Therapeutic and prognostic importance of epithelial-mesenchymal transition in liver cancers: Insights from experimental models

Critical Reviews in Oncology/Hematology

Volumn 83, Issue 3, 2012, Pages 319-328

  Ogunwobi, Olorunseun O ^a   Liu, Chen ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

Cancer metastasis; Epithelial mesenchymal transition; Liver; Prognostic factors; Therapeutic targets

Indexed keywords

CELECOXIB; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; INTERLEUKIN 8; OXALIPLATIN; SCATTER FACTOR; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; UVOMORULIN;

ADENOMATOUS POLYP; ADVANCED CANCER; CANCER GROWTH; CANCER PREVENTION; CANCER PROGNOSIS; CANCER RESISTANCE; CANCER STEM CELL; CARDIOVASCULAR DISEASE; CEREBROVASCULAR DISEASE; CHROMODOMAIN HELICASE ATPASE DNA BINDING PROTEIN 1 LIKE GENE; CIRCULATING TUMOR CELL; COLON CANCER; EPITHELIAL MESENCHYMAL TRANSITION; FAMILIAL ADENOMATOUS POLYPOSIS; GENE; HUMAN; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER METASTASIS; MICROSATELLITE INSTABILITY; NONHUMAN; OVERALL SURVIVAL; REVIEW; SURVIVAL TIME;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL TRANSFORMATION, NEOPLASTIC; COLONIC NEOPLASMS; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; LIVER NEOPLASMS; MODELS, ANIMAL; MOLECULAR TARGETED THERAPY; PROGNOSIS;

EID: 84864911235     PISSN: 10408428     EISSN: 18790461     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2011.11.007     Document Type: Review

References (107)

1. Chaffer C.L., Weinberg R.A. A perspective on cancer cell metastasis. Science 2011, 331(6024):1559-1564.
2. Kalluri R., Weinberg R.A. The basics of epithelial-mesenchymal transition. Journal of Clinical Investigation 2009, 119(6):1420-1428.
3. Polyak K., Weinberg R.A. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nature Reviews Cancer 2009, 9(4):265-273.
4. Thiery J.P., Acloque H., Huang R.Y.J., Angela Nieto M. Epithelial-mesenchymal transitions in development and disease. Cell 2009, 139(November 25 (5)):871-890.
5. Gotzmann J., Mario M., Eger A., et al. Molecular aspects of epithelial cell plasticity: implications for local tumor invasion and metastasis. Mutation Research-Reviews in Mutation Research 2004, 566(1):9-20.
6. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nature Reviews Molecular Cell Biology 2005, 6(8):622-634.
7. Wilm B., Ipenberg A., Hastie N.D., Burch J.B.E., Bader D.M. The serosal mesothelium is a major source of smooth muscle cells of the gut vasculature. Development 2005, 132(December (23)):5317-5328.
8. Su J., You P., Li W.-L., et al. The existence of multipotent stem cells with epithelial-mesenchymal transition features in the human liver bud. International Journal of Biochemistry & Cell Biology 2010, 42(December (12)):2047-2055.
9. Boyer B., Tucker G.C., Valles A.M., Franke W.W., Thiery J.P. Rearrangements of desmosomal and cytoskeletal proteins during the transition from epithelial to fibroblastoid organization in cultured rat bladder carcinoma cells. Journal of Cell Biology 1989, 109(4):1495-1509.
10. Barrallo-Gimeno A., Nieto M.A. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 2005, 132(14):3151-3161.
11. Franco D.L., Mainez J., Vega S., et al. Snail1 suppresses TGF-beta-induced apoptosis and is sufficient to trigger EMT in hepatocytes. Journal of Cell Science 2010, 123(20):3467-3477.
12. Valdes F., Alvarez A.M., Locascio A., et al. The epithelial mesenchymal transition confers resistance to the apoptotic effects of transforming growth factor beta in fetal rat hepatocytes. Molecular Cancer Research 2002, 1(November (1)):68-78.
13. Nitta T., Kim J.-S., Mohuczy D., Behrns K.E. Murine cirrhosis induces hepatocyte epithelial mesenchymal transition and alterations in survival signaling pathways. Hepatology 2008, 48(September (3)):909-919.
14. Bellusci S., Moens G., Thiery J.P., Jouanneau J. A scatter factor-like factor is produced by a metastatic variant of a rat bladder carcinoma cell line. Journal of Cell Science 1994, 107:1277-1287.
15. Savagner P., Valles A.M., Jouanneau J., Yamada K.M., Thiery J.P. Alternative splicing in fibroblast growth factor receptor 2 is associated with induced epithelial-mesenchymal transition in rat bladder carcinoma cells. Molecular Biology of the Cell 1994, 5(8):851-862.
16. Khoury H., Dankort D.L., Sadekova S., Naujokas M.A., Muller W.J., Park M. Distinct tyrosine autophosphorylation sites mediate induction of epithelial mesenchymal like transition by an activated ErbB-2/Neu receptor. Oncogene 2001, 20(7):788-799.
17. Bakin A.V., Tomlinson A.K., Bhowmick N.A., Moses H.L., Arteaga C.L. Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration. Journal of Biological Chemistry 2000, 275(47):36803-36810.
18. Grille S.J., Bellacosa A., Upson J., et al. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Research 2003, 63(9):2172-2178.
19. Li J.L., Zhou B.H.P. Activation of beta-catenin and Akt pathways by Twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC Cancer 2011, 11.
20. Shorning B.Y., Griffiths D., Clarke A.R. Lkb1 and; Pten synergise to suppress mTOR-mediated tumorigenesis and epithelial-mesenchymal transition in the mouse bladder. PLoS One 2011, 6(1).
21. Xue C.S., Plieth D., Venkov C., Xu C., Neilson E.G. The gatekeeper effect of epithelial-mesenchymal transition regulates the frequency of breast cancer metastasis. Cancer Research 2003, 63(12):3386-3394.
22. Huber M.A., Azoitei N., Baumann B., et al. NF-kappa B is essential for epithelial-mesenchymal transition and metastasis in a model of breast cancer progression. Journal of Clinical Investigation 2004, 114(4):569-581.
23. Blanco D., Vicent S., Elizegi E., et al. Altered expression of adhesion molecules and epithelial-mesenchymal transition in silica-induced rat lung carcinogenesis. Laboratory Investigation 2004, 84(8):999-1012.
24. Bates R.C., Bellovin D.I., Brown C., et al. Transcriptional activation of integrin beta 6 during the epithelial-mesenchymal transition defines a novel prognostic indicator of aggressive colon carcinoma. Journal of Clinical Investigation 2005, 115(2):339-347.
25. Miyazawa J., Mitoro A., Kawashiri S., Chada K.K., Imai K. Expression of mesenchyme-specific gene HMGA2 in squamous cell carcinomas of the oral cavity. Cancer Research 2004, 64(6):2024-2029.
26. Nakajima S., Doi R., Toyoda E., et al. N-cadherin expression and epithelial-mesenchymal transition in pancreatic carcinoma. Clinical Cancer Research 2004, 10(12):4125-4133.
27. Shibata T., Kokubu A., Sekine S., Kanai Y., Hirohashi S. Cytoplasmic p120ctn regulates the invasive phenotypes of E-cadherin-deficient breast cancer. American Journal of Pathology 2004, 164(6):2269-2278.
28. Thompson E.W., Newgreen D.F. Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition?. Cancer Research 2005, 65(14):5991-5995.
29. Tarin D. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Research 2005, 65(14):5996-6000.
30. Tarin D. Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition? Response. Cancer Research 2005, 65(14):5995.
31. Cardiff R.D. Epithelial to mesenchymal transition tumors: fallacious or Snail's pace?. Clinical Cancer Research 2005, 11(24):8534-8537.
32. Turley E.A., Veiseh M., Radisky D.C., Bissell M.J. Mechanisms of disease: epithelial-mesenchymal transition - does cellular plasticity fuel neoplastic progression?. Nature Clinical Practice Oncology 2008, 5(5):280-290.
33. Pinkas J., Leder P. MEK1 signaling mediates transformation and metastasis of EpH4 mammary epithelial cells independent of an epithelial to mesenchymal transition. Cancer Research 2002, 62(16):4781-4790.
34. Han G., Lu S.L., Li A.G., et al. Distinct mechanisms of TGF-beta(1)-mediated epithelial-to-mesenchymal transition and metastasis during skin carcinogenesis. Journal of Clinical Investigation 2005, 115(7):1714-1723.
35. Brown K.A., Aakre M.E., Gorska A.E., et al. Induction by transforming growth factor-beta 1 of epithelial to mesenchymal transition is a rare event in vitro. Breast Cancer Research 2004, 6(3):R215-R231.
36. Radisky D.C., Levy D.D., Littlepage L.E., et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 2005, 436(7047):123-127.
37. Thomson S., Buck E., Petti F., et al. Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Research 2005, 65(20):9455-9462.
38. Yauch R.L., Januario T., Eberhard D.A., et al. Epithelial versus mesenchymal phenotype determines in vitro sensitivity and predicts clinical activity of erlotinib in lung cancer patients. Clinical Cancer Research 2005, 11(24):8686-8698.
39. Ametller E., Garcia-Recio S., Costamagna D., et al. Tumor promoting effects of CD95 signaling in chemoresistant cells. Molecular Cancer 2010, 9.
40. Xiong W., Ren Z.G., Qiu S.J., et al. Residual hepatocellular carcinoma after oxaliplatin treatment has increased metastatic potential in a nude mouse model and is attenuated by Songyou Yin. BMC Cancer 2010, 10.
41. Li Q.Q., Xu J.D., Wang W.J., et al. Twist1-mediated adriamycin-induced epithelial-mesenchymal transition relates to multidrug resistance and invasive potential in breast cancer cells. Clinical Cancer Research 2009, 15(8):2657-2665.
42. Caja L., Conrad O., Esther B., et al. Differential intracellular signalling induced by TGF-beta in rat adult hepatocytes and hepatoma cells: implications in liver carcinogenesis. Cellular Signalling 2007, 19:683-694.
43. Ogunwobi O, Wang T, Zhang L, Liu C. COX-2 and Akt mediate multiple growth factor-induced epithelial-mesenchymal transition in human hepatocellular carcinoma. Journal of Gastroenterology and Hepatology; in press.
44. van Zijl F., Mair M., Csiszar A., et al. Hepatic tumor-stroma crosstalk guides epithelial to mesenchymal transition at the tumor edge. Oncogene 2009, 28(November 12 (45)):4022-4033.
45. Lei W., Zhang K., Pan X., et al. Histone deacetylase 1 is required for transforming growth factor-beta 1-induced epithelial-mesenchymal transition. International Journal of Biochemistry & Cell Biology 2010, 42(September (9)):1489-1497.
46. Ogunwobi O.O., Liu C. Hepatocyte growth factor upregulation promotes carcinogenesis and epithelial-mesenchymal transition in hepatocellular carcinoma via Akt and COX-2 pathways. Clinical and Experimental Metastasis 2011, 10.1007/s10585-011-9404-x.
47. Ding W., You H.N., Dang H., et al. Epithelial-to-mesenchymal transition of murine liver tumor cells promotes invasion. Hepatology 2010, 52(3):945-953.
48. Nagai T., Arao T., Furuta K., et al. Sorafenib inhibits the hepatocyte growth factor-mediated epithelial mesenchymal transition in hepatocellular carcinoma. Molecular Cancer Therapeutics 2011, 10(January (1)):169-177.
49. Ueki T., Fujimoto J., Suzuki T., Yamamoto H., Okamoto E. Expression of hepatocyte growth factor and its receptor c-met proto-oncogene in hepatocellular carcinoma. Hepatology 1997, 25(April (4)):862-866.
50. Kaposi-Novak P., Lee J.-S., Gomez-Quiroz L., Coulouarn C., Factor V.M., Thorgeirsson S.S. Met-regulated expression signature defines a subset of human hepatocellular carcinomas with poor prognosis and aggressive phenotype. Journal of Clinical Investigation 2006, 116(June (6)):1582-1595.
51. You H., Ding W., Dang H., Jiang Y., Rountree C.B. c-Met represents a potential therapeutic target for personalized treatment in hepatocellular carcinoma. Hepatology 2011, 54(September (3)):879-889.
52. Choi H.S., Yim S.H., Xu H.D., et al. Tropomyosin3 overexpression and a potential link to epithelial-mesenchymal transition in human hepatocellular carcinoma. BMC Cancer 2010, 10.
53. Chen L.L., Chan T.H.M., Yuan Y.F., et al. CHD1L promotes hepatocellular carcinoma progression and metastasis in mice and is associated with these processes in human patients. Journal of Clinical Investigation 2010, 120(4):1178-1191.
54. Vogelstein B., Fearon E.R., Hamilton S.R., et al. Genetic alterations during colorectal tumor development. New England Journal of Medicine 1988, 319(9):525-532.
55. Fearon E.R., Vogelstein B. A genetic model for colorectal tumorigenesis. Cell 1990, 61(5):759-767.
56. Bates R.C., Mercurio A.M. The epithelial-mesenchymal transition (EMT) and colorectal cancer progression. Cancer Biology & Therapy 2005, 4(4):365-370.
57. Wilmanns C., Steinhauer S., Grossmann J., Ruf G. Site-dependent differences in clinical, pathohistological, and molecular parameters in metastatic colon cancer. International Journal of Biological Sciences 2009, 5(5):458-465.
58. Loboda A., Nebozhyn M.V., Watters J.W., et al. EMT is the dominant program in human colon cancer. BMC Medical Genomics 2011, 4.
59. Brabletz T., Jung A., Hermann K., Gunther K., Hohenberger W., Kirchner T. Nuclear overexpression of the oncoprotein beta-catenin in colorectal cancer is localized predominantly at the invasion front. Pathology Research and Practice 1998, 194(10):701-704.
60. Bates R.C., Mercurio A.M. Tumor necrosis factor-alpha stimulates the epithelial-to-mesenchymal transition of human colonic organoids. Molecular Biology of the Cell 2003, 14(5):1790-1800.
61. Zhang W., Jiang B., Guo Z., et al. Four-and-a-half LIM protein 2 promotes invasive potential and epithelial-mesenchymal transition in colon cancer. Carcinogenesis 2010, 31(July (7)):1220-1229.
62. Larriba M.J., Casado-Vela J., Pendas-Franco N., et al. Novel Snail1 target proteins in human colon cancer identified by proteomic analysis. PLoS One 2010, 5(5).
63. Zhang W., Wang J., Zou B., et al. Four and a half LIM protein 2 (FHL2) negatively regulates the transcription of E-cadherin through interaction with Snail1. European Journal of Cancer 2011, 47(January (1)):121-130.
64. Bowen K.A., Doan H.Q., Zhou B.H.P., et al. PTEN loss induces epithelial-mesenchymal transition in human colon cancer cells. Anticancer Research 2009, 29(11):4439-4449.
65. Jang T.J., Jeon K.H., Jung K.H. Cyclooxygenase-2 expression is related to the epithelial-to-mesenchymal transition in human colon cancers. Yonsei Medical Journal 2009, 50(6):818-824.
66. Brown J.R., DuBois R.N. COX-2: a molecular target for colorectal cancer prevention. Journal of Clinical Oncology 2005, 23(12):2840-2855.
67. Kawamori T., Rao C.V., Seibert K., Reddy B.S. Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, against colon carcinogenesis. Cancer Research 1998, 58(3):409-412.
68. Reddy B.S., Rao C.V., Seibert K. Evaluation of cyclooxygenase-2 inhibitor for potential chemopreventive properties in colon carcinogenesis. Cancer Research 1996, 56(20):4566-4569.
69. Gavert N., Vivanti A., Hazin J., Brabletz T., Ben-Ze'ev A. L1-mediated colon cancer cell metastasis does not require changes in emt and cancer stem cell markers. Molecular Cancer Research 2011, 9(1):14-24.
70. Behrens J., Mareel M.M., Vanroy F.M., Birchmeier W. Dissecting tumor cell invasion - epithelial cells acquire invasive properties after the loss of uvomorulin-mediated cell-cell adhesion. Journal of Cell Biology 1989, 108(6):2435-2447.
71. Pino M.S., Kikuchi H., Zeng M., et al. Epithelial to mesenchymal transition is impaired in colon cancer cells with microsatellite instability. Gastroenterology 2010, 138(4):1406-1417.
72. Tay P.N., Tan P., Lan Y.H., et al. Palladin, an actin-associated protein, is required for adherens junction formation and intercellular adhesion in HCT116 colorectal cancer cells. International Journal of Oncology 2010, 37(4):909-926.
73. Shtutman M., Levina E., Ohouo P., Baig M., Roninson I.B. Cell adhesion molecule L1 disrupts E-cadherin-containing adherens junctions and increases scattering and motility of MCF7 breast carcinoma cells. Cancer Research 2006, 66(23):11370-11380.
74. Pardali K., Moustakas A. Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochimica et Biophysica Acta - Reviews on Cancer 2007, 1775(1):21-62.
75. Tang Y., Katuri V., Srinivasan R., et al. Transforming growth factor-beta suppresses nonmetastatic colon cancer through Smad4 and adaptor protein ELF at an early stage of tumorigenesis. Cancer Research 2005, 65(10):4228-4237.
76. Ponnusamy M.P., Lakshmanan I., Jain M., et al. MUC4 mucin-induced epithelial to mesenchymal transition: a novel mechanism for metastasis of human ovarian cancer cells. Oncogene 2010, 29(42):5741-5754.
77. Jung H., Lee K.P., Park S.J., et al. TMPRSS4 promotes invasion, migration and metastasis of human tumor cells by facilitating an epithelial-mesenchymal transition. Oncogene 2008, 27(18):2635-2647.
78. Chen L.L., Yuan Y.F., Li Y., et al. Clinical significance of CHD1L in hepatocellular carcinoma and therapeutic potentials of virus-mediated CHD1L depletion. Gut 2011, 60(4):534-543.
79. Fernando R.I., Litzinger M., Trono P., Hamilton D.H., Schlom J., Palena C. The T-box transcription factor Brachyury promotes epithelial-mesenchymal transition in human tumor cells. Journal of Clinical Investigation 2010, 120(2):533-544.
80. Bellovin D.I., Bates R.C., Muzikansky A., Rimm D.L., Mercurio A.M. Altered localization of p120 catenin during epithelial to mesenchymal transition of colon carcinoma is prognostic for aggressive disease. Cancer Research 2005, 65(23):10938-10945.
81. Koehne C.H., DuBois R.N. COX-2 inhibition and colorectal cancer. Seminars in Oncology 2004, 31(2):12-21.
82. Allen L.F., Sebolt-Leopold J., Meyer M.B. Cl-1040 (PD184352), a targeted signal transduction inhibitor of MEK (MAPKK). Seminars in Oncology 2003, 30(5):105-116.
83. Strumberg D., Richly H., Hilger R.A., et al. Phase I clinical and pharmacokinetic study of the novel Raf kinase and vascular endothelial growth factor receptor inhibitor BAY 43-9006 in patients with advanced refractory solid tumors. Journal of Clinical Oncology 2005, 23(5):965-972.
84. Gao M.Q., Kim B.G., Kang S., et al. Stromal fibroblasts from the interface zone of human breast carcinomas induce an epithelial-mesenchymal transition-like state in breast cancer cells in vitro. Journal of Cell Science 2010, 123(20):3507-3514.
85. Liu L., Ren Z.-G., Shen Y., et al. Influence of hepatic artery occlusion on tumor growth and metastatic potential in a human orthotopic hepatoma nude mouse model: relevance of epithelial-mesenchymal transition. Cancer Science 2010, 101(January (1)):120-128.
86. Fu J., Chen Y., Cao J., et al. p28(GANK) overexpression accelerates hepatocellular carcinoma invasiveness and metastasis via phosphoinositol 3-kinase/AKT/hypoxia-inducible factor-1 alpha pathways. Hepatology 2011, 53(January (1)):181-192.
87. Cannito S., Novo E., Compagnone A., et al. Redox mechanisms switch on hypoxia-dependent epithelial-mesenchymal transition in cancer cells. Carcinogenesis 2008, 29(12):2267-2278.
88. Fernando R.I., Castillo M.D., Litzinger M., Hamilton D.H., Palena C. IL-8 signaling plays a critical role in the epithelial-mesenchymal transition of human carcinoma cells. Cancer Research 2011, 71(August 1 (15)):5296-5306.
89. Soria G., Ofri-Shahak M., Haas I., et al. Inflammatory mediators in breast cancer: coordinated expression of TNF alpha & IL-1 beta with CCL2 & CCL5 and effects on epithelial-to-mesenchymal transition. BMC Cancer 2011, (April 12):11.
90. Bertran E., Caja L., Navarro E., et al. Role of CXCR4/SDF-1 alpha in the migratory phenotype of hepatoma cells that have undergone epithelial-mesenchymal transition in response to the transforming growth factor-beta. Cellular Signalling 2009, 21(November (11)):1595-1606.
91. Caja L., Bertran E., Campbell J., Fausto N., Fabregat I. The transforming growth factor-beta (TGF-beta) mediates acquisition of a mesenchymal stem cell-like phenotype in human liver cells. Journal of Cellular Physiology 2011, 226(May (5)):1214-1223.
92. Ning B.-F., Ding J., Yin C., et al. Hepatocyte nuclear factor 4 alpha suppresses the development of hepatocellular carcinoma. Cancer Research 2010, 70(October 1 (19)):7640-7651.
93. Chen X., Lingala S., Khoobyari S., Nolta J., Zern M.A., Wu J. Epithelial mesenchymal transition and hedgehog signaling activation are associated with chemoresistance and invasion of hepatoma subpopulations. Journal of Hepatology 2011, 55(October (4)):838-845.
94. Racila E., Euhus D., Weiss A.J., et al. Detection and characterization of carcinoma cells in the blood. Proceedings of the National Academy of Sciences of the United States of America 1998, 95(April 14 (8)):4589-4594.
95. Mego M., De Giorgi U., Dawood S., et al. Characterization of metastatic breast cancer patients with nondetectable circulating tumor cells. International Journal of Cancer 2011, 129(July 15 (2)):417-423.
96. Iinuma H., Watanabe T., Mimori K., et al. Clinical significance of circulating tumor cells, including cancer stem-like cells, in peripheral blood for recurrence and prognosis in patients with Dukes' Stage B and C colorectal cancer. Journal of Clinical Oncology 2011, 29(April 20 (12)):1547-1555.
97. Iinuma H., Watanabe T., Mimori K., et al. Identifying circulating tumor stem cells that matter: the key to prognostication and therapeutic targeting reply. Journal of Clinical Oncology 2011, 29(July 20 (21)):2947-2948.
98. Armstrong A.J., Marengo M.S., Oltean S., et al. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers. Molecular Cancer Research 2011, 9(August (8)):997-1007.
99. Lin H., Balic M., Zheng S.Y., Datar R., Cote R.J. Disseminated and circulating tumor cells: role in effective cancer management. Critical Reviews in Oncology Hematology 2011, 77(January (1)):2-12.
100. Glinskii A.B., Smith B.A., Jiang P., et al. Viable circulating metastatic cells produced in orthotopic but not ectopic prostate cancer models. Cancer Research 2003, 63(July 15 (14)):4239-4243.
101. Kolostova K., Pinterova D., Hoffman R.M., Bobek V. Circulating human prostate cancer cells from an orthotopic mouse model rapidly captured by immunomagnetic beads and imaged by GFP expression. Anticancer Research 2011, 31(May (5)):1535-1539.
102. Kallergi G., Papadaki M.A., Agelaki S., Mavroudis D., Georgoulias V. Epithelialmesenchymal transition markers are expressed in CTCS of breast cancer patients. Annals of Oncology 2009, 20(May):56.
103. Strauss R., Li Z.Y., Liu Y., et al. Analysis of epithelial and mesenchymal markers in ovarian cancer reveals phenotypic heterogeneity and plasticity. PLoS One 2011, 6(1).
104. Hur K., Takahashi M., Balaguer F., et al. MicroRNA-200c/141 cluster as a control switch between epithelial-to-mesenchymal transition (EMT) and mesenchymal-to-epithelial transition (MET) in human colorectal cancer metastasis. Gastroenterology 2011, 140(May (5)):S817-S820.
105. Clark W., Elahi A., Hernandez J.M., et al. MiR-675-induced mesenchymal to epithelial transition in HCC is associated with a reduction in Twist1. Gastroenterology 2011, 140(May (5)):S999-S1000.
106. Chen J., Wang L., Matyunina L.V., Hill C.G., McDonald J.F. Overexpression of miR-429 induces mesenchymal-to-epithelial transition (MET) in metastatic ovarian cancer cells. Gynecologic Oncology 2011, 121(April (1)):200-205.
107. Tiraby C., Hazen B.C., Gantner M.L., Kralli A. Estrogen-related receptor gamma promotes mesenchymal-to-epithelial transition and suppresses breast tumor growth. Cancer Research 2011, 71(April 1 (7)):2518-2528.