Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?
Tóm tắt
Từ khóa
Tài liệu tham khảo
Thiery, J. P. & Sleeman, J. P. Complex networks orchestrate epithelial-mesenchymal transitions. Nature Rev. Mol. Cell Biol. 7, 131–142 (2006).
Thiery, J. P. Epithelial-mesenchymal transitions in tumour progression. Nature Rev. Cancer 2, 442–454 (2002). The first comprehensive review to compile evidence for EMT in tumorigenesis.
Birchmeier, W. & Behrens, J. Cadherin expression in carcinomas: role in the formation of cell junctions and the prevention of invasiveness. Biochim. Biophys. Acta. 1198, 11–26 (1994).
Peinado, H. & Cano, A. New potential therapeutic targets to combat epithelial tumor invasion. Clin. Transl. Oncol. 8, 851–857 (2006).
Tarin, D., Thompson, E. W. & Newgreen, D. F. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res. 65, 5996–6000 (2005).
Christiansen, J. J. & Rajasekaran, A. K. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res. 66, 8319–8326 (2006).
Barrallo-Gimeno, A. & Nieto, M. A. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132, 3151–3161 (2005). An excellent review of the implication of Snail factors in processes other than EMT.
Batlle, E. et al. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nature Cell Biol. 2, 84–89 (2000).
Cano, A. et al. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nature Cell Biol. 2, 76–83 (2000). Together with reference 9, characterizes SNAI1 as the first E-cadherin repressor and EMT inducer in carcinoma cells.
Bolos, V. et al. The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J. Cell Sci. 116, 499–511 (2003).
Hajra, K. M., Chen, D. Y. & Fearon, E. R. The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res. 62, 1613–1618 (2002).
Comijn, J. et al. The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 7, 1267–1278 (2001).
Eger, A. et al. dEF1 is a transcriptional repressor of E-cadherin and regulates epithelial plasticity in breast cancer cells. Oncogene 24, 2375–2385 (2005).
Perez-Moreno, M. A. et al. A new role for E12/E47 in the repression of E-cadherin expression and epithelial-mesenchymal transitions. J. Biol. Chem. 276, 27424–27431 (2001).
Yang, J. et al. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927–939 (2004). The first demonstration of the capability of TWIST to induce EMT and metastasis.
Nieto, M. A. The snail superfamily of zinc-finger transcription factors. Nature Rev. Mol. Cell Biol. 3, 155–166 (2002).
De Craene, B., van Roy, F. & Berx, G. Unraveling signalling cascades for the Snail family of transcription factors. Cell Signal. 17, 535–547 (2005).
Huber, M. A., Kraut, N. & Beug, H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr. Opin. Cell Biol. 17, 548–558 (2005).
Lu, Z., Ghosh, S., Wang, Z. & Hunter, T. Downregulation of caveolin-1 function by EGF leads to the loss of E-cadherin, increased transcriptional activity of β-catenin, and enhanced tumor cell invasion. Cancer Cell 4, 499–515 (2003).
Barbera, M. J. et al. Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells. Oncogene 23, 7345–7354 (2004).
Peinado, H., Quintanilla, M. & Cano, A. Transforming growth factor β-1 induces snail transcription factor in epithelial cell lines: mechanisms for epithelial mesenchymal transitions. J. Biol. Chem. 278, 21113–21123 (2003).
Timmerman, L. A. et al. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 18, 99–115 (2004).
Zavadil, J., Cermak, L., Soto-Nieves, N. & Bottinger, E. P. Integration of TGF-β/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J. 23, 1155–1165 (2004).
Medici, D., Hay, E. D. & Goodenough, D. A. Cooperation between snail and LEF-1 transcription factors is essential for TGF-β1-induced epithelial-mesenchymal transition. Mol. Biol. Cell 17, 1871–1879 (2006).
Conacci-Sorrell, M. et al. Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of β-catenin signaling, Slug, and MAPK. J. Cell Biol. 163, 847–857 (2003).
Sakai, D., Suzuki, T., Osumi, N. & Wakamatsu, Y. Cooperative action of Sox9, Snail2 and PKA signaling in early neural crest development. Development 133, 1323–1333 (2006).
Vallin, J. et al. Cloning and characterization of three Xenopus slug promoters reveal direct regulation by Lef/β-catenin signaling. J. Biol. Chem. 276, 30350–30358 (2001).
Thuault, S. et al. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. J. Cell Biol. 174, 175–183 (2006).
Mann, J. R. et al. Repression of prostaglandin dehydrogenase by epidermal growth factor and snail increases prostaglandin E2 and promotes cancer progression. Cancer Res. 66, 6649–6656 (2006).
Dohadwala, M. et al. Cyclooxygenase-2-dependent regulation of E-cadherin: prostaglandin E(2) induces transcriptional repressors ZEB1 and snail in non-small cell lung cancer. Cancer Res. 66, 5338–5345 (2006).
Rosano, L. et al. Endothelin-1 promotes epithelial-to-mesenchymal transition in human ovarian cancer cells. Cancer Res. 65, 11649–11657 (2005).
Yang, A. D. et al. Vascular endothelial growth factor receptor-1 activation mediates epithelial to mesenchymal transition in human pancreatic carcinoma cells. Cancer Res. 66, 46–51 (2006).
Tsutsumi, S., Yanagawa, T., Shimura, T., Kuwano, H. & Raz, A. Autocrine motility factor signaling enhances pancreatic cancer metastasis. Clin. Cancer Res. 10, 7775–7784 (2004).
Perez-Losada, J. et al. Zinc-finger transcription factor Slug contributes to the function of the stem cell factor c-kit signaling pathway. Blood 100, 1274–1286 (2002).
Wang, Z. et al. Raf 1 represses expression of the tight junction protein occludin via activation of the zinc-finger transcription factor slug. Oncogene 26, 1222–1230 (2007).
Hayashida, Y. et al. Calreticulin represses E-cadherin gene expression in Madin-Darby canine kidney cells via Slug. J. Biol. Chem. 281, 32469–32484 (2006).
Evans, A. J. et al. VHL Promotes E2 Box-dependent E-cadherin Transcription by HIF-mediated Regulation of SIP1 and Snail. Mol. Cell Biol. (2006).
Radisky, D. C. et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature 436, 123–127 (2005).
Giannelli, G., Bergamini, C., Fransvea, E., Sgarra, C. & Antonaci, S. Laminin-5 with transforming growth factor-β1 induces epithelial to mesenchymal transition in hepatocellular carcinoma. Gastroenterology 129, 1375–1383 (2005).
Chen, M., Chen, L. M. & Chai, K. X. Androgen regulation of prostasin gene expression is mediated by sterol-regulatory element-binding proteins and SLUG. Prostate 66, 911–920 (2006).
Fujita, N. et al. MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 113, 207–219 (2003). Demonstration of the link between MTA3 and ligated ER with the negative regulation of Snail expression in breast carcinoma cells.
Dillner, N. B. & Sanders, M. M. Transcriptional activation by the zinc-finger homeodomain protein d EF1 in estrogen signaling cascades. DNA Cell Biol. 23, 25–34 (2004).
Peiro, S. et al. Snail1 transcriptional repressor binds to its own promoter and controls its expression. Nucleic Acids Res. 34, 2077–2084 (2006).
Sakai, D. et al. Regulation of Slug transcription in embryonic ectoderm by β-catenin-Lef/Tcf and BMP-Smad signaling. Dev. Growth Differ. 47, 471–482 (2005).
Bachelder, R. E., Yoon, S. O., Franci, C., de Herreros, A. G. & Mercurio, A. M. Glycogen synthase kinase-3 is an endogenous inhibitor of Snail transcription: implications for the epithelial-mesenchymal transition. J. Cell Biol. 168, 29–33 (2005).
Grotegut, S., von Schweinitz, D., Christofori, G. & Lehembre, F. Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail. EMBO J. 25, 3534–3545 (2006).
Hemavathy, K., Ashraf, S. I. & Ip, Y. T. Snail/slug family of repressors: slowly going into the fast lane of development and cancer. Gene 257, 1–12 (2000).
Perk, J., Iavarone, A. & Benezra, R. Id family of helix-loop-helix proteins in cancer. Nature Rev. Cancer 5, 603–614 (2005). An excellent review of the implication of Id proteins in cancer.
Ruzinova, M. B. & Benezra, R. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13, 410–418 (2003).
Postigo, A. A. Opposing functions of ZEB proteins in the regulation of the TGFβ/BMP signaling pathway. EMBO J. 22, 2443–2452 (2003).
Peinado, H. & Cano, A. Regulation of the E-cadherin Cell-Cell Adhesion Gene in DNA methylation, epigenetics and metastasis, 157–190 (ed. Esteller, M.) (Springer, 2005).
Peinado, H., Portillo, F. & Cano, A. Transcriptional regulation of cadherins during development and carcinogenesis. Int. J. Dev. Biol. 48, 365–375 (2004).
Hemavathy, K., Guru, S. C., Harris, J., Chen, J. D. & Ip, Y. T. Human Slug is a repressor that localizes to sites of active transcription. Mol. Cell Biol. 20, 5087–5095 (2000).
Peinado, H., Ballestar, E., Esteller, M. & Cano, A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol. Cell Biol. 24, 306–319 (2004).
Tripathi, M. K. et al. Regulation of BRCA2 gene expression by the SLUG repressor protein in human breast cells. J. Biol. Chem. 280, 17163–17171 (2005).
Bailey, C. K., Misra, S., Mittal, M. K. & Chaudhuri, G. Human SLUG does not directly bind to CtBP1. Biochem. Biophys. Res. Commun. 353, 661–664 (2006).
Shi, Y. et al. Coordinated histone modifications mediated by a CtBP co-repressor complex. Nature 422, 735–738 (2003).
van Grunsven, L. A. et al. Interaction between Smad-interacting protein-1 and the corepressor C-terminal binding protein is dispensable for transcriptional repression of E-cadherin. J. Biol. Chem. 278, 26135–26145 (2003).
Pena, C. et al. The expression levels of the transcriptional regulators p300 and CtBP modulate the correlations between SNAIL, ZEB1, E-cadherin and vitamin D receptor in human colon carcinomas. Int. J. Cancer 119, 2098–2104 (2006).
Postigo, A. A., Depp, J. L., Taylor, J. J. & Kroll, K. L. Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins. EMBO J. 22, 2453–2462 (2003).
Alpatov, R. et al. Nuclear speckle-associated protein Pnn/DRS binds to the transcriptional corepressor CtBP and relieves CtBP-mediated repression of the E-cadherin gene. Mol. Cell Biol. 24, 10223–10235 (2004).
Long, J., Zuo, D. & Park, M. Pc2-mediated sumoylation of Smad-interacting protein 1 attenuates transcriptional repression of E-cadherin. J. Biol. Chem. 280, 35477–35489 (2005).
Zhao, L. J., Subramanian, T., Zhou, Y. & Chinnadurai, G. Acetylation by p300 regulates nuclear localization and function of the transcriptional corepressor CtBP2. J. Biol. Chem. 281, 4183–4189 (2006).
Zhang, Q., Piston, D. W. & Goodman, R. H. Regulation of corepressor function by nuclear NADH. Science 295, 1895–1897 (2002).
Kondo, M. et al. A role for Id in the regulation of TGFβ-induced epithelial-mesenchymal transdifferentiation. Cell Death Differ. 11, 1092–1101 (2004).
Dominguez, D. et al. Phosphorylation regulates the subcellular location and activity of the snail transcriptional repressor. Mol. Cell Biol. 23, 5078–5089 (2003).
Yang, Z. et al. Pak1 phosphorylation of snail, a master regulator of epithelial-to-mesenchyme transition, modulates snail's subcellular localization and functions. Cancer Res. 65, 3179–3184 (2005).
Yamashita, S. et al. Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer. Nature 429, 298–302 (2004).
Zhou, B. P. et al. Dual regulation of Snail by GSK-3β-mediated phosphorylation in control of epithelial-mesenchymal transition. Nature Cell Biol. 6, 931–940 (2004). Pioneering study that showed the post-transcriptional regulation of SNAI1 subcellular localization and stability by GSK3β kinase.
Yook, J. I. et al. A Wnt-Axin2-GSK3β cascade regulates Snail1 activity in breast cancer cells. Nature Cell Biol. 8, 1398–1406 (2006).
Peinado, H. et al. A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression. EMBO J. 24, 3446–3458 (2005). Showed for the first time that LOXL2 and/or LOXL3 regulate SNAI1 protein stability and functional activity.
Peinado, H., Portillo, F. & Cano, A. Switching on-off Snail: LOXL2 versus GSK3β. Cell Cycle 4, 1749–1752 (2005).
Vernon, A. E. & Labonne, C. Slug stability is dynamically regulated during neural crest development by the F-box protein Ppa. Development 133, 3359–3370 (2006).
Lluis, F., Ballestar, E., Suelves, M., Esteller, M. & Munoz-Canoves, P. E47 phosphorylation by p38 MAPK promotes MyoD/E47 association and muscle-specific gene transcription. EMBO J. 24, 974–984 (2005).
Neufeld, B. et al. Serine/Threonine kinases 3pK and MAPK-activated protein kinase 2 interact with the basic helix-loop-helix transcription factor E47 and repress its transcriptional activity. J. Biol. Chem. 275, 20239–20242 (2000).
Chu, C. & Kohtz, D. S. Identification of the E2A gene products as regulatory targets of the G1 cyclin-dependent kinases. J. Biol. Chem. 276, 8524–8534 (2001).
Nie, L., Xu, M., Vladimirova, A. & Sun, X. H. Notch-induced E2A ubiquitination and degradation are controlled by MAP kinase activities. EMBO J. 22, 5780–5792 (2003).
Moreno-Bueno, G. et al. 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 (2006).
Bermejo-Rodriguez, C. et al. Mouse cDNA microarray analysis uncovers Slug targets in mouse embryonic fibroblasts. Genomics 87, 113–118 (2006).
Vandewalle, C. et al. SIP1/ZEB2 induces EMT by repressing genes of different epithelial cell-cell junctions. Nucleic Acids Res. 33, 6566–6578 (2005).
Boutet, A. et al. Snail activation disrupts tissue homeostasis and induces fibrosis in the adult kidney. EMBO J. 25, 5603–5613 (2006).
Cicchini, C. et al. Snail controls differentiation of hepatocytes by repressing HNF4a expression. J. Cell Physiol. 209, 230–238 (2006).
De Craene, B. et al. The transcription factor snail induces tumor cell invasion through modulation of the epithelial cell differentiation program. Cancer Res. 65, 6237–6244 (2005).
Palmer, H. G. et al. The transcription factor SNAIL represses vitamin D receptor expression and responsiveness in human colon cancer. Nature Med. 10, 917–919 (2004).
Kajita, M., McClinic, K. N. & Wade, P. A. Aberrant expression of the transcription factors snail and slug alters the response to genotoxic stress. Mol. Cell Biol. 24, 7559–7566 (2004).
Wu, W. S. et al. Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 123, 641–653 (2005).
Espineda, C. E., Chang, J. H., Twiss, J., Rajasekaran, S. A. & Rajasekaran, A. K. Repression of Na, K-ATPase β1-subunit by the transcription factor snail in carcinoma. Mol. Biol. Cell. 15, 1364–1373 (2004).
Park, J. H. et al. The zinc-finger transcription factor Snail downregulates proliferating cell nuclear antigen expression in colorectal carcinoma cells. Int. J. Oncol. 26, 1541–1547 (2005).
Takeuchi, T., Adachi, Y., Sonobe, H., Furihata, M. & Ohtsuki, Y. A ubiquitin ligase, skeletrophin, is a negative regulator of melanoma invasion. Oncogene 25, 7059–7069 (2006).
Vega, S. et al. Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 18, 1131–1143 (2004).
Seki, K. et al. Mouse Snail family transcription repressors regulate chondrocyte, extracellular matrix, type II collagen, and aggrecan. J. Biol. Chem. 278, 41862–41870 (2003).
Turner, F. E. et al. Slug regulates integrin expression and cell proliferation in human epidermal keratinocytes. J. Biol. Chem. 281, 21321–21331 (2006).
Takahashi, E. et al. Snail regulates p21(WAF/CIP1) expression in cooperation with E2A and Twist. Biochem. Biophys. Res. Commun. 325, 1136–1144 (2004).
Guaita, S. et al. Snail induction of epithelial to mesenchymal transition in tumor cells is accompanied by MUC1 repression and ZEB1 expression. J. Biol. Chem. 277, 39209–39216 (2002).
Yoshimoto, A., Saigou, Y., Higashi, Y. & Kondoh, H. Regulation of ocular lens development by Smad-interacting protein 1 involving Foxe3 activation. Development 132, 4437–4448 (2005).
Alexander, N. R. et al. N-cadherin gene expression in prostate carcinoma is modulated by integrin-dependent nuclear translocation of Twist1. Cancer Res. 66, 3365–3369 (2006).
Zheng, W., Wang, H., Xue, L., Zhang, Z. & Tong, T. Regulation of cellular senescence and p16(INK4a) expression by Id1 and E47 proteins in human diploid fibroblast. J. Biol. Chem. 279, 31524–31532 (2004).
Kumar, M. S., Hendrix, J. A., Johnson, A. D. & Owens, G. K. Smooth muscle α-actin gene requires two E-boxes for proper expression in vivo and is a target of class I basic helix-loop-helix proteins. Circ. Res. 92, 840–847 (2003).
Taki, M., Verschueren, K., Yokoyama, K., Nagayama, M. & Kamata, N. Involvement of Ets-1 transcription factor in inducing matrix metalloproteinase-2 expression by epithelial-mesenchymal transition in human squamous carcinoma cells. Int. J. Oncol. 28, 487–496 (2006).
Jorda, M. et al. Upregulation of MMP-9 in MDCK epithelial cell line in response to expression of the Snail transcription factor. J. Cell Sci. 118, 3371–3385 (2005).
Remacle, J. E. et al. New mode of DNA binding of multi-zinc finger transcription factors: dEF1 family members bind with two hands to two target sites. EMBO J. 18, 5073–5084 (1999).
Blanco, M. J. et al. Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 21, 3241–3246 (2002).
Cheng, C. W. et al. Mechanisms of inactivation of E-cadherin in breast carcinoma: modification of the two-hit hypothesis of tumor suppressor gene. Oncogene 20, 3814–3823 (2001). First indication that transcriptional repression mechanisms have a dynamic role in E-cadherin downregulation.
Come, C. et al. Snail and slug play distinct roles during breast carcinoma progression. Clin. Cancer Res. 12, 5395–5402 (2006).
Elloul, S. et al. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 103, 1631–1643 (2005).
Moody, S. E. et al. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8, 197–209 (2005). First implication of SNAI1 in breast cancer recurrence.
Martin, T. A., Goyal, A., Watkins, G. & Jiang, W. G. Expression of the transcription factors snail, slug, and twist and their clinical significance in human breast cancer. Ann. Surg. Oncol. 12, 488–496 (2005).
Elloul, S. et al. Expression of E-cadherin transcriptional regulators in ovarian carcinoma. Virchows Arch. 449, 520–528 (2006).
Pena, C. et al. E-cadherin and vitamin D receptor regulation by SNAIL and ZEB1 in colon cancer: clinicopathological correlations. Hum. Mol. Genet. 14, 3361–3370 (2005).
Gonzalez-Sancho, J. M., Larriba, M. J., Ordonez-Moran, P., Palmer, H. G. & Muñoz, A. Effects of 1α, 25-dihydroxyvitamin D3 in human colon cancer cells. Anticancer Res. 26, 2669–2681 (2006).
Roy, H. K., Smyrk, T. C., Koetsier, J., Victor, T. A. & Wali, R. K. The transcriptional repressor SNAIL is overexpressed in human colon cancer. Dig. Dis. Sci. 50, 42–46 (2005).
Shioiri, M. et al. Slug expression is an independent prognostic parameter for poor survival in colorectal carcinoma patients. Br. J. Cancer 94, 1816–1822 (2006).
Rosivatz, E. et al. Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am. J. Pathol. 161, 1881–1891 (2002).
Rosivatz, E. et al. Expression and nuclear localization of Snail, an E-cadherin repressor, in adenocarcinomas of the upper gastrointestinal tract. Virchows Arch. 448, 277–287 (2006).
Takeno, S. et al. E-cadherin expression in patients with esophageal squamous cell carcinoma: promoter hypermethylation, Snail overexpression, and clinicopathologic implications. Am. J. Clin. Pathol. 122, 78–84 (2004).
Yang, M. H. et al. Overexpression of NBS1 induces epithelial-mesenchymal transition and co-expression of NBS1 and Snail predicts metastasis of head and neck cancer. Clin. Cancer Res. 12, 507–515 (2006).
Yokoyama, K. et al. Increased invasion and matrix metalloproteinase-2 expression by Snail-induced mesenchymal transition in squamous cell carcinomas. Int. J. Oncol. 22, 891–898 (2003).
Miyoshi, A. et al. Snail accelerates cancer invasion by upregulating MMP expression and is associated with poor prognosis of hepatocellular carcinoma. Br. J. Cancer 92, 252–258 (2005).
Sugimachi, K. et al. Transcriptional repressor snail and progression of human hepatocellular carcinoma. Clin. Cancer Res. 9, 2657–2664 (2003).
Uchikado, Y. et al. Slug expression in the E-cadherin preserved tumors is related to prognosis in patients with esophageal squamous cell carcinoma. Clin. Cancer Res. 11, 1174–1180 (2005).
Shih, J. Y. et al. Transcription repressor slug promotes carcinoma invasion and predicts outcome of patients with lung adenocarcinoma. Clin. Cancer Res. 11, 8070–8078 (2005).
Sivertsen, S. et al. Expression of Snail, Slug and SIP1 in malignant mesothelioma effusions is associated with matrix metalloproteinase, but not with cadherin expression. Lung Cancer 54, 309–317 (2006).
Saito, T. et al. E-cadherin mutation and Snail overexpression as alternative mechanisms of E-cadherin inactivation in synovial sarcoma. Oncogene 23, 8629–8638 (2004).
Gupta, P. B. et al. The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nature Genet. 37, 1047–1054 (2005).
Locascio, A., Vega, S., de Frutos, C. A., Manzanares, M. & Nieto, M. A. Biological potential of a functional human SNAIL retrogene. J. Biol. Chem. 277, 38803–38809 (2002).
Franci, C. et al. Expression of Snail protein in tumor-stroma interface. Oncogene 25, 5134–5144 (2006). The first studty to show a reliable expression of SNAI1 by immunohistochemistry in human tumours.
Maeda, G. et al. Expression of SIP1 in oral squamous cell carcinomas: implications for E-cadherin expression and tumor progression. Int. J. Oncol. 27, 1535–1541 (2005).
Imamichi, Y., Konig, A., Gress, T. & Menke, A. Collagen type I-induced Smad-interacting protein 1 expression downregulates E-cadherin in pancreatic cancer. Oncogene 26, 2381–2385 (2007).
Spoelstra, N. S. et al. The transcription factor ZEB1 is aberrantly expressed in aggressive uterine cancers. Cancer Res. 66, 3893–3902 (2006).
Mironchik, Y. et al. Twist overexpression induces in vivo angiogenesis and correlates with chromosomal instability in breast cancer. Cancer Res. 65, 10801–10809 (2005).
Sarrio, D. et al. Epigenetic and genetic alterations of APC and CDH1 genes in lobular breast cancer: relationships with abnormal E-cadherin and catenin expression and microsatellite instability. Int. J. Cancer 106, 208–215 (2003).
Kwok, W. K. et al. Up-regulation of TWIST in prostate cancer and its implication as a therapeutic target. Cancer Res. 65, 5153–5162 (2005).
Yuen, H. F. et al. Up-regulation of TWIST in oesophageal squamous cell carcinoma is associated with neoplastic transformation and distant metastasis. J. Clin. Pathol. August 2006 (doi: 10.1036/jcp2006.039099).
Lee, T. K. et al. Twist overexpression correlates with hepatocellular carcinoma metastasis through induction of epithelial-mesenchymal transition. Clin. Cancer Res. 12, 5369–5376 (2006).
Kyo, S. et al. High Twist expression is involved in infiltrative endometrial cancer and affects patient survival. Hum. Pathol. 37, 431–438 (2006).
Hoek, K. et al. Expression profiling reveals novel pathways in the transformation of melanocytes to melanomas. Cancer Res. 64, 5270–5282 (2004).
Perk, J. et al. Reassessment of id1 protein expression in human mammary, prostate, and bladder cancers using a monospecific rabbit monoclonal anti-id1 antibody. Cancer Res. 66, 10870–10877 (2006).
Olmeda, D., Jorda, M., Peinado, H., Fabra, A. & Cano, A. Snail silencing effectively suppresses tumour growth and invasiveness. Oncogene 26, 1862–1874 (2007).
Jamora, C. et al. A signaling pathway involving TGFβ2 and Snail in hair follicle morphogenesis. PLoS Biol. 3, e11 (2005).
Metzstein, M. M. & Horvitz, H. R. The C. elegans cell death specification gene ces-1 encodes a snail family zinc finger protein. Mol. Cell 4, 309–319 (1999).
Inukai, T. et al. SLUG, a ces-1-related zinc finger transcription factor gene with antiapoptotic activity, is a downstream target of the E2A-HLF oncoprotein. Mol. Cell 4, 343–352 (1999).
Inoue, A. et al. Slug, a highly conserved zinc finger transcriptional repressor, protects hematopoietic progenitor cells from radiation-induced apoptosis in vivo. Cancer Cell 2, 279–288 (2002). Functional characterization of the role of SNAI2 in the survival of haematological precursor cells.
Perez-Losada, J., Sanchez-Martin, M., Perez-Caro, M., Perez-Mancera, P. A. & Sanchez-Garcia, I. The radioresistance biological function of the SCF/kit signaling pathway is mediated by the zinc-finger transcription factor Slug. Oncogene 22, 4205–4211 (2003).
Catalano, A., Rodilossi, S., Rippo, M. R., Caprari, P. & Procopio, A. Induction of stem cell factor/c-Kit/slug signal transduction in multidrug-resistant malignant mesothelioma cells. J. Biol. Chem. 279, 46706–46714 (2004).
Puisieux, A., Valsesia-Wittmann, S. & Ansieau, S. A twist for survival and cancer progression. Br. J. Cancer. 94, 13–17 (2006).
Wang, X. et al. Identification of a novel function of Twist, a bHLH protein, in the development of acquired taxol resistance in human cancer cells. Oncogene 23, 474–482 (2004).
Gyorffy, A. et al. Comparative promoter analysis of doxorubicin resistance-associated genes suggests E47 as a key regulatory element. Anticancer Res. 26, 2971–2976 (2006).
De Craene, B. & Berx, G. Snail in the frame of malignant tumor recurrence. Breast Cancer Res. 8, 105 (2006).
Brabletz, T., Jung, A., Spaderna, S., Hlubek, F. & Kirchner, T. Opinion: migrating cancer stem cells- an integrated concept of malignant tumour progression. Nature Rev. Cancer 5, 744–749 (2005).
Nelson, C. M. & Bissell, M. J. Of extracellular matrix, scaffolds, and signaling: tissue architecture regulates development, homeostasis, and cancer. Annu. Rev. Cell. Dev. Biol. 22, 287–309 (2006).
Zi, X. et al. Expression of Frzb/secreted Frizzled-related protein 3, a secreted Wnt antagonist, in human androgen-independent prostate cancer PC-3 cells suppresses tumor growth and cellular invasiveness. Cancer Res. 65, 9762–9770 (2005).
Chua, H. L. et al. NF-κB represses E-cadherin expression and enhances epithelial to mesenchymal transition of mammary epithelial cells: potential involvement of ZEB-1 and ZEB-2. Oncogene 26, 711–724 (2007).
Peinado, H. et al. Snail and E47 repressors of E-cadherin induce distinct invasive and angiogenic properties in vivo. J. Cell Sci. 117, 2827–2839 (2004).
Takkunen, M. et al. Snail-dependent and-independent epithelial-mesenchymal transition in oral squamous carcinoma cells. J. Histochem Cytochem. 54, 1263–1275 (2006).
Martinez-Estrada, O. M. et al. The transcription factors Slug and Snail act as repressors of Claudin-1 expression in epithelial cells. Biochem. J. 394, 449–457 (2006).
Friedl, P. & Wolf, K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nature Rev. Cancer 3, 362–374 (2003).
Savagner, P. et al. Developmental transcription factor slug is required for effective re-epithelialization by adult keratinocytes. J. Cell Physiol. 202, 858–866 (2005).
Zavadil, J. & Bottinger, E. P. TGF-β and epithelial-to-mesenchymal transitions. Oncogene 24, 5764–5774 (2005).
Esteban, M. A. et al. Regulation of E-cadherin expression by VHL and hypoxia-inducible factor. Cancer Res. 66, 3567–3575 (2006).
Krishnamachary, B. et al. Hypoxia-inducible factor-1-dependent repression of E-cadherin in von Hippel-Lindau tumor suppressor-null renal cell carcinoma mediated by TCF3, ZFHX1A, and ZFHX1B. Cancer Res. 66, 2725–2731 (2006).
Kurrey, N. K., K, A. & Bapat, S. A. Snail and Slug are major determinants of ovarian cancer invasiveness at the transcription level. Gynecol. Oncol. 97, 155–165 (2005).
Imai, T. et al. Hypoxia attenuates the expression of E-cadherin via up-regulation of SNAIL in ovarian carcinoma cells. Am. J. Pathol. 163, 1437–1447 (2003).
Erler, J. T. et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440, 1222–1226 (2006).
Pouyssegur, J., Dayan, F. & Mazure, N. M. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 441, 437–443 (2006). This study, together with reference 164, reflects the influence of the tumour microenvironment on the regulation of LOX proteins to promote tumour metastasis.
Carver, E. A., Jiang, R., Lan, Y., Oram, K. F. & Gridley, T. The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol. Cell Biol. 21, 8184–8188 (2001).
Murray, S. A. & Gridley, T. Snail family genes are required for left-right asymmetry determination, but not neural crest formation, in mice. Proc. Natl Acad. Sci. USA 103, 10300–10304 (2006).
Postigo, A. A. & Dean, D. C. Differential expression and function of members of the zfh-1 family of zinc finger/homeodomain repressors. Proc. Natl Acad. Sci. USA 97, 6391–6396 (2000).
Van de Putte, T. et al. Mice lacking ZFHX1B, the gene that codes for Smad-interacting protein-1, reveal a role for multiple neural crest cell defects in the etiology of Hirschsprung disease-mental retardation syndrome. Am. J. Hum. Genet. 72, 465–470 (2003).
Massari, M. E. & Murre, C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell Biol. 20, 429–440 (2000). A comprehensive review of the bHLH family of proteins.
Ellenberger, T., Fass, D., Arnaud, M. & Harrison, S. C. Crystal structure of transcription factor E47: E-box recognition by a basic region helix-loop-helix dimer. Genes Dev. 8, 970–980 (1994).
Quong, M. W., Massari, M. E., Zwart, R. & Murre, C. A new transcriptional-activation motif restricted to a class of helix-loop-helix proteins is functionally conserved in both yeast and mammalian cells. Mol. Cell Biol. 13, 792–800 (1993).