto AJ, van Roy F, et al. (2003) The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Research 63: 2172-2178.
45. Saegusa M, Hashimura M, Kuwata T, Okayasu I, (2009) Requirement of the Akt/beta-catenin pathway for uterine carcinosarcoma genesis, modulating E-cadherin expression through the transactivation of Slug. American Journal of Pathology 174: 2107-2115.
46. Larue L, Bellacosa A, (2005) Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3′ kinase/AKT pathways. Oncogene 24: 7443-7454.
47. Chen RQ, Yang QK, Lee JD, (2012) BMK1 kinase suppresses epithelial-mesenchymal transition through the Akt/GSK3 beta signaling pathway. Cancer Research 72: 1579-1587.
48. Julien S, Puig I, Caretti E, Bonaventure J, Nelles L, et al. (2007) Activation of NF-kappa B by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene 26: 7445-7456.
49. Liu CM, Li YM, Semenov M, Han C, Baeg GH, et al. (2002) Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108: 837-847.
50. Schmalhofer O, Brabletz S, Brabletz T, (2009) E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer and Metastasis Reviews 28: 151-166.