SNAIL induces epithelial-to-mesenchymal transition and cancer stem cell-like properties in aldehyde dehydroghenase-negative thyroid cancer cells

Thyroid

Volumn 23, Issue 8, 2013, Pages 989-996

  Yasui, Kazuaki ^a   Shimamura, Mika ^a   Mitsutake, Norisato ^a   Nagayama, Yuji ^a  

^a NAGASAKI UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; B RAF KINASE; MEMBRANE ANTIGEN; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN; VIMENTIN;

ARTICLE; CANCER STEM CELL; CARCINOGENESIS; CELL PROLIFERATION; CELL STRUCTURE; CHEMOSENSITIVITY; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINDLE CELL; THYROID CANCER; TUMOR GROWTH;

ALDEHYDE DEHYDROGENASE; CADHERINS; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; NEOPLASTIC STEM CELLS; PROTO-ONCOGENE PROTEINS B-RAF; THYROID NEOPLASMS; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; VIMENTIN;

EID: 84883069928     PISSN: 10507256     EISSN: 15579077     Source Type: Journal    
DOI: 10.1089/thy.2012.0319     Document Type: Article

References (40)

1. Kondo T, Ezzat S, Asa SL 2006 Pathogenetic mechanisms in thyroid follicular-cell neoplasia. Nat Rev Cancer 6: 292-306.
2. Sipos J, Mazzaferri E 2010 Thyroid cancer epidemiology and prognostic variables. Clin Oncol 22:395-404.
3. Floor S, van Staveren WC, Larsimont D, Dumont JE, Maenhaut C 2011 Cancer cells in epithelial-to-mesenchymal transition and tumor-propagating-cancer stem cells: distinct, overlapping or same populations. Oncogene 30:4609-4621.
4. Polyak K, Weinberg RA 2009 Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 9:265-273.
5. Thiery JP, Sleeman JP 2006 Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7:131-142.
6. Miyazono K 2009 Transforming growth factor-beta signaling in epithelial-mesenchymal transition and progression of cancer. Proc Jpn Acad Ser B Phys Biol Sci 85:314.
7. Janda E, Lehmann K, Killisch I, Jechlinger M, Herzig M, Downward J, Beug H, Grunert S 2002 Ras and TGFb cooperatively regulate epithelial cell plasticity and metastasis. J Cell Biol 156:299-314.
8. Scheel C, Eaton EN, Li SHJ, Chaffer CL, Reinhardt F, Kah KJ, Bell G, Guo W, Rubin J, Richardson AL 2011 Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 145:926-940.
9. 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.
10. Hardy RG, Vicente-Duenas C, Gonzalez-Herrero I, Anderson C, Flores T, Hughes S, Tselepis C, Ross JA, Sanchez-Garcia I 2007 Snail family transcription factors are implicated in thyroid carcinogenesis. Am J Pathol 171:1037-1046.
11. Vasko V, Espinosa AV, Scouten W, He H, Auer H, Liyanarachchi S, Larin A, Savchenko V, Francis GL, de la Chapelle A, Saji M, Ringel MD 2007 Gene expression and functional evidence of epithelial-to-mesenchymal transition in papillary thyroid carcinoma invasion. Proc Natl Acad Sci USA 104:2803-2808.
12. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M 2008 The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133:704-715.
13. Kong D, Banerjee S, Ahmad A, Li Y, Wang Z, Sethi S, Sarkar FH 2010 Epithelial to mesenchymal transition is mechanistically linked with stem cell signatures in prostate cancer cells. PLoS One 5:e12445.
14. Clarke MF, Dick JE, Dirks PB, Eaves CJ, Jamieson CH, Jones DL, Visvader J, Weissman IL, Wahl GM 2006 Cancer stem cells - perspectives on current status and future directions: AACR workshop on cancer stem cells. Cancer Res 66:9339- 9344.
15. Mitsutake N, Iwao A, Nagai K, Namba H, Ohtsuru A, Saenko V, Yamashita S 2007 Characterization of side population in thyroid cancer cell lines: cancer stem-like cells are enriched partly but not exclusively. Endocrinology 148: 1797-1803.
16. Friedman S, Lu M, Schultz A, Thomas D, Lin RY 2009 CD133 + anaplastic thyroid cancer cells initiate tumors in immunodeficient mice and are regulated by thyrotropin. PLoS One 4:e5395.
17. Todaro M, Iovino F, Eterno V, Cammareri P, Gambara G, Espina V, Gulotta G, Dieli F, Giordano S, De Maria R, Stassi G 2010 Tumorigenic and metastatic activity of human thyroid cancer stem cells. Cancer Res 70:8874-8885.
18. Liu J, Brown RE 2010 Immunohistochemical detection of epithelialmesenchymal transition associated with stemness phenotype in anaplastic thyroid carcinoma. Int J Clin Exp Pathol 3:755-762.
19. Chung SH, Onoda N, Ishikawa T, Ogisawa K, Takenaka C, Yano Y, Hato F, Hirakawa K 2002 Peroxisome proliferatoractivated receptor gamma activation induces cell cycle arrest via the p53-independent pathway in human anaplastic thyroid cancer cells. Jpn J Cancer Res 93:1358-1365.
20. Schweppe RE, Klopper JP, Korch C, Pugazhenthi U, Benezra M, Knauf JA, Fagin JA, Marlow LA, Copland JA, Smallridge RC, Haugen BR 2008 Deoxyribonucleic acid profiling analysis of 40 human thyroid cancer cell lines reveals crosscontamination resulting in cell line redundancy and misidentification. J Clin Endocrinol Metab 93:4331-4341.
21. Ory DS, Neugeboren BA, Mulligan RC 1996 A stable humanderived packaging cell line for production of high titer retrovirus/ vesicular stomatitis virus G pseudotypes. Proc Natl Acad Sci USA 93:11400-11406.
22. Matsuse M, Mitsutake N, Tanimura S, Ogi T, Nishihara E, Hirokawa M, Fuziwara CS, Saenko VA, Suzuki K, Miyauchi A, Yamashita S 2013 Functional characterization of the novel BRAF complex mutation, BRAF(V600delinsYM), identified in papillary thyroid carcinoma. Int J Cancer 132:738-743.
23. Riesco-Eizaguirre G, Rodriguez I, De la Vieja A, Costamagna E, Carrasco N, Nistal M, Santisteban P 2009 The BRAFV600E oncogene induces transforming growth factor beta secretion leading to sodium iodide symporter repression and increased malignancy in thyroid cancer. Cancer Res 69:8317-8325.
24. Zhu LF, Hu Y, Yang CC, Xu XH, Ning TY, Wang ZL, Ye JH, Liu LK 2012 Snail overexpression induces an epithelial to mesenchymal transition and cancer stem cell-like properties in SCC9 cells. Lab Invest 92:744-752.
25. Wong AS, Gumbiner BM 2003 Adhesion-independent mechanism for suppression of tumor cell invasion by Ecadherin. J Cell Biol 161:1191-1203.
26. Brabant G, Hoang-Vu C, Cetin Y, Dralle H, Scheumann G, Molne J, Hansson G, Jansson S, Ericson LE, Nilsson M 1993 E-cadherin: a differentiation marker in thyroid malignancies. Cancer Res 53:4987-4993.
27. Scheumman GF, Hoang-Vu C, Cetin Y, Gimm O, Behrends J, von Wasielewski R, Georgii A, Birchmeier W, von Zur Muhlen A, Dralle H, et al. 1995 Clinical significance of E-cadherin as a prognostic marker in thyroid carcinomas. J Clin Endocrinol Metab 80:2168-2172.
28. Braun J, Hoang-Vu C, Dralle H, Huttelmaier S 2010 Downregulation of microRNAs directs the EMT and invasive potential of anaplastic thyroid carcinomas. Oncogene 29:4237-4244.
29. Wiseman SM, Masoudi H, Niblock P, Turbin D, Rajput A, Hay J, Filipenko D, Huntsman D, Gilks B 2006 Derangement of the E-cadherin/catenin complex is involved in transformation of differentiated to anaplastic thyroid carcinoma. Am J Surg 191:581-587.
30. Aratake Y, Nomura H, Kotani T, Marutsuka K, Kobayashi K, Kuma K, Miyauchi A, Okayama A, Tamura K 2006 Coexistent anaplastic and differentiated thyroid carcinoma: an immunohistochemical study. Am J Clin Pathol 125:399-406.
31. Catalano MG, Fortunati N, Pugliese M, Marano F, Ortoleva L, Poli R, Asioli S, Bandino A, Palestini N, Grange C, Bussolati B, Boccuzzi G 2012 Histone deacetylase inhibition modulates E-cadherin expression and suppresses migration and invasion of anaplastic thyroid cancer cells. J Clin Endocrinol Metab 97:E1150-E1159.
32. Kim T, Veronese A, Pichiorri F, Lee TJ, Jeon YJ, Volinia S, Pineau P, Marchio A, Palatini J, Suh SS, Alder H, Liu CG, Dejean A, Croce CM 2011 p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J Exp Med 208:875-883.
33. Chang CJ, Chao CH, Xia W, Yang JY, Xiong Y, Li CW, Yu WH, Rehman SK, Hsu JL, Lee HH, Liu M, Chen CT, Yu D, Hung MC 2011 p53 regulates epithelial-mesenchymal transition and stem cell properties through modulating mi- RNAs. Nat Cell Biol 13:317-323.
34. Knauf JA, Sartor MA, Medvedovic M, Lundsmith E, Ryder M, Salzano M, Nikiforov YE, Giordano TJ, Ghossein RA, Fagin JA 2011 Progression of BRAF-induced thyroid cancer is associated with epithelial-mesenchymal transition requiring concomitant MAP kinase and TGFbeta signaling. Oncogene 30:3153-3162.
35. Leboeuf R, Baumgartner JE, Benezra M, Malaguarnera R, Solit D, Pratilas CA, Rosen N, Knauf JA, Fagin JA 2008 BRAFV600E mutation is associated with preferential sensitivity tomitogenactivated protein kinase kinase inhibition in thyroid cancer cell lines. J Clin Endocrinol Metab 93:2194-2201.
36. Petti C, Molla A, Vegetti C, Ferrone S, Anichini A, Sensi M 2006 Coexpression of NRASQ61R and BRAFV600E in human melanoma cells activates senescence and increases susceptibility to cell-mediated cytotoxicity. Cancer Res 66:6503-6511.
37. Salerno P, Garcia-Rostan G, Piccinin S, Bencivenga TC, Di Maro G, Doglioni C, Basolo F, Maestro R, Fusco A, Santoro M 2001 TWIST1 plays a pleiotropic role in determining the anaplastic thyroid cancer phenotype. J Clin Endocrinol Metab 96:E772-E781.
38. Ralhan R, Cao J, Lim T, Macmillan C, Freeman JL, Walfish PG 2010 EpCAM nuclear localization identifies aggressive thyroid cancer and is a marker for poor prognosis. BMC Cancer 10:331.
39. Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, Kieu C, Papior P, Baeuerle PA, Munz M, Gires O 2009 Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol 11:162-171.
40. Biddle A, Liang X, Gammon L, Fazil B, Harper LJ, Emich H, Costea DE, Mackenzie IC 2011 Cancer stem cells in squamous cell carcinoma switch between two distinct phenotypes that are preferentially migratory or proliferative. Cancer Res 71:5317.