Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer

Thiery JP (2002) Epithelial–mesenchymal transitions in tumour progression. Nat Rev Cancer 2:442–454 Thiery JP, Sleeman JP (2006) Complex networks orchestrate epithelial–mesenchymal transitions. Nat Rev Mol Cell Biol 7:131–142 Martin P (1997) Wound healing – aiming for perfect skin regeneration. Science 276:75–81 Kalluri R, Neilson EG (2003) Epithelial–mesenchymal transition and its implications for fibrosis. J Clin Invest 112:1776–1784 Nguyen DX, Massague J (2007) Genetic determinants of cancer metastasis. Nat Rev Genet 8:341–352 Christ B, Ordahl CP (1995) Early stages of chick somite development. Anat Embryol (Berl) 191:381–396 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 Horster MF, Braun GS, Huber SM (1999) Embryonic renal epithelia: induction, nephrogenesis, and cell differentiation. Physiol Rev 79:1157–1191 Vainio S, Lin Y (2002) Coordinating early kidney development: lessons from gene targeting. Nat Rev Genet 3:533–543 Christiansen JJ, Rajasekaran AK (2006) Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 66:8319–8326 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 Shin K, Fogg VC, Margolis B (2006) Tight junctions and cell polarity. Annu Rev Cell Dev Biol 22:207–235 Yin T, Green KJ (2004) Regulation of desmosome assembly and adhesion. Semin Cell Dev Biol 15:665–677 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) 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 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 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 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 LaGamba D, Nawshad A, Hay ED (2005) Microarray analysis of gene expression during epithelial–mesenchymal transformation. Dev Dyn 234:132–142 Hay ED (2005) The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev Dyn 233:706–720 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 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 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 Perou CM, Sorlie T, Eisen MB et al (2000) Molecular portraits of human breast tumours. Nature 406:747–752 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 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 Bierie B, Moses HL (2006) Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer 6:506–520 Blume-Jensen P, Hunter T (2001) Oncogenic kinase signalling. Nature 411:355–365 Bolos V, Grego-Bessa J, de la Pompa JL (2007) Notch signaling in development and cancer. Endocr Rev 28:339–363 Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127:469–480 Evangelista M, Tian H, de Sauvage FJ (2006) The hedgehog signaling pathway in cancer. Clin Cancer Res 12:5924–5928 Reya T, Clevers H (2005) Wnt signalling in stem cells and cancer. Nature 434:843–850 Siegel PM, Massague J (2003) Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 3:807–821 Huber MA, Kraut N, Beug H (2005) Molecular requirements for epithelial–mesenchymal transition during tumor progression. Curr Opin Cell Biol 17:548–558 Savagner P (2001) Leaving the neighborhood: molecular mechanisms involved during epithelial–mesenchymal transition. Bioessays 23:912–923 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 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 Venkov CD, Link AJ, Jennings JL et al (2007) A proximal activator of transcription in epithelial–mesenchymal transition. J Clin Invest 117:482–491 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 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 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 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 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 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 Hajra KM, Chen DY, Fearon ER (2002) The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res 62:1613–1618 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 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 Sleeman JP (2000) The lymph node as a bridgehead in the metastatic dissemination of tumors. Recent Results Cancer Res 157:55–81 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 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 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 Tarin D, Thompson EW, Newgreen DF (2005) The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 65:5996–6000; discussion 6000–5991 De Craene B, van Roy F, Berx G (2005) Unraveling signalling cascades for the Snail family of transcription factors. Cell Signal 17:535–547 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 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 Jechlinger M, Sommer A, Moriggl R et al (2006) Autocrine PDGFR signaling promotes mammary cancer metastasis. J Clin Invest 116:1561–1570 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 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 Eccles SA, Welch DR (2007) Metastasis: recent discoveries and novel treatment strategies. Lancet 369:1742–1757 Karin M (2006) Nuclear factor-kappaB in cancer development and progression. Nature 441:431–436 Moody SE, Perez D, Pan TC et al (2005) The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8:197–209 Wilmut I, Schnieke AE, McWhir J et al (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385:810–813 Slack JM (2007) Metaplasia and transdifferentiation: from pure biology to the clinic. Nat Rev Mol Cell Biol 8:369–378 Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676 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 Hendrix MJ, Seftor EA, Seftor RE et al (2007) Reprogramming metastatic tumour cells with embryonic microenvironments. Nat Rev Cancer 7:246–255 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 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 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 Friedl P, Hegerfeldt Y, Tusch M (2004) Collective cell migration in morphogenesis and cancer. Int J Dev Biol 48:441–449 Friedl P, Wolf K (2003) Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 3:362–374 Friedl P, Wolf K (2003) Proteolytic and non-proteolytic migration of tumour cells and leucocytes. Biochem Soc Symp (70):277–285 Wolf K, Friedl P (2006) Molecular mechanisms of cancer cell invasion and plasticity. Br J Dermatol 154(Suppl 1):11–15 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 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 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 Bissell MJ, Radisky D (2001) Putting tumours in context. Nat Rev Cancer 1:46–54 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 Sternlicht MD, Lochter A, Sympson CJ et al (1999) The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell 98:137–146 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 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 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 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 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 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 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 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 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 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 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 Wicki A, Christofori G (2007) The potential role of podoplanin in tumour invasion. Br J Cancer 96:1–5 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 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 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 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 Dalerba P, Cho RW, Clarke MF (2007) Cancer stem cells: models and concepts. Annu Rev Med 58:267–284 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 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 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 Shipitsin M, Campbell LL, Argani P et al (2007) Molecular definition of breast tumor heterogeneity. Cancer Cell 11:259–273 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