Contextual extracellular cues promote tumor cell EMT and metastasis by regulating miR-200 family expression

被引:412
作者
Gibbons, Don L. [1 ]
Lin, Wei [1 ]
Creighton, Chad J. [2 ]
Rizvi, Zain H. [1 ]
Gregory, Philip A. [3 ,4 ]
Goodall, Gregory J. [3 ,4 ]
Thilaganathan, Nishan [1 ]
Du, Liqin [5 ]
Zhang, Yiqun [2 ]
Pertsemlidis, Alexander [5 ]
Kurie, Jonathan M. [1 ]
机构
[1] Univ Texas MD Anderson Canc Ctr, Dept Thorac Head & Neck Med Oncol, Houston, TX 77030 USA
[2] Baylor Coll Med, Dan L Duncan Canc Ctr, Houston, TX 77030 USA
[3] Hanson Inst, Ctr Canc Biol, Div Human Immunol, Adelaide, SA 5000, Australia
[4] Univ Adelaide, Discipline Med, Adelaide, SA 5005, Australia
[5] Univ Texas SW Med Ctr Dallas, Eugene McDermott Ctr Human Growth & Dev, Dallas, TX 75390 USA
关键词
Lung cancer; EMT; microRNA-200; mouse model; metastasis; EPITHELIAL-MESENCHYMAL TRANSITION; GENETIC MOUSE MODEL; K-RAS ONCOGENE; LUNG-CANCER; E-CADHERIN; REPRESSORS ZEB1; STEM-CELLS; MICRORNAS; ADENOCARCINOMA; PROGRESSION;
D O I
10.1101/gad.1820209
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Metastatic disease is a primary cause of cancer-related death, and factors governing tumor cell metastasis have not been fully elucidated. Here, we address this question by using tumor cell lines derived from mice that develop metastatic lung adenocarcinoma owing to expression of mutant K-ras and p53. Despite having widespread somatic genetic alterations, the metastasis-prone tumor cells retained a marked plasticity. They transited reversibly between epithelial and mesenchymal states, forming highly polarized epithelial spheres in three-dimensional culture that underwent epithelial-to-mesenchymal transition (EMT) following treatment with transforming growth factor-beta or injection into syngeneic mice. This transition was entirely dependent on the microRNA (miR)-200 family, which decreased during EMT. Forced expression of miR-200 abrogated the capacity of these tumor cells to undergo EMT, invade, and metastasize, and conferred transcriptional features of metastasis-incompetent tumor cells. We conclude that tumor cell metastasis is regulated by miR-200 expression, which changes in response to contextual extracellular cues.
引用
收藏
页码:2140 / 2151
页数:12
相关论文
共 48 条
  • [1] The transcription factor ZEB1 (δEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity
    Aigner, K.
    Dampier, B.
    Descovich, L.
    Mikula, M.
    Sultan, A.
    Schreiber, M.
    Mikulits, W.
    Brabletz, T.
    Strand, D.
    Obrist, P.
    Sommergruber, W.
    Schweifer, N.
    Wernitznig, A.
    Beug, H.
    Foisner, R.
    Eger, A.
    [J]. ONCOGENE, 2007, 26 (49) : 6979 - 6988
  • [2] MicroRNAs: Genomics, biogenesis, mechanism, and function (Reprinted from Cell, vol 116, pg 281-297, 2004)
    Bartel, David P.
    [J]. CELL, 2007, 131 (04) : 11 - 29
  • [3] A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition
    Bracken, Cameron P.
    Gregory, Philip A.
    Kolesnikoff, Natasha
    Bert, Andrew G.
    Wang, Jun
    Shannon, M. Frances
    Goodall, Gregory J.
    [J]. CANCER RESEARCH, 2008, 68 (19) : 7846 - 7854
  • [4] A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells
    Burk, Ulrike
    Schubert, Joerg
    Wellner, Ulrich
    Schmalhofer, Otto
    Vincan, Elizabeth
    Spaderna, Simone
    Brabletz, Thomas
    [J]. EMBO REPORTS, 2008, 9 (06) : 582 - 589
  • [5] Regulatory element detection using correlation with expression
    Bussemaker, HJ
    Li, H
    Siggia, ED
    [J]. NATURE GENETICS, 2001, 27 (02) : 167 - 171
  • [6] A bioinformatics tool for linking gene expression profiling results with public databases of microRNA target predictions
    Creighton, Chad J.
    Nagaraja, Ankur K.
    Hanash, Samir M.
    Matzuk, Martin M.
    Gunaratne, Preethi H.
    [J]. RNA, 2008, 14 (11) : 2290 - 2296
  • [7] Insulin-like growth factor-I activates gene transcription programs strongly associated with poor breast cancer prognosis
    Creighton, Chad J.
    Casa, Angelo
    Lazard, ZaWaunyka
    Huang, Shixia
    Tsimelzon, Anna
    Hilsenbeck, Susan G.
    Osborne, Charles Kent
    Lee, Adrian V.
    [J]. JOURNAL OF CLINICAL ONCOLOGY, 2008, 26 (25) : 4078 - 4085
  • [8] Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures
    Debnath, J
    Muthuswamy, SK
    Brugge, JS
    [J]. METHODS, 2003, 30 (03) : 256 - 268
  • [9] DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells
    Eger, A
    Aigner, K
    Sonderegger, S
    Dampier, B
    Oehler, S
    Schreiber, M
    Berx, G
    Cano, A
    Beug, H
    Foisner, R
    [J]. ONCOGENE, 2005, 24 (14) : 2375 - 2385
  • [10] Induction and apoptotic regression of lung adenocarcinomas by regulation of a K-Ras transgene in the presence and absence of tumor suppressor genes
    Fisher, GH
    Wellen, SL
    Klimstra, D
    Lenczowski, JM
    Tichelaar, JW
    Lizak, MJ
    Whitsett, JA
    Koretsky, A
    Varmus, HE
    [J]. GENES & DEVELOPMENT, 2001, 15 (24) : 3249 - 3262