Home LiteratureArticle Details
PMID: 25566498 Published · epublish English Journal Article Review

Crosstalk of Oncogenic Signaling Pathways during Epithelial-Mesenchymal Transition.

Frontiers in oncology ·Vol. 4 ·2014-00-00 ·Pages 358

Lindsey S, Langhans SA

Abstract

Epithelial-mesenchymal transition (EMT) and cell transformation have been well-documented in multiple cancer cell models and are believed to be one of the earliest events in tumor progression. Genetic and epigenetic modifications shift cells toward either end of the EMT spectrum, and can be influenced by the microenvironment surrounding a tumor. EMT and mesenchymal-epithelial transition are critical to normal function and development and an intricate network of transcription factors and transcriptional regulators tightly regulates these processes. As evidenced in normal and transformed cell lines, many signaling pathways trigger EMT during development and differentiation. The signaling pathways include those triggered by different members of the transforming growth factor superfamily, epidermal growth factor, fibroblast growth factor, hepatocyte growth factor, hypoxia-inducible factor, Wnt, Notch, and many others. Functional redundancies allow cells to undergo EMT even if these key transcriptional regulators are lacking, but these same redundancies also make these pathways particularly susceptible to gain-of-function mutations or constitutive signal activation; the "forced" transition toward either a mesenchymal or epithelial phenotype.

Keywords
epithelial–mesenchymal transition invasion microenvironment motility transforming growth factor-beta
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Lindsey Stephan
Nemours Center for Childhood Cancer Research, Alfred I. duPont Hospital for Children , Wilmington, DE , USA.
Langhans Sigrid A
Nemours Center for Childhood Cancer Research, Alfred I. duPont Hospital for Children , Wilmington, DE , USA.
References (115)
115 references, click to expand
  1. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells.
    Immunity. 2009 Jan 16;30(1):155-67 PMID: 19144320
  2. 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
  3. Estrogen, DNA damage and mutations.
    Mutat Res. 1999 Mar 8;424(1-2):107-15 PMID: 10064854
  4. Src-mediated regulation of E-cadherin and EMT in pancreatic cancer.
    Front Biosci (Landmark Ed). 2012 Jun 01;17:2059-69 PMID: 22652764
  5. Epithelial to mesenchymal transition markers expressed in circulating tumour cells of early and metastatic breast cancer patients.
    Breast Cancer Res. 2011 Jun 10;13(3):R59 PMID: 21663619
  6. Notch1 oncoprotein antagonizes TGF-beta/Smad-mediated cell growth suppression via sequestration of coactivator p300.
    Cancer Sci. 2005 May;96(5):274-82 PMID: 15904468
  7. Notch Signaling Molecules Activate TGF- β in Rat Mesangial Cells under High Glucose Conditions.
    J Diabetes Res. 2013;2013:979702 PMID: 23691527
  8. Oncogenic roles of EMT-inducing transcription factors.
    Nat Cell Biol. 2014 Jun;16(6):488-94 PMID: 24875735
  9. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis.
    Cell. 1999 Jul 23;98(2):137-46 PMID: 10428026
  10. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation.
    Cell Stem Cell. 2009 Jan 9;4(1):80-93 PMID: 19128795
  11. Crosstalk between vascular endothelial growth factor, notch, and transforming growth factor-beta in vascular morphogenesis.
    Circ Res. 2008 Mar 28;102(6):637-52 PMID: 18369162
  12. Is estradiol a genotoxic mutagenic carcinogen?
    Endocr Rev. 2000 Feb;21(1):40-54 PMID: 10696569
  13. 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
  14. Blockade of epidermal growth factor receptor signaling in tumor cells and tumor-associated endothelial cells for therapy of androgen-independent human prostate cancer growing in the bone of nude mice.
    Clin Cancer Res. 2003 Mar;9(3):1200-10 PMID: 12631626
  15. The histone methyltransferase MMSET/WHSC1 activates TWIST1 to promote an epithelial-mesenchymal transition and invasive properties of prostate cancer.
    Oncogene. 2013 Jun 6;32(23 ):2882-90 PMID: 22797064
  16. Systemic analysis of TGFbeta proteomics revealed involvement of Plag1/CNK1/RASSF1A/Src network in TGFbeta1-dependent activation of Erk1/2 and cell proliferation.
    Proteomics. 2008 Nov;8(21):4507-20 PMID: 18821524
  17. The role of epithelial-mesenchymal transition in cancer pathology.
    Pathology. 2007 Jun;39(3):305-18 PMID: 17558857
  18. HDAC6 regulates epidermal growth factor receptor (EGFR) endocytic trafficking and degradation in renal epithelial cells.
    PLoS One. 2012;7(11):e49418 PMID: 23152903
  19. Crosstalk between breast cancer stem cells and metastatic niche: emerging molecular metastasis pathway?
    Tumour Biol. 2013 Aug;34(4):2019-30 PMID: 23686802
  20. 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
  21. TGFbeta in Cancer.
    Cell. 2008 Jul 25;134(2):215-30 PMID: 18662538
  22. 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
  23. Wnt/β-catenin signaling enhances hypoxia-induced epithelial-mesenchymal transition in hepatocellular carcinoma via crosstalk with hif-1α signaling.
    Carcinogenesis. 2013 May;34(5):962-73 PMID: 23358852
  24. Hypoxia-induced dedifferentiation of tumor cells--a mechanism behind heterogeneity and aggressiveness of solid tumors.
    Semin Cell Dev Biol. 2005 Aug-Oct;16(4-5):554-63 PMID: 16144692
  25. The role of hypoxia-induced factors in tumor progression.
    Oncologist. 2004;9 Suppl 5:10-7 PMID: 15591418
  26. Linking DNA methylation and histone modification: patterns and paradigms.
    Nat Rev Genet. 2009 May;10(5):295-304 PMID: 19308066
  27. Inflammation: a driving force speeds cancer metastasis.
    Cell Cycle. 2009 Oct 15;8(20):3267-73 PMID: 19770594
  28. 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
  29. The epithelial-mesenchymal transition: new insights in signaling, development, and disease.
    J Cell Biol. 2006 Mar 27;172(7):973-81 PMID: 16567498
  30. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis.
    Cell. 2004 Jun 25;117(7):927-39 PMID: 15210113
  31. TGFbeta/TNF(alpha)-mediated epithelial-mesenchymal transition generates breast cancer stem cells with a claudin-low phenotype.
    Cancer Res. 2011 Jul 1;71(13):4707-19 PMID: 21555371
  32. 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
  33. Activation of EGFR promotes squamous carcinoma SCC10A cell migration and invasion via inducing EMT-like phenotype change and MMP-9-mediated degradation of E-cadherin.
    J Cell Biochem. 2011 Sep;112(9):2508-17 PMID: 21557297
  34. The Tumor-Promoting Flow of Cells Into, Within and Out of the Tumor Site: Regulation by the Inflammatory Axis of TNFα and Chemokines.
    Cancer Microenviron. 2012 Aug;5(2):151-64 PMID: 22190050
  35. 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
  36. A bivalent chromatin structure marks key developmental genes in embryonic stem cells.
    Cell. 2006 Apr 21;125(2):315-26 PMID: 16630819
  37. IGF-1R/epithelial-to-mesenchymal transition (EMT) crosstalk suppresses the erlotinib-sensitizing effect of EGFR exon 19 deletion mutations.
    Sci Rep. 2013;3:2560 PMID: 23994953
  38. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2.
    Genes Dev. 2008 Apr 1;22(7):894-907 PMID: 18381893
  39. MicroRNAs as regulators of epithelial-mesenchymal transition.
    Cell Cycle. 2008 Oct;7(20):3112-8 PMID: 18927505
  40. Turning it up a Notch: cross-talk between TGF beta and Notch signaling.
    Bioessays. 2005 Feb;27(2):115-8 PMID: 15666349
  41. Hallmarks of cancer: the next generation.
    Cell. 2011 Mar 4;144(5):646-74 PMID: 21376230
  42. A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions.
    J Biol Chem. 2001 Jul 20;276(29):27424-31 PMID: 11309385
  43. Epithelial-mesenchymal transition (EMT) induced by TNF-α requires AKT/GSK-3β-mediated stabilization of snail in colorectal cancer.
    PLoS One. 2013;8(2):e56664 PMID: 23431386
  44. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression.
    Nat Cell Biol. 2000 Feb;2(2):76-83 PMID: 10655586
  45. Platelets from mice lacking the aryl hydrocarbon receptor exhibit defective collagen-dependent signaling.
    J Thromb Haemost. 2014;12(3):383-94 PMID: 24410994
  46. TGF-β/Smad3 inhibit vascular smooth muscle cell apoptosis through an autocrine signaling mechanism involving VEGF-A.
    Cell Death Dis. 2014 Jul 10;5:e1317 PMID: 25010983
  47. Molecular mechanisms of epithelial-mesenchymal transition.
    Nat Rev Mol Cell Biol. 2014 Mar;15(3):178-96 PMID: 24556840
  48. Notch signaling is necessary for epithelial growth arrest by TGF-beta.
    J Cell Biol. 2007 Feb 26;176(5):695-707 PMID: 17325209
  49. Genetic susceptibility to cancer from exogenous and endogenous exposures.
    J Cell Biochem Suppl. 1996;25:15-22 PMID: 9027593
  50. A novel lung metastasis signature links Wnt signaling with cancer cell self-renewal and epithelial-mesenchymal transition in basal-like breast cancer.
    Cancer Res. 2009 Jul 1;69(13):5364-73 PMID: 19549913
  51. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability.
    Nature. 2005 Jul 7;436(7047):123-7 PMID: 16001073
  52. An NF-kappaB and slug regulatory loop active in early vertebrate mesoderm.
    PLoS One. 2006 Dec 27;1:e106 PMID: 17205110
  53. The epithelial-mesenchymal transition generates cells with properties of stem cells.
    Cell. 2008 May 16;133(4):704-15 PMID: 18485877
  54. Looking back, to the future of circulating tumor cells.
    Pharmacol Ther. 2014 Jun;142(3):271-80 PMID: 24362084
  55. Wnt/beta-catenin signaling: components, mechanisms, and diseases.
    Dev Cell. 2009 Jul;17(1):9-26 PMID: 19619488
  56. Hypoxia-inducible factor-1alpha obstructs a Wnt signaling pathway by inhibiting the hARD1-mediated activation of beta-catenin.
    Cancer Res. 2008 Jul 1;68(13):5177-84 PMID: 18593917
  57. Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells.
    Cell Stem Cell. 2007 Sep 13;1(3):299-312 PMID: 18371364
  58. The Snail genes as inducers of cell movement and survival: implications in development and cancer.
    Development. 2005 Jul;132(14 ):3151-61 PMID: 15983400
  59. Cytokines in human breast cancer: IL-1alpha and IL-1beta expression.
    Oncol Rep. 1999 Jan-Feb;6(1):65-70 PMID: 9864403
  60. EGF-receptor signaling and epithelial-mesenchymal transition in human carcinomas.
    Front Biosci (Schol Ed). 2012 Jan 01;4:671-84 PMID: 22202084
  61. Hypoxia--a key regulatory factor in tumour growth.
    Nat Rev Cancer. 2002 Jan;2(1):38-47 PMID: 11902584
  62. Epidermal growth factor (EGF)-enhanced vascular cell adhesion molecule-1 (VCAM-1) expression promotes macrophage and glioblastoma cell interaction and tumor cell invasion.
    J Biol Chem. 2013 Nov 1;288(44):31488-95 PMID: 24045955
  63. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells.
    Nature. 2007 Aug 2;448(7153):553-60 PMID: 17603471
  64. E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex.
    Gastroenterology. 2009 Jul;137(1):361-71, 371.e1-5 PMID: 19362090
  65. Overexpression of HER2 (erbB2) in human breast epithelial cells unmasks transforming growth factor beta-induced cell motility.
    J Biol Chem. 2004 Jun 4;279(23 ):24505-13 PMID: 15044465
  66. MicroRNA control of epithelial-mesenchymal transition in cancer stem cells.
    Int J Cancer. 2014 Sep 1;135(5):1019-27 PMID: 24500893
  67. ErbB receptors: directing key signaling networks throughout life.
    Annu Rev Pharmacol Toxicol. 2004;44:195-217 PMID: 14744244
  68. MicroRNAs: genomics, biogenesis, mechanism, and function.
    Cell. 2004 Jan 23;116(2):281-97 PMID: 14744438
  69. Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers.
    Mol Cancer Res. 2011 Aug;9(8):997-1007 PMID: 21665936
  70. 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
  71. Oncogene-induced basement membrane invasiveness in human mammary epithelial cells.
    Clin Exp Metastasis. 1994 May;12(3):181-94 PMID: 8194193
  72. Tumor hypoxia blocks Wnt processing and secretion through the induction of endoplasmic reticulum stress.
    Mol Cell Biol. 2008 Dec;28(23 ):7212-24 PMID: 18824543
  73. Hypoxia-induced β-catenin downregulation involves p53-dependent activation of Siah-1.
    Cancer Sci. 2011 Jul;102(7):1322-8 PMID: 21466614
  74. Hyperoxic treatment induces mesenchymal-to-epithelial transition in a rat adenocarcinoma model.
    PLoS One. 2009 Jul 28;4(7):e6381 PMID: 19636430
  75. Epithelial-mesenchymal transition and its role in the pathogenesis of colorectal cancer.
    Asian Pac J Cancer Prev. 2013;14 (5):2689-98 PMID: 23803016
  76. Cross talk of signals between EGFR and IL-6R through JAK2/STAT3 mediate epithelial-mesenchymal transition in ovarian carcinomas.
    Br J Cancer. 2009 Jan 13;100(1):134-44 PMID: 19088723
  77. Genome-scale epigenetic reprogramming during epithelial-to-mesenchymal transition.
    Nat Struct Mol Biol. 2011 Jul 03;18(8):867-74 PMID: 21725293
  78. Dnmt3a and Dnmt3b have overlapping and distinct functions in hematopoietic stem cells.
    Cell Stem Cell. 2014 Sep 4;15(3):350-64 PMID: 25130491
  79. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling.
    Science. 2007 May 18;316(5827):1039-43 PMID: 17463250
  80. Biomarkers for epithelial-mesenchymal transitions.
    J Clin Invest. 2009 Jun;119(6):1429-37 PMID: 19487819
  81. Epigenetic coordination of signaling pathways during the epithelial-mesenchymal transition.
    Epigenetics Chromatin. 2013 Sep 02;6(1):28 PMID: 24004852
  82. Hypoxia and hypoxia-inducible factors: master regulators of metastasis.
    Clin Cancer Res. 2010 Dec 15;16(24):5928-35 PMID: 20962028
  83. Metastasis: from dissemination to organ-specific colonization.
    Nat Rev Cancer. 2009 Apr;9(4):274-84 PMID: 19308067
  84. Epithelial-mesenchymal transition induced by TNF-α requires NF-κB-mediated transcriptional upregulation of Twist1.
    Cancer Res. 2012 Mar 1;72 (5):1290-300 PMID: 22253230
  85. Targeting hypoxia in cancer therapy.
    Nat Rev Cancer. 2011 Jun;11(6):393-410 PMID: 21606941
  86. Global profiling of histone and DNA methylation reveals epigenetic-based regulation of gene expression during epithelial to mesenchymal transition in prostate cells.
    BMC Genomics. 2010 Nov 25;11:669 PMID: 21108828
  87. The role of angiogenesis in tumor growth.
    Semin Cancer Biol. 1992 Apr;3(2):65-71 PMID: 1378311
  88. Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia.
    Nat Cell Biol. 2007 Feb;9(2):210-7 PMID: 17220880
  89. Tumor stroma and regulation of cancer development.
    Annu Rev Pathol. 2006;1:119-50 PMID: 18039110
  90. Genome-wide profiling of histone h3 lysine 4 and lysine 27 trimethylation reveals an epigenetic signature in prostate carcinogenesis.
    PLoS One. 2009;4(3):e4687 PMID: 19262738
  91. The snail superfamily of zinc-finger transcription factors.
    Nat Rev Mol Cell Biol. 2002 Mar;3(3):155-66 PMID: 11994736
  92. A mechanism of repression of TGFbeta/ Smad signaling by oncogenic Ras.
    Genes Dev. 1999 Apr 1;13(7):804-16 PMID: 10197981
  93. Wnt signalling in stem cells and cancer.
    Nature. 2005 Apr 14;434(7035):843-50 PMID: 15829953
  94. Extracellular matrix proteins regulate epithelial-mesenchymal transition in mammary epithelial cells.
    Differentiation. 2013 Oct;86(3):126-32 PMID: 23660532
  95. Inactivation of TGF-β signaling and loss of PTEN cooperate to induce colon cancer in vivo.
    Oncogene. 2014 Mar 20;33(12):1538-47 PMID: 23604118
  96. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells.
    Cell Stem Cell. 2007 Sep 13;1(3):286-98 PMID: 18371363
  97. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors.
    J Cell Sci. 2003 Feb 1;116(Pt 3):499-511 PMID: 12508111
  98. MicroRNA-138 suppresses epithelial-mesenchymal transition in squamous cell carcinoma cell lines.
    Biochem J. 2011 Nov 15;440(1):23-31 PMID: 21770894
  99. Epithelial-mesenchymal transition markers expressed in circulating tumor cells in hepatocellular carcinoma patients with different stages of disease.
    Cell Death Dis. 2013 Oct 03;4:e831 PMID: 24091674
  100. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis.
    Cancer Cell. 2006 Nov;10(5):437-49 PMID: 17097565
  101. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease.
    J Clin Invest. 2009 Jun;119(6):1438-49 PMID: 19487820
  102. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma.
    Cancer. 2005 Apr 15;103(8):1631-43 PMID: 15742334
  103. Tumorigenesis: Twist1 links EMT to self-renewal.
    Nat Cell Biol. 2010 Oct;12 (10 ):924-5 PMID: 20885418
  104. Systemic inflammation increases cancer cell adhesion to hepatic sinusoids by neutrophil mediated mechanisms.
    Int J Cancer. 2009 Sep 15;125(6):1298-305 PMID: 19431213
  105. Epithelial-mesenchymal transitions in development and pathologies.
    Curr Opin Cell Biol. 2003 Dec;15(6):740-6 PMID: 14644200
  106. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis.
    Cell. 2006 Jan 27;124(2):263-6 PMID: 16439202
  107. Trail resistance induces epithelial-mesenchymal transition and enhances invasiveness by suppressing PTEN via miR-221 in breast cancer.
    PLoS One. 2014 Jun 06;9(6):e99067 PMID: 24905916
  108. Inflammatory factors of the tumor microenvironment induce plasticity in nontransformed breast epithelial cells: EMT, invasion, and collapse of normally organized breast textures.
    Neoplasia. 2013 Dec;15(12 ):1330-46 PMID: 24403855
  109. The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages.
    Crit Rev Oncol Hematol. 2008 Apr;66(1):1-9 PMID: 17913510
  110. Induction of an epithelial-mesenchymal transition by an in vivo adheron-like complex.
    Dev Biol. 1989 Nov;136(1):118-28 PMID: 2509260
  111. Direct regulation of TWIST by HIF-1alpha promotes metastasis.
    Nat Cell Biol. 2008 Mar;10 (3):295-305 PMID: 18297062
  112. Snail and slug play distinct roles during breast carcinoma progression.
    Clin Cancer Res. 2006 Sep 15;12 (18):5395-402 PMID: 17000672
  113. Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition.
    Bioessays. 2001 Oct;23(10):912-23 PMID: 11598958
  114. Signaling cross-talk between TGF-beta/BMP and other pathways.
    Cell Res. 2009 Jan;19(1):71-88 PMID: 19002158
  115. DNA damage and checkpoint pathways: molecular anatomy and interactions with repair.
    Cell. 1998 Sep 4;94(5):555-8 PMID: 9741620
Article Info
Journal
Frontiers in oncology
Abbr.
Front Oncol
ISSN
2234-943X
Published
2014-00-00
Epub
2014-00-11
Pages
358
Language
English
Region
Switzerland
NLM ID
101568867
PMCID
PMC4263086
Grants
NIGMS NIH HHS · P20 GM103464 · United States
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