Combinatorial TGF-β attenuation with paclitaxel inhibits the epithelial-to-mesenchymal transition and breast cancer stem-like cells

Oncotarget

Volumn 6, Issue 35, 2015, Pages 37526-37543

  Park, So Yeon ^a   Kim, Min Jin ^a   Park, Sang A ^a   Kim, Jung Shin ^a   Min, Kyung Nan ^b   Kim, Dae Kee ^a   Lim, Woosung ^c   Nam, Jeong Seok ^d   Sheen, Yhun Yhong ^a  

^a Ewha Womans University   (South Korea)

^b Korea Intellectual Property Office   (South Korea)

^c Ewha Womans University   (South Korea)

^d Gachon University   (South Korea)

Author keywords

Epithelial to mesenchymal transition (EMT); Metastasis; Paclitaxel; Snail; Transforming growth factor (TGF )

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD24 ANTIGEN; EW 7197; FIBRONECTIN; HERMES ANTIGEN; KRUPPEL LIKE FACTOR 4; MYC PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; PACLITAXEL; PROTEIN TYROSINE KINASE INHIBITOR; PROTEIN ZO1; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX2; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; VIMENTIN; ANTINEOPLASTIC AGENT; MESSENGER RNA; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER STEM CELL; CELLULAR PARAMETERS; CONTROLLED STUDY; DRUG POTENTIATION; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; MAMMOSPHERE FORMING EFFICIENCY; MDA MB 231 CELL LINE; MOUSE; MOUSE MODEL; MULTIPLE CYCLE TREATMENT; NONHUMAN; OXIDATIVE STRESS; PLURIPOTENT STEM CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SURVIVAL TIME; TUMOR XENOGRAFT; ANIMAL; ANTAGONISTS AND INHIBITORS; BREAST NEOPLASMS; CELL MOTION; CELL PROLIFERATION; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENETICS; LUNG NEOPLASMS; METABOLISM; MULTIMODALITY CANCER THERAPY; NONOBESE DIABETIC MOUSE; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCID MOUSE; SECONDARY; TUMOR CELL CULTURE; WESTERN BLOTTING; WOUND HEALING;

ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL MOVEMENT; CELL PROLIFERATION; COMBINED MODALITY THERAPY; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HUMANS; LUNG NEOPLASMS; MICE; MICE, INBRED NOD; MICE, SCID; NEOPLASTIC STEM CELLS; PACLITAXEL; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANSFORMING GROWTH FACTOR BETA; TUMOR CELLS, CULTURED; WOUND HEALING; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84947733386     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6063     Document Type: Article

References (60)

1. Siegel RL, Miller KD and Jemal A. Cancer statistics, 2015. CA: a cancer journal for clinicians. 2015; 65(1):5-29.
2. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D and Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. International Journal of Cancer. 2015; 136(5):E359-E386.
3. Bray F, McCarron P and Parkin DM. The changing global patterns of female breast cancer incidence and mortality. childhood. 2004; 6:229-39.
4. Hollier BG, Evans K and Mani SA. The epithelial-tomesenchymal transition and cancer stem cells: a coalition against cancer therapies. Journal of mammary gland biology and neoplasia. 2009; 14(1):29-43.
5. Heerboth S, Housman G, Leary M, Longacre M, Byler S, Lapinska K, Willbanks A and Sarkar S. EMT and tumor metastasis. Clinical and translational medicine. 2015; 4(1):6.
6. Yang J and Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Developmental cell. 2008; 14(6):818-829.
7. Scheel C and Weinberg RA. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Seminars in cancer biology. 2012; 22(5-6):396-403.
8. Heldin C-H, Vanlandewijck M and Moustakas A. Regulation of EMT by TGFβ in cancer. FEBS letters. 2012; 586(14):1959-1970.
9. Padua D and Massagué J. Roles of TGFβ in metastasis. Cell research. 2009; 19(1):89-102.
10. Katsuno Y, Lamouille S and Derynck R. TGF-β signaling and epithelial-mesenchymal transition in cancer progression. Current opinion in oncology. 2013; 25(1):76-84.
11. Zavadil J, Cermak L, Soto-Nieves N and Böttinger EP. Integration of TGF-β/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. The EMBO journal. 2004; 23(5):1155-1165.
12. Valcourt U, Kowanetz M, Niimi H, Heldin C-H and Moustakas A. TGF-β and the Smad signaling pathway support transcriptomic reprogramming during epithelialmesenchymal cell transition. Molecular biology of the cell. 2005; 16(4):1987-2002.
13. Vincent T, Neve EP, Johnson JR, Kukalev A, Rojo F, Albanell J, Pietras K, Virtanen I, Philipson L and Leopold PL. A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-β mediated epithelial-mesenchymal transition. Nature cell biology. 2009; 11(8):943-950.
14. Gavert N and Ben-Ze'ev A. Epithelial-mesenchymal transition and the invasive potential of tumors. Trends in molecular medicine. 2008; 14(5):199-209.
15. Thiery JP, Acloque H, Huang RY and Nieto MA. Epithelialmesenchymal transitions in development and disease. Cell. 2009; 139(5):871-890.
16. Mani SA, Guo W, Liao M-J, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC and Shipitsin M. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell. 2008; 133(4):704-715.
17. Morel A-P, Lièvre M, Thomas C, Hinkal G, Ansieau S and Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PloS one. 2008; 3(8):e2888.
18. Yu H, Zhang C and Wu Y. Research progress in cancer stem cells and their drug resistance. Chinese journal of cancer. 2010; 29(3):261-264.
19. Li J and Zhou BP. Activation of β-catenin and Akt pathways by Twist are critical for the maintenance of EMT associated cancer stem cell-like characters. BMC cancer. 2011; 11(1):49.
20. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A and Weinberg RA. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nature genetics. 2008; 40(5):499-507.
21. Singh A and Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene. 2010; 29(34):4741-4751.
22. Friedmann-Morvinski D and Verma IM. Dedifferentiation and reprogramming: origins of cancer stem cells. EMBO reports. 2014; 15(3):244-253
23. Medema JP. Cancer stem cells: the challenges ahead. Nature cell biology. 2013; 15(4):338-344.
24. Nicolini A, Ferrari P, Fini M, Borsari V, Fallahi P, Antonelli A, Berti P, Carpi A and Miccoli P. Stem cells: their role in breast cancer development and resistance to treatment. Current pharmaceutical biotechnology. 2011; 12(2):196-205.
25. Li X, Lewis MT, Huang J, Gutierrez C, Osborne CK, Wu M-F, Hilsenbeck SG, Pavlick A, Zhang X and Chamness GC. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. Journal of the National Cancer Institute. 2008; 100(9):672-679.
26. Li J, Liu H, Yu J and Yu H. Chemoresistance to doxorubicin induces epithelial-mesenchymal transition via upregulation of transforming growth factor β signaling in HCT116 colon cancer cells. Molecular medicine reports. 2015; 12(1):192-198.
27. Yamada D, Kobayashi S, Wada H, Kawamoto K, Marubashi S, Eguchi H, Ishii H, Nagano H, Doki Y and Mori M. Role of crosstalk between interleukin-6 and transforming growth factor-beta 1 in epithelial-mesenchymal transition and chemoresistance in biliary tract cancer. European Journal of Cancer. 2013; 49(7):1725-1740.
28. Steg AD, Bevis KS, Katre AA, Ziebarth A, Dobbin ZC, Alvarez RD, Zhang K, Conner M and Landen CN. Stem cell pathways contribute to clinical chemoresistance in ovarian cancer. Clinical Cancer Research. 2012; 18(3):869-881.
29. Han Z, Jing Y, Xia Y, Zhang S, Hou J, Meng Y, Yu F, Liu X, Wu M and Zhang P. Mesenchymal stem cells contribute to the chemoresistance of hepatocellular carcinoma cells in inflammatory environment by inducing autophagy. Cell & bioscience. 2014; 4(1):22.
30. Bhola NE, Balko JM, Dugger TC, Kuba MG, Sánchez V, Sanders M, Stanford J, Cook RS and Arteaga CL. TGF-β inhibition enhances chemotherapy action against triplenegative breast cancer. The Journal of clinical investigation. 2013; 123(3):1348.
31. Wang Y and Zhou BP. Epithelial-mesenchymal transition in breast cancer progression and metastasis. Chinese journal of cancer. 2011; 30(9):603.
32. Jungert K, Buck A, von Wichert G, Adler G, König A, Buchholz M, Gress TM and Ellenrieder V. Sp1 Is Required for Transforming Growth Factor-β-Induced Mesenchymal Transition and Migration in Pancreatic Cancer Cells. Cancer research. 2007; 67(4):1563-1570.
33. Bakiri L, Macho-Maschler S, Custic I, Niemiec J, Guío-Carrión A, Hasenfuss S, Eger A, Müller M, Beug H and Wagner E. Fra-1/AP-1 induces EMT in mammary epithelial cells by modulating Zeb1/2 and TGFβ expression. Cell Death & Differentiation. 2015; 22(2):336-350.
34. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH, Goulet Jr R, Badve S and Nakshatri H. CD44+/CD24-breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Research. 2006; 8(5):R59.
35. Holliday DL and Speirs V. Choosing the right cell line for breast cancer research. Breast Cancer Research. 2011; 13(4):215.
36. Kao J, Salari K, Bocanegra M, Choi Y-L, Girard L, Gandhi J, Kwei KA, Hernandez-Boussard T, Wang P and Gazdar AF. Molecular profiling of breast cancer cell lines defines relevant tumor models and provides a resource for cancer gene discovery. PloS one. 2009; 4(7):e6146.
37. Paletta-Silva R, Rocco-Machado N and Meyer-Fernandes JR. NADPH oxidase biology and the regulation of tyrosine kinase receptor signaling and cancer drug cytotoxicity. International journal of molecular sciences. 2013; 14(2):3683-3704.
38. Kajiyama H, Shibata K, Terauchi M, Yamashita M, Ino K, Nawa A and Kikkawa F. Chemoresistance to paclitaxel induces epithelial-mesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells. International journal of oncology. 2007; 31(2):277-283.
39. Iseri öD, Kars MD, Arpaci F, Atalay C, Pak I and Gündüz U. Drug resistant MCF-7 cells exhibit epithelialmesenchymal transition gene expression pattern. Biomedicine & Pharmacotherapy. 2011; 65(1):40-45.
40. Kim JJ, Yin B, Christudass CS, Terada N, Rajagopalan K, Fabry B, Lee DY, Shiraishi T, Getzenberg RH and Veltri RW. Acquisition of paclitaxel resistance is associated with a more aggressive and invasive phenotype in prostate cancer. Journal of cellular biochemistry. 2013; 114(6):1286-1293.
41. Hiscox S, Jiang WG, Obermeier K, Taylor K, Morgan L, Burmi R, Barrow D and Nicholson RI. Tamoxifen resistance in MCF7 cells promotes EMT-like behaviour and involves modulation of β-catenin phosphorylation. International journal of cancer. 2006; 118(2):290-301.
42. Kajita M, McClinic KN and Wade PA. Aberrant expression of the transcription factors snail and slug alters the response to genotoxic stress. Molecular and cellular biology. 2004; 24(17):7559-7566.
43. Gajewski TF, Schreiber H and Fu Y-X. Innate and adaptive immune cells in the tumor microenvironment. Nature immunology. 2013; 14(10):1014-1022.
44. Son JY, Park S-Y, Kim S-J, Lee SJ, Park S-A, Kim M-J, Kim SW, Kim D-K, Nam J-S and Sheen YY. EW-7197, a novel ALK-5 kinase inhibitor, potently inhibits breast to lung metastasis. Molecular cancer therapeutics. 2014; 13(7):1704-1716.
45. Kalluri R and Zeisberg M. Fibroblasts in cancer. Nature Reviews Cancer. 2006; 6(5):392-401.
46. van Nes JG, de Kruijf EM, Putter H, Faratian D, Munro A, Campbell F, Smit VT, Liefers G-J, Kuppen PJ and van de Velde CJ. Co-expression of SNAIL and TWIST determines prognosis in estrogen receptor-positive early breast cancer patients. Breast cancer research and treatment. 2012; 133(1):49-59.
47. Muenst S, Däster S, Obermann E, Droeser R, Weber W, von Holzen U, Gao F, Viehl C, Oertli D and Soysal S. Nuclear expression of snail is an independent negative prognostic factor in human breast cancer. Disease markers. 2013; 35(5):337-344.
48. Cannito S, Novo E, di Bonzo LV, Busletta C, Colombatto S and Parola M. Epithelial-mesenchymal transition: from molecular mechanisms, redox regulation to implications in human health and disease. Antioxidants & redox signaling. 2010; 12(12):1383-1430.
49. Rhyu DY, Yang Y, Ha H, Lee GT, Song JS, Uh S-t and Lee HB. Role of reactive oxygen species in TGF-β1-induced mitogen-activated protein kinase activation and epithelialmesenchymal transition in renal tubular epithelial cells. Journal of the American Society of Nephrology. 2005; 16(3):667-675.
50. Hiraga R, Kato M, Miyagawa S and Kamata T. Nox4-derived ROS signaling contributes to TGF-β-induced epithelial-mesenchymal transition in pancreatic cancer cells. Anticancer research. 2013; 33(10):4431-4438.
51. Cichon MA and Radisky DC. ROS-induced epithelialmesenchymal transition in mammary epithelial cells is mediated by NF-κB-dependent activation of Snail. Oncotarget. 2014; 5(9):2827.
52. Alexandre J, Hu Y, Lu W, Pelicano H and Huang P. Novel action of paclitaxel against cancer cells: bystander effect mediated by reactive oxygen species. Cancer research. 2007; 67(8):3512-3517.
53. Chiu W-H, Luo S-J, Chen C-L, Cheng J-H, Hsieh C-Y, Wang C-Y, Huang W-C, Su W-C and Lin C-F. Vinca alkaloids cause aberrant ROS-mediated JNK activation, Mcl-1 downregulation, DNA damage, mitochondrial dysfunction, and apoptosis in lung adenocarcinoma cells. Biochemical pharmacology. 2012; 83(9):1159-1171.
54. Park S-A, Kim M-J, Park S-Y, Kim J-S, Lee S-J, Woo HA, Kim D-K, Nam J-S and Sheen YY. EW-7197 inhibits hepatic, renal, and pulmonary fibrosis by blocking TGF-β/Smad and ROS signaling. Cellular and Molecular Life Sciences. 2014; 72(10):2023-2039.
55. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY and Bapat SA. Snail and Slug Mediate Radioresistance and Chemoresistance by Antagonizing p53□Mediated Apoptosis and Acquiring a Stem□Like Phenotype in Ovarian Cancer Cells. Stem cells. 2009; 27(9):2059-2068.
56. Fan F, Samuel S, Evans KW, Lu J, Xia L, Zhou Y, Sceusi E, Tozzi F, Ye XC and Mani SA. Overexpression of Snail induces epithelial-mesenchymal transition and a cancer stem cell-like phenotype in human colorectal cancer cells. Cancer medicine. 2012; 1(1):5-16.
57. Zhou W, Lv R, Qi W, Wu D, Xu Y, Liu W, Mou Y and Wang L. Snail contributes to the maintenance of stem celllike phenotype cells in human pancreatic cancer. PloS one. 2014; 9:e87409.
58. Yu F, Li J, Chen H, Fu J, Ray S, Huang S, Zheng H and Ai W. Kruppel-like factor 4 (KLF4) is required for maintenance of breast cancer stem cells and for cell migration and invasion. Oncogene. 2011; 30(18):2161-2172.
59. Hatzis C, Pusztai L, Valero V, Booser DJ, Esserman L, Lluch A, Vidaurre T, Holmes F, Souchon E and Wang H. A genomic predictor of response and survival following taxane-anthracycline chemotherapy for invasive breast cancer. JAMA. 2011; 305(18):1873-1881.
60. Korde LA, Lusa L, McShane L, Lebowitz PF, Lukes L, Camphausen K, Parker JS, Swain SM, Hunter K and Zujewski JA. Gene expression pathway analysis to predict response to neoadjuvant docetaxel and capecitabine for breast cancer. Breast cancer research and treatment. 2010; 119(3):685-699.