Abstract
The epithelial-mesenchymal transition (EMT) has recently been linked to stem cell phenotype. However, the molecular mechanism underlying EMT and regulation of stemness remains elusive. Here, using genomic approaches, we show that tumour suppressor p53 has a role in regulating both EMT and EMT-associated stem cell properties through transcriptional activation of the microRNA miR-200c. p53 transactivates miR-200c through direct binding to the miR-200c promoter. Loss of p53 in mammary epithelial cells leads to decreased expression of miR-200c and activates the EMT programme, accompanied by an increased mammary stem cell population. Re-expressing miR-200c suppresses genes that mediate EMT and stemness properties and thereby reverts the mesenchymal and stem-cell-like phenotype caused by loss of p53 to a differentiated epithelial cell phenotype. Furthermore, loss of p53 correlates with a decrease in the level of miR-200c, but an increase in the expression of EMT and stemness markers, and development of a high tumour grade in a cohort of breast tumours. This study elucidates a role for p53 in regulating EMT-MET (mesenchymal-epithelial transition) and stemness or differentiation plasticity, and reveals a potential therapeutic implication to suppress EMT-associated cancer stem cells through activation of the p53-miR-200c pathway.
MeSH Terms
Aneuploidy
Breast Neoplasms/metabolism
Cell Line, Tumor
Cell Lineage
Cytokinesis
Entosis
Epithelial-Mesenchymal Transition
Gene Expression Regulation, Neoplastic
Genes, p53
Humans
MicroRNAs/genetics
Microscopy, Fluorescence/methods
Mitosis
Stem Cells/cytology
Tumor Suppressor Protein p53/metabolism
Chemicals
MicroRNAs
TP53 protein, human
Tumor Suppressor Protein p53
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Chang Chun-Ju
Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA.
Chao Chi-Hong
Xia Weiya
Yang Jer-Yen
Xiong Yan
Li Chia-Wei
Yu Wen-Hsuan
Rehman Sumaiyah K
Hsu Jennifer L
Lee Heng-Huan
Liu Mo
Chen Chun-Te
Yu Dihua
Hung Mien-Chie
References (20)
20 references, click to expand
-
Patches of mutant p53-immunoreactive epidermal cells induced by chronic UVB Irradiation harbor the same p53 mutations as squamous cell carcinomas in the skin of hairless SKH-1 mice.
Cancer Res. 2005 May 1;65(9):3577-85
PMID: 15867351
-
Self-renewal and solid tumor stem cells.
Oncogene. 2004 Sep 20;23(43):7274-82
PMID: 15378087
-
Complex networks orchestrate epithelial-mesenchymal transitions.
Nat Rev Mol Cell Biol. 2006 Feb;7(2):131-42
PMID: 16493418
-
Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells.
Cell. 2009 Aug 7;138(3):592-603
PMID: 19665978
-
A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells.
EMBO Rep. 2008 Jun;9(6):582-9
PMID: 18483486
-
The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs.
Nat Cell Biol. 2009 Dec;11(12):1487-95
PMID: 19935649
-
Molecular evolution of the thermosensitive PAb1620 epitope of human p53 by DNA shuffling.
J Biol Chem. 1999 Sep 24;274(39):28042-9
PMID: 10488156
-
Different mutant/wild-type p53 combinations cause a spectrum of increased invasive potential in nonmalignant immortalized human mammary epithelial cells.
Neoplasia. 2008 May;10(5):450-61
PMID: 18472962
-
The effects of wild-type p53 tumor suppressor activity and mutant p53 gain-of-function on cell growth.
Gene. 2001 Oct 17;277(1-2):15-30
PMID: 11602342
-
Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits.
Nat Rev Cancer. 2009 Apr;9(4):265-73
PMID: 19262571
-
Tumor spectrum analysis in p53-mutant mice.
Curr Biol. 1994 Jan 1;4(1):1-7
PMID: 7922305
-
Phosphorylation/cytoplasmic localization of p21Cip1/WAF1 is associated with HER2/neu overexpression and provides a novel combination predictor for poor prognosis in breast cancer patients.
Clin Cancer Res. 2004 Jun 1;10(11):3815-24
PMID: 15173090
-
Tumor suppressor p53: analysis of wild-type and mutant p53 complexes.
Mol Cell Biol. 1991 Jan;11(1):12-9
PMID: 1986215
-
Activation of p53-dependent growth suppression in human cells by mutations in PTEN or PIK3CA.
Mol Cell Biol. 2007 Jan;27(2):662-77
PMID: 17060456
-
The epithelial-mesenchymal transition generates cells with properties of stem cells.
Cell. 2008 May 16;133(4):704-15
PMID: 18485877
-
Mutant p53 exerts a dominant negative effect by preventing wild-type p53 from binding to the promoter of its target genes.
Oncogene. 2004 Mar 25;23(13):2330-8
PMID: 14743206
-
p53 status correlates with histopathological response in patients with soft tissue sarcomas treated using isolated limb perfusion with TNF-alpha and melphalan.
Ann Oncol. 2008 Apr;19(4):793-800
PMID: 18065405
-
TGF-beta1-induced expression of human Mdm2 correlates with late-stage metastatic breast cancer.
J Clin Invest. 2010 Jan;120(1):290-302
PMID: 19955655
-
A third-generation lentivirus vector with a conditional packaging system.
J Virol. 1998 Nov;72(11):8463-71
PMID: 9765382
-
Efficacy of p53 adenovirus-mediated gene therapy against human breast cancer xenografts.
Cancer Gene Ther. 1997 Mar-Apr;4(2):129-38
PMID: 9080122