Cited by 2,299Cancer Cells and MetastasisTGF-β signaling in diseasesCell Adhesion Molecules Research

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Biomarkers for epithelial-mesenchymal transitions

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Zeisberg, Michael, Neilson, Eric G.·2009·Journal of Clinical Investigation

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Abstract

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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Caveolin-1-negative head and neck squamous cell carcinoma primary tumors display increased epithelial to mesenchymal transition and prometastatic properties
Jung, A. C., Ray, A., Ramolu, L., Macabre, C., Simon, F., Noulet, F., Blandin, A.-F., Renner, G., Lehmann, M., Choulier, L., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.6099 · Cited by 41
“Cells undergoing type 3 EMT (carcinoma-metastatic transitions) are characterized by an integrin switch and a change in the extracellular matrix (for review [35]).”
Combination Therapy Targeting BCL6 and Phospho-STAT3 Defeats Intratumor Heterogeneity in a Subset of Non–Small Cell Lung Cancers
Deb, D., Rajaram, S., Larsen, J. E., Dospoy, P. D., Marullo, R., Li, L. S., Avila, K., Xue, F., Cerchietti, L. C. A., Minna, J. D., et al. (2017) · Cancer Research · doi:10.1158/0008-5472.can-15-3052 · Cited by 41
“For β-CATENIN, we measured total intensity in the cytoplasm to capture its loss in the cell membrane and cytoplasm (as in other studies that make use of β-CATENIN as readout of Epithelial to Mesenchymal Transition (EMT)(17-19)).”
Cdc20 overexpression is involved in temozolomide-resistant glioma cells with epithelial-mesenchymal transition
Wang, J., Zhou, F., Li, Y., Li, Q., Wu, Z., Yu, L., Yuan, F., Liu, J., Tian, Y., Cao, Y. W., et al. (2017) · Cell Cycle · doi:10.1080/15384101.2017.1388972 · Cited by 41
The Many-Faced Program of Epithelial–Mesenchymal Transition: A System Biology-Based View
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“The recognition of EMT in tissues relies on the detection of specific epithelial and mesenchymal markers including cell-surface markers such as E-cadherin and cytoskeletal markers such as Vimentin and α-smooth muscle actin (5).”
Background
Angiopoietin-1 deficiency increases renal capillary rarefaction and tubulointerstitial fibrosis in mice
Loganathan, K., Said, E. S., Winterrowd, E., Orebrand, M., He, L., Vanlandewijck, M., Betsholtz, C., Quaggin, S. E., & Jeansson, M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0189433 · Cited by 41
Nogo-B receptor promotes epithelial–mesenchymal transition in non-small cell lung cancer cells through the Ras/ERK/Snail1 pathway
Wu, D., Zhao, B., Qi, X., Peng, F., Fu, H., Chi, X., Miao, Q., & Shao, S. (2018) · Cancer Letters · doi:10.1016/j.canlet.2018.01.030 · Cited by 41
“During lung carcinogenesis, normal lung epithelial cells undergo malignant transformation through an undefined etiology and mechanism; moreover, NSCLC progression may involve tumor epithelial–mesenchymal transition (EMT) to promote tumor cell invasion and metastasis [4,5].”
Background
Slug contributes to gemcitabine resistance through epithelial-mesenchymal transition in CD133+ pancreatic cancer cells
Tsukasa, K., Ding, Q., Yoshimitsu, M., Miyazaki, Y., Matsubara, S., & Takao, S. (2015) · Human Cell · doi:10.1007/s13577-015-0117-3 · Cited by 41
“In the present study, Slug knock-down of Capan-1M9 cells effectively reduced migratory and invasive abilities by migration, invasion and wound-healing assays, showing the consistency with the EMT phenotype [13].”
BackgroundResult
Impact of miR‐192 and miR‐194 on cyst enlargement through EMT in autosomal dominant polycystic kidney disease
Kim, D. Y., Woo, Y. M., Lee, S., Oh, S., Shin, Y., Shin, J.-O., Park, E. Y., Ko, J. Y., Lee, E. J., Bok, J., et al. (2018) · The FASEB Journal · doi:10.1096/fj.201800563rr · Cited by 41
Morphology-based prediction of cancer cell migration using an artificial neural network and a random decision forest
Zhang, Z., Chen, L., Humphries, B. A., Brien, R., Wicha, M. S., Luker, K. E., Luker, G. D., Chen, Y., & Yoon, E. (2018) · Integrative Biology · doi:10.1039/c8ib00106e · Cited by 41
Ataxin-1 regulates epithelial-mesenchymal transition of cervical cancer cells
Kang, A., An, H.-T., Ko, J., & Kang, S. (2017) · Oncotarget · doi:10.18632/oncotarget.15319 · Cited by 41
“…the epithelial–mesenchymal transition (EMT), a highly conserved process by which polarized epithelial cells are converted into mesenchymal cells characterized by the loss of E-cadherin-mediated cell–cell contacts, as well as the acquisition of increased migratory and invasive potential [15–19].”
A biomimetic tumor model of heterogeneous invasion in pancreatic ductal adenocarcinoma
Bradney, M. J., Venis, S. M., Yang, Y., Konieczny, S. F., & Han, B. (2020) · Small · doi:10.1002/smll.201905500 · Cited by 38
TRPM7 Ion Channel: Oncogenic Roles and Therapeutic Potential in Breast Cancer
Cordier, C., Prevarskaya, N. B., & Lehen’kyi, V. (2021) · Cancers · doi:10.3390/cancers13246322 · Cited by 42
From senescence to scarring: Exploring TGF-β signaling in cellular aging, fibrotic remodeling, and pulmonary fibrosis
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Decreased eIF3e/Int6 expression causes epithelial-to-mesenchymal transition in breast epithelial cells
Gillis, L. D., & Lewis, S. M. (2012) · Oncogene · doi:10.1038/onc.2012.371 · Cited by 40
Tumor necrosis factor‐α modulates epithelial mesenchymal transition mediators ZEB2 and S100A4 to promote cholangiocarcinoma progression
Techasen, A., Namwat, N., Loilome, W., Duangkumpha, K., Puapairoj, A., Saya, H., & Yongvanit, P. (2014) · Journal of Hepato-Biliary-Pancreatic Sciences · doi:10.1002/jhbp.125 · Cited by 40
“In particular, activation of the transcriptional factors enables the changes in gene expression patterns underlying EMT such as epithelial protein, E-cadherin and mesenchymal proteins, N-cadherin and S100A4 leading to trigger a metastatic potential phenotype of cancer cells [9–12].”
Background
Epithelial-Mesenchymal Transition Phenotype Is Associated with Clinicopathological Factors That Indicate Aggressive Biological Behavior and Poor Clinical Outcomes in Invasive Breast Cancer
Bae, Y. K., Choi, J. E., Kang, S. H., & Lee, S. J. (2015) · Journal of Breast Cancer · doi:10.4048/jbc.2015.18.3.256 · Cited by 40
“A variety of biomarkers, including transcription factors (zinc finger factor SNAIL [Snail], snail2 [slug], zinc finger Ebox-binding homeobox 1 [ZEB1], twist, and forkhead box protein 2 [FOXC2]), extracellular matrix proteins (fibronectin and laminin), cell surface proteins (E-cadherin and N-cadherin), and cytoskeletal…”
Background
Proteomics profiling identify CAPS as a potential predictive marker of tamoxifen resistance in estrogen receptor positive breast cancer
Johansson, H. J., Sanchez, B. C., Forshed, J., Stål, O., Fohlin, H., Lewensohn, R., Hall, P. N., Bergh, J. C. S., Lehtiö, J., & Linderholm, B. K. (2015) · Clinical Proteomics · doi:10.1186/s12014-015-9080-y · Cited by 40
“These were involved in processes such as calcium (Ca) signaling, metabolism, epithelial mesenchymal transition, metastasis and invasion [12-14].”
Background
The role of hERG1 ion channels in epithelial-mesenchymal transition and the capacity of riluzole to reduce cisplatin resistance in colorectal cancer cells
Fortunato, A. (2017) · Cellular Oncology · doi:10.1007/s13402-017-0328-6 · Cited by 40
“A number of genes associated with EMT has been identified [13, 14], but the role”
Galectin-8 induces partial epithelial–mesenchymal transition with invasive tumorigenic capabilities involving a FAK/EGFR/proteasome pathway in Madin–Darby canine kidney cells
Oyanadel, C., Holmes, C., Pardo, E., Retamal, C., Shaughnessy, R., Smith, P. C., Cortés, P., Bravo‐Zehnder, M., Metz, C., Feuerhake, T., et al. (2018) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-05-0301 · Cited by 40
“We also found nuclear translocation reflecting activation of β-catenin (Figure 6B), another well-characterized EMT marker (Zeisberg and Neilson, 2009).”
BackgroundInfluential
Twist Expression in Circulating Hepatocellular Carcinoma Cells Predicts Metastasis and Prognoses
Yin, L.-C., Luo, Z., Gao, Y.-X., Yang, L., Peng, Q., & Gao, Y. (2018) · BioMed Research International · doi:10.1155/2018/3789613 · Cited by 40
Tubastatin�A, an inhibitor of HDAC6, enhances temozolomide‑induced apoptosis and reverses the malignant phenotype of glioblastoma cells
Urdiciain, A., Erausquin, E., Mel�ndez, B., REY, J. A., Idoate, M. A., & Castresana, J. S. (2019) · International Journal of Oncology · doi:10.3892/ijo.2019.4739 · Cited by 40
“Epithelial-mesenchymal transition (EMT) is the biological process by which cells lose their epithelial characteristics and acquire a mesenchymal cell phenotype, which includes enhanced migratory capacity, invasiveness, elevated resistance to apoptosis and increased production of extracellular matrix components (22,24-…”
Background
Endoplasmic reticulum stress regulates epithelial‑mesenchymal transition in human lens epithelial cells
Zhou, S., Yang, J., Wang, M., Zheng, D., & Liu, Y. (2019) · Molecular Medicine Reports · doi:10.3892/mmr.2019.10814 · Cited by 40
“eMT cell characteristics include the acquisition of a spindle-shaped morphology that is accompanied by an accumulation of α-smooth muscle actin (α-SMa), a redistribution of actin stress fibers, a loss of cell polarity and epithelial markers such as cytokeratin, zonula occludens-1 and epithelial cadherin (e-cadherin),…”
Background
Mesothelial-to-Mesenchymal Transition Contributes to the Generation of Carcinoma-Associated Fibroblasts in Locally Advanced Primary Colorectal Carcinomas
Gordillo, C. H., Sandoval, P., Muñoz‐Hernández, P., Pascual‐Antón, L., López‐Cabrera, M., & Jiménez-Heffernan, J. A. (2020) · Cancers · doi:10.3390/cancers12020499 · Cited by 40
“However, our data strongly disagree with this theory, since we have frequently found Fsp-1 (fibroblast-specific protein) in the preserved mesothelium next to advanced neoplasm regions.”
BackgroundInfluential
Oviduct as a sensor of embryo quality: deciphering the extracellular vesicle (EV)-mediated embryo-maternal dialogue
Dissanayake, K., Nõmm, M., Lättekivi, F., Ord, J., Ressaissi, Y., Godakumara, K., Reshi, Q. U. A., Viil, J., Jääger, K., Velthut‐Meikas, A., et al. (2021) · Journal of Molecular Medicine · doi:10.1007/s00109-021-02042-w · Cited by 42
Cadherin-11 in Renal Cell Carcinoma Bone Metastasis
Satcher, R. L., Pan, T., Cheng, C.-J., Lee, Y.-C., Lin, S.-C., Yu, G., Li, X., Hoang, A. G., Tamboli, P., Jonasch, E. W., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089880 · Cited by 40
“This possibility is supported by recent studies indicating that cadherins play important roles in the process of EMT during both normal embryonic development and cancer progression [33,34,35].”
Result
Molecular events in endometrial carcinosarcomas and the role of high mobility group AT-hook 2 in endometrial carcinogenesis
Romero‐Pérez, L., Castilla, M. Á., López‐García, M. Á., Díaz‐Martín, J., Biscuola, M., Ramiro-Fuentes, S., Oliva, E., Matías‐Guiu, X., Prat, J., Cano, A., et al. (2012) · Human Pathology · doi:10.1016/j.humpath.2012.05.013 · Cited by 39
Over-expression of regulator of G protein signaling 5 promotes tumor metastasis by inducing epithelial-mesenchymal transition in hepatocellular carcinoma cells
Hu, M., Chen, X., Zhang, J., Wang, D., Fang, X., Wang, X., Wang, G., Chen, G., Jiang, X., Xia, H., et al. (2013) · Journal of Surgical Oncology · doi:10.1002/jso.23367 · Cited by 39
“The process of EMT involves a disassembly of cell–cell junctions and increased cell motility and invasion, as characterized by down‐regulation of E‐cadherin and up‐regulation of mesenchymal molecular markers such as vimentin [13].”
Background
SERPINI1 regulates epithelial–mesenchymal transition in an orthotopic implantation model of colorectal cancer
Matsuda, Y., Miura, K., Yamane, J., Shima, H., Fujibuchi, W., Ishida, K., Fujishima, F., Ohnuma, S., Sasaki, H., Nagao, M., et al. (2016) · Cancer Science · doi:10.1111/cas.12909 · Cited by 39
Signalling pathways associated with IL ‐6 production and epithelial–mesenchymal transition induction in prostate epithelial cells stimulated with Trichomonas vaginalis
Han, I., Kim, J. H., Kim, S. S., Ahn, M., & Ryu, J. S. (2016) · Parasite Immunology · doi:10.1111/pim.12357 · Cited by 40
FARNA: knowledgebase of inferred functions of non-coding RNA transcripts
Alam, T., Uludağ, M., Essack, M., Salhi, A., Ashoor, H., Hanks, J. B., Kapfer, C., Mineta, K., Gojobori, T., & Bajić, V. B. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw973 · Cited by 39
The metastasis suppressor CD82/KAI1 inhibits fibronectin adhesion-induced epithelial-to-mesenchymal transition in prostate cancer cells by repressing the associated integrin signaling
Lee, J., Byun, H.-J., Lee, M.-S., Jin, Y., Jeoung, D., Kim, Y., & Lee, H. (2016) · Oncotarget · doi:10.18632/oncotarget.13767 · Cited by 39
Korean Red Ginseng extract reduces hypoxia-induced epithelial-mesenchymal transition by repressing NF-κB and ERK1/2 pathways in colon cancer
Kim, E. J., Kwon, K. A., Lee, Y. E., Kim, J. H., Kim, S.-H., & Kim, J. H. (2017) · Journal of Ginseng Research · doi:10.1016/j.jgr.2017.03.008 · Cited by 39
“Loss of E-cadherin expression is an important prototypical event in EMT [19].”
Background
Mammalian Target of Rapamycin (mTOR) Regulates Transforming Growth Factor-β1 (TGF-β1)-Induced Epithelial-Mesenchymal Transition via Decreased Pyruvate Kinase M2 (PKM2) Expression in Cervical Cancer Cells
Cheng, K., & Hao, M. (2017) · Medical Science Monitor · doi:10.12659/msm.901542 · Cited by 39
“Moreover, Vimentin bestows a motile phenotype to cancer cells through changes in cellular architecture and cellmatrix interactions [4,5].”
Background
Epithelial-to-mesenchymal transition and drug resistance: transitioning away from death
Song, K.-A., & Faber, A. C. (2019) · Journal of Thoracic Disease · doi:10.21037/jtd.2019.06.11 · Cited by 38
Bleomycin induces epithelial-to-mesenchymal transition via bFGF/PI3K/ESRP1 signaling in pulmonary fibrosis
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Breast cancer metastasis to bone: From epithelial to mesenchymal transition to breast osteoblast-like cells
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MiR-182 inhibits proliferation, migration, invasion and inflammation of endometrial stromal cells through deactivation of NF-κB signaling pathway in endometriosis
Wu, M. Y., & Zhang, Y. (2021) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-020-03986-2 · Cited by 39
Epithelial-to-mesenchymal transition hinders interferon-γ-dependent immunosurveillance in lung cancer cells
Tseng, P., Chen, C., Lee, K.-Y., Feng, P., Wang, Y., Satria, R. D., & Lin, C. (2022) · Cancer Letters · doi:10.1016/j.canlet.2022.215712 · Cited by 38
Isoimperatorin down-regulates epithelial mesenchymal transition through modulating NF-κB signaling and CXCR4 expression in colorectal and hepatocellular carcinoma cells
Kim, N. Y., Jung, Y. Y., Yang, M. H., Um, J., Sethi, G., & Ahn, K. S. (2022) · Cellular Signalling · doi:10.1016/j.cellsig.2022.110433 · Cited by 40
Gene regulatory network underlying the immortalization of epithelial cells
Méndez-López, L. F., Dávila-Velderrain, J., Domínguez‐Hüttinger, E., Enríquez-Olguín, C., Martínez‐García, J. C., & Alvarez-Buylla, E. R. (2017) · BMC Systems Biology · doi:10.1186/s12918-017-0393-5 · Cited by 41
“Mesenchymal stem–like cells express the mesenchymal marker Snai2 [18], which acts as one of the key players during the EMT by orchestrating the repression of epithelium–specific genes [65] such as ESE–2 [18] and by inducing the expression of mesenchymal markers [63].”
Systematic review: predictive value of organoids in colorectal cancer
Sakshaug, B. C., Folkesson, E., Haukaas, T. H., Visnes, T., & Flobak, Å. (2023) · Scientific Reports · doi:10.1038/s41598-023-45297-8 · Cited by 40
IL-1β-activated PI3K/AKT and MEK/ERK pathways coordinately promote induction of partial epithelial–mesenchymal transition
Tabei, Y., & Nakajima, Y. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01775-8 · Cited by 37
“The hallmarks of EMT are the downregulation of epithelial markers such as E-cadherin and occludin and the upregulation of mesenchymal markers such as vimentin and fibronectin [5].”
Background

Authors: Zeisberg, M., & Neilson, E. G.
Affiliations: Beth Israel Deaconess Medical Center (US)
Vanderbilt University (US)
ORCID: Zeisberg, Michael
Neilson, Eric G.
Venue: Journal of Clinical Investigation
Publisher: American Society for Clinical Investigation
Published: 2009-06-01
Volume: 119
Issue: 6
Pages: 1429-1437
ISSN: 0021-9738 (ISSN-L)
DOI: 10.1172/jci36183
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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Biomarkers for epithelial-mesenchymal transitions

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