3’UTR Shortening Potentiates MicroRNA-Based Repression of Pro-differentiation Genes in Proliferating Human Cells
Open accessAbstract
Most mammalian genes often feature alternative polyadenylation (APA) sites and hence diverse 3'UTR lengths. Proliferating cells were reported to favor APA sites that result in shorter 3'UTRs. One consequence of such shortening is escape of mRNAs from targeting by microRNAs (miRNAs) whose binding sites are eliminated. Such a mechanism might provide proliferation-related genes with an expression gain during normal or cancerous proliferation. Notably, miRNA sites tend to be more active when located near both ends of the 3'UTR compared to those located more centrally. Accordingly, miRNA sites located near the center of the full 3'UTR might become more active upon 3'UTR shortening. To address this conjecture we performed 3' sequencing to determine the 3' ends of all human UTRs in several cell lines. Remarkably, we found that conserved miRNA binding sites are preferentially enriched immediately upstream to APA sites, and this enrichment is more prominent in pro-differentiation/anti-proliferative genes. Binding sites of the miR17-92 cluster, upregulated in rapidly proliferating cells, are particularly enriched just upstream to APA sites, presumably conferring stronger inhibitory activity upon shortening. Thus 3'UTR shortening appears not only to enable escape from inhibition of growth promoting genes but also to potentiate repression of anti-proliferative genes.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Many miRNAs have a strong tissue-specific expression pattern and the 3' UTR of target gene plays a critical role in determining miRNA-target interaction.
“Many miRNAs have a strong tissue-specific expression pattern and 3’ UTR of target gene plays a critical role in determining the miRNA-target interaction [136, 137].”
From MicroRNAs in brain cholesterol metabolism and their implications for Alzheimer's disease (2016) · cites this paper as [137]
The Introduction (page not provided) says that the position of a binding site along a target’s 3′ UTR can influence whether miRNA repression occurs, supporting the 3′ UTR part of the claim. The passages on miRNA expression concern changes between cellular states, not a strong tissue-specific expression pattern for many miRNAs; searches for tissue-specific miRNA expression did not establish that part. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506580102 · Cited by 53,625 · see citing works
Lewis, B. P., Burge, C. B., & Bartel, D. P. (2005) · Cell · doi:10.1016/j.cell.2004.12.035 · Cited by 11,855 · see citing works
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,477 · see citing works
Most mammalian mRNAs are conserved targets of microRNAs
Friedman, R. C., Farh, K. K.-H., Burge, C. B., & Bartel, D. P. (2009) · Genome Research · doi:10.1101/gr.082701.108 · Cited by 8,462 · see citing works
Predicting effective microRNA target sites in mammalian mRNAs
Agarwal, V., Bell, G. W., Nam, J.-W., & Bartel, D. P. (2015) · eLife · doi:10.7554/elife.05005 · Cited by 7,318 · see citing works
miRBase: microRNA sequences, targets and gene nomenclature
Griffiths‐Jones, S. (2005) · Nucleic Acids Research · doi:10.1093/nar/gkj112 · Cited by 4,713 · see citing works
Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes
Siepel, A., Bejerano, G., Pedersen, J. S., Hinrichs, A. S., Hou, M., Rosenbloom, K., Clawson, H., Spieth, J., Hillier, L. W., Richards, S., et al. (2005) · Genome Research · doi:10.1101/gr.3715005 · Cited by 4,408 · see citing works
MicroRNA Targeting Specificity in Mammals: Determinants beyond Seed Pairing
Grimson, A., Farh, K. K.-H., Johnston, W. K., Garrett-Engele, P., Lim, L. P., & Bartel, D. P. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.06.017 · Cited by 3,766 · see citing works
GOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists
Eden, E., Navon, R., Steinfeld, I., Lipson, D., & Yakhini, Z. (2009) · BMC Bioinformatics · doi:10.1186/1471-2105-10-48 · Cited by 3,356 · see citing works
Principles of MicroRNA–Target Recognition
Brennecke, J., Stark, A., Russell, R. B., & Cohen, S. M. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030085 · Cited by 2,384 · see citing works
Detection of nonneutral substitution rates on mammalian phylogenies
Pollard, K. S., Hubisz, M. J., Rosenbloom, K. R., & Siepel, A. (2010) · Genome Research · doi:10.1101/gr.097857.109 · Cited by 2,353 · see citing works
Mayr, C., & Bartel, D. P. (2009) · Cell · doi:10.1016/j.cell.2009.06.016 · Cited by 1,613 · see citing works
Sandberg, R., Neilson, J. R., Sarma, A., Sharp, P. A., & Burge, C. B. (2008) · Science · doi:10.1126/science.1155390 · Cited by 1,349 · see citing works
Mogilyansky, E., & Rigoutsos, I. (2013) · Cell Death & Differentiation · doi:10.1038/cdd.2013.125 · Cited by 810 · see citing works
Alternative cleavage and polyadenylation: extent, regulation and function
Elkon, R., Ugalde, A. P., & Agami, R. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3482 · Cited by 805 · see citing works
Self-citationA Dual Program for Translation Regulation in Cellular Proliferation and Differentiation
Gingold, H., Tehler, D., Christoffersen, N. R., Nielsen, M. M., Asmar, F., Kooistra, S. M., Christophersen, N. S., Christensen, L. L., Borre, M., Sørensen, K. D., et al. (2014) · Cell · doi:10.1016/j.cell.2014.08.011 · Cited by 487 · see citing works
Self-citationDesperately seeking microRNA targets
Thomas, M., Lieberman, J., & Lal, A. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1921 · Cited by 476 · see citing works
Martin, G., Gruber, A. R., Keller, W., & Zavolan, M. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.05.003 · Cited by 361 · see citing works
The Poly(A)-Binding Protein Nuclear 1 Suppresses Alternative Cleavage and Polyadenylation Sites
Jenal, M., Elkon, R., Loayza‐Puch, F., van Haaften, G. W., Kühn, U., Menzies, F. M., Vrielink, J. A. F. O., Bos, A., Drost, J., Rooijers, K., et al. (2012) · Cell · doi:10.1016/j.cell.2012.03.022 · Cited by 338 · see citing works
Self-citationGlobal Analyses of the Effect of Different Cellular Contexts on MicroRNA Targeting
Nam, J., Rissland, O. S., Koppstein, D., Abreu‐Goodger, C., Jan, C. H., Agarwal, V., Yıldırım, M. A., Rodríguez, A., & Bartel, D. P. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.02.013 · Cited by 337 · see citing works
Biased alternative polyadenylation in human tissues
Zhang, H., Lee, J. Y., & Tian, B. (2005) · Genome biology · doi:10.1186/gb-2005-6-12-r100 · Cited by 292 · see citing works
Ji, Z., & Tian, B. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008419 · Cited by 264 · see citing works
Alternative polyadenylation: New insights from global analyses
Shi, Y. (2012) · RNA · doi:10.1261/rna.035899.112 · Cited by 212 · see citing works
E2F mediates enhanced alternative polyadenylation in proliferation
Elkon, R., Drost, J., van Haaften, G. W., Jenal, M., Schrier, M., Vrielink, J. A. F. O., & Agami, R. (2012) · Genome biology · doi:10.1186/gb-2012-13-7-r59 · Cited by 155 · see citing works
Self-citationLópez‐Romero, P. (2011) · BMC Genomics · doi:10.1186/1471-2164-12-64 · Cited by 147 · see citing works
(2003) · PubMed · Cited by 146 · see citing works
Escape from hsa-miR-519c enables drug-resistant cells to maintain high expression of ABCG2
To, K. K. W., Robey, R. W., Knutsen, T., Zhan, Z., Ried, T., & Bates, S. E. (2009) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-09-0292 · Cited by 112 · see citing works
Aylon, Y., Yabuta, N., Besserglick, H., Buganim, Y., Rotter, V., Nojima, H., & Oren, M. (2009) · Oncogene · doi:10.1038/onc.2009.270 · Cited by 71 · see citing works
Self-citationTranter, M., Helsley, R. N., Paulding, W. R., McGuinness, M., Brokamp, C., Haar, L., Liu, Y., Ren, X., & Jones, W. K. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.221796 · Cited by 68 · see citing works
The majority of endogenous microRNA targets within Alu elements avoid the microRNA machinery
Hoffman, Y., Dahary, D., Bublik, D. R., Oren, M., & Pilpel, Y. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt044 · Cited by 34 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Alternative polyadenylation of mRNA precursors
Tian, B., & Manley, J. L. (2017) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.116 · Cited by 1,179 · see citing works
Regulation by 3′-Untranslated Regions
Mayr, C. (2017) · Annual Review of Genetics · doi:10.1146/annurev-genet-120116-024704 · Cited by 588 · see citing works
Alternative cleavage and polyadenylation in health and disease
Gruber, A. J., & Zavolan, M. (2019) · Nature Reviews Genetics · doi:10.1038/s41576-019-0145-z · Cited by 468 · see citing works
RNA-binding proteins in tumor progression
Qin, H., Ni, H., Liu, Y., Yuan, Y., Xi, T., Li, X., & Zheng, L. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00927-w · Cited by 382 · see citing works
The miRNA–target interactions: An underestimated intricacy
Diener, C., Keller, A., & Meese, E. U. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad1142 · Cited by 237 · see citing works
Alternative polyadenylation: methods, mechanism, function, and role in cancer
Zhang, Y., Liu, L., Qiu, Q., Zhou, Q. H., Ding, J., Lü, Y., & Liu, P. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-01852-7 · Cited by 152 · see citing works
SCAF4 and SCAF8, mRNA Anti-Terminator Proteins
Gregersen, L. H., Mitter, R., Ugalde, A. P., Nojima, T., Proudfoot, N. J., Agami, R., Stewart, A., & Svejstrup, J. Q. (2019) · Cell · doi:10.1016/j.cell.2019.04.038 · Cited by 140 · see citing works
Self-citationmicroRNA ‐based diagnostic and therapeutic applications in cancer medicine
Sempere, L. F., Azmi, A. S., & Moore, A. V. (2021) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1662 · Cited by 134 · see citing works
MicroRNA-210 Enhances Fibrous Cap Stability in Advanced Atherosclerotic Lesions
Eken, S. M., Jin, H. H., Chernogubova, E., Li, Y., Simon, N. L., Sun, C., Korzunowicz, G., Busch, A., Bäcklund, A., Österholm, C., et al. (2016) · Circulation Research · doi:10.1161/circresaha.116.309318 · Cited by 124 · see citing works
3′ UTR lengthening as a novel mechanism in regulating cellular senescence.
Chen, M., Lyu, G., Han, M., Nie, H., Shen, T., Chen, W., Niu, Y., Song, Y., Li, X., Li, H., et al. (2018) · Genome Research · doi:10.1101/gr.224451.117 · Cited by 111 · see citing works
Alternative Polyadenylation: Methods, Findings, and Impacts
Chen, W., Jia, Q., Song, Y., Fu, H., Wei, G., & Ni, T. (2017) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2017.06.001 · Cited by 103 · see citing works
de Oliveira, A. C., Bovolenta, L. A., Nachtigall, P. G., Herkenhoff, M. E., Lemke, N., & Pinhal, D. (2017) · Frontiers in Genetics · doi:10.3389/fgene.2017.00059 · Cited by 98 · see citing works
Alternative polyadenylation of mRNA and its role in cancer
Yuan, F., Hankey, W., Wagner, E. J., Li, W., & Wang, Q. (2019) · Genes & Diseases · doi:10.1016/j.gendis.2019.10.011 · Cited by 90 · see citing works
Cell-type-specific analysis of alternative polyadenylation using single-cell transcriptomics data
Shulman, E. D., & Elkon, R. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz781 · Cited by 91 · see citing works
Self-citation3’UTR Diversity: Expanding Repertoire of RNA Alterations in Human mRNAs
Hong, D., & Jeong-Yu, S. (2023) · Molecules and Cells · doi:10.14348/molcells.2023.0003 · Cited by 87 · see citing works
Yang, S. W., Li, L., Connelly, J. P., Porter, S. N., Kodali, K., Gan, H., Park, J. M., Tacer, K. F., Tillman, H., Peng, J., et al. (2020) · Molecular Cell · doi:10.1016/j.molcel.2019.12.022 · Cited by 79 · see citing works
The contribution of alternative polyadenylation to the cancer phenotype
Masamha, C. P., & Wagner, E. J. (2017) · Carcinogenesis · doi:10.1093/carcin/bgx096 · Cited by 77 · see citing works
Vaklavas, C., Blume, S. W., & Grizzle, W. E. (2017) · Frontiers in Oncology · doi:10.3389/fonc.2017.00158 · Cited by 73 · see citing works
de la Fuente, L., Arzalluz-Luque, Á., Tardáguila, M., del Risco, H., Martí, C., Tarazona, S., Salguero, P., Scott, R., Lerma-Aguilera, A., Alastrue‐Agudo, A., et al. (2020) · Genome biology · doi:10.1186/s13059-020-02028-w · Cited by 66 · see citing works
The landscape of alternative polyadenylation in single cells of the developing mouse embryo
Agarwal, V., Lopez-Darwin, S. L., Kelley, D. R., & Shendure, J. (2021) · Nature Communications · doi:10.1038/s41467-021-25388-8 · Cited by 64 · see citing works
Malka, Y., Steiman‐Shimony, A., Rosenthal, E., Argaman, L., Cohen‐Daniel, L., Arbib, E., Margalit, H., Kaplan, T., & Berger, M. (2017) · Nature Communications · doi:10.1038/s41467-017-02099-7 · Cited by 58 · see citing works
Regulation of alternative polyadenylation by the C2H2-zinc-finger protein Sp1
Song, J., Nabeel‐Shah, S., Pu, S., Lee, H., Braunschweig, U., Ni, Z., Ahmed, N., Marcon, E., Zhong, G., Ray, D., et al. (2022) · Molecular Cell · doi:10.1016/j.molcel.2022.06.031 · Cited by 59 · see citing works
Roar: detecting alternative polyadenylation with standard mRNA sequencing libraries
Grassi, E., Mariella, E., Lembo, A., Molineris, I., & Provero, P. (2016) · BMC Bioinformatics · doi:10.1186/s12859-016-1254-8 · Cited by 57 · see citing works
Fu, Y., Chen, L., Chen, C., Ge, Y., Kang, M., Song, Z., Li, J., Feng, Y., Huo, Z., He, G., et al. (2018) · Genome Research · doi:10.1101/gr.231506.117 · Cited by 56 · see citing works
Gao, Y., Li, L., Amos, C. I., & Li, W. (2021) · Genome Research · doi:10.1101/gr.271346.120 · Cited by 52 · see citing works
Alternative Polyadenylation of Mammalian Transcripts Is Generally Deleterious, Not Adaptive
Xu, C., & Zhang, J. (2018) · Cell Systems · doi:10.1016/j.cels.2018.05.007 · Cited by 47 · see citing works
Fang, S., Zhang, D., Weng, W., Lv, X., Zheng, L., Chen, M., Fan, X., Mao, J., Mao, C., Ye, Y., et al. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2019.118624 · Cited by 44 · see citing works
Alternative polyadenylation: An enigma of transcript length variation in health and disease
Mohanan, N. K., Shaji, F., Koshre, G. R., & Laishram, R. S. (2021) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1692 · Cited by 41 · see citing works
Guo, Q., Li, L., Bo, Q., Chen, L., Sun, L. J., & Shi, H. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.110072 · Cited by 40 · see citing works
Systematic identification of functional SNPs interrupting 3’UTR polyadenylation signals
Shulman, E. D., & Elkon, R. (2020) · PLoS Genetics · doi:10.1371/journal.pgen.1008977 · Cited by 40 · see citing works
Self-citationAlternative polyadenylation and RNA-binding proteins
Erson-Bensan, A. E. (2016) · Journal of Molecular Endocrinology · doi:10.1530/jme-16-0070 · Cited by 39 · see citing works
CFIm25 and alternative polyadenylation: Conflicting roles in cancer
Abadi, M. H. J. N., Shafabakhsh, R., Asemi, Z., Mirzaei, H. R., Sahebnasagh, R., Mirzaei, H., & Hamblin, M. R. (2019) · Cancer Letters · doi:10.1016/j.canlet.2019.114430 · Cited by 36 · see citing works
Recurrent tumor-specific regulation of alternative polyadenylation of cancer-related genes
Xue, Z., Warren, R. L., Gibb, E. A., MacMillan, D., Wong, J., Chiu, R., Hammond, S. A., Yang, C., Nip, K. M., Ennis, C. A., et al. (2018) · BMC Genomics · doi:10.1186/s12864-018-4903-7 · Cited by 33 · see citing works
Alternative polyadenylation confers PtenmRNAs stability and resistance to microRNAs
Thivierge, C., Tseng, H.-W., Mayya, V. K., Lussier, C. R., Gravel, S., & Duchaîne, T. F. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky666 · Cited by 34 · see citing works
Upregulation of miR-1306-5p decreases cerebral ischemia/reperfusion injury in vitro by targeting BIK
Chen, X., Li, C., Li, J., Sheng, L., & Liu, X. (2019) · Bioscience Biotechnology and Biochemistry · doi:10.1080/09168451.2019.1654846 · Cited by 29 · see citing works
Gillen, S. L., Waldron, J. A., & Bushell, M. (2021) · Oncogene · doi:10.1038/s41388-021-02022-x · Cited by 29 · see citing works
Co-Transcriptional RNA Processing in Plants: Exploring from the Perspective of Polyadenylation
Yang, J., Cao, Y., & Ma, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22073300 · Cited by 24 · see citing works
MicroRNAs in brain cholesterol metabolism and their implications for Alzheimer's disease
Yoon, H., Flores, L. F., & Kim, J. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2016.04.020 · Cited by 23 · see citing works
Gendreau, K. L., Unruh, B. A., Zhou, C., & Kojima, S. (2018) · G3 Genes Genomes Genetics · doi:10.1534/g3.118.200559 · Cited by 18 · see citing works
Dong, X., Cao, R., Li, Q., & Yin, L. (2021) · The Nephron journals/Nephron journals · doi:10.1159/000518756 · Cited by 21 · see citing works
Fahmi, N. A., Ahmed, K. T., Chang, J., Nassereddeen, H., Fan, D., Yong, J., & Zhang, W. (2022) · BMC Bioinformatics · doi:10.1186/s12859-022-04939-w · Cited by 21 · see citing works
A systematic review of mechanisms of PTEN gene down-regulation mediated by miRNA in prostate cancer
Bergez‐Hernández, F., Arredondo, M. I., & Martínez-Camberos, A. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e34950 · Cited by 19 · see citing works
Alternative Polyadenylation Patterns for Novel Gene Discovery and Classification in Cancer
Begik, O., Oyken, M., Alican, T. C., Can, T., & Erson-Bensan, A. E. (2017) · Neoplasia · doi:10.1016/j.neo.2017.04.008 · Cited by 19 · see citing works
The quantitative impact of 3′UTRs on gene expression
West, J. D., Smith, H. J., Vu, L. T., Fogarty, E. A., Matreyek, K. A., Fowler, D. M., & Grimson, A. (2025) · Nucleic Acids Research · doi:10.1093/nar/gkaf568 · Cited by 17 · see citing works
Parkins, E. V., & Groß, C. (2024) · Journal of Neuroscience · doi:10.1523/jneurosci.0365-24.2024 · Cited by 14 · see citing works
Single-cell alternative polyadenylation analysis delineates GABAergic neuron types
Yang, Y., Paul, A., Bach, T. N., Huang, Z. J., & Zhang, M. Q. (2021) · BMC Biology · doi:10.1186/s12915-021-01076-3 · Cited by 15 · see citing works
Tseng, H.-W., Mota-Sydor, A., Leventis, R., Jovanović, P., Topisirović, I., & Duchaîne, T. F. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac704 · Cited by 15 · see citing works
Dysregulation of Alternative Poly-adenylation as a Potential Player in Autism Spectrum Disorder
Szkop, K. J., Cooke, P. I. C., Humphries, J. A., Kalna, V., Moss, D. S., Schuster, E. F., & Nobeli, I. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00279 · Cited by 12 · see citing works
Meyer, E. A., Chaung, K., Dehghannasiri, R., & Salzman, J. (2022) · Genome biology · doi:10.1186/s13059-022-02795-8 · Cited by 11 · see citing works
mRNA isoform balance in neuronal development and disease
LaForce, G. R., Philippidou, P., & Schaffer, A. E. (2022) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1762 · Cited by 14 · see citing works
MicroRNAs as Prognostic Biomarkers and Therapeutic Targets in Chondrosarcoma
Skipar, P., Dey, M., Piątkowski, J., Sulejczak, D., Rutkowski, P. L., & Czarnecka, A. M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25063176 · Cited by 12 · see citing works
Therapeutic applications of cell engineering using mRNA technology
He, Y., Johnston, A. P. R., & Pouton, C. W. (2024) · Trends in biotechnology · doi:10.1016/j.tibtech.2024.07.012 · Cited by 12 · see citing works
LncRNA HOTTIP leads to osteoarthritis progression via regulating miR-663a/ Fyn-related kinase axis
He, X., Gao, K., Lu, S., & Wu, R. (2021) · BMC Musculoskeletal Disorders · doi:10.1186/s12891-020-03861-7 · Cited by 12 · see citing works
Relationship between NUDT21 mediated alternative polyadenylation process and tumor
Xiao, S., Gu, H., Li Juan, D. E. N. G., Yang, X., Qiao, D., Zhang, X., Zhang, T., & Yu, T. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1052012 · Cited by 10 · see citing works
Ma, Y., Zhou, A., & Song, J. (2020) · Oncology Letters · doi:10.3892/ol.2020.12352 · Cited by 10 · see citing works
RNA polyadenylation patterns in the human transcriptome
Xu, S.-M., Curry‐Hyde, A., Sytnyk, V., & Janitz, M. (2022) · Gene · doi:10.1016/j.gene.2021.146133 · Cited by 9 · see citing works
In silico model for miRNA-mediated regulatory network in cancer
Ahmed, K. T., Sun, J., Chen, W., Martinez, I., Cheng, S. L. A., Zhang, W. C., Yong, J., & Zhang, W. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab264 · Cited by 9 · see citing works
Gaither, K. A., Watson, C. J. W., Madarampalli, B., & Lazarus, P. J. (2020) · PLoS ONE · doi:10.1371/journal.pone.0225044 · Cited by 8 · see citing works
Evaluating the Oncogenic and Tumor Suppressor Role of XPO5 in Different Tissue Tumor Types
Khan, M. S., Khan, Z. U., Uddin, Y., Mustafa, S. R., Shaukat, I., Pan, J., & Höti, N. (2018) · Europe PMC (PubMed Central) · doi:10.22034/apjcp.2018.19.4.1119 · Cited by 8 · see citing works
Ge, S., Li, J., Ma, H., Sánchez-Bermúdez, M., Wu, S., Lv, Q., Guo, F., Dong, J., Ma, G., Li, Q. Q., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-63406-1 · Cited by 7 · see citing works
CRISPR Editing Enables Consequential Tag-Activated MicroRNA-Mediated Endogene Deactivation
Papasavva, P. L., Patsali, P., Loucari, C. C., Kurita, R., Nakamura, Y., Kleanthous, M., & Lederer, C. W. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23031082 · Cited by 7 · see citing works
Pan‐tissue analysis of allelic alternative polyadenylation suggests widespread functional regulation
Li, Y., Schaefke, B., Zou, X., Zhang, M., Heyd, F., Sun, W., Zhang, B., Li, G., Liang, W., He, Y., et al. (2020) · Molecular Systems Biology · doi:10.15252/msb.20199367 · Cited by 6 · see citing works
Analysis of RNA Polyadenylation in Healthy and Osteoarthritic Human Articular Cartilage
Winstanley‐Zarach, P., Rot, G., Kuba, S. Y., Smagul, A., Peffers, M. J., & Tew, S. R. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24076611 · Cited by 6 · see citing works
Computational Detection of MicroRNA Targets
Nachtigall, P. G., & Bovolenta, L. A. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1170-8_10 · Cited by 6 · see citing works
The role of alternative polyadenylation in cancer progression
Jain, B. P. (2018) · Gene Reports · doi:10.1016/j.genrep.2018.05.003 · Cited by 6 · see citing works
SINE Retrotransposons Import Polyadenylation Signals to 3’UTRs in Dog ( Canis familiaris )Preprint
Choi, J. D., Pinto, L. A. D., & Sutter, N. B. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.30.405357 · Cited by 6 · see citing works
Pang, F., Yang, P., Wang, T. A., Li, X., Wu, X., Yue, R., Bai, B., & Zhao, Q. (2023) · Current Genomics · doi:10.2174/1389202924666230503122134 · Cited by 5 · see citing works
miR‑4458 directly targets IGF1R to inhibit cell proliferation and promote apoptosis in hemangioma
Wu, M., Tang, Y., Hu, G., Yang, C., Ye, K., & Liu, X. (2020) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2020.8546 · Cited by 5 · see citing works
Gao, Y., Li, L., Amos, C. I., & Li, W. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.23.310649 · Cited by 5 · see citing works
Staff, T. P. G. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006254 · Cited by 5 · see citing works
Genetics of cell-type-specific post-transcriptional gene regulation during human neurogenesis
Aygün, N., Vuong, C. K., Krupa, O., Mory, J. T., Le, B. D., Valone, J. M., Liang, D., Shafie, B., Zhang, P., Salinda, A., et al. (2024) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2024.07.015 · Cited by 4 · see citing works
Zhang, F., Chen, L., Li, W., Yang, C., Xiong, M., Zhou, M., Kazobinka, G., Zhao, J., & Hou, T. (2023) · Laboratory Investigation · doi:10.1016/j.labinv.2023.100125 · Cited by 3 · see citing works
The 3′ UTR Landscape in Cancer
Schmidt, R., Ghosh, S., & Zavolan, M. (2018) · Wiley eBooks · doi:10.1002/9780470015902.a0027958 · Cited by 3 · see citing works
Wei, J., Zhang, D., Lu, X., Zhang, K., Liu, R., Wu, X., Zhu, J., Lai, J., Su, G., & Wang, L. (2025) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2025.102624 · Cited by 2 · see citing works
Szewc, Ł., Zhang, X., Bajczyk, M., Bielewicz, D., Zimna, M., Yura, K., Kato, M., Nomoto, M., García-León, M., Rubio, V., et al. (2025) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiaf483 · Cited by 2 · see citing works
Stalling of elongating Pol II triggers Ser7 phosphorylation in trans to drive transcription recoveryPreprint
Shlamovitz, I., Bao, Y., Toteva, T., Crisp, A., Ye, S., Wingett, S., Cacioppo, R., Edmondson, A., Castiblanco, D., Boemo, M. A., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.04.692291 · Cited by 2 · see citing works
Alternative polyadenylation in cancer: mechanisms, functions, and therapeutic potential
Huang, Y., Li, Z., Yu, F., & Wang, L. (2026) · Molecular Cancer · doi:10.1186/s12943-026-02760-0 · Cited by 1 · see citing works
SINE retrotransposons import polyadenylation signals to 3’UTRs in dog (Canis familiaris)
Choi, J. D., Pinto, L. A. D., & Sutter, N. B. (2025) · Mobile DNA · doi:10.1186/s13100-024-00338-5 · Cited by 1 · see citing works
microRNAs in Nutritional Signaling and Metabolic Syndrome
Wade, H., & Su, Q. (2019) · Elsevier eBooks · doi:10.1016/b978-0-08-100596-5.22723-6 · Cited by 1 · see citing works
Gao, Y., & Li, W. (2021) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2021.03.015
The Role of miRNAs and Alternative Polyadenylation in Modulating the P53 Response
Browning, J. W. L. (2018) · doi:10.22215/etd/2018-13260
Alternative polyadenylation shapes the molecular and clinical features of lung adenocarcinoma
Gao, Y., Shaw, V. R., & Amos, C. I. (2024) · Human Molecular Genetics · doi:10.1093/hmg/ddae150
Fahmi, N. A., Ahmed, K. T., Chang, J.-W., Nassereddeen, H., Fan, D., Yong, J., & Zhang, W. (2022) · Figshare · doi:10.6084/m9.figshare.21229240
Yang, Y., Paul, A., Bach, T. N., Huang, Z. J., & Zhang, M. Q. (2021) · Figshare · doi:10.6084/m9.figshare.15047700
Meyer, E. A., Chaung, K., Dehghannasiri, R., & Salzman, J. (2022) · Figshare · doi:10.6084/m9.figshare.21397906
Fahmi, N. A., Ahmed, K. T., Chang, J.-W., Nassereddeen, H., Fan, D., Yong, J., & Zhang, W. (2022) · Figshare · doi:10.6084/m9.figshare.21229243
Global mRNA 3′UTR lengthening in small-cell neuroendocrine carcinomaPreprint
Zhang, Y., Zhao, X., Wang, H., Hu, Y., Sun, X., Zhao, F., Du, S., Dai, R. S., Andeen, N. K., Sears, R. C., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.26.701900
Alternative polyadenylation mediated by CPSF5 regulates pro-inflammatory gene expressionPreprint
Lemmer, M., Lindner, D., Stoecklin, G., & Schott, J. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.31.703030
Regulation of alternative splicing and polyadenylation by genotoxic anti-cancer agents
Tanaka, I. (2019) · theses.fr (ABES) · doi:10.70675/8177333az76a6z4204z808az958753142caf
Xiao, Q., Ai, L., Jia, B., Kuang, M., Xiao, S., Bi, X., Zhu, Y., Li, G., Huang, W., & Duan, R. (2026) · Cell & Bioscience · doi:10.1186/s13578-026-01578-z
- Authors
- Hoffman, Y., Bublik, D. R., P. Ugalde, A., Elkon, R., Biniashvili, T., Agami, R., Oren, M., & Pilpel, Y.
- Affiliations
- Weizmann Institute of Science (IL)
- The Netherlands Cancer Institute (NL)
- Corresponding author
- Oren, Moshe
- Pilpel, Yitzhak
- Venue
- PLOS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2016-02-23
- Volume
- 12
- Issue
- 2
- Pages
- e1005879
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC4764332
- OpenAlex
- W2283446040
- Cited by
- 90
- References
- 30
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 6 · 2023: 6 · 2022: 10 · 2021: 14 · 2020: 11 · 2019: 9 · 2018: 10 · 2017: 8 · 2016: 6
- FWCI
- 5.72
- Type
- journal article
- Language
- en
- Update notices
- correction (2016-08-05)
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Figshare (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- 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
- Keywords
- 3' UTR shortening, alternative polyadenylation, microRNA binding sites, cell proliferation, miR-17-92 cluster, gene expression regulation
- MeSH terms
- Binding Sites, Cell Line, Humans, Gene Expression Regulation, Developmental, 3' Untranslated Regions, Polyadenylation, MicroRNAs, Cell Proliferation, RNA, Long Noncoding
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 ›
Are you an author, or do you see a problem with this page? Request a review
