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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Background
Intragraft Tubular Vimentin and CD44 Expression Correlate With Long-Term Renal Allograft Function and Interstitial Fibrosis and Tubular Atrophy
Kers, J., Xu, Y., Rondeau, É., Claessen, N., Idu, M. M., Roelofs, J. J. T. H., Bemelman, F. J., ten Berge, I. J. M., & Florquin, S. (2010) · Transplantation · doi:10.1097/tp.0b013e3181e86b42 · Cited by 29
Changes in Protein Expression in Two Cholangiocarcinoma Cell Lines Undergoing Formation of Multicellular Tumor Spheroids In Vitro
Mischiati, C., Ura, B., Roncoroni, L., Elli, L., Cervellati, C., Squerzanti, M., Conte, D., Doneda, L., de Laureto, P. P., Franceschi, G. D., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0118906 · Cited by 28
“EMT occurrence is usually linked to the reprogramming in protein expression via the action of transcription factors (Snail, Slug and Twist) ([33], and references therein) and miRNAs, which together control the shift from E-cadherin to N-cadherin in response to the treatment with cytokines or mechanical stimuli [3,34].”
Background
Sequence variation among members of the miR-200 microRNA family is correlated with variation in the ability to induce hallmarks of mesenchymal-epithelial transition in ovarian cancer cells
Jabbari, N., Reavis, A. N., & McDonald, J. F. (2014) · Journal of Ovarian Research · doi:10.1186/1757-2215-7-12 · Cited by 29
“The slides were incubated with mouse monoclonal primary antibodies against CDH1 (E-cadherin) and FN1 (Fibronectin, 1:200; Santa Cruz Biotechnology, Inc., Santa Cruz, CA) in 5% BSA for 1 hour at room temperature.”
BackgroundInfluential
The prognostic role of E ‐cadherin and β‐catenin overexpression in laryngeal squamous cell carcinoma
Greco, A., VIRGILIO, A. D., Rizzo, M. I., Pandolfi, F., Rosati, D., & VINCENTIIS, M. D. (2015) · The Laryngoscope · doi:10.1002/lary.25736 · Cited by 29
“1).(4,9,11) Although some studies have investigated the phenomenon of EMT in head and neck cancers and produced conflicting results, we believe that laryngeal cancer should be studied separately.”
Background
miR‐203 inhibits augmented proliferation and metastasis of hepatocellular carcinoma residual in the promoted regenerating liver
Zheng, X., Chen, X., Xu, L., Zhang, M., Feng, L., Yi, P., Tang, J., & Xu, M. (2017) · Cancer Science · doi:10.1111/cas.13167 · Cited by 29
miR-21 and KLF4 jointly augment epithelial-mesenchymal transition via the Akt/ERK1/2 pathway
Liu, C., Huang, Q., Jin, Z., Zhu, C., Liu, Z., & Wang, C. (2017) · International Journal of Oncology · doi:10.3892/ijo.2017.3876 · Cited by 29
“Transformed cells downregulate epithelial cell marker E-cadherin whilst upregulating mesenchymal markers N-cadherin and vimentin (3-6).”
High expression of PDLIM5 facilitates cell tumorigenesis and migration by maintaining AMPK activation in prostate cancer
Liu, X., Chen, L., Huang, H., Lv, J.-M., Chen, M., Qu, F., Pan, X., Li, L., Yin, L., Cui, X., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.20981 · Cited by 27
“Snail and slug, two key regulators of EMT, can bind to the CDH1 promoter region of the E-cadherin protein and downregulate its expression; loss of E-cadherin can increase the expression of other corresponding mesenchymal-related genes, including coding for vimentin and N-cadherin [35].”
Overexpression of long non‑coding RNA CRNDE facilitates epithelial‑mesenchymal transition and correlates with poor prognosis in intrahepatic cholangiocarcinoma
Xia, X., Dong, X., Xiang, T., Xu, H.-Y., Song, D., Cheng, P., & Wang, J. (2018) · Oncology Letters · doi:10.3892/ol.2018.7815 · Cited by 29
“This study investigated the role of CRNDE on IHCC EMT by evaluating the expression of epithelial markers (E-cadherin and α-catenin) and mesenchymal markers (N-cadherin and Vimentin) (14).”
The Escherichia coli protein toxin cytotoxic necrotizing factor 1 induces epithelial mesenchymal transition
Fabbri, A., Travaglione, S., Rosadi, F., Ballan, G., Maroccia, Z., Giambenedetti, M., Guidotti, M., Ødum, N., Krejsgaard, T., & Fiorentini, C. (2019) · Cellular Microbiology · doi:10.1111/cmi.13138 · Cited by 31
“We treated HT‐29 cells with CNF1 for 4, 24, and 48 hr and analysed by Western blot the expression of the EMT‐driving transcription factors ZEB1 and Snail1, whose up‐regulation is observed during EMT (Zeisberg & Neilson, 2009).”
BackgroundMethodInfluential
Dysregulated FAM215A Stimulates LAMP2 Expression to Confer Drug-Resistant and Malignant in Human Liver Cancer
Huang, P.-S., Lin, Y.-H., Chi, H., Tseng, Y., Chen, C. Y., Lin, T.-K., Yeh, C., & Lin, K. (2020) · Cells · doi:10.3390/cells9040961 · Cited by 29
“We also assessed the epithelial-mesenchymal transition (EMT), which is classically associated with the relocation of cells from a basement membrane microenvironment into a fibrillar ECM [24,25].”
Background
Vimentin plays an important role in the promotion of breast cancer cell migration and invasion by leucine aminopeptidase 3
Wang, X., Ji, S., Ma, Y., Xing, X., Zhou, Y., Xu, X., Song, J., Wang, S., Jiang, W., Wang, X., et al. (2020) · Cytotechnology · doi:10.1007/s10616-020-00402-x · Cited by 29
BYSL Promotes Glioblastoma Cell Migration, Invasion, and Mesenchymal Transition Through the GSK-3β/β-Catenin Signaling Pathway
Sha, Z., Zhou, J., Wu, Y., Zhang, T., Li, C., Meng, Q., Musunuru, P. P., You, F., Wu, Y., Yu, R., et al. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.565225 · Cited by 30
“β-catenin is not only a hallmark of EMT but also an effector of the WNT/β-catenin signaling pathway (28, 34, 35).”
Background
CircRNA UBAP2 serves as a sponge of miR-1294 to increase tumorigenesis in hepatocellular carcinoma through regulating c-Myc expression
Yu, M., Ding, G., Ma, P., Chen, Y., Zhu, X., Cai, J., Shen, Y.-H., Zhou, J., Fan, J., Sun, H., et al. (2021) · Carcinogenesis · doi:10.1093/carcin/bgab068 · Cited by 29
FGL1 as a Novel Mediator and Biomarker of Malignant Progression in Clear Cell Renal Cell Carcinoma
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“Epithelial mesenchymal-transition (EMT) is now widely recognized as an indispensable step in tumor invasion and metastasis (31), and E−cadherin, N−cadherin, and Vimentin are generally accepted as important molecular markers of EMT (32).”
Background
Tetraspanin 7 promotes osteosarcoma cell invasion and metastasis by inducing EMT and activating the FAK-Src-Ras-ERK1/2 signaling pathway
Shao, S., Piao, L., Guo, L., Wang, J., Wang, L., Wang, J., Tong, L., Yuan, X., Zhu, J., Fang, S., et al. (2022) · Cancer Cell International · doi:10.1186/s12935-022-02591-1 · Cited by 31
“Changes in ECM interactions and adhesion molecule expression play central roles in EMT induction [51].”
Background
SIRT2 promotes the viability, invasion and metastasis of osteosarcoma cells by inhibiting the degradation of Snail
Tian, Y., Liu, R., Hou, X., Gao, Z., Liu, X., & Zhang, W. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-05388-2 · Cited by 29
“Epithelial-mesenchymal transition (EMT) plays a key role in wound healing, embryonic development and tumor metastasis [6].”
Background
β-asarone inhibits gastric cancer cell proliferation
Wu, J., Zhang, X., Sun, Q., Chen, M., LIU, S.-L., Zhang, X., Zhou, J., & Zou, X. (2015) · Oncology Reports · doi:10.3892/or.2015.4316 · Cited by 29
Effect of Sedum sarmentosum BUNGE Extract on Aristolochic Acid–Induced Renal Tubular Epithelial Cell Injury
Bai, Y., Lu, H., Hu, L., Hong, D., Ding, L., & Chen, B. (2014) · Journal of Pharmacological Sciences · doi:10.1254/jphs.13216fp · Cited by 29
Epithelial-to-mesenchymal transition in pancreatic islet β cells
Joglekar, M. V., & Hardikar, A. A. (2010) · Cell Cycle · doi:10.4161/cc.9.20.13590 · Cited by 29
Human Bone Marrow Mesenchymal Stem Cells Induce Collagen Production and Tongue Cancer Invasion
Salo, S., Bitu, C. C., Merkku, K., Nyberg, P., Bello, I. O., Vuoristo, J. T., Sutinen, M., Vähänikkilä, H., Costea, D. E., Kauppila, J. H., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077692 · Cited by 30
“Although in our OTSCC cells there were no remarkable changes in the gene expression of traditional EMT markers [49], after the interaction with BMMSCs, up-regulation in the expression of EMT plasticity biomarkers, such as cadherin-11, was detected.”
Background
P63 regulates tubular formation via epithelial-to-mesenchymal transition
Zhang, Y., Yan, W., & Chen, X. (2013) · Oncogene · doi:10.1038/onc.2013.101 · Cited by 29
Human EAG1 potassium channels in the epithelial-to-mesenchymal transition in lung cancer cells.
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Hyperglycemia as a mechanism of pancreatic cancer metastasis
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Immune Processes and Pathogenic Fibrosis in Ocular Chronic Graft-Versus-Host Disease and Clinical Manifestations after Allogeneic Hematopoietic Stem Cell Transplantation
Ogawa, Y., Shimmura, S., Doğru, M., & Tsubota, K. (2010) · Cornea · doi:10.1097/ico.0b013e3181ea9a6b · Cited by 29
“As biomarkers of EMT, abundant intermediate filaments and microfilaments, gain of rough endoplasmic reticulum, abundant lysosomal granules, and loss of intercellular junctions on electron microscopy have been reported.(33) In cGVHD lacrimal gland myoepithelia, electron microscopy revealed remarkable changes in the mic…”
Background
Tumorigenic WAP-T Mouse Mammary Carcinoma Cells: A Model for a Self-Reproducing Homeostatic Cancer Cell System
Wegwitz, F., Kluth, M.-A., Maenz, C., Otto, B., Gruner, K., Heinlein, C., Kühl, M., Warnecke, G., Schumacher, U., Deppert, W., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012103 · Cited by 27
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Background
Is the Epithelial-to-Mesenchymal Transition Clinically Relevant for the Cancer Patient?
Krasnapolski, M. A., Todaro, L. B., & Joffé, E. B. D. K. (2011) · Current Pharmaceutical Biotechnology · doi:10.2174/138920111798377021 · Cited by 28
Depletion of dAKAP1–protein kinase A signaling islands from the outer mitochondrial membrane alters breast cancer cell metabolism and motility
Aggarwal, S., Gabrovsek, L., Langeberg, L. K., Golkowski, M. G., Ong, S., Smith, F. D., & Scott, J. D. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.006741 · Cited by 30
“changes in cell motility are hallmarks of a mesenchymal profile (4, 11).”
BackgroundInfluential
Pseudophosphatase STYX promotes tumor growth and metastasis by inhibiting FBXW7 function in colorectal cancer
He, D., Ma, Z., Fang, C., Ding, J., Yang, W., Chen, P., Huang, L., Wang, C., Yu, Y., Yang, L., et al. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.04.014 · Cited by 28
Trichostatin A reverses epithelial‑mesenchymal transition and attenuates invasion and migration in MCF‑7 breast cancer cells
Wang, X., Chen, S., Shen, T., Lü, H., Dingqiong, X., Zhao, M., Yao, Y., Li, X., Zhang, G., Zhou, X. W., et al. (2020) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2020.8422 · Cited by 28
“Clinical studies have revealed that breast cancer, when accompanied by a low expression of E-cadherin and robust expression of vimentin or N-cadherin, usually exhibits an aggressive tumor phenotype and a high rate of metastasis (7,11).”
Background
GPER Activation Inhibits Cancer Cell Mechanotransduction and Basement Membrane Invasion via RhoA
Rice, A. J., Cortés, E., Lachowski, D., Oertle, P., Matellan, C., Thorpe, S. D., Ghose, R., Wang, H., Lee, D. A., Plodinec, M., et al. (2020) · Cancers · doi:10.3390/cancers12020289 · Cited by 29
“High expression of the intermediate filament protein vimentin and nuclear localisation of the transcriptional regulator β-catenin are indicative of the mesenchymal phenotype [49].”
Background
Tranilast Inhibits TGF-β1–induced Epithelial-mesenchymal Transition and Invasion/Metastasis via the Suppression of Smad4 in Human Lung Cancer Cell Lines
Takahashi, K., Menju, T., Nishikawa, S., Miyata, R., Tanaka, S., Yutaka, Y., Yamada, Y., Nakajima, D., Hamaji, M., Ohsumi, A., et al. (2020) · Anticancer Research · doi:10.21873/anticanres.14311 · Cited by 28
Pristimerin exerts antitumor activity against MDA-MB-231 triple-negative breast cancer cells by reversing of epithelial-mesenchymal transition via downregulation of integrin β3
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An engineered pancreatic cancer model with intra-tumoral heterogeneity of driver mutations
Moon, H., Özçelikkale, A., Yang, Y., Elzey, B. D., Konieczny, S. F., & Han, B. (2020) · Lab on a Chip · doi:10.1039/d0lc00707b · Cited by 27
GABARAP suppresses EMT and breast cancer progression via the AKT/mTOR signaling pathway
Liu, Y., Wang, D., Lei, M., Gao, J., Cui, Y., Jin, X., Yu, Q., Jiang, Y., Guo, Y., Liu, Y., et al. (2021) · Aging · doi:10.18632/aging.202510 · Cited by 28
Targeting the ILK/YAP axis by LFG-500 blocks epithelial–mesenchymal transition and metastasis
Li, C., Li, J., Gong, S., Huang, M., Li, R., Xiong, G., Wang, F., Zou, Q.-M., Qi, Q., & Yin, X. (2021) · Acta Pharmacologica Sinica · doi:10.1038/s41401-021-00655-y · Cited by 28
The diverse roles of circular RNAs in pancreatic cancer
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Classification of High-Grade Serous Ovarian Carcinoma by Epithelial-to-Mesenchymal Transition Signature and Homologous Recombination Repair Genes
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“In contrast, VIM (vimentin), another key indicator of EMT highly expressed in mesenchymal rather than in epithelial tissue [23], was upregulated in cluster B (Figure 3D, bottom left).”
Background
Secreted Phospholipases A2 - not just Enzymes: Revisited
Ivanušec, A., Šribar, J., & Križaj, I. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.68093 · Cited by 30
“GIIA sPLA2 is overexpressed in many types of cancers, while vimentin is one of the signature biomarkers of tumour dedifferentiation through epithelial-mesenchymal transition [121, 122].”
Background
Cardiac forces regulate zebrafish heart valve delamination by modulating Nfat signaling
Chow, R., Fukui, H., Chan, W. X., Tan, J. K. S., Roth, S., Duchemin, A., Messaddeq, N., Nakajima, H., Liu, F., Faggianelli, N., et al. (2022) · PLoS Biology · doi:10.1371/journal.pbio.3001505 · Cited by 29
“Fibronectin deposition is considered a biomarker of EMT [29,30].”
Background
Human antigen R mediated post‐transcriptional regulation of epithelial‐mesenchymal transition related genes in diabetic nephropathy 人抗原R调节糖尿病肾病中上皮细胞间质转化相关基因的转录后调控
Yu, C., Xin, W., Zhen, J., Liu, Y., Akhtar, J., Wang, R., & Wan, Q. (2014) · Journal of Diabetes · doi:10.1111/1753-0407.12220 · Cited by 29

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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