TGF-β-activated SMAD3/4 complex transcriptionally upregulates N-cadherin expression in non-small cell lung cancer

Lung Cancer

Volumn 87, Issue 3, 2015, Pages 249-257

  Yang, Haiping ^a,b   Wang, Longqiang ^a,b   Zhao, Jun ^c   Chen, Yongbing ^d   Lei, Zhe ^a,b   Liu, Xia ^a,b   Xia, Wei ^d   Guo, Lingling ^d   Zhang, Hong Tao ^a,b  

^a MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

^b Suzhou Key Laboratory for Molecular Cancer Genetics   (China)

^c THE FIRST AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

^d THE SECOND AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

Author keywords

CDH2; EMT; NSCLC; SMAD; TGF ; Transcription regulation

Indexed keywords

MESSENGER RNA; NERVE CELL ADHESION MOLECULE; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; CADHERIN; CDH2 PROTEIN, HUMAN; LEUKOCYTE ANTIGEN; PROTEIN BINDING; TRANSFORMING GROWTH FACTOR BETA;

A549 CELL LINE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LUCIFERASE ASSAY; LUNG PARENCHYMA; NON SMALL CELL LUNG CANCER; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; BINDING SITE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; LUNG TUMOR; METABOLISM; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; TRANSCRIPTION INITIATION; TUMOR CELL LINE;

ANTIGENS, CD; BASE SEQUENCE; BINDING SITES; CADHERINS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LUNG NEOPLASMS; NUCLEOTIDE MOTIFS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; TRANSFORMING GROWTH FACTOR BETA;

EID: 84924082957     PISSN: 01695002     EISSN: 18728332     Source Type: Journal    
DOI: 10.1016/j.lungcan.2014.12.015     Document Type: Article

References (40)

1. Lei Z., Liu R.Y., Zhao J., Liu Z., Jiang X., You W., et al. TGFBR1 haplotypes and risk of non-small-cell lung cancer. Cancer Res 2009, 69:7046-7052.
2. Gupta G.P., Massague J. Cancer metastasis: building a framework. Cell 2006, 127:679-695.
3. Kang Y., Massague J. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 2004, 118:277-279.
4. Thiery J.P., Acloque H., Huang R.Y., Nieto M.A. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139:871-890.
5. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.
6. Miettinen P.J., Ebner R., Lopez A.R., Derynck R. TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 1994, 127:2021-2036.
7. Pirozzi G., Tirino V., Camerlingo R., Franco R., La Rocca A., Liguori E., et al. Epithelial to mesenchymal transition by TGFbeta-1 induction increases stemness characteristics in primary non small cell lung cancer cell line. PLoS ONE 2011, 6:e21548.
8. Roberts A.B., Tian F., Byfield S.D., Stuelten C., Ooshima A., Saika S., et al. Smad3 is key to TGF-beta-mediated epithelial-to-mesenchymal transition, fibrosis, tumor suppression and metastasis. Cytokine Growth Factor Rev 2006, 17:19-27.
9. Bardeesy N., Cheng K.H., Berger J.H., Chu G.C., Pahler J., Olson P., et al. Smad4 is dispensable for normal pancreas development yet critical in progression and tumor biology of pancreas cancer. Genes Dev 2006, 20:3130-3146.
10. Deckers M., van Dinther M., Buijs J., Que I., Lowik C., van der Pluijm G., et al. The tumor suppressor Smad4 is required for transforming growth factor beta-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells. Cancer Res 2006, 66:2202-2209.
11. Massague J., Chen Y.G. Controlling TGF-beta signaling. Genes Dev 2000, 14:627-644.
12. Hoot K.E., Lighthall J., Han G., Lu S.L., Li A., Ju W., et al. Keratinocyte-specific Smad2 ablation results in increased epithelial-mesenchymal transition during skin cancer formation and progression. J Clin Invest 2008, 118:2722-2732.
13. Morita T., Mayanagi T., Sobue K. Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling. J Cell Biol 2007, 179:1027-1042.
14. Batlle E., Sancho E., Franci C., Dominguez D., Monfar M., Baulida J., et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell Biol 2000, 2:84-89.
15. Hajra K.M., Chen D.Y., Fearon E.R. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 2002, 62:1613-1618.
16. Thuault S., Valcourt U., Petersen M., Manfioletti G., Heldin C.H., Moustakas A. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. J Cell Biol 2006, 174:175-183.
17. Vincent T., Neve E.P., Johnson J.R., Kukalev A., Rojo F., Albanell J., et al. A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition. Nat Cell Biol 2009, 11:943-950.
18. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. J Clin Invest 2009, 119:1420-1428.
19. Llorens A., Rodrigo I., Lopez-Barcons L., Gonzalez-Garrigues M., Lozano E., Vinyals A., et al. Down-regulation of E-cadherin in mouse skin carcinoma cells enhances a migratory and invasive phenotype linked to matrix metalloproteinase-9 gelatinase expression. Lab Invest 1998, 78:1131-1142.
20. Zhang X., Liu G., Kang Y., Dong Z., Qian Q., Ma X. N-cadherin expression is associated with acquisition of EMT phenotype and with enhanced invasion in erlotinib-resistant lung cancer cell lines. PLoS ONE 2013, 8:e57692.
21. Tiwari N., Tiwari V.K., Waldmeier L., Balwierz P.J., Arnold P., Pachkov M., et al. Sox4 is a master regulator of epithelial-mesenchymal transition by controlling Ezh2 expression and epigenetic reprogramming. Cancer Cell 2013, 23:768-783.
22. De Wever O., Westbroek W., Verloes A., Bloemen N., Bracke M., Gespach C., et al. Critical role of N-cadherin in myofibroblast invasion and migration in vitro stimulated by colon-cancer-cell-derived TGF-beta or wounding. J Cell Sci 2004, 117:4691-4703.
23. Yang Y.A., Zhang G.M., Feigenbaum L., Zhang Y.E. Smad3 reduces susceptibility to hepatocarcinoma by sensitizing hepatocytes to apoptosis through downregulation of Bcl-2. Cancer Cell 2006, 9:445-457.
24. Jazag A., Kanai F., Ijichi H., Tateishi K., Ikenoue T., Tanaka Y., et al. Single small-interfering RNA expression vector for silencing multiple transforming growth factor-beta pathway components. Nucleic Acids Res 2005, 33:e131.
25. Liu R.Y., Zeng Y., Lei Z., Wang L., Yang H., Liu Z., et al. JAK/STAT3 signaling is required for TGF-beta-induced epithelial-mesenchymal transition in lung cancer cells. Int J Oncol 2014, 44:1643-1651.
26. Principe D.R., Doll J.A., Bauer J., Jung B., Munshi H.G., Bartholin L., et al. TGF-beta: duality of function between tumor prevention and carcinogenesis. J Natl Cancer Inst 2014, 106:djt369.
27. Shi Y., Wang Y.F., Jayaraman L., Yang H., Massague J., Pavletich N.P. Crystal structure of a Smad MH1 domain bound to DNA: insights on DNA binding in TGF-beta signaling. Cell 1998, 94:585-594.
28. Shirakihara T., Saitoh M., Miyazono K. Differential regulation of epithelial and mesenchymal markers by deltaEF1 proteins in epithelial mesenchymal transition induced by TGF-beta. Mol Biol Cell 2007, 18:3533-3544.
29. Lascombe I., Clairotte A., Fauconnet S., Bernardini S., Wallerand H., Kantelip B., et al. N-cadherin as a novel prognostic marker of progression in superficial urothelial tumors. Clin Cancer Res 2006, 12:2780-2787.
30. Hui L., Zhang S., Dong X., Tian D., Cui Z., Qiu X. Prognostic significance of twist and N-cadherin expression in NSCLC. PLoS ONE 2013, 8:e62171.
31. Moustakas A., Heldin C.H. Signaling networks guiding epithelial-mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 2007, 98:1512-1520.
32. Le Mee S., Fromigue O., Marie P.J. Sp1/Sp3 and the myeloid zinc finger gene MZF1 regulate the human N-cadherin promoter in osteoblasts. Exp Cell Res 2005, 302:129-142.
33. Alexander N.R., Tran N.L., Rekapally H., Summers C.E., Glackin C., Heimark R.L. N-cadherin gene expression in prostate carcinoma is modulated by integrin-dependent nuclear translocation of Twist1. Cancer Res 2006, 66:3365-3369.
34. Pardali K., Moustakas A. Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim Biophys Acta 2007, 1775:21-62.
35. Seoane J., Le H.V., Shen L., Anderson S.A., Massague J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 2004, 117:211-223.
36. Allen R.R., Qi L., Higgins P.J. Upstream stimulatory factor regulates E box-dependent PAI-1 transcription in human epidermal keratinocytes. J Cell Physiol 2005, 203:156-165.
37. Derynck R., Akhurst R.J. Differentiation plasticity regulated by TGF-beta family proteins in development and disease. Nat Cell Biol 2007, 9:1000-1004.
38. Massague J. TGF beta in cancer. Cell 2008, 134:215-230.
39. Bhowmick N.A., Ghiassi M., Bakin A., Aakre M., Lundquist C.A., Engel M.E., et al. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol Biol Cell 2001, 12:27-36.
40. Lamouille S., Derynck R. Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J Cell Biol 2007, 178:437-451.