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Implications of the Hybrid Epithelial/Mesenchymal Phenotype in Metastasis

Mohit Kumar Jolly

Frontiers in Oncology · 2015 · Review

doi:10.3389/fonc.2015.00155

Abstract

Transitions between epithelial and mesenchymal phenotypes - the epithelial to -mesenchymal transition (EMT) and its reverse the mesenchymal to epithelial transition (MET) - are hallmarks of cancer metastasis. While transitioning between the epithelial and mesenchymal phenotypes, cells can also attain a hybrid epithelial/mesenchymal (E/M) (i.e., partial or intermediate EMT) phenotype. Cells in this phenotype have mixed epithelial (e.g., adhesion) and mesenchymal (e.g., migration) properties, thereby allowing them to move collectively as clusters. If these clusters reach the bloodstream intact, they can give rise to clusters of circulating tumor cells (CTCs), as have often been seen experimentally. Here, we review the operating principles of the core regulatory network for EMT/MET that acts as a "three-way" switch giving rise to three distinct phenotypes - E, M and hybrid E/M - and present a theoretical framework that can elucidate the role of many other players in regulating epithelial plasticity. Furthermore, we highlight recent studies on partial EMT and its association with drug resistance and tumor-initiating potential; and discuss how cell-cell communication between cells in a partial EMT phenotype can enable the formation of clusters of CTCs. These clusters can be more apoptosis-resistant and have more tumor-initiating potential than singly moving CTCs with a wholly mesenchymal (complete EMT) phenotype. Also, more such clusters can be formed under inflammatory conditions that are often generated by various therapies. Finally, we discuss the multiple advantages that the partial EMT or hybrid E/M phenotype have as compared to a complete EMT phenotype and argue that these collectively migrating cells are the primary "bad actors" of metastasis.

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Baccelli I Schneeweiss A Riethdorf S Stenzinger A Schillert A Vogel V Identification of a population of blood circulating tumor cells from breast cancer patients that initiates metastasis in a xenograft assay. Nat Biotechnol (2013 ) 31:539–44.
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Corrected
125.
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Samavarchi-Tehrani P Golipour A David L Sung HK Beyer TA Datti A Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming. Cell Stem Cell (2010 ) 7:64–77.
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Zhang C Li C He F Cai Y Yang H. Identification of CD44+CD24+ gastric cancer stem cells. J Cancer Res Clin Oncol (2011 ) 137:1679–86.
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Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy · 2008
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Azzam DJ Zhao D Sun J Minn AJ Ranganathan P Drews-Elger K Triple negative breast cancer initiating cell subsets differ in functional and molecular characteristics and in γ-secretase inhibitor drug responses. EMBO Mol Med (2013 ) 5:1502–22.
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162.
SLUG/SNAI2 and Tumor Necrosis Factor Generate Breast Cells With CD44+/CD24- Phenotype · 2010
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Identification of CD24 as a cancer stem cell marker in human nasopharyngeal carcinoma. · 2014
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164.
Giannoni E Bianchini F Masieri L Serni S Torre E Calorini L Reciprocal activation of prostate cancer cells and cancer-associated fibroblasts stimulates epithelial-mesenchymal transition and cancer stemness. Cancer Res (2010 ) 70:6945–56.
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Espinoza I Miele L. Deadly crosstalk: Notch signaling at the intersection of EMT and cancer stem cells. Cancer Lett (2013 ) 341:41–5.
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Jolly MK Boareto M Lu M Onuchic JN Clementi C Ben-Jacob E Operating principles of Notch-delta-jagged module of cell-cell communication. New J Phys (2015 ) 17:055021
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Shaya O Sprinzak D. From Notch signaling to fine-grained patterning: modeling meets experiments. Curr Opin Genet Dev (2011 ) 21:732–9.
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Hartman BH Reh TA Bermingham-McDonogh O. Notch signaling specifies prosensory domains via lateral induction in the developing mammalian inner ear. Proc Natl Acad Sci U S A (2010 ) 107:15792–7.
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Involvement of Notch Signaling in Wound Healing · 2007
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Brabletz S Bajdak K Meidhof S Burk U Niedermann G Firat E The ZEB1/miR-200 feedback loop controls Notch signalling in cancer cells. EMBO J (2011 ) 30:770–82.
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184.
MiR-34a Targeting of Notch Ligand Delta-Like 1 Impairs CD15+/CD133+ Tumor-Propagating Cells and Supports Neural Differentiation in Medulloblastoma · 2011
No notice
185.
Bu P Chen K-Y Chen JH Wang L Walters J Shin YJ A microRNA miR-34a-regulated bimodal switch targets Notch in colon cancer stem cells. Cell Stem Cell (2013 ) 12:602–15.
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Sahlgren C Gustafsson MV Jin S Poellinger L Lendahl U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc Natl Acad Sci U S A (2008 ) 105:6392–7.
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187.
Duluc D Delneste Y Tan F Moles M-P Grimaud L Lenoir J Tumor-associated leukemia inhibitory factor and IL-6 skew monocyte differentiation into tumor-associated macrophage-like cells. Blood (2007 ) 110:4319–30.
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Johnston DA Dong B Hughes CC. TNF induction of jagged-1 in endothelial cells is NFkappaB-dependent. Gene (2009 ) 435:36–44.
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Benedito R Roca C Sörensen I Adams S Gossler A Fruttiger M The Notch ligands Dll4 and jagged1 have opposing effects on angiogenesis. Cell (2009 ) 137:1124–35.
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Colotta F Allavena P Sica A Garlanda C Mantovani A. Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability. Carcinogenesis (2009 ) 30:1073–81.
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194.
Arumugam T Ramachandran V Fournier KF Wang H Marquis L Abbruzzese JL Epithelial to mesenchymal transition contributes to drug resistance in pancreatic cancer. Cancer Res (2009 ) 69:5820–8.
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Witta SE Gemmill RM Hirsch FR Coldren CD Hedman K Ravdel L Restoring E-cadherin expression increases sensitivity to epidermal growth factor receptor inhibitors in lung cancer cell lines. Cancer Res (2006 ) 66:944–50.
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199.
Hiscox S Jiang WG Obermeier K Taylor K Morgan L Burmi R Tamoxifen resistance in MCF7 cells promotes EMT-like behaviour and involves modulation of β-catenin phosphorylation. Int J Cancer (2006 ) 118:290–301.
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203.
Zhu H Bhaijee F Ishaq N Pepper DJ Backus K Brown AS Correlation of Notch1, pAKT and nuclear NF-κB expression in triple negative breast cancer. Am J Cancer Res (2013 ) 3:230–9.
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Schaue D Micewicz ED Ratikan JA Xie MW Cheng G McBride WH Radiation and inflammation. Semin Radiat Oncol (2015 ) 25:4–10.
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205.
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206.
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McInnes LM Jacobson N Redfern A Dowling A Thompson EW Saunders CM. Clinical implications of circulating tumor cells of breast cancer patients: role of epithelial mesenchymal plasticity. Front Oncol (2015 ) 5:42.
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Not in our library10.1038/nmeth.3404

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