TGF-beta induces serous borderline ovarian tumor cell invasion by activating EMT but triggers apoptosis in low-grade serous ovarian carcinoma cells

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Cheng, Jung Chien ^a   Auersperg, Nelly ^a   Leung, Peter C K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 [4 (1,3 BENZODIOXOL 5 YL) 5 (2 PYRIDINYL) 1H IMIDAZOL 2 YL]BENZAMIDE; CASPASE 3; PROTEIN ZEB1; SMAD2 PROTEIN; SMAD3 PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR TWIST; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRYPAN BLUE; UNCLASSIFIED DRUG; UVOMORULIN;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER GRADING; CANCER INVASION; CELL ACTIVATION; CELL PROTECTION; DOWN REGULATION; EPITHELIAL MESENCHYMAL TRANSITION; OVARY CARCINOMA; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UPREGULATION;

APOPTOSIS; BENZAMIDES; CASPASE 3; CYSTADENOCARCINOMA, SEROUS; DIOXOLES; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM INVASIVENESS; OVARIAN NEOPLASMS; PHOSPHORYLATION; PROGNOSIS; RNA, SMALL INTERFERING; SMAD2 PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRYPAN BLUE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84865059388     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0042436     Document Type: Article

References (47)

1. Bierie B, Moses HL, (2006) Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer 6: 506-520.
2. Shi Y, Massague J, (2003) Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113: 685-700.
3. Heldin CH, Miyazono K, ten Dijke P, (1997) TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 390: 465-471.
4. Levy L, Hill CS, (2006) Alterations in components of the TGF-beta superfamily signaling pathways in human cancer. Cytokine Growth Factor Rev 17: 41-58.
5. Bierie B, Moses HL, (2006) TGF-beta and cancer. Cytokine Growth Factor Rev 17: 29-40.
6. Inman GJ, (2011) Switching TGFbeta from a tumor suppressor to a tumor promoter. Curr Opin Genet Dev 21: 93-99.
7. Ikushima H, Miyazono K, (2010) TGFbeta signalling: a complex web in cancer progression. Nat Rev Cancer 10: 415-424.
8. Thiery JP, Acloque H, Huang RY, Nieto MA, (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
9. Kang Y, Massague J, (2004) Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118: 277-279.
10. Miettinen PJ, Ebner R, Lopez AR, Derynck R, (1994) TGF-beta induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J Cell Biol 127: 2021-2036.
11. Xu J, Lamouille S, Derynck R, (2009) TGF-beta-induced epithelial to mesenchymal transition. Cell Res 19: 156-172.
12. Valcourt U, Kowanetz M, Niimi H, Heldin CH, Moustakas A, (2005) TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol Biol Cell 16: 1987-2002.
13. Bartlett JM, Langdon SP, Scott WN, Love SB, Miller EP, et al. (1997) Transforming growth factor-beta isoform expression in human ovarian tumours. Eur J Cancer 33: 2397-2403.
14. Auersperg N, Wong AS, Choi KC, Kang SK, Leung PC, (2001) Ovarian surface epithelium: biology, endocrinology, and pathology. Endocr Rev 22: 255-288.
15. Choi KC, Kang SK, Tai CJ, Auersperg N, Leung PC, (2001) The regulation of apoptosis by activin and transforming growth factor-beta in early neoplastic and tumorigenic ovarian surface epithelium. J Clin Endocrinol Metab 86: 2125-2135.
16. Chou JL, Chen LY, Lai HC, Chan MW, (2010) TGF-beta: friend or foe? The role of TGF-beta/SMAD signaling in epigenetic silencing of ovarian cancer and its implication in epigenetic therapy. Expert Opin Ther Targets 14: 1213-1223.
17. Do TV, Kubba LA, Du H, Sturgis CD, Woodruff TK, (2008) Transforming growth factor-beta1, transforming growth factor-beta2, and transforming growth factor-beta3 enhance ovarian cancer metastatic potential by inducing a Smad3-dependent epithelial-to-mesenchymal transition. Mol Cancer Res 6: 695-705.
18. Shih Ie M, Kurman RJ, (2004) Ovarian tumorigenesis: a proposed model based on morphological and molecular genetic analysis. Am J Pathol 164: 1511-1518.
19. Seidman JD, Horkayne-Szakaly I, Cosin JA, Ryu HS, Haiba M, et al. (2006) Testing of two binary grading systems for FIGO stage III serous carcinoma of the ovary and peritoneum. Gynecol Oncol 103: 703-708.
20. Gershenson DM, Silva EG, Tortolero-Luna G, Levenback C, Morris M, et al. (1998) Serous borderline tumors of the ovary with noninvasive peritoneal implants. Cancer 83: 2157-2163.
21. May T, Virtanen C, Sharma M, Milea A, Begley H, et al. (2010) Low malignant potential tumors with micropapillary features are molecularly similar to low-grade serous carcinoma of the ovary. Gynecol Oncol 117: 9-17.
22. Vergara D, Merlot B, Lucot JP, Collinet P, Vinatier D, et al. (2010) Epithelial-mesenchymal transition in ovarian cancer. Cancer Lett 291: 59-66.
23. Cheng JC, Auersperg N, Leung PC, (2011) Inhibition of p53 represses E-cadherin expression by increasing DNA methyltransferase-1 and promoter methylation in serous borderline ovarian tumor cells. Oncogene 30: 3930-3942.
24. Cheng JC, Auersperg N, Leung PC, (2011) Inhibition of p53 induces invasion of serous borderline ovarian tumor cells by accentuating PI3K/Akt-mediated suppression of E-cadherin. Oncogene 30: 1020-1031.
25. Cheng JC, Auersperg N, Leung PC, (2012) EGF-Induced EMT and Invasiveness in Serous Borderline Ovarian Tumor Cells: A Possible Step in the Transition to Low-Grade Serous Carcinoma Cells? PLoS One 7: e34071.
26. Woo MM, Salamanca CM, Miller M, Symowicz J, Leung PC, et al. (2008) Serous borderline ovarian tumors in long-term culture: phenotypic and genotypic distinction from invasive ovarian carcinomas. Int J Gynecol Cancer 18: 1234-1247.
27. Woo MM, Salamanca CM, Symowicz J, Stack MS, Miller DM, et al. (2008) SV40 early genes induce neoplastic properties in serous borderline ovarian tumor cells. Gynecol Oncol 111: 125-131.
28. Pohl G, Ho CL, Kurman RJ, Bristow R, Wang TL, et al. (2005) Inactivation of the mitogen-activated protein kinase pathway as a potential target-based therapy in ovarian serous tumors with KRAS or BRAF mutations. Cancer Res 65: 1994-2000.
29. Woo MM, Salamanca CM, Minor A, Auersperg N, (2007) An improved assay to quantitate the invasiveness of cells in modified Boyden chambers. In Vitro Cell Dev Biol Anim 43: 7-9.
30. Inman GJ, Nicolas FJ, Callahan JF, Harling JD, Gaster LM, et al. (2002) SB-431542 is a potent and specific inhibitor of transforming growth factor-beta superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol Pharmacol 62: 65-74.
31. Bodurka DC, Deavers MT, Tian C, Sun CC, Malpica A, et al. (2011) Reclassification of serous ovarian carcinoma by a 2-tier system: A Gynecologic Oncology Group Study. Cancer.
32. Massague J, (2008) TGFbeta in Cancer. Cell 134: 215-230.
33. Smith Sehdev AE, Sehdev PS, Kurman RJ, (2003) Noninvasive and invasive micropapillary (low-grade) serous carcinoma of the ovary: a clinicopathologic analysis of 135 cases. Am J Surg Pathol 27: 725-736.
34. Bonome T, Lee JY, Park DC, Radonovich M, Pise-Masison C, et al. (2005) Expression profiling of serous low malignant potential, low-grade, and high-grade tumors of the ovary. Cancer Res 65: 10602-10612.
35. Cordenonsi M, Dupont S, Maretto S, Insinga A, Imbriano C, et al. (2003) Links between tumor suppressors: p53 is required for TGF-beta gene responses by cooperating with Smads. Cell 113: 301-314.
36. Adorno M, Cordenonsi M, Montagner M, Dupont S, Wong C, et al. (2009) A Mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis. Cell 137: 87-98.
37. Zhang B, Halder SK, Kashikar ND, Cho YJ, Datta A, et al. (2010) Antimetastatic role of Smad4 signaling in colorectal cancer. Gastroenterology 138: 969-980 e961-963.
38. Zhang YE, (2009) Non-Smad pathways in TGF-beta signaling. Cell Res 19: 128-139.
39. Hoot KE, Lighthall J, Han G, Lu SL, Li A, et al. (2008) Keratinocyte-specific Smad2 ablation results in increased epithelial-mesenchymal transition during skin cancer formation and progression. J Clin Invest 118: 2722-2732.
40. Ju W, Ogawa A, Heyer J, Nierhof D, Yu L, et al. (2006) Deletion of Smad2 in mouse liver reveals novel functions in hepatocyte growth and differentiation. Mol Cell Biol 26: 654-667.
41. 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.
42. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, et al. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117: 927-939.
43. Vandewalle C, Comijn J, De Craene B, Vermassen P, Bruyneel E, et al. (2005) SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res 33: 6566-6578.
44. Hua F, Mu R, Liu J, Xue J, Wang Z, et al. (2011) TRB3 interacts with SMAD3 promoting tumor cell migration and invasion. J Cell Sci 124: 3235-3246.
45. Morita T, Mayanagi T, Sobue K, (2007) Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling. J Cell Biol 179: 1027-1042.
46. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A, (2003) Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest 112: 1486-1494.
47. Shirakihara T, Saitoh M, Miyazono K, (2007) Differential regulation of epithelial and mesenchymal markers by deltaEF1 proteins in epithelial mesenchymal transition induced by TGF-beta. Mol Biol Cell 18: 3533-3544.