Transcriptional regulation of EMT transcription factors in cancer

Kalluri, 2009, The basics of epithelial-mesenchymal transition, J. Clin. Invest., 119, 1420, 10.1172/JCI39104 Pastushenko, 2019, EMT transition states during tumor progression and metastasis, Trends Cell Biol., 29, 212, 10.1016/j.tcb.2018.12.001 Brabletz, 2021, Dynamic EMT: a multi-tool for tumor progression, EMBO J., 40, 10.15252/embj.2021108647 Matysiak, 2017, EMT promoting transcription factors as prognostic markers in human breast cancer, Arch. Gynecol. Obstet., 295, 817, 10.1007/s00404-017-4304-1 Nieto, 2016, Emt: 2016, Cell, 166, 21, 10.1016/j.cell.2016.06.028 Krebs, 2017, The EMT-activator Zeb1 is a key factor for cell plasticity and promotes metastasis in pancreatic cancer, Nat. Cell Biol., 19, 518, 10.1038/ncb3513 Fischer, 2015, Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance, Nature, 527, 472, 10.1038/nature15748 Genetta, 1994, Displacement of an E-box-binding repressor by basic helix-loop-helix proteins: implications for B-cell specificity of the immunoglobulin heavy-chain enhancer, Mol. Cell Biol., 14, 6153 Funahashi, 1993, Delta-crystallin enhancer binding protein delta EF1 is a zinc finger-homeodomain protein implicated in postgastrulation embryogenesis, Development, 119, 433, 10.1242/dev.119.2.433 Vanderperre, 2013, Direct detection of alternative open reading frames translation products in human significantly expands the proteome, PloS One, 8, 10.1371/journal.pone.0070698 Takagi, 1998, DeltaEF1, a zinc finger and homeodomain transcription factor, is required for skeleton patterning in multiple lineages, Development, 125, 21, 10.1242/dev.125.1.21 Verschueren, 1999, SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5′-CACCT sequences in candidate target genes, J. Biol. Chem., 274, 20489, 10.1074/jbc.274.29.20489 Van de Putte, 2003, 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, 10.1086/346092 Beltran, 2008, A natural antisense transcript regulates Zeb2/Sip1 gene expression during Snail1-induced epithelial-mesenchymal transition, Genes Dev., 22, 756, 10.1101/gad.455708 McKinsey, 2013, Dlx1&2-dependent expression of Zfhx1b (Sip1, Zeb2) regulates the fate switch between cortical and striatal interneurons, Neuron, 77, 83, 10.1016/j.neuron.2012.11.035 Birkhoff, 2020, Targeted chromatin conformation analysis identifies novel distal neural enhancers of ZEB2 in pluripotent stem cell differentiation, Hum. Mol. Genet., 29, 2535, 10.1093/hmg/ddaa141 Postigo, 2003, Opposing functions of ZEB proteins in the regulation of the TGFbeta/BMP signaling pathway, Embo J., 22, 2443, 10.1093/emboj/cdg225 Postigo, 2003, Regulation of Smad signaling through a differential recruitment of coactivators and corepressors by ZEB proteins, Embo J., 22, 2453, 10.1093/emboj/cdg226 Comijn, 2001, The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion, Mol. Cell, 7, 1267, 10.1016/S1097-2765(01)00260-X Shirakihara, 2007, Differential regulation of epithelial and mesenchymal markers by δEF1 proteins in epithelial mesenchymal transition induced by TGF-β, Mol. Biol. Cell, 18, 3533, 10.1091/mbc.e07-03-0249 Neve, 2006, A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes, Cancer Cell, 10, 515, 10.1016/j.ccr.2006.10.008 Charafe-Jauffret, 2006, Gene expression profiling of breast cell lines identifies potential new basal markers, Oncogene, 25, 2273, 10.1038/sj.onc.1209254 Horiguchi, 2012, TGF-β drives epithelial-mesenchymal transition through δEF1-mediated downregulation of ESRP, Oncogene, 31, 3190, 10.1038/onc.2011.493 Fukagawa, 2015, δEF1 associates with DNMT1 and maintains DNA methylation of the E-cadherin promoter in breast cancer cells, Cancer Med, 4, 125, 10.1002/cam4.347 Yamamoto, 2013, NF-kappaB non-cell-autonomously regulates cancer stem cell populations in the basal-like breast cancer subtype, Nat. Commun., 4, 2299, 10.1038/ncomms3299 Sakamoto, 2021, EHF suppresses cancer progression by inhibiting ETS1-mediated ZEB expression, Oncogenesis, 10, 26, 10.1038/s41389-021-00313-2 Suzuki, 2018, Expression of ZEBs in gliomas is associated with invasive properties and histopathological grade, Oncol. Lett., 16, 1758 Manchado, 2016, A combinatorial strategy for treating KRAS-mutant lung cancer, Nature, 534, 647, 10.1038/nature18600 Dittmer, 2015, The role of the transcription factor Ets1 in carcinoma, Semin. Cancer Biol., 35, 20, 10.1016/j.semcancer.2015.09.010 Sinh, 2017, Ets1 and ESE1 reciprocally regulate expression of ZEB1/ZEB2, dependent on ERK1/2 activity, in breast cancer cells, Cancer Sci., 108, 952, 10.1111/cas.13214 Shirakihara, 2013, Identification of integrin α3 as a molecular marker of cells undergoing epithelial-mesenchymal transition and of cancer cells with aggressive phenotypes, Cancer Sci., 104, 1189, 10.1111/cas.12220 Ichikawa, 2022, Ets family proteins regulate the EMT transcription factors Snail and ZEB in cancer cells, FEBS Open Biol., 10.1002/2211-5463.13415 Luk, 2018, ELF3, ELF5, EHF and SPDEF transcription factors in tissue homeostasis and cancer, Molecules, 23, 10.3390/molecules23092191 Yachida, 2016, Genomic sequencing identifies ELF3 as a driver of ampullary carcinoma, Cancer Cell, 29, 229, 10.1016/j.ccell.2015.12.012 Suzuki, 2021, E74-Like Factor 3 is a key regulator of epithelial integrity and immune response genes in biliary tract cancer, Cancer Res., 81, 489, 10.1158/0008-5472.CAN-19-2988 Warzecha, 2010, An ESRP-regulated splicing programme is abrogated during the epithelial-mesenchymal transition, EMBO J., 29, 3286, 10.1038/emboj.2010.195 Ishii, 2014, Epithelial splicing regulatory proteins 1 (ESRP1) and 2 (ESRP2) suppress cancer cell motility via different mechanisms, J. Biol. Chem., 289, 27386, 10.1074/jbc.M114.589432 Preca, 2017, A novel ZEB1/HAS2 positive feedback loop promotes EMT in breast cancer, Oncotarget, 8, 11530, 10.18632/oncotarget.14563 Yamaguchi, 2009, Constitutive activation of nuclear factor-kappaB is preferentially involved in the proliferation of basal-like subtype breast cancer cell lines, Cancer Sci., 100, 1668, 10.1111/j.1349-7006.2009.01228.x Du, 2019, Forkhead box K2 promotes human colorectal cancer metastasis by upregulating ZEB1 and EGFR, Theranostics, 9, 3879, 10.7150/thno.31716 Katsuno, 2021, Epithelial plasticity, epithelial-mesenchymal transition, and the TGF-β family, Dev. Cell, 56, 726, 10.1016/j.devcel.2021.02.028 Tsubakihara, 2018, Epithelial-mesenchymal transition and metastasis under the control of transforming growth factor β, Int. J. Mol. Sci., 19, 3672, 10.3390/ijms19113672 Nishimura, 2006, DeltaEF1 mediates TGF-beta signaling in vascular smooth muscle cell differentiation, Dev. Cell, 11, 93, 10.1016/j.devcel.2006.05.011 Moustakas, 2016, Mechanisms of TGFbeta-induced epithelial-mesenchymal transition, J. Clin. Med., 5, 10.3390/jcm5070063 Saitoh, 2018, Involvement of partial EMT in cancer progression, J. Biochem., 164, 257, 10.1093/jb/mvy047 Shirakihara, 2011, TGF-β regulates isoform switching of FGF receptors and epithelial-mesenchymal transition, EMBO J., 30, 783, 10.1038/emboj.2010.351 Kee, 2000, E2A proteins: essential regulators at multiple stages of B-cell development, Immunol. Rev., 175, 138, 10.1111/j.1600-065X.2000.imr017514.x Norton, 2000, ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis, J. Cell Sci., 113, 3897, 10.1242/jcs.113.22.3897 Kang, 2003, A self-enabling TGFbeta response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells, Mol. Cell, 11, 915, 10.1016/S1097-2765(03)00109-6 Kowanetz, 2004, Id2 and Id3 define the potency of cell proliferation and differentiation responses to transforming growth factor beta and bone morphogenetic protein, Mol. Cell Biol., 24, 4241, 10.1128/MCB.24.10.4241-4254.2004 Kondo, 2004, A role for Id in the regulation of TGF-beta-induced epithelial-mesenchymal transdifferentiation, Cell Death Differ., 11, 1092, 10.1038/sj.cdd.4401467 Batlle, 2000, De Herreros, The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells, Nat. Cell Biol., 2, 84, 10.1038/35000034 Oda, 1998, Dynamic behavior of the cadherin-based cell-cell adhesion system during Drosophila gastrulation, Dev. Biol., 203, 435, 10.1006/dbio.1998.9047 Carver, 2001, The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition, Mol. Cell Biol., 21, 8184, 10.1128/MCB.21.23.8184-8188.2001 Barrallo-Gimeno, 2005, The Snail genes as inducers of cell movement and survival: implications in development and cancer, Development, 132, 3151, 10.1242/dev.01907 Zheng, 2015, Epithelial-to-mesenchymal transition is dispensable for metastasis but induces chemoresistance in pancreatic cancer, Nature, 527, 525, 10.1038/nature16064 Horiguchi, 2009, Role of Ras signaling in the induction of snail by transforming growth factor-β, J. Biol. Chem., 284, 245, 10.1074/jbc.M804777200 Peinado, 2003, Transforming growth factor beta-1 induces snail transcription factor in epithelial cell lines: mechanisms for epithelial mesenchymal transitions, J. Biol. Chem., 278, 21113, 10.1074/jbc.M211304200 Su, 2020, TGF-β orchestrates fibrogenic and developmental EMTs via the RAS effector RREB1, Nature, 577, 566, 10.1038/s41586-019-1897-5 Saitoh, 2016, STAT3 integrates cooperative Ras and TGF-β signals that induce Snail expression, Oncogene, 35, 1049, 10.1038/onc.2015.161 Thuault, 2006, Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition, J. Cell Biol., 174, 175, 10.1083/jcb.200512110 Kaufhold, 2014, Central role of Snail1 in the regulation of EMT and resistance in cancer: a target for therapeutic intervention, J. Exp. Clin. Cancer Res, 33, 62, 10.1186/s13046-014-0062-0 Zhu, 2013, Hypoxia-induced snail expression through transcriptional regulation by HIF-1α in pancreatic cancer cells, Dig. Dis. Sci., 58, 3503, 10.1007/s10620-013-2841-4 Barberà, 2004, Regulation of Snail transcription during epithelial to mesenchymal transition of tumor cells, Oncogene, 23, 7345, 10.1038/sj.onc.1207990 Grotegut, 2006, Hepatocyte growth factor induces cell scattering through MAPK/Egr-1-mediated upregulation of Snail, Embo J., 25, 3534, 10.1038/sj.emboj.7601213 Palmer, 2009, Yin yang 1 regulates the expression of snail through a distal enhancer, Mol. Cancer Res., 7, 221, 10.1158/1541-7786.MCR-08-0229 Jiang, 1998, The Slug gene is not essential for mesoderm or neural crest development in mice, Dev. Biol., 198, 277, 10.1016/S0012-1606(98)80005-5 Chen, 2013, Compensatory regulation of the Snai1 and Snai2 genes during chondrogenesis, J. Bone Min. Res., 28, 1412, 10.1002/jbmr.1871 Inoue, 2002, Slug, a highly conserved zinc finger transcriptional repressor, protects hematopoietic progenitor cells from radiation-induced apoptosis in vivo, Cancer Cell, 2, 279, 10.1016/S1535-6108(02)00155-1 Lee, 2017, Evaluation of Slug expression is useful for predicting lymph node metastasis and survival in patients with gastric cancer, BMC Cancer, 17, 670, 10.1186/s12885-017-3668-8 Yao, 2016, IGF/STAT3/NANOG/Slug signaling axis simultaneously controls epithelial-mesenchymal transition and stemness maintenance in colorectal cancer, Stem Cells, 34, 820, 10.1002/stem.2320 Nakamura, 2018, Reciprocal expression of Slug and Snail in human oral cancer cells, PLoS One, 13, 10.1371/journal.pone.0199442 Bradley, 2013, The snail family gene snai3 is not essential for embryogenesis in mice, PLoS One, 8, 10.1371/journal.pone.0065344 Thisse, 1987, The twist gene: isolation of a Drosophila zygotic gene necessary for the establishment of dorsoventral pattern, Nucleic Acids Res., 15, 3439, 10.1093/nar/15.8.3439 Firulli, 2008, Phosphoregulation of Twist1 provides a mechanism of cell fate control, Curr. Med. Chem., 15, 2641, 10.2174/092986708785908987 Firulli, 2005, Altered Twist1 and Hand2 dimerization is associated with Saethre-Chotzen syndrome and limb abnormalities, Nat. Genet., 37, 373, 10.1038/ng1525 Zhao, 2017, Multiple biological functions of Twist1 in various cancers, Oncotarget, 8, 20380, 10.18632/oncotarget.14608 Bourgeois, 1998, The variable expressivity and incomplete penetrance of the twist-null heterozygous mouse phenotype resemble those of human Saethre-Chotzen syndrome, Hum. Mol. Genet., 7, 945, 10.1093/hmg/7.6.945 Sosic, 2003, Twist regulates cytokine gene expression through a negative feedback loop that represses NF-kappaB activity, Cell, 112, 169, 10.1016/S0092-8674(03)00002-3 Yang, 2004, Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis, Cell, 117, 927, 10.1016/j.cell.2004.06.006 Lee, 2006, Twist overexpression correlates with hepatocellular carcinoma metastasis through induction of epithelial-mesenchymal transition, Clin. Cancer Res., 12, 5369, 10.1158/1078-0432.CCR-05-2722 Meng, 2018, Twist1 regulates vimentin through Cul2 circular RNA to promote EMT in hepatocellular carcinoma, Cancer Res., 78, 4150, 10.1158/0008-5472.CAN-17-3009 Sadrkhanloo, 2022, STAT3-EMT axis in tumors: Modulation of cancer metastasis, stemness and therapy response, Pharmacol. Res., 182, 10.1016/j.phrs.2022.106311 Shiota, 2012, Clusterin mediates TGF-β-induced epithelial-mesenchymal transition and metastasis via Twist1 in prostate cancer cells, Cancer Res., 72, 5261, 10.1158/0008-5472.CAN-12-0254 Cho, 2013, STAT3 mediates TGF-β1-induced TWIST1 expression and prostate cancer invasion, Cancer Lett., 336, 167, 10.1016/j.canlet.2013.04.024 Hu, 2018, Sox5 contributes to prostate cancer metastasis and is a master regulator of TGF-beta-induced epithelial mesenchymal transition through controlling Twist1 expression, Br. J. Cancer, 118, 88, 10.1038/bjc.2017.372 Cherukunnath, 2022, KLF8 is activated by TGF-beta1 via Smad2 and contributes to ovarian cancer progression, J. Cell Biochem., 123, 921, 10.1002/jcb.30235 Wang, 2011, KLF8 promotes human breast cancer cell invasion and metastasis by transcriptional activation of MMP9, Oncogene, 30, 1901, 10.1038/onc.2010.563 Reichert, 2013, The Prrx1 homeodomain transcription factor plays a central role in pancreatic regeneration and carcinogenesis, Genes Dev., 27, 288, 10.1101/gad.204453.112 Ocana, 2012, Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1, Cancer Cell, 22, 709, 10.1016/j.ccr.2012.10.012 Zheng, 2015, Down-regualtion of miR-106b induces epithelial-mesenchymal transition but suppresses metastatic colonization by targeting Prrx1 in colorectal cancer, Int. J. Clin. Exp. Pathol., 8, 10534 Takano, 2016, Prrx1 isoform switching regulates pancreatic cancer invasion and metastatic colonization, Genes Dev., 30, 233, 10.1101/gad.263327.115 Liu, 2014, Overexpressed FOXC2 in ovarian cancer enhances the epithelial-to-mesenchymal transition and invasion of ovarian cancer cells, Oncol. Rep., 31, 2545, 10.3892/or.2014.3119 Yu, 2009, A developmentally regulated inducer of EMT, LBX1, contributes to breast cancer progression, Genes Dev., 23, 1737, 10.1101/gad.1809309 Micalizzi, 2009, The Six1 homeoprotein induces human mammary carcinoma cells to undergo epithelial-mesenchymal transition and metastasis in mice through increasing TGF-beta signaling, J. Clin. Invest., 119, 2678, 10.1172/JCI37815 Hartwell, 2006, The Spemann organizer gene, Goosecoid, promotes tumor metastasis, Proc. Natl. Acad. Sci. USA, 103, 18969, 10.1073/pnas.0608636103 Campbell, 2011, Specific GATA factors act as conserved inducers of an endodermal-EMT, Dev. Cell, 21, 1051, 10.1016/j.devcel.2011.10.005