Epigenetic regulation of miR-21 in colorectal cancer: ITGB4 as a novel miR-21 target and a three-gene network (miR-21-ITGΒ4-PDCD4) as predictor of metastatic tumor potential
Open accessAbstract
Previous studies have uncovered several transcription factors that determine biological alterations in tumor cells to execute the invasion-metastasis cascade, including the epithelial-mesenchymal transition (EMT). We sought to investigate the role of miR-21 in colorectal cancer regulation. For this purpose, miR-21 expression was quantified in a panel of colorectal cancer cell lines and clinical specimens. High expression was found in cell lines with EMT properties and in the vast majority of human tumor specimens. We demonstrate in a cell-specific manner the occupancy of MIR-21 gene promoter by AP-1 and ETS1 transcription factors and, for the first time, the pattern of histone posttranslational modifications necessary for miR-21 overexpression. We also show that Integrin-β4 (ITGβ4), exclusively expressed in polarized epithelial cells, is a novel miR-21 target gene and plays a role in the regulation of EMT, since it is remarkably de-repressed after transient miR-21 silencing and downregulated after miR-21 overexpression. miR-21-dependent change of ITGβ4 expression significantly affects cell migration properties of colon cancer cells. Finally, in a subgroup of tumor specimens, ROC curve analysis performed on quantitative PCR data sets for miR-21, ITGβ4, and PDCD4 shows that the combination of high miR-21 with low ITGβ4 and PDCD4 expression is able to predict presence of metastasis. In conclusion, miR-21 is a key player in oncogenic EMT, its overexpression is controlled by the cooperation of genetic and epigenetic alterations, and its levels, along with ITGβ4 and PDCD4 expression, could be exploited as a prognostic tool for CRC metastasis.
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miRNAs play a key role in the progression of malignant tumors and are considered potential anti-tumor therapeutic targets.
“miRNAs play a key role in the progression of malignant tumors, they are considered potential anti-tumor therapeutic targets24, 25.”
From miR-21-5p Inhibits the Proliferation, Migration, and Invasion of Glioma by Targeting S100A10 (2023) · cites this paper as [25]
The Introduction and the section on the three-gene assay say that miRNAs contribute to cancer pathogenesis and regulate metastatic progression. The miR-21 inhibition results also show reduced migration of colon cancer cells. However, the paper proposes a potential diagnostic tool, not miRNAs as anti-tumor therapeutic targets; that part of the claim is unsupported by our copy. Page numbers are unavailable in the indexed passages. (LLM, conf=0.84)
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ITGB4 is a novel prognostic factor in colon cancer
Li, M., Jiang, X., Wang, G., Zhai, C., Liu, Y., Li, H., Zhang, Y., Yu, W., & Zhao, Z. (2019) · Journal of Cancer · doi:10.7150/jca.29269 · Cited by 73 · see citing works
“have suggested that ITGB4 was a target of miR-21 and regulated by miR-21 in colon cancer [30].”
BackgroundThe use of circulating microRNAs as diagnostic biomarkers in colorectal cancer
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“It is a key regulator of oncogenic Epithelial-Mesenchymal Transition (EMT) targeting proteins such as T-Cell Lymphoma Invasion and Meta-stases Inducing Protein-1 (TIAM1) which is known to regulate migration and invasion of cancer cells [34,35].”
Targeting strategies on miRNA-21 and PDCD4 for glioblastoma
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“Ferraro and colleagues, for example, demonstrated that Activator protein 1 (AP-1) and ETS Proto-Oncogene 1 (ETS1) TFs negatively regulate the expression of miR-21 gene by occupying its promoter in a sequence-specific manner [18].”
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“Epigenetic regulation of ITGB4 expression has also been suggested after identification of microRNAs that may target the ITGB4 transcript such as miR-21 [33] and miR-335-5p [32] as well as hypomethylation of the ITGB4 promoter [32].”
BackgroundClassification of gene signatures for their information value and functional redundancy
Cantini, L., Calzone, L., Martignetti, L., Rydenfelt, M., Blüthgen, N., Barillot, E., & Zinovyev, A. Y. (2017) · npj Systems Biology and Applications · doi:10.1038/s41540-017-0038-8 · Cited by 54 · see citing works
“31,32 Moreover, the areas: splicing, mRNA metabolism, and protein metabolism, resulted to be signi fi cantly upregulated.”
BackgroundCellular senescence or stemness: hypoxia flips the coin
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Regulation of hemidesmosome dynamics and cell signaling by integrin α6β4
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Effects of pericytes and colon cancer stem cells in the tumor microenvironment
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miR-339-3p inhibits proliferation and metastasis of colorectal cancer
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“For instance, Ferraro et al.(42) reported that miR-21 could regulate the metastasis of CRC cells through ITGB4 expression”
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“cancer [17], prognostic cancer [16], gastric cancer [16] and et al.”
MicroRNA-21 controls hTERT via PTEN in human colorectal cancer cell proliferation
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Hippo kinases regulate cell junctions to inhibit tumor metastasis in response to oxidative stress
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miR-21: A Key Small Molecule with Great Effects in Combination Cancer Therapy
Arghiani, N., & Matin, M. M. (2021) · Nucleic Acid Therapeutics · doi:10.1089/nat.2020.0914 · Cited by 46 · see citing works
“It has been demonstrated that inhibition of MSH2 by miR-21 confers TGF-b -induced resistance to PARP inhibitor (PARPi), which selectively targets tumor cells with a DNA repair deficiency, in breast cancer cells [117].”
The role of miRNA-21 and epithelial mesenchymal transition (EMT) process in colorectal cancer
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The mechanisms and clinical significance of PDCD4 in colorectal cancer
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“ROC curve analysis validated that the combination of high miR‐21 with low ITGβ4 and PDCD4 expression may be considered as a factor indicating metastasis in CRC (Ferraro et al., 2014).”
BackgroundEpigenetic alterations in cancer and personalized cancer treatment
Miozzo, M. R., Vaira, V., & Sirchia, S. M. (2015) · Future Oncology · doi:10.2217/fon.14.237 · Cited by 37 · see citing works
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Downregulation of miR-21 as a promising strategy to overcome drug resistance in cancer
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Berberine regulates the microRNA‑21‑ITGΒ4‑PDCD4 axis and inhibits colon cancer viability
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“…and a transmembrane domain, and the intracellular region ITG β 4 determines the specificity to physiological and pathological processes, including the inflammatory response, the immune response, proliferation, differentiation, vascularization, fertilization, embryo implantation and growth (29).”
microRNAs as therapeutic targets in intestinal diseases
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“As the well-studied miRNA, miR-21 is almost omnipresent overexpressed in many human tumours, such as colorectal cancer [109, 110].”
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“28 Emerging studies have demonstrated that aberrant expression of miRNAs is associated with prognosis of CRC.”
InfluentialThe role of microRNAs involved in PI3‐kinase signaling pathway in colorectal cancer
Noorolyai, S., Mokhtarzadeh, A., Baghbani, E., Asadi, M., Baghbanzadeh, A., Moghaddam, M. M., & Baradaran, B. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27415 · Cited by 30 · see citing works
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Roles of Integrins in Gastrointestinal Cancer Metastasis
Hou, S., Wang, J., Li, W., Hao, X., & Hang, Q. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.708779 · Cited by 30 · see citing works
Tsiakanikas, P., Kontos, C. K., Kerimis, D., Papadopoulos, I. N., & Scorilas, A. (2018) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm-2017-0430 · Cited by 27 · see citing works
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“Due to the cellular dynamics of tsRNAs, it is speculated that they play a key role in the epigenetic regulation of the protein-coding genes, using RNA interference (RNAi) in a similar way to other sncRNAs such as miRNAs and piRNAs [38,39].”
BackgroundSelf-citationIntegrin β4 as a Potential Diagnostic and Therapeutic Tumor Marker
Yang, H., Xu, Z., Peng, Y., Wang, J., & Xiang, Y. (2021) · Biomolecules · doi:10.3390/biom11081197 · Cited by 26 · see citing works
“Therefore, except for indicating cancer progression by integrin β4, the combination of high miR-21 and low ITGβ4 and PDCD4 expression can predict the presence of metastasis and can be used as a predictive tool for colorectal cancer metastasis [77].”
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KH-type splicing regulatory protein is involved in esophageal squamous cell carcinoma progression
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“In this study, we report that KHSRP exerts oncogenic activity in ESCC cells, at least partly, by inducing the expression of a set of oncogenic miRNAs, including miR-21, miR-130b, and miR-301a, and by suppressing the downstream inhibitors of epithelial-tomesenchymal transition (EMT), such as BMP6, PDCD4, and TIMP3, res…”
BackgroundInfluentialAdamopoulos, P. G., Theodoropoulou, M. C., & Scorilas, A. (2018) · Annals of Translational Medicine · doi:10.21037/atm.2018.06.32 · Cited by 25 · see citing works
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miR-21-5p Inhibits the Proliferation, Migration, and Invasion of Glioma by Targeting S100A10
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“miRNAs play a key role in the progression of malignant tumors, they are considered potential anti-tumor therapeutic targets[24, 25].”
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“Besides genetic events, epigenetic changes, including DNA methylation, histone modifications, and deregulation of non-coding RNAs may play a crucial role in tumor progression [8,9].”
ITGB4 as a novel serum diagnosis biomarker and potential therapeutic target for colorectal cancer
Jiang, X., Wang, J., Wang, M., Xuan, M., Han, S., Li, C., Li, M., Sun, X., Yu, W., & Zhao, Z. (2021) · Cancer Medicine · doi:10.1002/cam4.4216 · Cited by 22 · see citing works
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“A variety of apoptosis inducers upregulate the expression of PDCD4, thus affecting multiple signaling pathways (7-9).”
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miR-21 expression analysis in budding colon cancer cells by confocal slide scanning microscopy
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“Kang et al. found that high stromal miR-21 and low E-cadherin was correlated [10].”
BackgroundInfluentialmiR-30c-5p inhibits glioma proliferation and invasion via targeting Bcl2
Yuan, L., Zhang, T., Xu, L., Han, H., & Liu, S. (2021) · Translational Cancer Research · doi:10.21037/tcr-19-2957 · Cited by 18 · see citing works
Epigenetically regulated microRNAs and their prospect in cancer diagnosis
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“miR-21 Histone post-translational modification Breast, prostate, glioblastoma Overexpressed/ oncogenic P53, TPM1, PDCD4 ITGb4 and PDCD4 expression [80,81]”
The mechanism of ITGB4 in tumor migration and invasion
Huang, G., Zhou, M., Lu, D., Li, J., Tang, Q., Xiong, C., Liang, F., & Chen, R. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1421902 · Cited by 16 · see citing works
“Additionally, the microRNA miR-21 has been shown to regulate the colorectal cancer invasion-metastasis cascade by targeting ITGB4 (54).”
BackgroundChen, X., Xie, B., Cao, L., Zhu, F., Chen, B., Lv, H., Fan, X., Han, L., Bie, L., Cao, X., et al. (2017) · Journal of Molecular Graphics and Modelling · doi:10.1016/j.jmgm.2017.02.004 · Cited by 16 · see citing works
Identification of prognostic and bone metastatic alternative splicing signatures in bladder cancer
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“To date, several miRNAs have been shown to regulate expression of BCL2L12 and/or other members of the BCL2 family; most of them constitute important biomarkers (48,72-81).”
BackgroundMa, D., Liu, S., Liu, K., Kong, L., Xiao, L., Xin, Q., Jiang, C., & Wu, J. (2024) · Cancer Biology & Therapy · doi:10.1080/15384047.2024.2314324 · Cited by 14 · see citing works
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“As in the case of members of the TGFß family, some integrins such as integrin β4 go in the opposite direction of some of the other integrins, such as β8 or A3, but in addition, these effects may be associated with potential metastatic ability, since the combination of low ITGβ4, exclusively expressed in polarized epit…”
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Programmed cell death factor 4 enhances the chemosensitivity of colorectal cancer cells to Taxol
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MicroRNA Expression and Correlation with mRNA Levels of Colorectal Cancer-Related Genes
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“According to previous investigations, expression levels of the miR-21 molecule were the highest in invasive carcinomas and gradually decreased towards non-transformed tissue [32, 33].”
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“2014), epithelial-to-mesenchymal transition (Ferraro et al. 2014), and chemoresistance (Chao et al.”
Relationship between the microRNAs and PI3K/AKT/mTOR axis: Focus on non-small cell lung cancer
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MiR-486-5p Downregulation Marks an Early Event in Colorectal Carcinogenesis
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“In addition, miR-21 could aggravate CRC by potentiating EMT through inactivating Integrin-β4 (ITGβ4), and Programmed cell death protein 4 (PDCD4) (Ferraro et al. 2014).”
Molecular therapies delaying cardiovascular aging: disease- or health-oriented approaches
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Stem Cell-Like Properties of CK2β-down Regulated Mammary Cells
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“As mentioned above, integrins are also regulated by miRNAs [24].”
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The impact of microRNAs on myeloid-derived suppressor cells in cancer
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Machine Learning-based Prediction of the Likelihood of Colorectal Cancer Using miRNA Expression
Sultan, A., de Asa, A. A., Guimbangunan, T. M., Serapio, E. D., Fellizar, A., Albano, P. M., & Tomas, R. C. (2023) · The Philippine journal of science · doi:10.56899/152.04.12 · Cited by 2 · see citing works
Shabab, N., Afshar, S., & Saidijam, M. (2019) · Avicenna Journal of Medical Biochemistry · doi:10.34172/ajmb.2019.05 · Cited by 1 · see citing works
“The miR 21 is a specific miRNA which was upregulated in many epithelial-derived cancers including breast, pancreas, lung, gastric, prostate, and colon cancers (33-35).”
Background
- Authors
- Ferraro, A., Kontos, C. K., Boni, T., Bantounas, I., Siakouli, D., Kosmidou, V., Vlassi, M., Spyridakis, Y., Tsipras, I., Zografos, G., & Pintzas, A.
- Affiliations
- National Hellenic Research Foundation (GR)
- General Hospital of Athens G. Genimatas (GR)
- Corresponding author
- Pintzas, Alexander
- ORCID
- Venue
- Epigenetics
- Publisher
- Informa UK Limited
- Published
- 2013-10-22
- Volume
- 9
- Issue
- 1
- Pages
- 129-141
- ISSN
- 1559-2294 (ISSN-L)
- 1559-2308
- PMC
- PMC3928175
- OpenAlex
- W2090786568
- Cited by
- 111
- References
- 66
- Citations by year
- 2026: 5 · 2025: 1 · 2024: 5 · 2023: 8 · 2022: 8 · 2021: 14 · 2020: 6 · 2019: 11 · 2018: 19 · 2017: 10 · 2016: 9 · 2015: 11 · 2014: 4
- FWCI
- 2.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Epigenetics (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- National Hellenic Research Foundation Helios Repository (National Hellenic Research Foundation) (submittedVersion)
- Funders
- General Secretariat for Research and Technology
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- miR-21, colorectal cancer, epithelial-mesenchymal transition, ITGB4, PDCD4, histone modifications, AP-1 transcription factor, Ets-1 transcription factor, cell migration, metastasis prediction, prognostic factors, microRNA overexpression
- MeSH terms
- Histones, Humans, Neoplasm Metastasis, Protein Processing, Post-Translational, Biomarkers, Tumor, Colorectal Neoplasms, RNA-Binding Proteins, Transcription Factor AP-1, MicroRNAs, Integrin beta4, Epigenesis, Genetic, Cell Line, Tumor, Proto-Oncogene Protein c-ets-1, Apoptosis Regulatory Proteins, Gene Regulatory Networks, Epithelial-Mesenchymal Transition
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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