Cited by 314MicroRNA in disease regulationTGF-β signaling in diseasesCancer-related molecular mechanisms research
The miR-17-92 MicroRNA Cluster Regulates Multiple Components of the TGF-β Pathway in Neuroblastoma
Open accessMestdagh, Pieter, Boström, Anna-Karin, Impens, Francis, Fredlund, Erik, Van Peer, Gert, De Antonellis, Pasqualino, von Stedingk, Kristoffer, Ghesquière, Bart +10 more·2010·Molecular Cell
Abstract
The miR-17-92 microRNA cluster is often activated in cancer cells, but the identity of its targets remains elusive. Using SILAC and quantitative mass spectrometry, we examined the effects of activation of the miR-17-92 cluster on global protein expression in neuroblastoma (NB) cells. Our results reveal cooperation between individual miR-17-92 miRNAs and implicate miR-17-92 in multiple hallmarks of cancer, including proliferation and cell adhesion. Most importantly, we show that miR-17-92 is a potent inhibitor of TGF-β signaling. By functioning both upstream and downstream of pSMAD2, miR-17-92 activation triggers downregulation of multiple key effectors along the TGF-β signaling cascade as well as direct inhibition of TGF-β-responsive genes.
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miRNAs selectively regulate genes within the same pathway.
“Recent studies demonstrated that miRNAs selectively regulate genes within the same pathway [97, 131-133].”
From MicroRNAs in brain cholesterol metabolism and their implications for Alzheimer's disease (2016) · cites this paper as [131]
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References 50 · Cited by 314
Research works printed but not linked: 35
- Bartel DP MicroRNAs: genomics, biogenesis, mechanism, and function Cell 2004 116 281 297 14744438
- Bartel DP MicroRNAs: target recognition and regulatory functions Cell 2009 136 215 233 19167326 PMC3794896
- Calin GA Croce CM MicroRNA signatures in human cancers Nat Rev Cancer 2006 6 857 866 17060945
- Castellano L Giamas G Jacob J Coombes RC Lucchesi W Thiruchelvam P Barton G Jiao LR Wait R Waxman J The estrogen receptor-alpha-induced microRNA signature regulates itself and its transcriptional response Proc Natl Acad Sci U S A 2009 106 15732 15737 19706389 PMC2747188
- Cohen PS Letterio JJ Gaetano C Chan J Matsumoto K Sporn MB Thiele CJ Induction of transforming growth factor beta 1 and its receptors during all-trans-retinoic acid (RA) treatment of RA-responsive human neuroblastoma cell lines Cancer Res 1995 55 2380 2386 7757990
- Colaert N Helsens K Impens F Vandekerckhove J Gevaert K Rover: a tool to visualize and validate quantitative proteomics data from different sources Proteomics 2010 10 1226 1229 20058247
- Dews M Fox JL Hultine S Sundaram P Wang W Liu YY Furth E Enders GH El-Deiry W Schelter JM The myc-miR-17~92 axis blunts TGF{beta} signaling and production of multiple TGF{beta}-dependent antiangiogenic factors Cancer Res 2010 70 8233 8246 20940405 PMC3007123
- Dews M Homayouni A Yu D Murphy D Sevignani C Wentzel E Furth EE Lee WM Enders GH Mendell JT Thomas-Tikhonenko A Augmentation of tumor angiogenesis by a Myc-activated microRNA cluster Nat Genet 2006 38 1060 1065 16878133 PMC2669546
- Esquela-Kerscher A Slack FJ Oncomirs - microRNAs with a role in cancer Nat Rev Cancer 2006 6 259 269 16557279
- Fontana L Fiori ME Albini S Cifaldi L Giovinazzi S Forloni M Boldrini R Donfrancesco A Federici V Giacomini P Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM PLoS One 2008 3 e2236 18493594 PMC2375057
- Fredlund E Ringner M Maris JM Pahlman S High Myc pathway activity and low stage of neuronal differentiation associate with poor outcome in neuroblastoma Proc Natl Acad Sci U S A 2008 105 14094 14099 18780787 PMC2544584
- Gevaert K Van Damme J Goethals M Thomas GR Hoorelbeke B Demol H Martens L Puype M Staes A Vandekerckhove J Chromatographic isolation of methionine-containing peptides for gel-free proteome analysis: identification of more than 800 Escherichia coli proteins Mol Cell Proteomics 2002 1 896 903 12488465
- Hayashita Y Osada H Tatematsu Y Yamada H Yanagisawa K Tomida S Yatabe Y Kawahara K Sekido Y Takahashi T A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation Cancer Res 2005 65 9628 9632 16266980
- He L He X Lim LP de Stanchina E Xuan Z Liang Y Xue W Zender L Magnus J Ridzon D A microRNA component of the p53 tumour suppressor network Nature 2007 447 1130 1134 17554337 PMC4590999
- He L Thomson JM Hemann MT Hernando-Monge E Mu D Goodson S Powers S Cordon-Cardo C Lowe SW Hannon GJ Hammond SM A microRNA polycistron as a potential human oncogene Nature 2005 435 828 833 15944707 PMC4599349
- Lanza G Ferracin M Gafa R Veronese A Spizzo R Pichiorri F Liu CG Calin GA Croce CM Negrini M mRNA/microRNA gene expression profile in microsatellite unstable colorectal cancer Mol Cancer 2007 6 54 17716371 PMC2048978
- Laping NJ Grygielko E Mathur A Butter S Bomberger J Tweed C Martin W Fornwald J Lehr R Harling J Inhibition of transforming growth factor (TGF)-beta1-induced extracellular matrix with a novel inhibitor of the TGF-beta type I receptor kinase activity: SB-431542 Mol Pharmacol 2002 62 58 64 12065755
- Lefever S Hellemans J Pattyn F Przybylski DR Taylor C Geurts R Untergasser A Vandesompele J RDML: structured language and reporting guidelines for real-time quantitative PCR data Nucleic Acids Res 2009 37 2065 2069 19223324 PMC2673419
- Loven J Zinin N Wahlstrom T Muller I Brodin P Fredlund E Ribacke U Pivarcsi A Pahlman S Henriksson M MYCN-regulated microRNAs repress estrogen receptor-alpha (ESR1) expression and neuronal differentiation in human neuroblastoma Proc Natl Acad Sci U S A 107 1553 1558 20080637 PMC2824410
- Mestdagh P Fredlund E Pattyn F Schulte JH Muth D Vermeulen J Kumps C Schlierf S De Preter K Van Roy N MYCN/c-MYC-induced microRNAs repress coding gene networks associated with poor outcome in MYCN/c-MYC-activated tumors Oncogene 2009a 19946337
- Mestdagh P Van Vlierberghe P De Weer A Muth D Westermann F Speleman F Vandesompele J A novel and universal method for microRNA RT-qPCR data normalization Genome Biol 2009b 10 R64 19531210 PMC2718498
- O'Donnell KA Wentzel EA Zeller KI Dang CV Mendell JT c-Myc-regulated microRNAs modulate E2F1 expression Nature 2005 435 839 843 15944709
- Oberthuer A Berthold F Warnat P Hero B Kahlert Y Spitz R Ernestus K Konig R Haas S Eils R Customized oligonucleotide microarray gene expression-based classification of neuroblastoma patients outperforms current clinical risk stratification J Clin Oncol 2006 24 5070 5078 17075126
- Olive V Bennett MJ Walker JC Ma C Jiang I Cordon-Cardo C Li QJ Lowe SW Hannon GJ He L miR-19 is a key oncogenic component of mir-17-92 Genes Dev 2009 23 2839 2849 20008935 PMC2800084
- Ong SE Blagoev B Kratchmarova I Kristensen DB Steen H Pandey A Mann M Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics Mol Cell Proteomics 2002 1 376 386 12118079
- Padua D Zhang XH Wang Q Nadal C Gerald WL Gomis RR Massague J TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4 Cell 2008 133 66 77 18394990 PMC2390892
- Petrocca F Visone R Onelli MR Shah MH Nicoloso MS de Martino I Iliopoulos D Pilozzi E Liu CG Negrini M E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer Cancer Cell 2008 13 272 286 18328430
- Raver-Shapira N Marciano E Meiri E Spector Y Rosenfeld N Moskovits N Bentwich Z Oren M Transcriptional activation of miR-34a contributes to p53-mediated apoptosis Mol Cell 2007 26 731 743 17540598
- Scarpa S Coppa A Ragano-Caracciolo M Mincione G Giuffrida A Modesti A Colletta G Transforming growth factor beta regulates differentiation and proliferation of human neuroblastoma Exp Cell Res 1996 229 147 154 8940258
- Schweigerer L Breit S Wenzel A Tsunamoto K Ludwig R Schwab M Augmented MYCN expression advances the malignant phenotype of human neuroblastoma cells: evidence for induction of autocrine growth factor activity Cancer Res 1990 50 4411 4416 2364393
- Turco A Scarpa S Coppa A Baccheschi G Palumbo C Leonetti C Zupi G Colletta G Increased TGFbeta type II receptor expression suppresses the malignant phenotype and induces differentiation of human neuroblastoma cells Exp Cell Res 2000 255 77 85 10666336
- Verrecchia F Chu ML Mauviel A Identification of novel TGF-beta /Smad gene targets in dermal fibroblasts using a combined cDNA microarray/promoter transactivation approach J Biol Chem 2001 276 17058 17062 11279127
- Volinia S Calin GA Liu CG Ambs S Cimmino A Petrocca F Visone R Iorio M Roldo C Ferracin M A microRNA expression signature of human solid tumors defines cancer gene targets Proc Natl Acad Sci U S A 2006 103 2257 2261 16461460 PMC1413718
- Xiao C Srinivasan L Calado DP Patterson HC Zhang B Wang J Henderson JM Kutok JL Rajewsky K Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes Nat Immunol 2008 9 405 414 18327259 PMC2533767
- Zhang H Gao P Fukuda R Kumar G Krishnamachary B Zeller KI Dang CV Semenza GL HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity Cancer Cell 2007 11 407 420 17482131
- Authors
- Mestdagh, P., Boström, A.-K., Impens, F., Fredlund, E., Van Peer, G., De Antonellis, P., von Stedingk, K., Ghesquière, B., Schulte, S., Dews, M., Thomas-Tikhonenko, A., Schulte, J. H., Zollo, M., Schramm, A., Gevaert, K., Axelson, H., Speleman, F., & Vandesompele, J.
- Affiliations
- Ghent University Hospital (BE)
- Lund University (SE)
- Ghent University (BE)
- Essen University Hospital (DE)
- Children's Hospital of Philadelphia (US)
- CEINGE Biotecnologie Avanzate Franco Salvatore (Italy) (IT)
- Corresponding author
- Vandesompele, Jo
- ORCID
- Venue
- Molecular Cell
- Publisher
- Elsevier BV
- Published
- 2010-12
- Volume
- 40
- Issue
- 5
- Pages
- 762-773
- ISSN
- 1097-2765 (ISSN-L)
- PMC
- PMC3032380
- OpenAlex
- W2037275886
- Cited by
- 314
- References
- 50
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 14 · 2023: 7 · 2022: 15 · 2021: 13 · 2020: 11 · 2019: 20 · 2018: 16 · 2017: 19 · 2016: 24 · 2015: 26 · 2014: 28 · 2013: 42 · 2012: 33
- FWCI
- 10.38
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Molecular Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Ghent University Academic Bibliography (Ghent University) (submittedVersion, other-oa)
- Universitätsbibliographie, Universität Duisburg-Essen (submittedVersion)
- Lirias (submittedVersion)
- Lund University Publications (Lund University) (submittedVersion)
- Funders
- National Cancer Institute (R01CA122334, P30CA016520)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › TGF-β signaling in diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer-related molecular mechanisms research
- Keywords
- neuroblastoma, TGF-beta signaling, Smad2 phosphorylation, microRNA target regulation, cell proliferation, cell adhesion, cancer hallmarks
- MeSH terms
- Animals, Cell Adhesion, Cell Line, Mice, Nude, Neuroblastoma, Transplantation, Heterologous, Transforming Growth Factor beta, MicroRNAs, Cell Proliferation, Mice, Smad2 Protein
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