Home LiteratureArticle Details
PMID: 23799116 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

SNAI1-mediated epithelial-mesenchymal transition confers chemoresistance and cellular plasticity by regulating genes involved in cell death and stem cell maintenance.

PloS one ·Vol. 8 ·No. 6 ·2013-00-00 ·Pages e66558

Lim S, Becker A, Zimmer A, Lu J, Buettner R, Kirfel J

Abstract

Tumor cells at the tumor margin lose epithelial properties and acquire features of mesenchymal cells, a process called epithelial-to-mesenchymal transition (EMT). Recently, features of EMT were shown to be linked to cells with tumor-founding capability, so-called cancer stem cells (CSCs). Inducers of the EMT include several transcription factors, such as Snail (SNAI1) and Slug (SNAI2), as well as the secreted transforming growth factor (TGFß). In the present study, we found that EMT induction in MCF10A cells by stably expressing SNAI1 contributed to drug resistance and acquisition of stem/progenitor-like character as shown by increased cell population for surface marker CD44(+)/CD24(-) and mammosphere forming capacity. Using a microarray approach, we demonstrate that SNAI1 overexpression results in a dramatic change in signaling pathways involved in the regulation of cell death and stem cell maintenance. We showed that NF-κB/MAPK signaling pathways are highly activated in MCF10A-SNAI1 cells by IL1ß stimulation, leading to the robust induction in IL6 and IL8. Furthermore, MCF10A-SNAI1 cells showed enhanced TCF/ß-catenin activity responding to the exogenous Wnt3a treatment. However, EMT-induced stem/progenitor cell activation process is tightly regulated in non-transformed MCF10A cells, as WNT5A and TGFB2 are strongly upregulated in MCF10A-SNAI1 cells antagonizing canonical Wnt pathway. In summary, our data provide new molecular findings how EMT contributes to the enhanced chemoresistance and the acquisition of stem/progenitor-like character by regulating signaling pathways.

MeSH Terms
Cell Death/physiology Cell Line, Tumor Cytokines/biosynthesis Drug Resistance, Neoplasm/physiology Epithelial-Mesenchymal Transition/physiology Gene Expression Regulation, Neoplastic/physiology Homeostasis Humans Inflammation Mediators/physiology Neoplastic Stem Cells/pathology Signal Transduction Snail Family Transcription Factors Transcription Factors/metabolism,physiology
Chemicals
Cytokines Inflammation Mediators SNAI1 protein, human SNAI2 protein, human Snail Family Transcription Factors Transcription Factors
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Lim Soyoung
Institute of Pathology, University of Cologne, Cologne, Germany.
Becker Astrid
Zimmer Andreas
Lu Jianrong
Buettner Reinhard
Kirfel Jutta
References (41)
41 references, click to expand
  1. Cancer stem cells and chemosensitivity.
    Clin Cancer Res. 2011 Aug 1;17(15):4942-7 PMID: 21622723
  2. Wnt5a as an effector of TGFβ in mammary development and cancer.
    J Mammary Gland Biol Neoplasia. 2011 Jun;16(2):157-67 PMID: 21416313
  3. Self-renewal and solid tumor stem cells.
    Oncogene. 2004 Sep 20;23(43):7274-82 PMID: 15378087
  4. Lysine-specific demethylase 1 is strongly expressed in poorly differentiated neuroblastoma: implications for therapy.
    Cancer Res. 2009 Mar 1;69(5):2065-71 PMID: 19223552
  5. Stem cell quiescence.
    Clin Cancer Res. 2011 Aug 1;17(15):4936-41 PMID: 21593194
  6. Increased serum interleukin-8 in patients with early and metastatic breast cancer correlates with early dissemination and survival.
    Clin Cancer Res. 2004 Nov 1;10(21):7157-62 PMID: 15534087
  7. NF-κB, stem cells and breast cancer: the links get stronger.
    Breast Cancer Res. 2011 Jul 26;13(4):214 PMID: 21867572
  8. Regulation of cancer stem cells by cytokine networks: attacking cancer's inflammatory roots.
    Clin Cancer Res. 2011 Oct 1;17(19):6125-9 PMID: 21685479
  9. Lysine-specific demethylase 1 (LSD1) is highly expressed in ER-negative breast cancers and a biomarker predicting aggressive biology.
    Carcinogenesis. 2010 Mar;31(3):512-20 PMID: 20042638
  10. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells.
    Cancer Res. 2006 Jun 15;66(12):6063-71 PMID: 16778178
  11. Role of Notch signaling in cell-fate determination of human mammary stem/progenitor cells.
    Breast Cancer Res. 2004;6(6):R605-15 PMID: 15535842
  12. Transcriptional crosstalk between TGF-β and stem cell pathways in tumor cell invasion: role of EMT promoting Smad complexes.
    Cell Cycle. 2010 Jun 15;9(12):2363-74 PMID: 20519943
  13. STAT3 activation of miR-21 and miR-181b-1 via PTEN and CYLD are part of the epigenetic switch linking inflammation to cancer.
    Mol Cell. 2010 Aug 27;39(4):493-506 PMID: 20797623
  14. 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 Sep;27(9):2059-68 PMID: 19544473
  15. Epithelial-mesenchymal transition and the invasive potential of tumors.
    Trends Mol Med. 2008 May;14(5):199-209 PMID: 18406208
  16. The role of PI3K/AKT, MAPK/ERK and NFkappabeta signalling in the maintenance of human embryonic stem cell pluripotency and viability highlighted by transcriptional profiling and functional analysis.
    Hum Mol Genet. 2006 Jun 1;15(11):1894-913 PMID: 16644866
  17. The epithelial-mesenchymal transition generates cells with properties of stem cells.
    Cell. 2008 May 16;133(4):704-15 PMID: 18485877
  18. Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling.
    PLoS Biol. 2009 Jun 2;7(6):e1000121 PMID: 19492080
  19. Requirement of the histone demethylase LSD1 in Snai1-mediated transcriptional repression during epithelial-mesenchymal transition.
    Oncogene. 2010 Sep 2;29(35):4896-904 PMID: 20562920
  20. Snail blocks the cell cycle and confers resistance to cell death.
    Genes Dev. 2004 May 15;18(10):1131-43 PMID: 15155580
  21. An epigenetic switch involving NF-kappaB, Lin28, Let-7 MicroRNA, and IL6 links inflammation to cell transformation.
    Cell. 2009 Nov 13;139(4):693-706 PMID: 19878981
  22. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links.
    Semin Cancer Biol. 2012 Oct;22(5-6):396-403 PMID: 22554795
  23. Tumor-derived JAGGED1 promotes osteolytic bone metastasis of breast cancer by engaging notch signaling in bone cells.
    Cancer Cell. 2011 Feb 15;19(2):192-205 PMID: 21295524
  24. Mechanisms of metastasis: epithelial-to-mesenchymal transition and contribution of tumor microenvironment.
    J Cell Biochem. 2007 Jul 1;101(4):816-29 PMID: 17243120
  25. Signaling pathways in cancer and embryonic stem cells.
    Stem Cell Rev. 2007 Jan;3(1):7-17 PMID: 17873377
  26. CXCR1 blockade selectively targets human breast cancer stem cells in vitro and in xenografts.
    J Clin Invest. 2010 Feb;120(2):485-97 PMID: 20051626
  27. The interleukin-1 family of cytokines and receptors in human breast cancer: implications for tumor progression.
    Int J Oncol. 2003 Aug;23(2):269-84 PMID: 12851675
  28. Inflammation and cancer: IL-6 and STAT3 complete the link.
    Cancer Cell. 2009 Feb 3;15(2):79-80 PMID: 19185839
  29. Transcriptional mechanisms of WNT5A based on NF-kappaB, Hedgehog, TGFbeta, and Notch signaling cascades.
    Int J Mol Med. 2009 Jun;23(6):763-9 PMID: 19424602
  30. Tumorigenicity of pluripotent stem cells: biological insights from molecular imaging.
    J R Soc Interface. 2010 Dec 6;7 Suppl 6:S753-63 PMID: 20880852
  31. IL-6 triggers malignant features in mammospheres from human ductal breast carcinoma and normal mammary gland.
    J Clin Invest. 2007 Dec;117(12):3988-4002 PMID: 18060036
  32. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer.
    Oncogene. 2010 Aug 26;29(34):4741-51 PMID: 20531305
  33. 4-hydroxyestradiol induces anchorage-independent growth of human mammary epithelial cells via activation of IkappaB kinase: potential role of reactive oxygen species.
    Cancer Res. 2009 Mar 15;69(6):2416-24 PMID: 19276383
  34. p66Shc/Notch-3 interplay controls self-renewal and hypoxia survival in human stem/progenitor cells of the mammary gland expanded in vitro as mammospheres.
    Stem Cells. 2007 Mar;25(3):807-15 PMID: 17158237
  35. The p65 (RelA) subunit of NF-kappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression.
    Mol Cell Biol. 2001 Oct;21(20):7065-77 PMID: 11564889
  36. Direct evidence for epithelial-mesenchymal transitions in breast cancer.
    Cancer Res. 2008 Feb 1;68(3):937-45 PMID: 18245497
  37. Breast cancer stem cell markers CD44, CD24 and ALDH1: expression distribution within intrinsic molecular subtype.
    J Clin Pathol. 2011 Nov;64(11):937-46 PMID: 21680574
  38. Gain or loss of TGFbeta signaling in mammary carcinoma cells can promote metastasis.
    Cell Cycle. 2009 Oct 15;8(20):3319-27 PMID: 19806012
  39. WNT signaling pathway and stem cell signaling network.
    Clin Cancer Res. 2007 Jul 15;13(14):4042-5 PMID: 17634527
  40. Ras and TGF[beta] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways.
    J Cell Biol. 2002 Jan 21;156(2):299-313 PMID: 11790801
  41. Activation of the PTEN/mTOR/STAT3 pathway in breast cancer stem-like cells is required for viability and maintenance.
    Proc Natl Acad Sci U S A. 2007 Oct 9;104(41):16158-63 PMID: 17911267
Article Info
Journal
PloS one
Abbr.
PLoS One
ISSN
1932-6203
Published
2013-00-00
Epub
2013-00-17
Pages
e66558
Language
English
Region
United States
NLM ID
101285081
PMCID
PMC3684605
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com