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PMID: 24556840 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Molecular mechanisms of epithelial-mesenchymal transition.

Nature reviews. Molecular cell biology ·Vol. 15 ·No. 3 ·2014-03-00 ·Pages 178-96

Lamouille S, Xu J, Derynck R

Abstract

The transdifferentiation of epithelial cells into motile mesenchymal cells, a process known as epithelial-mesenchymal transition (EMT), is integral in development, wound healing and stem cell behaviour, and contributes pathologically to fibrosis and cancer progression. This switch in cell differentiation and behaviour is mediated by key transcription factors, including SNAIL, zinc-finger E-box-binding (ZEB) and basic helix-loop-helix transcription factors, the functions of which are finely regulated at the transcriptional, translational and post-translational levels. The reprogramming of gene expression during EMT, as well as non-transcriptional changes, are initiated and controlled by signalling pathways that respond to extracellular cues. Among these, transforming growth factor-β (TGFβ) family signalling has a predominant role; however, the convergence of signalling pathways is essential for EMT.

MeSH Terms
Cell Movement Cytoskeleton/physiology Epithelial-Mesenchymal Transition/genetics,physiology Gene Expression Regulation, Developmental Humans Models, Biological RNA/genetics Signal Transduction Transcription Factors/metabolism
Chemicals
Transcription Factors RNA
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Lamouille Samy
Departments of Cell and Tissue Biology and Anatomy and Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California at San Francisco, San Francisco, California 94143-0669, USA.
Xu Jian
Center for Craniofacial Molecular Biology, University of Southern California, Los Angeles, California 90033, USA.
Derynck Rik
Departments of Cell and Tissue Biology and Anatomy and Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California at San Francisco, San Francisco, California 94143-0669, USA.
References (275)
275 references, click to expand
  1. A p120 catenin isoform switch affects Rho activity, induces tumor cell invasion, and predicts metastatic disease.
    J Biol Chem. 2008 Jun 27;283(26):18344-54 PMID: 18407999
  2. miR-194 is a marker of hepatic epithelial cells and suppresses metastasis of liver cancer cells in mice.
    Hepatology. 2010 Dec;52(6):2148-57 PMID: 20979124
  3. Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithelial-to-mesenchymal transition in human prostate cancer cells.
    Cancer Res. 2008 Apr 1;68(7):2479-88 PMID: 18381457
  4. EZH2 supports nasopharyngeal carcinoma cell aggressiveness by forming a co-repressor complex with HDAC1/HDAC2 and Snail to inhibit E-cadherin.
    Oncogene. 2012 Feb 2;31(5):583-94 PMID: 21685935
  5. The RNA-binding protein Rbfox2: an essential regulator of EMT-driven alternative splicing and a mediator of cellular invasion.
    Oncogene. 2014 Feb 27;33(9):1082-92 PMID: 23435423
  6. Smad-dependent and Smad-independent pathways in TGF-beta family signalling.
    Nature. 2003 Oct 9;425(6958):577-84 PMID: 14534577
  7. IL-8 signaling plays a critical role in the epithelial-mesenchymal transition of human carcinoma cells.
    Cancer Res. 2011 Aug 1;71(15):5296-306 PMID: 21653678
  8. LIM-kinase 2 and cofilin phosphorylation mediate actin cytoskeleton reorganization induced by transforming growth factor-beta.
    J Biol Chem. 2005 Mar 25;280(12):11448-57 PMID: 15647284
  9. EMT, the cytoskeleton, and cancer cell invasion.
    Cancer Metastasis Rev. 2009 Jun;28(1-2):15-33 PMID: 19169796
  10. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1.
    Cancer Cell. 2012 Dec 11;22(6):709-24 PMID: 23201163
  11. mTORC1 and mTORC2 regulate EMT, motility, and metastasis of colorectal cancer via RhoA and Rac1 signaling pathways.
    Cancer Res. 2011 May 1;71(9):3246-56 PMID: 21430067
  12. Epithelial-mesenchymal interactions in pulmonary fibrosis.
    Annu Rev Physiol. 2011;73:413-35 PMID: 21054168
  13. Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo.
    Genes Dev. 1999 Jul 15;13(14):1834-46 PMID: 10421635
  14. The epithelial-mesenchymal transition generates cells with properties of stem cells.
    Cell. 2008 May 16;133(4):704-15 PMID: 18485877
  15. Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers.
    Proc Natl Acad Sci U S A. 2007 Jun 12;104(24):10069-74 PMID: 17537911
  16. NCAM-induced focal adhesion assembly: a functional switch upon loss of E-cadherin.
    EMBO J. 2008 Oct 8;27(19):2603-15 PMID: 18772882
  17. A SNAIL1-SMAD3/4 transcriptional repressor complex promotes TGF-beta mediated epithelial-mesenchymal transition.
    Nat Cell Biol. 2009 Aug;11(8):943-50 PMID: 19597490
  18. ERK5/MAPK is activated by TGFbeta in hepatocytes and required for the GSK-3beta-mediated Snail protein stabilization.
    Cell Signal. 2008 Nov;20(11):2113-8 PMID: 18760348
  19. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts.
    Cancer Res. 2007 Nov 1;67(21):10123-8 PMID: 17974953
  20. Insulin-like growth factor-I receptor, E-cadherin and alpha v integrin form a dynamic complex under the control of alpha-catenin.
    Int J Cancer. 2008 Feb 1;122(3):572-82 PMID: 17955485
  21. Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition.
    FASEB J. 2010 Jun;24(6):1838-51 PMID: 20097873
  22. TGF beta-mediated RhoA expression is necessary for epithelial-mesenchymal transition in the embryonic chick heart.
    Dev Dyn. 2006 Jun;235(6):1589-98 PMID: 16598712
  23. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells.
    Nat Cell Biol. 2000 Feb;2(2):84-9 PMID: 10655587
  24. A poised chromatin platform for TGF-β access to master regulators.
    Cell. 2011 Dec 23;147(7):1511-24 PMID: 22196728
  25. Epithelial-to-mesenchymal transformation alters electrical conductivity of human epicardial cells.
    J Cell Mol Med. 2011 Dec;15(12):2675-83 PMID: 21251220
  26. Tumor cell invasiveness correlates with changes in integrin expression and localization.
    Oncogene. 2005 Mar 17;24(12):2032-41 PMID: 15688013
  27. New regulatory mechanisms of TGF-beta receptor function.
    Trends Cell Biol. 2009 Aug;19(8):385-94 PMID: 19648010
  28. The mechanisms of Hedgehog signalling and its roles in development and disease.
    Nat Rev Mol Cell Biol. 2013 Jul;14(7):416-29 PMID: 23719536
  29. TGF-{beta}-induced MiR-491-5p expression promotes Par-3 degradation in rat proximal tubular epithelial cells.
    J Biol Chem. 2010 Dec 17;285(51):40019-27 PMID: 20966078
  30. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?
    Nat Rev Cancer. 2007 Jun;7(6):415-28 PMID: 17508028
  31. 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
  32. Conversion of vascular endothelial cells into multipotent stem-like cells.
    Nat Med. 2010 Dec;16(12):1400-6 PMID: 21102460
  33. A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells.
    Nat Cell Biol. 2006 Dec;8(12):1398-406 PMID: 17072303
  34. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity.
    Science. 2005 Mar 11;307(5715):1603-9 PMID: 15761148
  35. TGF-β-induced activation of mTOR complex 2 drives epithelial-mesenchymal transition and cell invasion.
    J Cell Sci. 2012 Mar 1;125(Pt 5):1259-73 PMID: 22399812
  36. Specificity and versatility in tgf-beta signaling through Smads.
    Annu Rev Cell Dev Biol. 2005;21:659-93 PMID: 16212511
  37. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease.
    J Clin Invest. 2009 Jun;119(6):1438-49 PMID: 19487820
  38. Loss of FOXA1/2 is essential for the epithelial-to-mesenchymal transition in pancreatic cancer.
    Cancer Res. 2010 Mar 1;70(5):2115-25 PMID: 20160041
  39. Opposing LSD1 complexes function in developmental gene activation and repression programmes.
    Nature. 2007 Apr 19;446(7138):882-7 PMID: 17392792
  40. The tumor suppressor Smad4 is required for transforming growth factor beta-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells.
    Cancer Res. 2006 Feb 15;66(4):2202-9 PMID: 16489022
  41. Small C-terminal domain phosphatase enhances snail activity through dephosphorylation.
    J Biol Chem. 2009 Jan 2;284(1):640-648 PMID: 19004823
  42. Transforming growth factor beta (TGFbeta) signalling in palatal growth, apoptosis and epithelial mesenchymal transformation (EMT).
    Arch Oral Biol. 2004 Sep;49(9):675-89 PMID: 15275855
  43. TGF-beta activates Erk MAP kinase signalling through direct phosphorylation of ShcA.
    EMBO J. 2007 Sep 5;26(17):3957-67 PMID: 17673906
  44. PTTG induces EMT through integrin αVβ3-focal adhesion kinase signaling in lung cancer cells.
    Oncogene. 2012 Jun 28;31(26):3124-35 PMID: 22081074
  45. ZEB1 represses E-cadherin and induces an EMT by recruiting the SWI/SNF chromatin-remodeling protein BRG1.
    Oncogene. 2010 Jun 17;29(24):3490-500 PMID: 20418909
  46. The mammalian Scribble polarity protein regulates epithelial cell adhesion and migration through E-cadherin.
    J Cell Biol. 2005 Dec 19;171(6):1061-71 PMID: 16344308
  47. Lats2 kinase potentiates Snail1 activity by promoting nuclear retention upon phosphorylation.
    EMBO J. 2012 Jan 4;31(1):29-43 PMID: 21952048
  48. Opposing functions of ZEB proteins in the regulation of the TGFbeta/BMP signaling pathway.
    EMBO J. 2003 May 15;22(10):2443-52 PMID: 12743038
  49. TGF-beta-mediated phosphorylation of hnRNP E1 induces EMT via transcript-selective translational induction of Dab2 and ILEI.
    Nat Cell Biol. 2010 Mar;12(3):286-93 PMID: 20154680
  50. Hallmarks of cancer: the next generation.
    Cell. 2011 Mar 4;144(5):646-74 PMID: 21376230
  51. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer.
    Nat Rev Cancer. 2004 Feb;4(2):118-32 PMID: 14964308
  52. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal.
    Cell. 2007 Nov 30;131(5):980-93 PMID: 18045539
  53. Bone morphogenic protein-7 induces mesenchymal to epithelial transition in adult renal fibroblasts and facilitates regeneration of injured kidney.
    J Biol Chem. 2005 Mar 4;280(9):8094-100 PMID: 15591043
  54. Functional genomics reveals a BMP-driven mesenchymal-to-epithelial transition in the initiation of somatic cell reprogramming.
    Cell Stem Cell. 2010 Jul 2;7(1):64-77 PMID: 20621051
  55. An overview of epithelio-mesenchymal transformation.
    Acta Anat (Basel). 1995;154(1):8-20 PMID: 8714286
  56. Slug is a direct Notch target required for initiation of cardiac cushion cellularization.
    J Cell Biol. 2008 Jul 28;182(2):315-25 PMID: 18663143
  57. Deletion of Smad2 in mouse liver reveals novel functions in hepatocyte growth and differentiation.
    Mol Cell Biol. 2006 Jan;26(2):654-67 PMID: 16382155
  58. Endocardial and epicardial epithelial to mesenchymal transitions in heart development and disease.
    Circ Res. 2012 Jun 8;110(12):1628-45 PMID: 22679138
  59. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex.
    Mol Cell Biol. 2004 Jan;24(1):306-19 PMID: 14673164
  60. Multiple targets of miR-302 and miR-372 promote reprogramming of human fibroblasts to induced pluripotent stem cells.
    Nat Biotechnol. 2011 May;29(5):443-8 PMID: 21490602
  61. Cell polarity in eggs and epithelia: parallels and diversity.
    Cell. 2010 May 28;141(5):757-74 PMID: 20510924
  62. The basics of epithelial-mesenchymal transition.
    J Clin Invest. 2009 Jun;119(6):1420-8 PMID: 19487818
  63. Alpha 2 beta 1 integrin is required for the collagen and FGF-1 induced cell dispersion in a rat bladder carcinoma cell line.
    Cell Adhes Commun. 1996 Sep;4(3):187-99 PMID: 8969864
  64. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links.
    Semin Cancer Biol. 2012 Oct;22(5-6):396-403 PMID: 22554795
  65. Snail induction is an early response to Gli1 that determines the efficiency of epithelial transformation.
    Oncogene. 2006 Jan 26;25(4):609-21 PMID: 16158046
  66. Pc2-mediated sumoylation of Smad-interacting protein 1 attenuates transcriptional repression of E-cadherin.
    J Biol Chem. 2005 Oct 21;280(42):35477-89 PMID: 16061479
  67. FOXOs: signalling integrators for homeostasis maintenance.
    Nat Rev Mol Cell Biol. 2013 Feb;14(2):83-97 PMID: 23325358
  68. A gene regulatory network orchestrates neural crest formation.
    Nat Rev Mol Cell Biol. 2008 Jul;9(7):557-68 PMID: 18523435
  69. p120 catenin: an essential regulator of cadherin stability, adhesion-induced signaling, and cancer progression.
    Prog Mol Biol Transl Sci. 2013;116:409-32 PMID: 23481205
  70. BRAF and RAS oncogenes regulate Rho GTPase pathways to mediate migration and invasion properties in human colon cancer cells: a comparative study.
    Mol Cancer. 2011 Sep 23;10:118 PMID: 21943101
  71. Regulation of Rho GTPases by p120-catenin.
    Curr Opin Cell Biol. 2001 Oct;13(5):604-10 PMID: 11544030
  72. Stabilization of snail by NF-kappaB is required for inflammation-induced cell migration and invasion.
    Cancer Cell. 2009 May 5;15(5):416-28 PMID: 19411070
  73. Tgfbeta signal inhibition cooperates in the induction of iPSCs and replaces Sox2 and cMyc.
    Curr Biol. 2009 Nov 3;19(20):1718-23 PMID: 19765992
  74. Polycomb complex 2 is required for E-cadherin repression by the Snail1 transcription factor.
    Mol Cell Biol. 2008 Aug;28(15):4772-81 PMID: 18519590
  75. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism.
    Mol Biol Cell. 2001 Jan;12(1):27-36 PMID: 11160820
  76. Fibrosis and cancer: do myofibroblasts come also from epithelial cells via EMT?
    J Cell Biochem. 2007 Jul 1;101(4):830-9 PMID: 17211838
  77. Snail and Sonic Hedgehog activation in neuroendocrine tumors of the ileum.
    Endocr Relat Cancer. 2007 Sep;14(3):865-74 PMID: 17914115
  78. Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition.
    EMBO J. 2004 Mar 10;23(5):1155-65 PMID: 14976548
  79. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation.
    Genes Dev. 2004 Jan 1;18(1):99-115 PMID: 14701881
  80. Junctional recruitment of mammalian Scribble relies on E-cadherin engagement.
    Oncogene. 2005 Jun 23;24(27):4330-9 PMID: 15806148
  81. Scar wars: mapping the fate of epithelial-mesenchymal-myofibroblast transition.
    Kidney Int. 2011 Jul;80(1):41-50 PMID: 21430641
  82. Epithelial-Mesenchymal Transition in tumor microenvironment.
    Cell Biosci. 2011 Aug 31;1:29 PMID: 21880137
  83. Interleukin-6 induces an epithelial-mesenchymal transition phenotype in human breast cancer cells.
    Oncogene. 2009 Aug 20;28(33):2940-7 PMID: 19581928
  84. Dynamic actin remodeling during epithelial-mesenchymal transition depends on increased moesin expression.
    Mol Biol Cell. 2011 Dec;22(24):4750-64 PMID: 22031288
  85. TGF-beta signaling by Smad proteins.
    Adv Immunol. 2000;75:115-57 PMID: 10879283
  86. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease.
    Am J Physiol Lung Cell Mol Physiol. 2007 Sep;293(3):L525-34 PMID: 17631612
  87. Specific GATA factors act as conserved inducers of an endodermal-EMT.
    Dev Cell. 2011 Dec 13;21(6):1051-61 PMID: 22172671
  88. TGF-beta signal transduction and mesangial cell fibrogenesis.
    Am J Physiol Renal Physiol. 2003 Feb;284(2):F243-52 PMID: 12529270
  89. Transforming growth factor beta is essential for spindle cell conversion of mouse skin carcinoma in vivo: implications for tumor invasion.
    Cell Growth Differ. 1998 May;9(5):393-404 PMID: 9607560
  90. Integration of a Notch-dependent mesenchymal gene program and Bmp2-driven cell invasiveness regulates murine cardiac valve formation.
    J Clin Invest. 2010 Oct;120(10):3493-507 PMID: 20890042
  91. HMGA2 and Smads co-regulate SNAIL1 expression during induction of epithelial-to-mesenchymal transition.
    J Biol Chem. 2008 Nov 28;283(48):33437-46 PMID: 18832382
  92. Synergistic effect between EGF and TGF-beta1 in inducing oncogenic properties of intestinal epithelial cells.
    Oncogene. 2008 Apr 17;27(18):2626-34 PMID: 17982486
  93. DeltaEF1 mediates TGF-beta signaling in vascular smooth muscle cell differentiation.
    Dev Cell. 2006 Jul;11(1):93-104 PMID: 16824956
  94. Misexpression of Cwnt8C in the mouse induces an ectopic embryonic axis and causes a truncation of the anterior neuroectoderm.
    Development. 1997 Aug;124(15):2997-3005 PMID: 9247341
  95. Cell polarity in motion: redefining mammary tissue organization through EMT and cell polarity transitions.
    J Mammary Gland Biol Neoplasia. 2010 Jun;15(2):149-68 PMID: 20461450
  96. Constitutively active type I insulin-like growth factor receptor causes transformation and xenograft growth of immortalized mammary epithelial cells and is accompanied by an epithelial-to-mesenchymal transition mediated by NF-kappaB and snail.
    Mol Cell Biol. 2007 Apr;27(8):3165-75 PMID: 17296734
  97. Integrin alpha3beta1-dependent beta-catenin phosphorylation links epithelial Smad signaling to cell contacts.
    J Cell Biol. 2009 Jan 26;184(2):309-22 PMID: 19171760
  98. Complex networks orchestrate epithelial-mesenchymal transitions.
    Nat Rev Mol Cell Biol. 2006 Feb;7(2):131-42 PMID: 16493418
  99. Maternal wnt11 activates the canonical wnt signaling pathway required for axis formation in Xenopus embryos.
    Cell. 2005 Mar 25;120(6):857-71 PMID: 15797385
  100. The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition.
    J Cell Biol. 1997 Jun 16;137(6):1403-19 PMID: 9182671
  101. Breaking away: matrix remodeling from the leading edge.
    Trends Cell Biol. 2013 Jan;23(1):16-21 PMID: 22999190
  102. TGFβ signalling in context.
    Nat Rev Mol Cell Biol. 2012 Oct;13(10):616-30 PMID: 22992590
  103. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability.
    Nature. 2005 Jul 7;436(7047):123-7 PMID: 16001073
  104. FOXQ1 regulates epithelial-mesenchymal transition in human cancers.
    Cancer Res. 2011 Apr 15;71(8):3076-86 PMID: 21346143
  105. Slug is an essential target of TGFbeta2 signaling in the developing chicken heart.
    Dev Biol. 2000 Jul 1;223(1):91-102 PMID: 10864463
  106. Notch Signaling Pathway in Pancreatic Cancer Progression.
    Pancreat Disord Ther. 2013 May 30;3(114): PMID: 24027656
  107. Bmi1 is essential in Twist1-induced epithelial-mesenchymal transition.
    Nat Cell Biol. 2010 Oct;12(10):982-92 PMID: 20818389
  108. Back and forth between cell fate specification and movement during vertebrate gastrulation.
    Curr Opin Genet Dev. 2008 Aug;18(4):311-6 PMID: 18721878
  109. A proximal activator of transcription in epithelial-mesenchymal transition.
    J Clin Invest. 2007 Feb;117(2):482-91 PMID: 17273560
  110. Development of heart valves requires Gata4 expression in endothelial-derived cells.
    Development. 2006 Sep;133(18):3607-18 PMID: 16914500
  111. Differential regulation of the two RhoA-specific GEF isoforms Net1/Net1A by TGF-β and miR-24: role in epithelial-to-mesenchymal transition.
    Oncogene. 2012 Jun 7;31(23):2862-75 PMID: 21986943
  112. Molecular definition of breast tumor heterogeneity.
    Cancer Cell. 2007 Mar;11(3):259-73 PMID: 17349583
  113. Regulation of endothelial cell plasticity by TGF-β.
    Cell Tissue Res. 2012 Jan;347(1):177-86 PMID: 21866313
  114. Mouse snail is a target gene for HIF.
    Mol Cancer Res. 2011 Feb;9(2):234-45 PMID: 21257819
  115. Non-Smad TGF-beta signals.
    J Cell Sci. 2005 Aug 15;118(Pt 16):3573-84 PMID: 16105881
  116. Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition.
    J Cell Biol. 2005 Jan 3;168(1):29-33 PMID: 15631989
  117. A novel network integrating a miRNA-203/SNAI1 feedback loop which regulates epithelial to mesenchymal transition.
    PLoS One. 2012;7(4):e35440 PMID: 22514743
  118. Wnt activity defines colon cancer stem cells and is regulated by the microenvironment.
    Nat Cell Biol. 2010 May;12(5):468-76 PMID: 20418870
  119. Mechanical induction of Twist in the Drosophila foregut/stomodeal primordium.
    Curr Biol. 2003 Aug 19;13(16):1365-77 PMID: 12932320
  120. A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition.
    Cancer Res. 2008 Oct 1;68(19):7846-54 PMID: 18829540
  121. Sam68 regulates EMT through alternative splicing-activated nonsense-mediated mRNA decay of the SF2/ASF proto-oncogene.
    J Cell Biol. 2010 Oct 4;191(1):87-99 PMID: 20876280
  122. p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2.
    J Exp Med. 2011 May 9;208(5):875-83 PMID: 21518799
  123. A bivalent chromatin structure marks key developmental genes in embryonic stem cells.
    Cell. 2006 Apr 21;125(2):315-26 PMID: 16630819
  124. Collagen type I induces disruption of E-cadherin-mediated cell-cell contacts and promotes proliferation of pancreatic carcinoma cells.
    Cancer Res. 2006 May 1;66(9):4662-71 PMID: 16651417
  125. miR-30 inhibits TGF-β1-induced epithelial-to-mesenchymal transition in hepatocyte by targeting Snail1.
    Biochem Biophys Res Commun. 2012 Jan 20;417(3):1100-5 PMID: 22227196
  126. Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion.
    Cancer Metastasis Rev. 2009 Jun;28(1-2):65-76 PMID: 19160018
  127. TGF-beta-induced epithelial to mesenchymal transition.
    Cell Res. 2009 Feb;19(2):156-72 PMID: 19153598
  128. ATF-2 is a common nuclear target of Smad and TAK1 pathways in transforming growth factor-beta signaling.
    J Biol Chem. 1999 Mar 26;274(13):8949-57 PMID: 10085140
  129. Nuclear Janus-activated kinase 2/nuclear factor 1-C2 suppresses tumorigenesis and epithelial-to-mesenchymal transition by repressing Forkhead box F1.
    Cancer Res. 2010 Mar 1;70(5):2020-9 PMID: 20145151
  130. Signalling to cancer cell invasion through PAK family kinases.
    Front Biosci (Landmark Ed). 2011 Jan 01;16:849-64 PMID: 21196207
  131. Epithelial-mesenchymal transition events during human embryonic stem cell differentiation.
    Cancer Res. 2007 Dec 1;67(23):11254-62 PMID: 18056451
  132. ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing.
    Mol Cell. 2009 Mar 13;33(5):591-601 PMID: 19285943
  133. Vascular endothelial growth factor receptor-1 activation mediates epithelial to mesenchymal transition in human pancreatic carcinoma cells.
    Cancer Res. 2006 Jan 1;66(1):46-51 PMID: 16397214
  134. Differential regulation of epithelial and mesenchymal markers by deltaEF1 proteins in epithelial mesenchymal transition induced by TGF-beta.
    Mol Biol Cell. 2007 Sep;18(9):3533-44 PMID: 17615296
  135. Transforming growth factor-beta1 induces an epithelial-to-mesenchymal transition state in mouse hepatocytes in vitro.
    J Biol Chem. 2007 Jul 27;282(30):22089-101 PMID: 17513865
  136. Cell size and invasion in TGF-beta-induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway.
    J Cell Biol. 2007 Jul 30;178(3):437-51 PMID: 17646396
  137. Multiple transforming growth factor-beta isoforms and receptors function during epithelial-mesenchymal cell transformation in the embryonic heart.
    Cells Tissues Organs. 2007;185(1-3):146-56 PMID: 17587820
  138. Activation of Notch-1 enhances epithelial-mesenchymal transition in gefitinib-acquired resistant lung cancer cells.
    J Cell Biochem. 2012 May;113(5):1501-13 PMID: 22173954
  139. Bone morphogenetic proteins induce pancreatic cancer cell invasiveness through a Smad1-dependent mechanism that involves matrix metalloproteinase-2.
    Carcinogenesis. 2009 Feb;30(2):238-48 PMID: 19056927
  140. Small RNA-mediated regulation of iPS cell generation.
    EMBO J. 2011 Mar 2;30(5):823-34 PMID: 21285944
  141. G9a interacts with Snail and is critical for Snail-mediated E-cadherin repression in human breast cancer.
    J Clin Invest. 2012 Apr;122(4):1469-86 PMID: 22406531
  142. Zyxin is a transforming growth factor-β (TGF-β)/Smad3 target gene that regulates lung cancer cell motility via integrin α5β1.
    J Biol Chem. 2012 Sep 7;287(37):31393-405 PMID: 22778267
  143. The role of endothelial-mesenchymal transition in heterotopic ossification.
    J Bone Miner Res. 2012 Aug;27(8):1619-22 PMID: 22806925
  144. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of beta-catenin, and enhanced tumor cell invasion.
    Cancer Cell. 2003 Dec;4(6):499-515 PMID: 14706341
  145. CD44 splice isoform switching in human and mouse epithelium is essential for epithelial-mesenchymal transition and breast cancer progression.
    J Clin Invest. 2011 Mar;121(3):1064-74 PMID: 21393860
  146. SET8 promotes epithelial-mesenchymal transition and confers TWIST dual transcriptional activities.
    EMBO J. 2012 Jan 4;31(1):110-23 PMID: 21983900
  147. MicroRNA-155 is regulated by the transforming growth factor beta/Smad pathway and contributes to epithelial cell plasticity by targeting RhoA.
    Mol Cell Biol. 2008 Nov;28(22):6773-84 PMID: 18794355
  148. Keratinocyte-specific Smad2 ablation results in increased epithelial-mesenchymal transition during skin cancer formation and progression.
    J Clin Invest. 2008 Aug;118(8):2722-32 PMID: 18618014
  149. The activity of guanine exchange factor NET1 is essential for transforming growth factor-beta-mediated stress fiber formation.
    J Biol Chem. 2001 May 4;276(18):15362-8 PMID: 11278519
  150. TGFβ and BMP signaling in cardiac cushion formation: lessons from mice and chicken.
    Differentiation. 2012 Jul;84(1):89-102 PMID: 22656450
  151. Genome-scale epigenetic reprogramming during epithelial-to-mesenchymal transition.
    Nat Struct Mol Biol. 2011 Jul 03;18(8):867-74 PMID: 21725293
  152. Epithelial mesenchymal transition and pancreatic tumor initiating CD44+/EpCAM+ cells are inhibited by γ-secretase inhibitor IX.
    PLoS One. 2012;7(10):e46514 PMID: 23094026
  153. Hierarchical model of gene regulation by transforming growth factor beta.
    Proc Natl Acad Sci U S A. 2003 Sep 2;100(18):10269-74 PMID: 12930890
  154. Beta-catenin regulates Cripto- and Wnt3-dependent gene expression programs in mouse axis and mesoderm formation.
    Development. 2003 Dec;130(25):6283-94 PMID: 14623818
  155. A Smad action turnover switch operated by WW domain readers of a phosphoserine code.
    Genes Dev. 2011 Jun 15;25(12):1275-88 PMID: 21685363
  156. Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling.
    J Cell Biol. 2007 Dec 3;179(5):1027-42 PMID: 18056415
  157. Cadherin switching.
    J Cell Sci. 2008 Mar 15;121(Pt 6):727-35 PMID: 18322269
  158. SOX-partner code for cell specification: Regulatory target selection and underlying molecular mechanisms.
    Int J Biochem Cell Biol. 2010 Mar;42(3):391-9 PMID: 19747562
  159. Contact inhibition of locomotion in vivo controls neural crest directional migration.
    Nature. 2008 Dec 18;456(7224):957-61 PMID: 19078960
  160. The mesenchymal-to-epithelial transition in somatic cell reprogramming.
    Curr Opin Genet Dev. 2012 Oct;22(5):423-8 PMID: 23084025
  161. Transcriptional regulation of cell polarity in EMT and cancer.
    Oncogene. 2008 Nov 24;27(55):6958-69 PMID: 19029937
  162. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression.
    Nat Cell Biol. 2000 Feb;2(2):76-83 PMID: 10655586
  163. The putative tumour suppressor microRNA-124 modulates hepatocellular carcinoma cell aggressiveness by repressing ROCK2 and EZH2.
    Gut. 2012 Feb;61(2):278-89 PMID: 21672940
  164. FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak.
    Dev Cell. 2001 Jul;1(1):37-49 PMID: 11703922
  165. The complex world of WNT receptor signalling.
    Nat Rev Mol Cell Biol. 2012 Dec;13(12):767-79 PMID: 23151663
  166. Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development.
    Development. 2006 Apr;133(7):1323-33 PMID: 16510505
  167. miR-9, a MYC/MYCN-activated microRNA, regulates E-cadherin and cancer metastasis.
    Nat Cell Biol. 2010 Mar;12(3):247-56 PMID: 20173740
  168. Endothelial-mesenchymal transition and its contribution to the emergence of stem cell phenotype.
    Semin Cancer Biol. 2012 Oct;22(5-6):379-84 PMID: 22554794
  169. Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition.
    Oncogene. 2007 Nov 22;26(53):7445-56 PMID: 17563753
  170. Transforming growth factor-β2 promotes Snail-mediated endothelial-mesenchymal transition through convergence of Smad-dependent and Smad-independent signalling.
    Biochem J. 2011 Aug 1;437(3):515-20 PMID: 21585337
  171. Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells.
    Am J Pathol. 2003 Oct;163(4):1437-47 PMID: 14507651
  172. The Snail genes as inducers of cell movement and survival: implications in development and cancer.
    Development. 2005 Jul;132(14):3151-61 PMID: 15983400
  173. Diminished matrix metalloproteinase 2 (MMP-2) in ectomesenchyme-derived tissues of the Patch mutant mouse: regulation of MMP-2 by PDGF and effects on mesenchymal cell migration.
    Dev Biol. 1999 Aug 15;212(2):255-63 PMID: 10433819
  174. Snail is required for TGFbeta-induced endothelial-mesenchymal transition of embryonic stem cell-derived endothelial cells.
    J Cell Sci. 2008 Oct 15;121(Pt 20):3317-24 PMID: 18796538
  175. Immunoediting of cancers may lead to epithelial to mesenchymal transition.
    J Immunol. 2006 Aug 1;177(3):1526-33 PMID: 16849459
  176. Emergence of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin axis in transforming growth factor-β-induced epithelial-mesenchymal transition.
    Cells Tissues Organs. 2011;193(1-2):8-22 PMID: 21041997
  177. Life at the leading edge.
    Cell. 2011 Jun 24;145(7):1012-22 PMID: 21703446
  178. Cellular integrity plus: organelle-related and protein-targeting functions of intermediate filaments.
    Trends Cell Biol. 2005 Nov;15(11):608-17 PMID: 16202602
  179. Endothelial-to-mesenchymal transition contributes to cardiac fibrosis.
    Nat Med. 2007 Aug;13(8):952-61 PMID: 17660828
  180. p53 controls cancer cell invasion by inducing the MDM2-mediated degradation of Slug.
    Nat Cell Biol. 2009 Jun;11(6):694-704 PMID: 19448627
  181. IL-6 promotes head and neck tumor metastasis by inducing epithelial-mesenchymal transition via the JAK-STAT3-SNAIL signaling pathway.
    Mol Cancer Res. 2011 Dec;9(12):1658-67 PMID: 21976712
  182. Regulatory networks defining EMT during cancer initiation and progression.
    Nat Rev Cancer. 2013 Feb;13(2):97-110 PMID: 23344542
  183. TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-beta.
    Mol Cell. 2008 Sep 26;31(6):918-24 PMID: 18922473
  184. Transforming growth factor-β-induced epithelial-mesenchymal transition facilitates epidermal growth factor-dependent breast cancer progression.
    Oncogene. 2010 Dec 9;29(49):6485-98 PMID: 20802523
  185. Activation of FOXO3a by the green tea polyphenol epigallocatechin-3-gallate induces estrogen receptor alpha expression reversing invasive phenotype of breast cancer cells.
    Cancer Res. 2007 Jun 15;67(12):5763-70 PMID: 17575143
  186. Ectodermal Wnt function as a neural crest inducer.
    Science. 2002 Aug 2;297(5582):848-51 PMID: 12161657
  187. Mesenchymal to epithelial transition in development and disease.
    Cells Tissues Organs. 2007;185(1-3):7-19 PMID: 17587803
  188. The transcriptional control of trunk neural crest induction, survival, and delamination.
    Dev Cell. 2005 Feb;8(2):179-92 PMID: 15691760
  189. Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6686-91 PMID: 11390996
  190. Notch and epithelial-mesenchyme transition in development and tumor progression: another turn of the screw.
    Cell Cycle. 2004 Jun;3(6):718-21 PMID: 15197341
  191. Role of Cripto-1 during epithelial-to-mesenchymal transition in development and cancer.
    Am J Pathol. 2012 Jun;180(6):2188-200 PMID: 22542493
  192. Sclerotome development and morphogenesis: when experimental embryology meets genetics.
    Int J Dev Biol. 2005;49(2-3):301-8 PMID: 15906245
  193. Epithelial-mesenchymal transitions in development and disease.
    Cell. 2009 Nov 25;139(5):871-90 PMID: 19945376
  194. Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression.
    Nat Rev Cancer. 2005 Sep;5(9):744-9 PMID: 16148886
  195. An epithelial scatter factor released by embryo fibroblasts.
    J Cell Sci. 1985 Aug;77:209-23 PMID: 3841349
  196. Regulation of leading edge microtubule and actin dynamics downstream of Rac1.
    J Cell Biol. 2003 Jun 9;161(5):845-51 PMID: 12796474
  197. Epithelial mesenchymal transition is a characteristic of hyperplasias and tumors in mammary gland from MMTV-Cripto-1 transgenic mice.
    J Cell Physiol. 2004 Nov;201(2):266-76 PMID: 15334661
  198. Snail and E47 repressors of E-cadherin induce distinct invasive and angiogenic properties in vivo.
    J Cell Sci. 2004 Jun 1;117(Pt 13):2827-39 PMID: 15169839
  199. An EMT-driven alternative splicing program occurs in human breast cancer and modulates cellular phenotype.
    PLoS Genet. 2011 Aug;7(8):e1002218 PMID: 21876675
  200. Pak1 phosphorylation of snail, a master regulator of epithelial-to-mesenchyme transition, modulates snail's subcellular localization and functions.
    Cancer Res. 2005 Apr 15;65(8):3179-84 PMID: 15833848
  201. Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins.
    EMBO J. 2003 May 15;22(10):2453-62 PMID: 12743039
  202. Molecular pathways regulating EGF-induced epithelio-mesenchymal transition in human ovarian surface epithelium.
    Am J Physiol Cell Physiol. 2006 Jun;290(6):C1532-42 PMID: 16394028
  203. Association of the HGF/SF receptor, c-met, with the cell-surface adhesion molecule, E-cadherin, and catenins in human tumor cells.
    Biochem Biophys Res Commun. 1999 Aug 2;261(2):406-11 PMID: 10425198
  204. HMGA2 maintains oncogenic RAS-induced epithelial-mesenchymal transition in human pancreatic cancer cells.
    Am J Pathol. 2009 Mar;174(3):854-68 PMID: 19179606
  205. Zeppo1 is a novel metastasis promoter that represses E-cadherin expression and regulates p120-catenin isoform expression and localization.
    Genes Dev. 2011 Mar 1;25(5):471-84 PMID: 21317240
  206. Epithelial-mesenchymal transition process in human embryonic stem cells cultured in feeder-free conditions.
    Mol Hum Reprod. 2007 Jan;13(1):21-32 PMID: 17090644
  207. Phosphorylation of serine 68 of Twist1 by MAPKs stabilizes Twist1 protein and promotes breast cancer cell invasiveness.
    Cancer Res. 2011 Jun 1;71(11):3980-90 PMID: 21502402
  208. TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition.
    Mol Biol Cell. 2005 Apr;16(4):1987-2002 PMID: 15689496
  209. Concurrent suppression of integrin alpha5, radixin, and RhoA phenocopies the effects of miR-31 on metastasis.
    Cancer Res. 2010 Jun 15;70(12):5147-54 PMID: 20530680
  210. Early events in cell adhesion and polarity during epithelial-mesenchymal transition.
    J Cell Sci. 2012 Oct 1;125(Pt 19):4417-22 PMID: 23165231
  211. Cellular mechanisms of tissue fibrosis. 1. Common and organ-specific mechanisms associated with tissue fibrosis.
    Am J Physiol Cell Physiol. 2013 Feb 1;304(3):C216-25 PMID: 23255577
  212. The Müllerian duct: recent insights into its development and regression.
    Sex Dev. 2007;1(5):271-8 PMID: 18391537
  213. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1.
    Nat Cell Biol. 2008 May;10(5):593-601 PMID: 18376396
  214. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition.
    J Cell Biol. 2006 Jul 17;174(2):175-83 PMID: 16831886
  215. Epithelial-mesenchymal transition: general principles and pathological relevance with special emphasis on the role of matrix metalloproteinases.
    Cold Spring Harb Perspect Biol. 2012 Feb 01;4(2): PMID: 22300978
  216. Upregulation of MMP-9 in MDCK epithelial cell line in response to expression of the Snail transcription factor.
    J Cell Sci. 2005 Aug 1;118(Pt 15):3371-85 PMID: 16079281
  217. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition.
    Nat Cell Biol. 2004 Oct;6(10):931-40 PMID: 15448698
  218. miR-34 and SNAIL form a double-negative feedback loop to regulate epithelial-mesenchymal transitions.
    Cell Cycle. 2011 Dec 15;10(24):4256-71 PMID: 22134354
  219. The miR-106b-25 cluster targets Smad7, activates TGF-β signaling, and induces EMT and tumor initiating cell characteristics downstream of Six1 in human breast cancer.
    Oncogene. 2012 Dec 13;31(50):5162-71 PMID: 22286770
  220. Nuclear overexpression of the oncoprotein beta-catenin in colorectal cancer is localized predominantly at the invasion front.
    Pathol Res Pract. 1998;194(10):701-4 PMID: 9820866
  221. Antagonistic SR proteins regulate alternative splicing of tumor-related Rac1b downstream of the PI3-kinase and Wnt pathways.
    Hum Mol Genet. 2009 Oct 1;18(19):3696-707 PMID: 19602482
  222. Remodeling epithelial cell organization: transitions between front-rear and apical-basal polarity.
    Cold Spring Harb Perspect Biol. 2009 Jul;1(1):a000513 PMID: 20066074
  223. Phosphatidylinositol 3-kinase function is required for transforming growth factor beta-mediated epithelial to mesenchymal transition and cell migration.
    J Biol Chem. 2000 Nov 24;275(47):36803-10 PMID: 10969078
  224. The RhoA activator GEF-H1/Lfc is a transforming growth factor-beta target gene and effector that regulates alpha-smooth muscle actin expression and cell migration.
    Mol Biol Cell. 2010 Mar 15;21(6):860-70 PMID: 20089843
  225. miRNA-29b suppresses prostate cancer metastasis by regulating epithelial-mesenchymal transition signaling.
    Mol Cancer Ther. 2012 May;11(5):1166-73 PMID: 22402125
  226. Requirement for Wnt3 in vertebrate axis formation.
    Nat Genet. 1999 Aug;22(4):361-5 PMID: 10431240
  227. Functional cooperation between Snail1 and twist in the regulation of ZEB1 expression during epithelial to mesenchymal transition.
    J Biol Chem. 2011 Apr 8;286(14):12024-32 PMID: 21317430
  228. TGF-(beta) type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells.
    J Cell Sci. 1999 Dec;112 ( Pt 24):4557-68 PMID: 10574705
  229. Slug and Sox9 cooperatively determine the mammary stem cell state.
    Cell. 2012 Mar 2;148(5):1015-28 PMID: 22385965
  230. Signaling mechanisms of neurite outgrowth induced by the cell adhesion molecules NCAM and N-cadherin.
    Cell Mol Life Sci. 2008 Nov;65(23):3809-21 PMID: 18791849
  231. Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition.
    J Cell Biol. 2005 Dec 19;171(6):1023-34 PMID: 16365168
  232. Cadherin junctions and their cytoskeleton(s).
    Curr Opin Cell Biol. 2013 Feb;25(1):39-46 PMID: 23127608
  233. TGF-β signaling and epithelial-mesenchymal transition in cancer progression.
    Curr Opin Oncol. 2013 Jan;25(1):76-84 PMID: 23197193
  234. TGFbeta3 inhibits E-cadherin gene expression in palate medial-edge epithelial cells through a Smad2-Smad4-LEF1 transcription complex.
    J Cell Sci. 2007 May 1;120(Pt 9):1646-53 PMID: 17452626
  235. P68 RNA helicase mediates PDGF-induced epithelial mesenchymal transition by displacing Axin from beta-catenin.
    Cell. 2006 Oct 6;127(1):139-55 PMID: 17018282
  236. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment.
    Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10356-61 PMID: 11526241
  237. Direct regulation of TWIST by HIF-1alpha promotes metastasis.
    Nat Cell Biol. 2008 Mar;10(3):295-305 PMID: 18297062
  238. TGF-beta receptor-activated p38 MAP kinase mediates Smad-independent TGF-beta responses.
    EMBO J. 2002 Jul 15;21(14):3749-59 PMID: 12110587
  239. Epidermal growth factor receptor cooperates with signal transducer and activator of transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression.
    Cancer Res. 2007 Oct 1;67(19):9066-76 PMID: 17909010
  240. Mechanisms of motility in metastasizing cells.
    Mol Cancer Res. 2010 May;8(5):629-42 PMID: 20460404
  241. A novel mechanism by which hepatocyte growth factor blocks tubular epithelial to mesenchymal transition.
    J Am Soc Nephrol. 2005 Jan;16(1):68-78 PMID: 15537870
  242. Protein kinase D1 suppresses epithelial-to-mesenchymal transition through phosphorylation of snail.
    Cancer Res. 2010 Oct 15;70(20):7810-9 PMID: 20940406
  243. Myocardin enhances Smad3-mediated transforming growth factor-beta1 signaling in a CArG box-independent manner: Smad-binding element is an important cis element for SM22alpha transcription in vivo.
    Circ Res. 2005 Nov 11;97(10):983-91 PMID: 16224064
  244. The transcriptional repressor Snail promotes mammary tumor recurrence.
    Cancer Cell. 2005 Sep;8(3):197-209 PMID: 16169465
  245. Notch signaling at a glance.
    J Cell Sci. 2013 May 15;126(Pt 10):2135-40 PMID: 23729744
  246. A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells.
    Mol Cell. 2003 Apr;11(4):915-26 PMID: 12718878
  247. Fate-determining mechanisms in epithelial-myofibroblast transition: major inhibitory role for Smad3.
    J Cell Biol. 2010 Feb 8;188(3):383-99 PMID: 20123992
  248. Regulation of beta 4-integrin expression by epigenetic modifications in the mammary gland and during the epithelial-to-mesenchymal transition.
    J Cell Sci. 2009 Jul 15;122(Pt 14):2473-80 PMID: 19549682
  249. Roles of TGF-beta in hepatic fibrosis.
    Front Biosci. 2002 Apr 01;7:d793-807 PMID: 11897555
  250. Dissecting direct reprogramming through integrative genomic analysis.
    Nature. 2008 Jul 3;454(7200):49-55 PMID: 18509334
  251. Inverse association between miR-194 expression and tumor invasion in gastric cancer.
    Ann Surg Oncol. 2012 Jul;19 Suppl 3:S509-17 PMID: 21845495
  252. TGF-β-induced mesenchymal transition of MS-1 endothelial cells requires Smad-dependent cooperative activation of Rho signals and MRTF-A.
    J Biochem. 2012 Feb;151(2):145-56 PMID: 21984612
  253. miR-661 expression in SNAI1-induced epithelial to mesenchymal transition contributes to breast cancer cell invasion by targeting Nectin-1 and StarD10 messengers.
    Oncogene. 2010 Aug 5;29(31):4436-48 PMID: 20543867
  254. β-catenin and Smad3 regulate the activity and stability of myocardin-related transcription factor during epithelial-myofibroblast transition.
    Mol Biol Cell. 2011 Dec;22(23):4472-85 PMID: 21965288
  255. MiR-1 and miR-200 inhibit EMT via Slug-dependent and tumorigenesis via Slug-independent mechanisms.
    Oncogene. 2013 Jan 17;32(3):296-306 PMID: 22370643
  256. GATA switches as developmental drivers.
    J Biol Chem. 2010 Oct 8;285(41):31087-93 PMID: 20670937
  257. Notch signaling mediates hypoxia-induced tumor cell migration and invasion.
    Proc Natl Acad Sci U S A. 2008 Apr 29;105(17):6392-7 PMID: 18427106
  258. RSK is a principal effector of the RAS-ERK pathway for eliciting a coordinate promotile/invasive gene program and phenotype in epithelial cells.
    Mol Cell. 2009 Aug 28;35(4):511-22 PMID: 19716794
  259. Epithelial-mesenchymal transitions: insights from development.
    Development. 2012 Oct;139(19):3471-86 PMID: 22949611
  260. Notch signaling: targeting cancer stem cells and epithelial-to-mesenchymal transition.
    Onco Targets Ther. 2013 Sep 06;6:1249-59 PMID: 24043949
  261. Vascular endothelial growth factor-A stimulates Snail expression in breast tumor cells: implications for tumor progression.
    Exp Cell Res. 2008 Aug 1;314(13):2448-53 PMID: 18554584
  262. Activation of the Erk pathway is required for TGF-beta1-induced EMT in vitro.
    Neoplasia. 2004 Sep-Oct;6(5):603-10 PMID: 15548370
  263. TGF-β regulates isoform switching of FGF receptors and epithelial-mesenchymal transition.
    EMBO J. 2011 Feb 16;30(4):783-95 PMID: 21224849
  264. Modulation of several waves of gene expression during FGF-1 induced epithelial-mesenchymal transition of carcinoma cells.
    J Cell Biochem. 2008 Jun 1;104(3):826-39 PMID: 18189245
  265. MiR-365 regulates lung cancer and developmental gene thyroid transcription factor 1.
    Cell Cycle. 2012 Jan 1;11(1):177-86 PMID: 22185756
  266. Transforming growth factor-beta and epidermal growth factor synergistically stimulate epithelial to mesenchymal transition (EMT) through a MEK-dependent mechanism in primary cultured pig thyrocytes.
    J Cell Sci. 2002 Nov 15;115(Pt 22):4227-36 PMID: 12376555
  267. Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail.
    EMBO J. 2006 Aug 9;25(15):3534-45 PMID: 16858414
  268. Regulation of epithelial-mesenchymal and mesenchymal-epithelial transitions by microRNAs.
    Curr Opin Cell Biol. 2013 Apr;25(2):200-7 PMID: 23434068
  269. The type I TGF-beta receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner.
    Nat Cell Biol. 2008 Oct;10(10):1199-207 PMID: 18758450
  270. An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition.
    EMBO J. 2010 Oct 6;29(19):3286-300 PMID: 20711167
  271. TGF-beta and epithelial-to-mesenchymal transitions.
    Oncogene. 2005 Aug 29;24(37):5764-74 PMID: 16123809
  272. Integrin-mediated activation of latent transforming growth factor beta.
    Cancer Metastasis Rev. 2005 Sep;24(3):395-402 PMID: 16258727
  273. Cadherins in collective cell migration of mesenchymal cells.
    Curr Opin Cell Biol. 2012 Oct;24(5):677-84 PMID: 22944726
  274. Interaction with Suv39H1 is critical for Snail-mediated E-cadherin repression in breast cancer.
    Oncogene. 2013 Mar 14;32(11):1351-62 PMID: 22562246
  275. JNK mediates TGF-beta1-induced epithelial mesenchymal transdifferentiation of mouse transformed keratinocytes.
    FEBS Lett. 2006 Oct 2;580(22):5385-91 PMID: 16989819
Article Info
Journal
Nature reviews. Molecular cell biology
Abbr.
Nat Rev Mol Cell Biol
ISSN
1471-0080
DOI
10.1038/nrm3758
Published
2014-03-00
Pages
178-96
Language
English
Region
England
NLM ID
100962782
PMCID
PMC4240281
Subset
IM
Grants
NCI NIH HHS · R01 CA136690 · United States
External Links
PubMed source DOI: 10.1038/nrm3758 PMC Full Text View journal details
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