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Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer

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Abstract

EMT (epithelial–mesenchymal transition) is a morphogenetic process in which cells loose their epithelial characteristics and gain mesenchymal properties during embryogenesis. Similar processes regulated by similar pathways are recapitulated during tumour progression, endowing cells with invasive properties, thereby contributing to the formation of metastases. In this review, we outline key features of EMT and discuss the evidence for its involvement in the dissemination of tumours. Finally we review the recent literature concerning the mechanisms that regulate EMT in the tumour context, with a particular focus on breast cancer.

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References

  1. Thiery JP (2002) Epithelial–mesenchymal transitions in tumour progression. Nat Rev Cancer 2:442–454

    Article  PubMed  CAS  Google Scholar 

  2. Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial–mesenchymal transitions. Nat Rev Mol Cell Biol 7:131–142

    Article  PubMed  CAS  Google Scholar 

  3. Martin P (1997) Wound healing – aiming for perfect skin regeneration. Science 276:75–81

    Article  PubMed  CAS  Google Scholar 

  4. Kalluri R, Neilson EG (2003) Epithelial–mesenchymal transition and its implications for fibrosis. J Clin Invest 112:1776–1784

    PubMed  CAS  Google Scholar 

  5. Nguyen DX, Massague J (2007) Genetic determinants of cancer metastasis. Nat Rev Genet 8:341–352

    Article  PubMed  CAS  Google Scholar 

  6. Christ B, Ordahl CP (1995) Early stages of chick somite development. Anat Embryol (Berl) 191:381–396

    Article  CAS  Google Scholar 

  7. Takahashi Y, Sato Y, Suetsugu R et al (2005) Mesenchymal-to-epithelial transition during somitic segmentation: a novel approach to studying the roles of Rho family GTPases in morphogenesis. Cells Tissues Organs 179:36–42

    Article  PubMed  CAS  Google Scholar 

  8. Horster MF, Braun GS, Huber SM (1999) Embryonic renal epithelia: induction, nephrogenesis, and cell differentiation. Physiol Rev 79:1157–1191

    PubMed  CAS  Google Scholar 

  9. Vainio S, Lin Y (2002) Coordinating early kidney development: lessons from gene targeting. Nat Rev Genet 3:533–543

    Article  PubMed  CAS  Google Scholar 

  10. Christiansen JJ, Rajasekaran AK (2006) Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 66:8319–8326

    Article  PubMed  CAS  Google Scholar 

  11. Nollet F, Kools P, van Roy F (2000) Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J Mol Biol 299:551–572

    Article  PubMed  CAS  Google Scholar 

  12. Shin K, Fogg VC, Margolis B (2006) Tight junctions and cell polarity. Annu Rev Cell Dev Biol 22:207–235

    Article  PubMed  CAS  Google Scholar 

  13. Yin T, Green KJ (2004) Regulation of desmosome assembly and adhesion. Semin Cell Dev Biol 15:665–677

    PubMed  CAS  Google Scholar 

  14. Aigner K, Dampier B, Descovich L et al (2007) The transcription factor ZEB1 (deltaEF1) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene (Epub ahead of print)

  15. De Craene B, Gilbert B, Stove C et al (2005) The transcription factor snail induces tumor cell invasion through modulation of the epithelial cell differentiation program. Cancer Res 65:6237–6244

    Article  PubMed  Google Scholar 

  16. Ikenouchi J, Matsuda M, Furuse M et al (2003) Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J Cell Sci 116:1959–1967

    Article  PubMed  CAS  Google Scholar 

  17. Moreno-Bueno G, Cubillo E, Sarrio D et al (2006) Genetic profiling of epithelial cells expressing e-cadherin repressors reveals a distinct role for snail, slug, and e47 factors in epithelial–mesenchymal transition. Cancer Res 66:9543–9556

    Article  PubMed  CAS  Google Scholar 

  18. Vandewalle C, Comijn J, De Craene B et al (2005) SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell–cell junctions. Nucleic Acids Res 33:6566–6578

    Article  PubMed  CAS  Google Scholar 

  19. LaGamba D, Nawshad A, Hay ED (2005) Microarray analysis of gene expression during epithelial–mesenchymal transformation. Dev Dyn 234:132–142

    Article  PubMed  CAS  Google Scholar 

  20. Hay ED (2005) The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev Dyn 233:706–720

    Article  PubMed  CAS  Google Scholar 

  21. Andersen H, Mejlvang J, Mahmood S et al (2005) Immediate and delayed effects of E-cadherin inhibition on gene regulation and cell motility in human epidermoid carcinoma cells. Mol Cell Biol 25:9138–9150

    Article  PubMed  CAS  Google Scholar 

  22. Capaldo CT, Macara IG (2007) Depletion of E-cadherin disrupts establishment but not maintenance of cell junctions in Madin-Darby canine kidney epithelial cells. Mol Biol Cell 18:189–200

    Article  PubMed  CAS  Google Scholar 

  23. Neve RM, Chin K, Fridlyand J et al (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10:515–527

    Article  PubMed  CAS  Google Scholar 

  24. Perou CM, Sorlie T, Eisen MB et al (2000) Molecular portraits of human breast tumours. Nature 406:747–752

    Article  PubMed  CAS  Google Scholar 

  25. van de Wetering M, Barker N, Harkes IC et al (2001) Mutant E-cadherin breast cancer cells do not display constitutive Wnt signaling. Cancer Res 61:278–284

    PubMed  Google Scholar 

  26. Ferlicot S, Vincent-Salomon A, Medioni J et al (2004) Wide metastatic spreading in infiltrating lobular carcinoma of the breast. Eur J Cancer 40:336–341

    Article  PubMed  CAS  Google Scholar 

  27. Bierie B, Moses HL (2006) Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer 6:506–520

    Article  PubMed  CAS  Google Scholar 

  28. Blume-Jensen P, Hunter T (2001) Oncogenic kinase signalling. Nature 411:355–365

    Article  PubMed  CAS  Google Scholar 

  29. Bolos V, Grego-Bessa J, de la Pompa JL (2007) Notch signaling in development and cancer. Endocr Rev 28:339–363

    Article  PubMed  CAS  Google Scholar 

  30. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127:469–480

    Article  PubMed  CAS  Google Scholar 

  31. Evangelista M, Tian H, de Sauvage FJ (2006) The hedgehog signaling pathway in cancer. Clin Cancer Res 12:5924–5928

    Article  PubMed  CAS  Google Scholar 

  32. Reya T, Clevers H (2005) Wnt signalling in stem cells and cancer. Nature 434:843–850

    Article  PubMed  CAS  Google Scholar 

  33. Siegel PM, Massague J (2003) Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 3:807–821

    Article  PubMed  CAS  Google Scholar 

  34. Huber MA, Kraut N, Beug H (2005) Molecular requirements for epithelial–mesenchymal transition during tumor progression. Curr Opin Cell Biol 17:548–558

    Article  PubMed  CAS  Google Scholar 

  35. Savagner P (2001) Leaving the neighborhood: molecular mechanisms involved during epithelial–mesenchymal transition. Bioessays 23:912–923

    Article  PubMed  CAS  Google Scholar 

  36. Berx G, Van Roy F (2001) The E-cadherin/catenin complex: an important gatekeeper in breast cancer tumorigenesis and malignant progression. Breast Cancer Res 3:289–293

    Article  PubMed  CAS  Google Scholar 

  37. Cano A, Perez-Moreno MA, Rodrigo I et al (2000) The transcription factor snail controls epithelial–mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2:76–83

    Article  PubMed  CAS  Google Scholar 

  38. Venkov CD, Link AJ, Jennings JL et al (2007) A proximal activator of transcription in epithelial–mesenchymal transition. J Clin Invest 117:482–491

    Article  PubMed  CAS  Google Scholar 

  39. Perez-Moreno MA, Locascio A, Rodrigo I et al (2001) A new role for E12/E47 in the repression of E-cadherin expression and epithelial–mesenchymal transitions. J Biol Chem 276:27424–27431

    Article  PubMed  CAS  Google Scholar 

  40. Mani SA, Yang J, Brooks M et al (2007) Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Proc Natl Acad Sci USA 104:10069–10074

    Article  PubMed  CAS  Google Scholar 

  41. Hartwell KA, Muir B, Reinhardt F et al (2006) The Spemann organizer gene, Goosecoid, promotes tumor metastasis. Proc Natl Acad Sci USA 103:18969–18974

    Article  PubMed  CAS  Google Scholar 

  42. Wu X, Chen H, Parker B et al (2006) HOXB7, a homeodomain protein, is overexpressed in breast cancer and confers epithelial–mesenchymal transition. Cancer Res 66:9527–9534

    Article  PubMed  CAS  Google Scholar 

  43. Comijn J, Berx G, Vermassen P et al (2001) The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 7:1267–1278

    Article  PubMed  CAS  Google Scholar 

  44. Battle MA, Konopka G, Parviz F et al (2006) Hepatocyte nuclear factor 4alpha orchestrates expression of cell adhesion proteins during the epithelial transformation of the developing liver. Proc Natl Acad Sci USA 103:8419–8424

    Article  PubMed  CAS  Google Scholar 

  45. Hajra KM, Chen DY, Fearon ER (2002) The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 62:1613–1618

    PubMed  CAS  Google Scholar 

  46. Yang J, Mani SA, Donaher JL et al (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:927–939

    Article  PubMed  CAS  Google Scholar 

  47. Eger A, Aigner K, Sonderegger S et al (2005) DeltaEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 24:2375–2385

    Article  PubMed  CAS  Google Scholar 

  48. Sleeman JP (2000) The lymph node as a bridgehead in the metastatic dissemination of tumors. Recent Results Cancer Res 157:55–81

    PubMed  CAS  Google Scholar 

  49. Peinado H, Marin F, Cubillo E et al (2004) Snail and E47 repressors of E-cadherin induce distinct invasive and angiogenic properties in vivo. J Cell Sci 117:2827–2839

    Article  PubMed  CAS  Google Scholar 

  50. Korsching E, Packeisen J, Liedtke C et al (2005) The origin of vimentin expression in invasive breast cancer: epithelial–mesenchymal transition, myoepithelial histogenesis or histogenesis from progenitor cells with bilinear differentiation potential? J Pathol 206:451–457

    Article  PubMed  CAS  Google Scholar 

  51. Petersen OW, Nielsen HL, Gudjonsson T et al (2003) Epithelial to mesenchymal transition in human breast cancer can provide a nonmalignant stroma. Am J Pathol 162:391–402

    PubMed  CAS  Google Scholar 

  52. Tarin D, Thompson EW, Newgreen DF (2005) The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 65:5996–6000; discussion 6000–5991

    Article  PubMed  CAS  Google Scholar 

  53. De Craene B, van Roy F, Berx G (2005) Unraveling signalling cascades for the Snail family of transcription factors. Cell Signal 17:535–547

    Article  PubMed  Google Scholar 

  54. Valcourt U, Kowanetz M, Niimi H et al (2005) TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial–mesenchymal cell transition. Mol Biol Cell 16:1987–2002

    Article  PubMed  CAS  Google Scholar 

  55. Zavadil J, Bitzer M, Liang D et al (2001) Genetic programs of epithelial cell plasticity directed by transforming growth factor-beta. Proc Natl Acad Sci USA 98:6686–6691

    Article  PubMed  CAS  Google Scholar 

  56. Jechlinger M, Sommer A, Moriggl R et al (2006) Autocrine PDGFR signaling promotes mammary cancer metastasis. J Clin Invest 116:1561–1570

    Article  PubMed  CAS  Google Scholar 

  57. Huber MA, Azoitei N, Baumann B et al (2004) NF-kappaB is essential for epithelial–mesenchymal transition and metastasis in a model of breast cancer progression. J Clin Invest 114:569–581

    PubMed  CAS  Google Scholar 

  58. Dong M, How T, Kirkbride KC et al (2007) The type III TGF-beta receptor suppresses breast cancer progression. J Clin Invest 117:206–217

    Article  PubMed  CAS  Google Scholar 

  59. Eccles SA, Welch DR (2007) Metastasis: recent discoveries and novel treatment strategies. Lancet 369:1742–1757

    Article  PubMed  CAS  Google Scholar 

  60. Karin M (2006) Nuclear factor-kappaB in cancer development and progression. Nature 441:431–436

    Article  PubMed  CAS  Google Scholar 

  61. Moody SE, Perez D, Pan TC et al (2005) The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8:197–209

    Article  PubMed  CAS  Google Scholar 

  62. Wilmut I, Schnieke AE, McWhir J et al (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385:810–813

    Article  PubMed  CAS  Google Scholar 

  63. Slack JM (2007) Metaplasia and transdifferentiation: from pure biology to the clinic. Nat Rev Mol Cell Biol 8:369–378

    Article  PubMed  CAS  Google Scholar 

  64. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    Article  PubMed  CAS  Google Scholar 

  65. Wernig M, Meissner A, Foreman R et al (2007) In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature 448:318–324

    Article  PubMed  CAS  Google Scholar 

  66. Hendrix MJ, Seftor EA, Seftor RE et al (2007) Reprogramming metastatic tumour cells with embryonic microenvironments. Nat Rev Cancer 7:246–255

    Article  PubMed  CAS  Google Scholar 

  67. Xue C, Plieth D, Venkov C et al (2003) The gatekeeper effect of epithelial–mesenchymal transition regulates the frequency of breast cancer metastasis. Cancer Res 63:3386–3394

    PubMed  CAS  Google Scholar 

  68. Derksen PW, Liu X, Saridin F et al (2006) Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 10:437–449

    Article  PubMed  CAS  Google Scholar 

  69. Wicki A, Lehembre F, Wick N et al (2006) Tumor invasion in the absence of epithelial–mesenchymal transition: podoplanin-mediated remodeling of the actin cytoskeleton. Cancer Cell 9:261–272

    Article  PubMed  CAS  Google Scholar 

  70. Friedl P, Hegerfeldt Y, Tusch M (2004) Collective cell migration in morphogenesis and cancer. Int J Dev Biol 48:441–449

    Article  PubMed  CAS  Google Scholar 

  71. Friedl P, Wolf K (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3:362–374

    Article  PubMed  CAS  Google Scholar 

  72. Friedl P, Wolf K (2003) Proteolytic and non-proteolytic migration of tumour cells and leucocytes. Biochem Soc Symp (70):277–285

  73. Wolf K, Friedl P (2006) Molecular mechanisms of cancer cell invasion and plasticity. Br J Dermatol 154(Suppl 1):11–15

    Article  PubMed  CAS  Google Scholar 

  74. Barrallo-Gimeno A, Nieto MA (2005) The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132:3151–3161

    Article  PubMed  CAS  Google Scholar 

  75. Thuault S, Valcourt U, Petersen M et al (2006) Transforming growth factor-beta employs HMGA2 to elicit epithelial–mesenchymal transition. J Cell Biol 174:175–183

    Article  PubMed  CAS  Google Scholar 

  76. Mironchik Y, Winnard PT Jr, Vesuna F et al (2005) Twist overexpression induces in vivo angiogenesis and correlates with chromosomal instability in breast cancer. Cancer Res 65:10801–10809

    Article  PubMed  CAS  Google Scholar 

  77. Bissell MJ, Radisky D (2001) Putting tumours in context. Nat Rev Cancer 1:46–54

    Article  PubMed  CAS  Google Scholar 

  78. Radisky DC, Levy DD, Littlepage LE et al (2005) Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436:123–127

    Article  PubMed  CAS  Google Scholar 

  79. Sternlicht MD, Lochter A, Sympson CJ et al (1999) The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 98:137–146

    Article  PubMed  CAS  Google Scholar 

  80. Yang L, Lin C, Zhao S et al (2007) Phosphorylation of p68 RNA helicase plays a role in platelet-derived growth factor-induced cell proliferation by up-regulating cyclin D1 and c-Myc expression. J Biol Chem 282:16811–16819

    Article  PubMed  CAS  Google Scholar 

  81. Kim HJ, Litzenburger BC, Cui X et al (2007) 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 27:3165–3175

    Article  PubMed  CAS  Google Scholar 

  82. Lopez T, Hanahan D (2002) Elevated levels of IGF-1 receptor convey invasive and metastatic capability in a mouse model of pancreatic islet tumorigenesis. Cancer Cell 1:339–353

    Article  PubMed  CAS  Google Scholar 

  83. Yook JI, Li XY, Ota I et al (2006) A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat Cell Biol 8:1398–1406

    Article  PubMed  CAS  Google Scholar 

  84. Imanishi Y, Hu B, Jarzynka MJ et al (2007) Angiopoietin-2 stimulates breast cancer metastasis through the alpha(5)beta(1) integrin-mediated pathway. Cancer Res 67:4254–4263

    Article  PubMed  CAS  Google Scholar 

  85. Waerner T, Alacakaptan M, Tamir I et al (2006) ILEI: a cytokine essential for EMT, tumor formation, and late events in metastasis in epithelial cells. Cancer Cell 10:227–239

    Article  PubMed  CAS  Google Scholar 

  86. Grunert S, Jechlinger M, Beug H (2003) Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat Rev Mol Cell Biol 4:657–665

    Article  PubMed  Google Scholar 

  87. Janda E, Lehmann K, Killisch I et al (2002) Ras and TGF[beta] cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 156:299–313

    Article  PubMed  CAS  Google Scholar 

  88. Zhu Y, Xu G, Patel A et al (2002) Cloning, expression, and initial characterization of a novel cytokine-like gene family. Genomics 80:144–150

    Article  PubMed  CAS  Google Scholar 

  89. Brabletz T, Jung A, Spaderna S et al (2005) Opinion: migrating cancer stem cells – an integrated concept of malignant tumour progression. Nat Rev Cancer 5:744–749

    Article  PubMed  CAS  Google Scholar 

  90. Breiteneder-Geleff S, Soleiman A, Kowalski H et al (1999) Angiosarcomas express mixed endothelial phenotypes of blood and lymphatic capillaries: podoplanin as a specific marker for lymphatic endothelium. Am J Pathol 154:385–394

    PubMed  CAS  Google Scholar 

  91. Wicki A, Christofori G (2007) The potential role of podoplanin in tumour invasion. Br J Cancer 96:1–5

    Article  PubMed  CAS  Google Scholar 

  92. Scholl FG, Gamallo C, Vilaro S et al (1999) Identification of PA2.26 antigen as a novel cell-surface mucin-type glycoprotein that induces plasma membrane extensions and increased motility in keratinocytes. J Cell Sci 112(Pt 24):4601–4613

    Google Scholar 

  93. Martin-Villar E, Scholl FG, Gamallo C et al (2005) Characterization of human PA2.26 antigen (T1alpha-2, podoplanin), a small membrane mucin induced in oral squamous cell carcinomas. Int J Cancer 113:899–910

    Article  PubMed  CAS  Google Scholar 

  94. Martin-Villar E, Megias D, Castel S et al (2006) Podoplanin binds ERM proteins to activate RhoA and promote epithelial–mesenchymal transition. J Cell Sci 119:4541–4553

    Article  PubMed  CAS  Google Scholar 

  95. Kunita A, Kashima TG, Morishita Y et al (2007) The platelet aggregation-inducing factor aggrus/podoplanin promotes pulmonary metastasis. Am J Pathol 170:1337–1347

    Article  PubMed  CAS  Google Scholar 

  96. Dalerba P, Cho RW, Clarke MF (2007) Cancer stem cells: models and concepts. Annu Rev Med 58:267–284

    Article  PubMed  CAS  Google Scholar 

  97. Balic M, Lin H, Young L et al (2006) Most early disseminated cancer cells detected in bone marrow of breast cancer patients have a putative breast cancer stem cell phenotype. Clin Cancer Res 12:5615–5621

    Article  PubMed  CAS  Google Scholar 

  98. Dontu G, Al-Hajj M, Abdallah WM et al (2003) Stem cells in normal breast development and breast cancer. Cell Prolif 36(Suppl 1):59–72

    Article  PubMed  CAS  Google Scholar 

  99. Sheridan C, Kishimoto H, Fuchs RK et al (2006) CD44+/CD24− breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 8:R59

    Article  PubMed  Google Scholar 

  100. Shipitsin M, Campbell LL, Argani P et al (2007) Molecular definition of breast tumor heterogeneity. Cancer Cell 11:259–273

    Article  PubMed  CAS  Google Scholar 

  101. Sleeman KE, Kendrick H, Ashworth A et al (2006) CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and non-epithelial cells. Breast Cancer Res 8:R7

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by grants from the European Union (FP6 STREP Project BRECOSM, Contract No. LSHC-CT-2004-503224), from the BMBF NGFN2 CancerNet Programme (JPS) and from the Deutsche Forschungsgemeinschaft under the auspices of SPP 1190 “The tumor-vessel interface” (JPS).

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Authors and Affiliations

  1. Department for Molecular Biomedical Research, Molecular and Cellular Oncology, VIB, Technologiepark 927, 9052, Ghent (Zwijnaarde), Belgium

    Geert Berx & Eric Raspé

  2. Department of Molecular Biology, Ghent University, Technologiepark 927, 9052, Ghent (Zwijnaarde), Belgium

    Geert Berx & Eric Raspé

  3. Institute of Biochemistry and Genetics, Department of Clinical-Biological Sciences (DKBW), Center for Biomedicine, University of Basel, Mattenstrasse 28, 4058, Basel, Switzerland

    Gerhard Christofori

  4. Institute of Molecular and Cell Biology, 61 Biopolis Drive, Proteos, Singapore, 138673, Singapore

    Jean Paul Thiery

  5. Forschungszentrum Karlsruhe, Institut für Toxikologie und Genetik, Postfach 3640, 76021, Karlsruhe, Germany

    Jonathan P. Sleeman

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  1. Geert Berx
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  2. Eric Raspé
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Correspondence to Jonathan P. Sleeman.

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Berx, G., Raspé, E., Christofori, G. et al. Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer. Clin Exp Metastasis 24, 587–597 (2007). https://doi.org/10.1007/s10585-007-9114-6

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  • DOI: https://doi.org/10.1007/s10585-007-9114-6

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