Knockdown of ZEB1, a master epithelial-to-mesenchymal transition (EMT) gene, suppresses anchorage-independent cell growth of lung cancer cells

Cancer Letters

Volumn 296, Issue 2, 2010, Pages 216-224

  Takeyama, Yoshihiro ^a   Sato, Mitsuo ^a   Horio, Mihoko ^a   Hase, Tetsunari ^a   Yoshida, Kenya ^a   Yokoyama, Toshihiko ^b   Nakashima, Harunori ^a   Hashimoto, Naozumi ^a   Sekido, Yoshitaka ^a,c   Gazdar, Adi F ^d   Minna, John D ^d   Kondo, Masashi ^a   Hasegawa, Yoshinori ^a  

^a NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b JAPANESE RED CROSS NAGOYA FIRST HOSPITAL   (Japan)

^c AICHI CANCER CENTER HOSPITAL   (Japan)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Anchorage independent growth; EMT; Epidermal growth factor receptor; Lung cancer; MicroRNA; RNA interference

Indexed keywords

MESSENGER RNA; PROTEIN SIP1; PROTEIN ZEB1; REPRESSOR PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER INHIBITION; CANCER TISSUE; CELL CYCLE; COLONY FORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA ISOLATION; SENESCENCE; WESTERN BLOTTING;

APOPTOSIS; CADHERINS; CARCINOMA, NON-SMALL-CELL LUNG; CELL DIVISION; CELL LINE, TUMOR; EPITHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HOMEODOMAIN PROTEINS; HUMANS; LUNG NEOPLASMS; MESODERM; MESOTHELIOMA; MICRORNAS; MUTATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, SMALL INTERFERING; TRANSCRIPTION FACTORS; VIMENTIN;

GASTROPODA;

EID: 77955270730     PISSN: 03043835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.canlet.2010.04.008     Document Type: Article

References (39)

1. Christiansen J.J., Rajasekaran A.K. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res. 2006, 66:8319-8326.
2. Klymkowsky M.W., Savagner P. Epithelial-mesenchymal transition: a cancer researcher's conceptual friend and foe. Am. J. Pathol. 2009, 174:1588-1593.
3. Vandewalle C., Van Roy F., Berx G. The role of the ZEB family of transcription factors in development and disease. Cell. Mol. Life Sci. 2009, 66:773-787.
4. Batlle E., Sancho E., Franci C., Dominguez D., Monfar M., Baulida J., Garcia De Herreros A. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2000, 2:84-89.
5. Cano A., Perez-Moreno M.A., Rodrigo I., Locascio A., Blanco M.J., del Barrio M.G., Portillo F., Nieto M.A. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2000, 2:76-83.
6. Yang J., Mani S.A., Donaher J.L., Ramaswamy S., Itzykson R.A., Come C., Savagner P., Gitelman I., Richardson A., Weinberg R.A. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117:927-939.
7. Miyoshi A., Kitajima Y., Kido S., Shimonishi T., Matsuyama S., Kitahara K., Miyazaki K. Snail accelerates cancer invasion by upregulating MMP expression and is associated with poor prognosis of hepatocellular carcinoma. Br. J. Cancer 2005, 92:252-258.
8. Yan-Qi Z., Xue-Yan G., Shuang H., Yu C., Fu-Lin G., Fei-Hu B., Shi-Ren S., Xu-Feng W., Jie D., Dai-Ming F. Expression and significance of TWIST basic helix-loop-helix protein over-expression in gastric cancer. Pathology 2007, 39:470-475.
9. Vesuna F., van Diest P., Chen J.H., Raman V. Twist is a transcriptional repressor of E-cadherin gene expression in breast cancer. Biochem. Biophys. Res. Commun. 2008, 367:235-241.
10. Valdes-Mora F., Gomez del Pulgar T., Bandres E., Cejas P., Ramirez de Molina A., Perez-Palacios R., Gallego-Ortega D., Garcia-Cabezas M.A., Casado E., Larrauri J., Nistal M., Gonzalez-Baron M., Garcia-Foncillas J., Lacal J.C. TWIST1 overexpression is associated with nodal invasion and male sex in primary colorectal cancer. Ann. Surg. Oncol. 2009, 16:78-87.
11. Parkin D.M., Bray F., Ferlay J., Pisani P. Global cancer statistics, 2002. CA Cancer J. Clin. 2005, 55:74-108.
12. Sato M., Shames D.S., Gazdar A.F., Minna J.D. A translational view of the molecular pathogenesis of lung cancer. J. Thorac. Oncol. 2007, 2:327-343.
13. Sekido Y., Fong K.M., Minna J.D. Molecular genetics of lung cancer. Annu. Rev. Med. 2003, 54:73-87.
14. Prudkin L., Liu D.D., Ozburn N.C., Sun M., Behrens C., Tang X., Brown K.C., Bekele B.N., Moran C., Wistuba Epithelial-to-mesenchymal transition in the development and progression of adenocarcinoma and squamous cell carcinoma of the lung. Mod. Pathol. 2009, 22:668-678.
15. Spaderna S., Schmalhofer O., Wahlbuhl M., Dimmler A., Bauer K., Sultan A., Hlubek F., Jung A., Strand D., Eger A., Kirchner T., Behrens J., Brabletz T. The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res. 2008, 68:537-544.
16. Arumugam T., Ramachandran V., Fournier K.F., Wang H., Marquis L., Abbruzzese J.L., Gallick G.E., Logsdon C.D., McConkey D.J., Choi W. Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res. 2009, 69:5820-5828.
17. Li Y., VandenBoom T.G., Kong D., Wang Z., Ali S., Philip P.A., Sarkar F.H. Up-regulation of miR-200 and let-7 by natural agents leads to the reversal of epithelial-to-mesenchymal transition in gemcitabine-resistant pancreatic cancer cells. Cancer Res. 2009, 69:6704-6712.
18. Ohira T., Gemmill R.M., Ferguson K., Kusy S., Roche J., Brambilla E., Zeng C., Baron A., Bemis L., Erickson P., Wilder E., Rustgi A., Kitajewski J., Gabrielson E., Bremnes R., Franklin W., Drabkin H.A. WNT7a induces E-cadherin in lung cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100:10429-10434.
19. Dohadwala M., Yang S.C., Luo J., Sharma S., Batra R.K., Huang M., Lin Y., Goodglick L., Krysan K., Fishbein M.C., Hong L., Lai C., Cameron R.B., Gemmill R.M., Drabkin H.A., Dubinett S.M. Cyclooxygenase-2-dependent regulation of E-cadherin: prostaglandin E(2) induces transcriptional repressors ZEB1 and snail in non-small cell lung cancer. Cancer Res. 2006, 66:5338-5345.
20. Clarhaut J., Gemmill R.M., Potiron V.A., Ait-Si-Ali S., Imbert J., Drabkin H.A., Roche J. ZEB-1, a repressor of the semaphorin 3F tumor suppressor gene in lung cancer cells. Neoplasia 2009, 11:157-166.
21. Gandhi J., Zhang J., Xie Y., Soh J., Shigematsu H., Zhang W., Yamamoto H., Peyton M., Girard L., Lockwood W.W., Lam W.L., Varella-Garcia M., Minna J.D., Gazdar A.F. Alterations in genes of the EGFR signaling pathway and their relationship to EGFR tyrosine kinase inhibitor sensitivity in lung cancer cell lines. PLoS One 2009, 4:e4576.
22. Usami N., Fukui T., Kondo M., Taniguchi T., Yokoyama T., Mori S., Yokoi K., Horio Y., Shimokata K., Sekido Y., Hida T. Establishment and characterization of four malignant pleural mesothelioma cell lines from Japanese patients. Cancer Sci. 2006, 97:387-394.
23. Yokoyama T., Kondo M., Goto Y., Fukui T., Yoshioka H., Yokoi K., Osada H., Imaizumi K., Hasegawa Y., Shimokata K., Sekido Y. EGFR point mutation in non-small cell lung cancer is occasionally accompanied by a second mutation or amplification. Cancer Sci. 2006, 97:753-759.
24. Sato M., Vaughan M.B., Girard L., Peyton M., Lee W., Shames D.S., Ramirez R.D., Sunaga N., Gazdar A.F., Shay J.W., Minna J.D. Multiple oncogenic changes (K-RAS(V12), p53 knockdown, mutant EGFRs, p16 bypass, telomerase) are not sufficient to confer a full malignant phenotype on human bronchial epithelial cells. Cancer Res. 2006, 66:2116-2128.
25. Hurteau G.J., Carlson J.A., Spivack S.D., Brock G.J. Overexpression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res. 2007, 67:7972-7976.
26. Burk U., Schubert J., Wellner U., Schmalhofer O., Vincan E., Spaderna S., Brabletz T. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 2008, 9:582-589.
27. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., Vadas M.A., Khew-Goodall Y., Goodall G.J. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 2008, 10:593-601.
28. Park S.M., Gaur A.B., Lengyel E., Peter M.E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 2008, 22:894-907.
29. Liu Y., El-Naggar S., Darling D.S., Higashi Y., Dean D.C. Zeb1 links epithelial-mesenchymal transition and cellular senescence. Development 2008, 135:579-588.
30. Deng Q.F., Zhou C.C., Su C.X. Clinicopathological features and epidermal growth factor receptor mutations associated with epithelial-mesenchymal transition in non-small cell lung cancer. Respirology 2009, 14:371-376.
31. Larue L., Bellacosa A. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3′ kinase/AKT pathways. Oncogene 2005, 24:7443-7454.
32. Witta S.E., Gemmill R.M., Hirsch F.R., Coldren C.D., Hedman K., Ravdel L., Helfrich B., Dziadziuszko R., Chan D.C., Sugita M., Chan Z., Baron A., Franklin W., Drabkin H.A., Girard L., Gazdar A.F., Minna J.D., Bunn P.A. Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res. 2006, 66:944-950.
33. Grooteclaes M.L., Frisch S.M. Evidence for a function of CtBP in epithelial gene regulation and anoikis. Oncogene 2000, 19:3823-3828.
34. Guaita S., Puig I., Franci C., Garrido M., Dominguez D., Batlle E., Sancho E., Dedhar S., De Herreros A.G., Baulida J. Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. J. Biol. Chem. 2002, 277:39209-39216.
35. Suzuki M., Sunaga N., Shames D.S., Toyooka S., Gazdar A.F., Minna J.D. RNA interference-mediated knockdown of DNA methyltransferase 1 leads to promoter demethylation and gene re-expression in human lung and breast cancer cells. Cancer Res. 2004, 64:3137-3143.
36. Kajita M., McClinic K.N., Wade P.A. Aberrant expression of the transcription factors snail and slug alters the response to genotoxic stress. Mol. Cell Biol. 2004, 24:7559-7566.
37. Vega S., Morales A.V., Ocana O.H., Valdes F., Fabregat I., Nieto M.A. Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 2004, 18:1131-1143.
38. Sayan A.E., Griffiths T.R., Pal R., Browne G.J., Ruddick A., Yagci T., Edwards R., Mayer N.J., Qazi H., Goyal S., Fernandez S., Straatman K., Jones G.D., Bowman K.J., Colquhoun A., Mellon J.K., Kriajevska M., Tulchinsky E. SIP1 protein protects cells from DNA damage-induced apoptosis and has independent prognostic value in bladder cancer. Proc. Natl. Acad. Sci. USA 2009.
39. Valsesia-Wittmann S., Magdeleine M., Dupasquier S., Garin E., Jallas A.C., Combaret V., Krause A., Leissner P., Puisieux A. Oncogenic cooperation between H-Twist and N-Myc overrides failsafe programs in cancer cells. Cancer Cell 2004, 6:625-630.