MicroRNA-147 induces a mesenchymal-to-epithelial transition (MET) and reverses EGFR inhibitor resistance

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Lee, Chang Gong ^a   McCarthy, Susan ^b   Gruidl, Mike ^b   Timme, Cindy ^b   Yeatman, Timothy J ^a  

^a Gibbs Cancer Center   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; GEFITINIB; MICRORNA; MICRORNA 147; PROTEIN P27; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG; EPIDERMAL GROWTH FACTOR; MIRN147 MICRORNA, HUMAN;

ARTICLE; CANCER CELL; CELL CYCLE ARREST; CELL INVASION; CELL MOTILITY; CELL PROLIFERATION; COLON CANCER; DOWNSTREAM PROCESSING; DRUG SENSITIVITY; EPITHELIAL MESENCHYMAL TRANSITION; G1 PHASE CELL CYCLE CHECKPOINT; GENE CONTROL; GENE EXPRESSION; HUMAN; HUMAN CELL; LUNG CANCER; PROTEIN PHOSPHORYLATION; UPREGULATION; ANTAGONISTS AND INHIBITORS; GENETICS; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TUMOR INVASION; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL PROLIFERATION; EPIDERMAL GROWTH FACTOR; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; MICRORNAS; NEOPLASM INVASIVENESS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84898636549     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0084597     Document Type: Article

References (43)

1. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelialmesenchymal transitions (Pubitemid 43278296)
2. Lopez-Novoa JM, Nieto MA (2009) Inflammation and EMT: an alliance towards organ fibrosis and cancer progression. EMBO Mol Med 1:303-314.
3. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281-297.
4. Esquela-Kerscher A, Slack FJ (2006) Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 6:259-269.
5. Xia H, Hui KM (2012) MicroRNAs involved in regulating epithelialmesenchymal transition and cancer stem cells as molecular targets for cancer therapeutics. Cancer Gene Ther 19:723-730.
6. Gregory PA, Bert AG, Paterson EL, Barry SC, Tsykin A, et al. (2008) The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat Cell Biol 10:593-601. (Pubitemid 351627379)
7. Korpal M, Lee ES, Hu G, Kang Y (2008) The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J Biol Chem 283:14910-14914.
8. Park SM, Gaur AB, Lengyel E, Peter ME (2008) The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev 22:894-907. (Pubitemid 351482843)
9. Harazono Y, Muramatsu T, Endo H, Uzawa N, Kawano T, et al. (2013) miR-655 Is an EMT-suppressive MicroRNA targeting ZEB1 and TGFBR2. PLoS One 8:e62757.
10. Bullock MD, Sayan AE, Packham GK, Mirnezami AH (2012) MicroRNAs: critical regulators of epithelial to mesenchymal (EMT) and mesenchymal to epithelial transition (MET) in cancer progression. Biol Cell 104:3-12.
11. Liu G, Friggeri A, Yang Y, Park YJ, Tsuruta Y, et al. (2009) miR-147, a microRNA that is induced upon Toll-like receptor stimulation, regulates murine macrophage inflammatory responses. Proc Natl Acad Sci U S A 106:15819-15824.
12. Uhlmann S, Mannsperger H, Zhang JD, Horvat EA, Schmidt C, et al. (2012) Global microRNA level regulation of EGFR-driven cell-cycle protein network in breast cancer. Mol Syst Biol 8:570.
13. Loboda A, Nebozhyn MV, Watters JW, Buser CA, Shaw PM, et al. (2011) EMT is the dominant program in human colon cancer. BMC Med Genomics 4:9.
14. Umbas R, Isaacs WB, Bringuier PP, Schaafsma HE, Karthaus HF, et al. (1994) Decreased E-cadherin expression is associated with poor prognosis in patients with prostate cancer. Cancer Res 54:3929-3933. (Pubitemid 24241218)
15. Semb H, Christofori G (1998) The tumor-suppressor function of E-cadherin. Am J Hum Genet 63:1588-1593. (Pubitemid 30415720)
16. Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, et al. (2009) The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol 11:1487-1495.
17. Brabletz S, Bajdak K, Meidhof S, Burk U, Niedermann G, et al. (2011) The ZEB1/miR-200 feedback loop controls Notch signalling in cancer cells. EMBO J 30:770-782.
18. Brabletz S, Brabletz T (2010) The ZEB/miR-200 feedback loop-a motor of cellular plasticity in development and cancer? EMBO Rep 11:670-677.
19. Ramaswamy S, Nakamura N, Vazquez F, Batt DB, Perera S, et al. (1999) Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc Natl Acad Sci U S A 96:2110-2115. (Pubitemid 29117876)
20. Nawshad A, Lagamba D, Polad A, Hay ED (2005) Transforming growth factorbeta signaling during epithelial-mesenchymal transformation: implications for embryogenesis and tumor metastasis. Cells Tissues Organs 179:11-23. (Pubitemid 40976285)
21. 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.
22. Kasai H, Allen JT, Mason RM, Kamimura T, Zhang Z (2005) TGF-beta1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir Res 6:56.
23. Kosaka T, Yamaki E, Mogi A, Kuwano H (2011) Mechanisms of resistance to EGFR TKIs and development of a new generation of drugs in non-small-cell lung cancer. J Biomed Biotechnol 2011:165214.
24. Lamouille S, Derynck R (2007) Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J Cell Biol 178:437-451. (Pubitemid 47196152)
25. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM (2005) Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098-1101. (Pubitemid 40262113)
26. Wang X, Gorospe M, Huang Y, Holbrook NJ (1997) p27Kip1 overexpression causes apoptotic death of mammalian cells. Oncogene 15:2991-2997. (Pubitemid 28008992)
27. Kwon TK, Nordin AA (1997) Overexpression of cyclin E and cyclin-dependent kinase inhibitor (p27Kip1): effect on cell cycle regulation in HeLa cells. Biochem Biophys Res Commun 238:534-538. (Pubitemid 27464422)
28. Li J, Yang XK, Yu XX, Ge ML, Wang WL, et al. (2000) Overexpression of p27 (KIP1) induced cell cycle arrest in G (1) phase and subsequent apoptosis in HCC-9204 cell line. World J Gastroenterol 6:513-521. (Pubitemid 30665261)
29. Baldin V, Lukas J, Marcote MJ, Pagano M, Draetta G (1993) Cyclin D1 is a nuclear protein required for cell cycle progression in G1. Genes Dev 7:812-821. (Pubitemid 23163585)
30. Xia W, Li J, Chen L, Huang B, Li S, et al. (2010) MicroRNA-200b regulates cyclin D1 expression and promotes S-phase entry by targeting RND3 in HeLa cells. Mol Cell Biochem 344:261-266.
31. Scaltriti M, Baselga J (2006) The epidermal growth factor receptor pathway: a model for targeted therapy. Clin Cancer Res 12:5268-5272. (Pubitemid 44497237)
32. Alfieri RR, Galetti M, Tramonti S, Andreoli R, Mozzoni P, et al. (2011) Metabolism of the EGFR tyrosin kinase inhibitor gefitinib by cytochrome P450 1A1 enzyme in EGFR-wild type non small cell lung cancer cell lines. Mol Cancer 10:143.
33. Birnbaum A, Ready N (2005) Gefitinib therapy for non-small cell lung cancer. Curr Treat Options Oncol 6:75-81. (Pubitemid 40220539)
34. Koizumi F, Kanzawa F, Ueda Y, Koh Y, Tsukiyama S, et al. (2004) Synergistic interaction between the EGFR tyrosine kinase inhibitor gefitinib ("Iressa") and the DNA topoisomerase I inhibitor CPT-11 (irinotecan) in human colorectal cancer cells. Int J Cancer 108:464-472. (Pubitemid 37549614)
35. Ware KE, Hinz TK, Kleczko E, Singleton KR, Marek LA, et al. (2013) A mechanism of resistance to gefitinib mediated by cellular reprogramming and the acquisition of an FGF2-FGFR1 autocrine growth loop. Oncogenesis 2:e39.
36. Thomson S, Petti F, Sujka-Kwok I, Epstein D, Haley JD (2008) Kinase switching in mesenchymal-like non-small cell lung cancer lines contributes to EGFR inhibitor resistance through pathway redundancy. Clin Exp Metastasis 25:843-854.
37. Frederick BA, Helfrich BA, Coldren CD, Zheng D, Chan D, et al. (2007) Epithelial to mesenchymal transition predicts gefitinib resistance in cell lines of head and neck squamous cell carcinoma and non-small cell lung carcinoma. Mol Cancer Ther 6:1683-1691. (Pubitemid 46954044)
38. Suda K, Tomizawa K, Fujii M, Murakami H, Osada H, et al. (2011) Epithelial to mesenchymal transition in an epidermal growth factor receptor-mutant lung cancer cell line with acquired resistance to erlotinib. J Thorac Oncol 6:1152-1161.
39. Yao Z, Fenoglio S, Gao DC, Camiolo M, Stiles B, et al. (2010) TGF-beta IL-6 axis mediates selective and adaptive mechanisms of resistance to molecular targeted therapy in lung cancer. Proc Natl Acad Sci U S A 107:15535-15540.
40. Glickman MS, Sawyers CL (2012) Converting cancer therapies into cures: lessons from infectious diseases. Cell 148:1089-1098.
41. Rho JK, Choi YJ, Lee JK, Ryoo BY, Na, II, et al. (2009) Epithelial to mesenchymal transition derived from repeated exposure to gefitinib determines the sensitivity to EGFR inhibitors in A549, a non-small cell lung cancer cell line. Lung Cancer 63:219-226.
42. Jain A, Tindell CA, Laux I, Hunter JB, Curran J, et al. (2005) Epithelial membrane protein-1 is a biomarker of gefitinib resistance. Proc Natl Acad Sci U S A 102:11858-11863. (Pubitemid 41170815)
43. Maseki S, Ijichi K, Tanaka H, Fujii M, Hasegawa Y, et al. (2012) Acquisition of EMT phenotype in the gefitinib-resistant cells of a head and neck squamous cell carcinoma cell line through Akt/GSK-3beta/snail signalling pathway. Br J Cancer 106:1196-1204.