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Biomarkers for epithelial-mesenchymal transitions
Open accessAbstract
Somatic cells that change from one mature phenotype to another exhibit the property of plasticity. It is increasingly clear that epithelial and endothelial cells enjoy some of this plasticity, which is easily demonstrated by studying the process of epithelial-mesenchymal transition (EMT). Published reports from the literature typically rely on ad hoc criteria for determining EMT events; consequently, there is some uncertainty as to whether the same process occurs under different experimental conditions. As we discuss in this Personal Perspective, we believe that context and various changes in plasticity biomarkers can help identify at least three types of EMT and that using a collection of criteria for EMT increases the likelihood that everyone is studying the same phenomenon - namely, the transition of epithelial and endothelial cells to a motile phenotype.
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“Moreover, proteins in the most significantly up-regulated network module (Extended Data Fig. 10d, 10f) included collagens (COL1A1 and COL3A1) and extracellular matrix glycoproteins (FN1, BGN, FBN1, and FBN2) that also are markers of EMT34, 35.”
From Proteogenomic characterization of human colon and rectal cancer (2014) · cites this paper as [35]
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“Individual genes upregulated by TWIST1 known to promote EMT and/or GBM invasion included SNAI2, MMP2, HGF, FAP and FN1.”
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“…increased motility and has the potential to cross through the basal membrane by loosing the adherent and tight junction that helps them to communicate with the neighboring cells (Figure 2; Heerboth et al., 2015; Kalluri & Neilson, 2003; Kim et al., 2017; Son & Moon, 2010; Zeisberg & Neilson, 2009).”
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“homeobox 1 (ZEB1), ZEB2, and/or E47, which can bind to E-cadherin promoter and inhibit its transcription activity and expression [2].”
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“In this line, downregulation or loss of function of proteins involved in epithelial homeostasis such as tight junction components [claudins, occludins, ZO-1 (zonula occludens-1)] is frequently observed in several carcinomas (Steinestel et al., 2014; Zeisberg and Neilson, 2009), whereas the expression shift from epithe…”
BackgroundInfluentialEpithelial-to-Mesenchymal Transition in Diabetic Nephropathy: Fact or Fiction?
Loeffler, I., & Wolf, G. (2015) · Cells · doi:10.3390/cells4040631 · Cited by 254
“four key events, to increase the likelihood that everyone is studying the same phenomenon [51].”
BackgroundInfluentialJolly, M. K., Ward, C., Eapen, M. S., Myers, S., Hällgren, O., Levine, H., & Sohal, S. S. (2017) · Developmental Dynamics · doi:10.1002/dvdy.24541 · Cited by 252
The role of EMT and MET in cancer dissemination
Banyard, J., & Bielenberg, D. R. (2015) · Connective Tissue Research · doi:10.3109/03008207.2015.1060970 · Cited by 248
“Evidence compiled from references within this review and other literatures (13,27,103).”
BackgroundZhang, Q., Bai, X., Chen, W., Ma, T., Hu, Q., Liang, C., Xie, S., Chen, C.-L., Hu, L., Xu, S., et al. (2013) · Carcinogenesis · doi:10.1093/carcin/bgt027 · Cited by 251
“Meanwhile, the cells undergo sophisticated biomolecular changes, such as altered expression of cadherins, rearrangement of the cytoskeleton and activation of specific transcription factors (3,4).”
BackgroundCannito, S., Novo, E., di Bonzo, L. V., Busletta, C., Colombatto, S., & Parola, M. (2010) · Antioxidants & Redox Signaling · doi:10.1089/ars.2009.2737 · Cited by 239
“Moreover, in order to facilitate the reader interested in analyzing recent literature on EMT, we also provide a reference to the recent classification made by Kalluri and Weinberg (114) and by Zeisberg and Neilson (298).”
InfluentialNF-kappaB: Two Sides of the Same Coin
Pires, B. R. B., Silva, R. C. M. C., Ferreira, G. M., & Abdelhay, E. S. F. W. (2018) · Genes · doi:10.3390/genes9010024 · Cited by 243
“During this biological process, transcription factors, such as SNAIL, SLUG, ZEB1, SIP1, and TWIST1, repress adhesion molecules (E-cadherin, claudins, and occludins) and stimulate markers of the mesenchymal phenotype (N-cadherin, imentin, and ibronectin) [133,134].”
BackgroundShaykhiev, R., Otaki, F. A., Bonsu, P., Dang, D. T., Teater, M. R., Strulovici‐Barel, Y., Salit, J., Harvey, B., & Crystal, R. G. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0500-x · Cited by 236
“Upregulation of CDH2 and downregulation of CDH1 are the central EMT features in human lung cancer [28].”
BackgroundInfluentialRichardson, A. M., Havel, L. S., Koyen, A. E., Konen, J. M., Shupe, J. A., Wiles, W. G., Martin, W. D., Grossniklaus, H. E., Sica, G., Gilbert‐Ross, M., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-17-1776 · Cited by 229
“These events can be transient as cells transition through partial and reversible EMT states (6-9), and it is debated whether a full EMT is necessary for metastasis (10, 11).”
Epithelial to mesenchymal transition in head and neck squamous cell carcinoma
Smith, A., Teknos, T. N., & Pan, Q. (2012) · Oral Oncology · doi:10.1016/j.oraloncology.2012.10.009 · Cited by 233
“2).(8) Epithelial cells are characterized by stable cell–cell contacts and the formation of adherents junctions.”
BackgroundInfluentialMicro‐RNA signature of the epithelial–mesenchymal transition in endometrial carcinosarcoma
Castilla, M. Á., Moreno‐Bueno, G., Romero‐Pérez, L., de Vijver, K. K. V., Biscuola, M., López‐García, M. Á., Prat, J., Matías‐Guiu, X., Cano, A., Oliva, E., et al. (2010) · The Journal of Pathology · doi:10.1002/path.2802 · Cited by 228
“Since TGFβ signalling is one of the major events implicated in EMT in different cell systems [6], we investigated TGFβ1 and TGFβ2 expression in the two components of ECS.”
BackgroundInfluentialTGF‐β regulates isoform switching of FGF receptors and epithelial–mesenchymal transition
Shirakihara, T., Horiguchi, K., Miyazawa, K., Ehata, S., Shibata, T., Morita, I., Miyazono, K., & Saitoh, M. (2011) · The EMBO Journal · doi:10.1038/emboj.2010.351 · Cited by 225
“Recent studies have proposed that EMT can be classified into three subtypes based on the biological context (Thiery and Sleeman, 2006; Kalluri and Weinberg, 2009; Kalluri, 2009; Zeisberg and Neilson, 2009).”
Scholten, D., Österreicher, C. H., Scholten, A., Iwaisako, K., Gu, G., Brenner, D. A., & Kisseleva, T. (2010) · Gastroenterology · doi:10.1053/j.gastro.2010.05.005 · Cited by 231
Pancreatic stellate cells promote epithelial-mesenchymal transition in pancreatic cancer cells
Kikuta, K., Masamune, A., Watanabe, T., Ariga, H., Itoh, H., Hamada, S., Satoh, K., Egawa, S., Unno, M., & Shimosegawa, T. (2010) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2010.11.040 · Cited by 224
Zeisberg, M., & Duffield, J. S. (2010) · Journal of the American Society of Nephrology · doi:10.1681/asn.2010060616 · Cited by 224
Self-citationPeng, X., Guo, W., Liu, T., Wang, X., Tu, X.-A., Xiong, D., Chen, S., Lai, Y., Du, H., Chen, G., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020341 · Cited by 225
“Recent work has demonstrated several miRNAs, including miR-200 family and miR-205, played critical roles in EMT [41,42].”
BackgroundChoi, S. S., Omenetti, A., Witek, R. P., Moylan, C. A., Syn, W.-K., Jung, Y., Yang, L., Sudan, D. L., Sicklick, J. K., Michelotti, G. A., et al. (2009) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00292.2009 · Cited by 219
Decoding the transcriptome of calcified atherosclerotic plaque at single-cell resolution
Alsaigh, T., Evans, D., Frankel, D. A., & Torkamani, A. (2022) · Communications Biology · doi:10.1038/s42003-022-04056-7 · Cited by 241
Jordan, N. V., Johnson, G. L., & Abell, A. N. (2011) · Cell Cycle · doi:10.4161/cc.10.17.17188 · Cited by 230
“1).(4,10) Developmental EMTs constitute the first EMT subtype and include implantation, gastrulation and neural crest formation.”
BackgroundOrigin and functional heterogeneity of fibroblasts
LeBleu, V. S., & Neilson, E. G. (2020) · The FASEB Journal · doi:10.1096/fj.201903188r · Cited by 231
Self-citationTissue geometry patterns epithelial–mesenchymal transition via intercellular mechanotransduction
Gomez, E. W., Chen, Q. K., Gjorevski, N., & Nelson, C. M. (2010) · Journal of Cellular Biochemistry · doi:10.1002/jcb.22545 · Cited by 214
“Endogenous (cell-generated) mechanical stresses arising from isometric cytoskeletal tension are transmitted within tissues between cells, their neighbors, and the surrounding extracellular matrix.”
BackgroundRoads to melanoma: Key pathways and emerging players in melanoma progression and oncogenic signaling
Paluncic, J., Kovačević, Ž., Jansson, P. J., Kalinowski, D. S., Merlot, A. M., Huang, M., Lok, H. C., Sahni, S., Lane, D. J. R., & Richardson, D. R. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2016.01.025 · Cited by 236
Fu, X., Liu, M., Qu, S., Ma, J., Zhang, Y., Shi, T., Wen, H., Yang, Y., Wang, S., Wang, J., et al. (2018) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-018-0677-7 · Cited by 217
“the main criteria for EMT [41] in miR-32-5p up- and down-regulated cell lines as well as in xenograft tumors”
BackgroundRetractedChen, Y. S., Pelekanos, R., Ellis, R., Horne, R., Wolvetang, E. J., & Fisk, N. M. (2012) · Stem Cells Translational Medicine · doi:10.5966/sctm.2011-0022 · Cited by 210
Plasticity of disseminating cancer cells in patients with epithelial malignancies
Bednarz‐Knoll, N., Alix‐Panabières, C., & Pantel, K. (2012) · Cancer and Metastasis Reviews · doi:10.1007/s10555-012-9370-z · Cited by 221
“smooth-muscle actin, fibronectin and vitronectin—the mesenchymal one [12–14].”
BackgroundInfluentialMesothelial cells in tissue repair and fibrosis
Mutsaers, S. E., Birnie, K. A., Lansley, S. M., Herrick, S. E., Lim, C.-B., & PrÃale, C. M. (2015) · Frontiers in Pharmacology · doi:10.3389/fphar.2015.00113 · Cited by 223
“…et al., 1992; Cannistra et al., 1994; Liberek et al., 1996; van Grevenstein et al., 2007) to further recruit more leukocytes to the site of injury and facilitate leukocyte adherence and migration across the mesothelium (Liberek et al., 1996; Jantz and Antony, 2008; Yung and Chan, 2009, 2012).”
BackgroundInfluentialTissue remodelling in chronic bronchial diseases: from the epithelial to mesenchymal phenotype
Pain, M., Bermúdez, O. M., Lacoste, P., Royer, P., Botturi, K., Tissot, A., Brouard, S., Eickelberg, O., & Magnan, A. (2014) · European Respiratory Review · doi:10.1183/09059180.00004413 · Cited by 212
Zhang, Q., Duan, J., Liu, X., & Guo, S.-W. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.03.015 · Cited by 211
Astrocytes, the rising stars of the glioblastoma microenvironment
Brandao, M., Simon, T. R., Critchley, G. R., & Giamas, G. (2018) · Glia · doi:10.1002/glia.23520 · Cited by 218
“Furthermore, the ECM of astrocytes with mutated p53 also showed increased levels of fibronectin and laminin—proteins known to trigger epithelial to mesenchymal transition (EMT), through which tumor cells acquire a more migratory and invasive phenotype (Chen et al., 2013; Zeisberg & Neilson, 2009).”
BackgroundYan, L., Zhou, J., Gao, Y. H., Ghazal, S., Lu, L., Bellone, S., Yang, Y., Liu, N., Zhao, X., Santin, A. D., et al. (2014) · Oncogene · doi:10.1038/onc.2014.236 · Cited by 209
Mitochondrial ROS and cancer drug resistance: Implications for therapy
Okon, I. S., & Zou, M.-H. (2015) · Pharmacological Research · doi:10.1016/j.phrs.2015.06.013 · Cited by 207
“During EMT, non-motile parental cells, gain motility with associated expression of targets typically required during early developmental stages [6,7].”
Background
Metadata
- Authors
- Zeisberg, M., & Neilson, E. G.
- Affiliations
- Beth Israel Deaconess Medical Center (US)
- Vanderbilt University (US)
- Venue
- Journal of Clinical Investigation
- Published
- 2009-06-01
- Volume
- 119
- Issue
- 6
- Pages
- 1429-1437
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC2689132
- OpenAlex
- W1996118868
- Cited by
- 2,299
- References
- 124
- Citations by year
- 2026: 50 · 2025: 79 · 2024: 127 · 2023: 113 · 2022: 146 · 2021: 148 · 2020: 180 · 2019: 163 · 2018: 170 · 2017: 189 · 2016: 153 · 2015: 162 · 2014: 162 · 2013: 149 · 2012: 109
- FWCI
- 8.93
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R03DK081687, R01DK046282, DK46282, K08DK074558, DK-081687, DK074558)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Health Sciences › Medicine › Immunology and Allergy › Cell Adhesion Molecules Research
- Keywords
- epithelial-mesenchymal transition, cellular plasticity, epithelial cells, endothelial cells, cell motility
- MeSH terms
- Animals, Cell Differentiation, Epithelial Cells, Fibroblasts, Humans, Neoplasms, Biomarkers, Mesenchymal Stem Cells
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