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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Basic Transcription Factor 3 Is Required for Proliferation and Epithelial‐Mesenchymal Transition via Regulation of FOXM1 and JAK2/STAT3 Signaling in Gastric Cancer
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Testes-specific protease 50 (TSP50) promotes invasion and metastasis by inducing EMT in gastric cancer
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CLCA4 inhibits cell proliferation and invasion of hepatocellular carcinoma by suppressing epithelial-mesenchymal transition via PI3K/AKT signaling
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An in vitro study of scarring formation mediated by human Tenon fibroblasts: Effect of Y‐27632, a Rho kinase inhibitor
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The critical role of glucose deprivation in epithelial-mesenchymal transition in hepatocellular carcinoma under hypoxia
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UDP-glucose 6-dehydrogenase knockout impairs migration and decreases in vivo metastatic ability of breast cancer cells
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Genes involved in the epithelial-mesenchymal transition in oral cancer: A systematic review
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“This transition can impair the adhesion of epithelial cells and enhance motility [24].”
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N-cadherin expression is correlated with metastasis of spindle cell carcinoma of head and neck region
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Short hairpin RNA targeting FOXQ1 inhibits invasion and metastasis via the reversal of epithelialmesenchymal transition in bladder cancer
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USP22 knockdown enhanced chemosensitivity of hepatocellular carcinoma cells to 5-Fu by up-regulation of Smad4 and suppression of Akt
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The Prognostic Impact of TGF-β1, Fascin, NF-κB and PKC-ζ Expression in Soft Tissue Sarcomas
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Lack of Radiation Dose or Quality Dependence of Epithelial-to-Mesenchymal Transition (EMT) Mediated by Transforming Growth Factor β
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MicroRNA-328 Inhibits Renal Tubular Cell Epithelial-to-Mesenchymal Transition by Targeting the CD44 in Pressure-Induced Renal Fibrosis
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Mesenchymal to Epithelial Transition Mediated by CDH1 Promotes Spontaneous Reprogramming of Male Germline Stem Cells to Pluripotency
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“CDH1 is one of the defining features of the epithelial state (Zeisberg and Neilson, 2009).”
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LncRNA FUNDC2P4 down-regulation promotes epithelial–mesenchymal transition by reducing E-cadherin expression in residual hepatocellular carcinoma after insufficient radiofrequency ablation
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Oxidized low density lipoprotein induces endothelial-to-mesenchymal transition by stabilizing Snail in human aortic endothelial cells
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Identification of LIMK2 as a therapeutic target in castration resistant prostate cancer
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Proteomics Highlights Common and Distinct Pathophysiological Processes Associated with Ileal and Colonic Ulcers in Crohn’s Disease
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Wilms’ tumor 1 ( WT1 ) promotes ovarian cancer progression by regulating E-cadherin and ERK1/2 signaling
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NSC 74859 enhances doxorubicin cytotoxicity via inhibition of epithelial–mesenchymal transition in hepatocellular carcinoma cells
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Inhibition of Epithelial-to-Mesenchymal Transition (EMT) in Cancer by Nitric Oxide: Pivotal Roles of Nitrosylation of NF-κB, YY1 and Snail
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“no studies of markers prominently discussed in the EMT literature (2, 4) were missed.”
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NOP14 promotes proliferation and metastasis of pancreatic cancer cells
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Insulin resistance and necroinflammation drives ductular reaction and epithelial-mesenchymal transition in chronic hepatitis C
Svegliati‐Baroni, G., Faraci, G., Fabris, L., Saccomanno, S., Cadamuro, M., Pierantonelli, I., Trozzi, L., Bugianesi, E., Guido, M., Strazzabosco, M., et al. (2010) · Gut · doi:10.1136/gut.2010.219741 · Cited by 34
“The main findings of our study are that in CHC (1) IR and the degree of necroinflammation are independent predictors of advanced fibrosis; (2) IR and the degree of necroinflammation are significantly associated with expansion of the DR; (3) ductular reactive cells express phenotypic markers suggestive of EMT.”
BackgroundResultInfluential
Metformin Increases E-cadherin in Tumors of Diabetic Patients With Endometrial Cancer and Suppresses Epithelial-Mesenchymal Transition in Endometrial Cancer Cell Lines
Laskov, I., Abou-Nader, P., Amin, O., Philip, C., Beauchamp, M.-C., Yasmeen, A., & Gotlieb, W. H. (2016) · International Journal of Gynecological Cancer · doi:10.1097/igc.0000000000000761 · Cited by 34
“This EMT promotes the interaction of tumorcellswith the stroma, facilitating invasionandmetastasis.(9,10) Several transcription factors have emerged in recent years that trigger the down-regulation of E-cadherin and consequently promote EMT in different types of cancer.”
Background
WISP-2 in human gastric cancer and its potential metastatic suppressor role in gastric cancer cells mediated by JNK and PLC-γ pathways
Ji, J., Jia, S., Jia, Y., Ji, K., Hargest, R., & Jiang, W. G. (2015) · British Journal of Cancer · doi:10.1038/bjc.2015.285 · Cited by 33
“At transcription and translation levels, WISP-2 knockdown in GC cells triggers an upregulation of Twist, N-cadherin and Vimentin, markers of mesenchymal genotype (Zeisberg and Neilson, 2009).”
Background
Estrogen receptor β (ERβ) is a novel prognostic marker of recurrence survival in non-muscle-invasive bladder cancer potentially by inhibiting cadherin switch
Han, B., Cui, D., Jing, Y., Hong, Y., & Xia, S. (2012) · World Journal of Urology · doi:10.1007/s00345-011-0819-4 · Cited by 33
Epithelial to mesenchymal transition (EMT) induced by bleomycin or TFGb1/EGF in murine induced pluripotent stem cell-derived alveolar Type II-like cells
Alipio, Z., Jones, N., Liao, W., Yang, J., Kulkarni, S. S., Kumar, K. S., Hauer‐Jensen, M., Ward, D. C., Ma, Y., & Fink, L. M. (2011) · Differentiation · doi:10.1016/j.diff.2011.05.001 · Cited by 33
“To further document that EMT is occurring in ATII-like cells, we analyzed gene expression of 52 EMT-related markers that were shown to be significantly upregulated during EMT by qRT-PCR (Kalluri and Neilson, 2003; Zeisberg and Neilson, 2009).”
BackgroundInfluential
Expression of podoplanin and vimentin is correlated with prognosis in esophageal squamous cell carcinoma
Tanaka, M. R., Kijima, H., Shimada, H., Makuuchi, H., Ozawa, S., & Inokuchi, S. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3966 · Cited by 33
“Vimentin is an important protein constituent of cellular intermediate filaments in normal and tumor mesenchymal cells (13,14).”
Gene-expression signatures in ovarian cancer: Promise and challenges for patient stratification
Konecny, G. E., Winterhoff, B. J. N., & Wang, C. (2016) · Gynecologic Oncology · doi:10.1016/j.ygyno.2016.01.026 · Cited by 33
“Importantly, this level of gene expression that is primarily derived from host cell infiltrates (immunoreactive and stromal) may be distinct from a tumor cell related epithelial-mesenchymal plasticity (differentiated and proliferative/mesenchymal) [49, 50].”
Background
S100A8+stroma cells predict a good prognosis and inhibit aggressiveness in colorectal carcinoma
Li, S., Xu, F., Li, H., Zhang, J., Zhong, A., Huang, B., & Lai, M. (2016) · OncoImmunology · doi:10.1080/2162402x.2016.1260213 · Cited by 33
“N-cadherin (N-CAD), along with activated transcription factors like SNAIL.(16) Cells that acquire an EMT phenotype are resistant to”
Background
1,25( OH )2D3 inhibited Th17 cells differentiation via regulating the NF ‐κB activity and expression of IL ‐17
Sun, D., Luo, F., Xing, J., Zhang, F., Xu, J., & Zhang, Z. (2018) · Cell Proliferation · doi:10.1111/cpr.12461 · Cited by 33
Muscleblind‑like 1 destabilizes Snail mRNA and suppresses the metastasis of colorectal cancer cells via the Snail/E‑cadherin axis
Tang, L., Zhao, P., & Kong, D. (2019) · International Journal of Oncology · doi:10.3892/ijo.2019.4691 · Cited by 33
“In general, the downregulation of E-cadherin and upregulation of Vimentin are considered as the hallmarks of EMT (17), along with a number of key transcription factors, such as Snail, Slug and ZEB, which have been shown to potentiate EMT progression (18).”
Background
Depletion of MLKL inhibits invasion of radioresistant nasopharyngeal carcinoma cells by suppressing epithelial-mesenchymal transition
Dong, Y., Sun, Y., Huang, Y., Fang, X., Sun, P., Dwarakanath, B. S. R., Kong, L., & Lu, J. J. (2019) · Annals of Translational Medicine · doi:10.21037/atm.2019.11.104 · Cited by 33
Acinar to ductal cell trans-differentiation: A prelude to dysplasia and pancreatic ductal adenocarcinoma
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CXCR4 3′UTR functions as a ceRNA in promoting metastasis, proliferation and survival of MCF-7 cells by regulating miR-146a activity
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Trachoma and Ocular Chlamydial Infection in the Era of Genomics
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Neratinib shows efficacy in the treatment of HER2 amplified carcinosarcoma in vitro and in vivo
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Overexpression of epithelial-mesenchymal transition–related markers according to cell dedifferentiation: clinical implications as an independent predictor of poor prognosis in cholangiocarcinoma
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“[4] Research demonstrated that ZEB-1 promotes the process of EMT through regulation of the relevant protein binding domains, such as the p300-P/CAF binding domain, Smad interaction domain, and C-terminal-binding protein interaction domain.”
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Pitx3 directly regulates Foxe3 during early lens development
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“The HDDCs phenotype corresponded to a partial EMT, different from classical in vivo EMT models (Zeisberg and Neilson, 2009) because it appeared de novo in speciﬁc culture conditions.”
Influential
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“The expression of EMT associated transcription factors such as Snail1, Snail2, Twist and FOXC2 is up-regulated in invasive colon cancer and these transcription factors have been reported to play important roles in driving cancer progression and the EMT process.(40,41) Next, we determined the expression level of these…”
Background
Alteration of integrin‐dependent adhesion and signaling in EMT‐like MDCK cells established through overexpression of calreticulin
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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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