RNA-Binding Proteins in Cancer: Old Players and New Actors
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Dreyfuss, 2002, Messenger-RNA-binding proteins and the messages they carry, Nat. Rev. Mol. Cell Biol., 3, 195, 10.1038/nrm760
Mitchell, 2014, Principles and properties of eukaryotic mRNPs, Mol. Cell, 54, 547, 10.1016/j.molcel.2014.04.033
Neelamraju, 2015, The human RBPome: from genes and proteins to human disease, J. Proteomics, 127, 61, 10.1016/j.jprot.2015.04.031
Gerstberger, 2014, A census of human RNA-binding proteins, Nat. Rev. Genet., 15, 829, 10.1038/nrg3813
Beckmann, 2015, The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs, Nat. Commun., 6, 10127, 10.1038/ncomms10127
Anantharaman, 2002, Comparative genomics and evolution of proteins involved in RNA metabolism, Nucleic Acids Res., 30, 1427, 10.1093/nar/30.7.1427
Matia-González, 2015, Conserved mRNA-binding proteomes in eukaryotic organisms, Nat. Struct. Mol. Biol., 22, 1027, 10.1038/nsmb.3128
Lunde, 2007, RNA-binding proteins: modular design for efficient function, Nat. Rev. Mol. Cell Biol., 8, 479, 10.1038/nrm2178
Jankowsky, 2015, Specificity and nonspecificity in RNA-protein interactions, Nat. Rev. Mol. Cell. Biol., 16, 533, 10.1038/nrm4032
Calabretta, 2015, Emerging roles of disordered sequences in RNA-binding proteins, Trends Biochem. Sci., 40, 662, 10.1016/j.tibs.2015.08.012
Castello, 2016, Comprehensive identification of RNA-binding domains in human cells, Mol. Cell, 63, 696, 10.1016/j.molcel.2016.06.029
Järvelin, 2016, The new (dis)order in RNA regulation, Cell Commun. Signal., 14, 9, 10.1186/s12964-016-0132-3
Lukong, 2008, RNA-binding proteins in human genetic disease, Trends Genet., 24, 416, 10.1016/j.tig.2008.05.004
Sahu, 2015, Long noncoding RNAs in cancer: from function to translation, Trends Cancer, 1, 93, 10.1016/j.trecan.2015.08.010
David, 2010, Alternative pre-mRNA splicing regulation in cancer: pathways and programs unhinged, Genes Dev., 24, 2343, 10.1101/gad.1973010
Chabot, 2016, Defective control of pre-messenger RNA splicing in human disease, J. Cell. Biol., 212, 13, 10.1083/jcb.201510032
Bhat, 2015, Targeting the translation machinery in cancer, Nat. Rev. Drug Discov., 14, 261, 10.1038/nrd4505
Hinnebusch, 2016, Translational control by 5′-untranslated regions of eukaryotic mRNAs, Science, 352, 1413, 10.1126/science.aad9868
Truitt, 2016, New frontiers in translational control of the cancer genome, Nat. Rev. Cancer, 16, 288, 10.1038/nrc.2016.27
Patry, 2003, Small interfering RNA-mediated reduction in heterogeneous nuclear ribonucleoparticule A1/A2 proteins induces apoptosis in human cancer cells but not in normal mortal cell lines, Cancer Res., 63, 7679
Busà, 2007, The RNA-binding protein Sam68 contributes to proliferation and survival of human prostate cancer cells, Oncogene, 26, 4372, 10.1038/sj.onc.1210224
Yang, 2010, RNA-binding protein quaking, a critical regulator of colon epithelial differentiation and a suppressor of colon cancer, Gastroenterology, 138, 231, 10.1053/j.gastro.2009.08.001
King, 2011, LIN28B promotes colon cancer progression and metastasis, Cancer Res., 71, 4260, 10.1158/0008-5472.CAN-10-4637
Ortiz-Zapater, 2011, Key contribution of CPEB4-mediated translational control to cancer progression, Nat. Med., 18, 83, 10.1038/nm.2540
Janiszewska, 2012, Imp2 controls oxidative phosphorylation and is crucial for preserving glioblastoma cancer stem cells, Genes Dev., 26, 1926, 10.1101/gad.188292.112
Vo, 2012, The RNA-binding protein Musashi1 affects medulloblastoma growth via a network of cancer-related genes and is an indicator of poor prognosis, Am. J. Pathol., 181, 1762, 10.1016/j.ajpath.2012.07.031
Ishii, 2014, Epithelial splicing regulatory proteins 1 (ESRP1) and 2 (ESRP2) suppress cancer cell motility via different mechanisms, J. Biol. Chem., 289, 27386, 10.1074/jbc.M114.589432
Sánchez-Jiménez, 2015, T-cell intracellular antigens function as tumor suppressor genes, Cell Death Dis., 6, e1669, 10.1038/cddis.2015.43
Hopkins, 2016, The RNA-binding protein LARP1 is a post-transcriptional regulator of survival and tumorigenesis in ovarian cancer, Nucleic Acids Res., 44, 1227, 10.1093/nar/gkv1515
Wurth, 2016, UNR/CSDE1 drives a post-transcriptional program to promote melanoma invasion and metastasis, Cancer Cell, 30, 694, 10.1016/j.ccell.2016.10.004
Kechavarzi, 2014, Dissecting the expression landscape of RNA-binding proteins in human cancers, Genome Biol., 15, R14, 10.1186/gb-2014-15-1-r14
Wang, 2015, Dysregulated transcription across diverse cancer types reveals the importance of RNA-binding protein in carcinogenesis, BMC Genomics, 16, S5, 10.1186/1471-2164-16-S7-S5
Sebestyén, 2016, Large-scale analysis of genome and transcriptome alterations in multiple tumors unveils novel cancer-relevant splicing networks, Genome Res., 26, 732, 10.1101/gr.199935.115
Wahl, 2009, The spliceosome: design principles of a dynamic RNP machine, Cell, 136, 701, 10.1016/j.cell.2009.02.009
Castello, 2013, RNA-binding proteins in Mendelian disease, Trends Genet., 29, 318, 10.1016/j.tig.2013.01.004
Hill, 2009, DICER1 mutations in familial pleuropulmonary blastoma, Science, 325, 965, 10.1126/science.1174334
Foulkes, 2014, DICER1: mutations, microRNAs and mechanisms, Nat. Rev. Cancer, 14, 662, 10.1038/nrc3802
Selvanathan, 2015, Oncogenic fusion protein EWS-FLI1 is a network hub that regulates alternative splicing, Proc. Natl. Acad. Sci. U. S. A., 112, E1307, 10.1073/pnas.1500536112
Clower, 2010, The alternative splicing repressors hnRNP A1/A2 and PTB influence pyruvate kinase isoform expression and cell metabolism, Proc. Natl. Acad. Sci. U. S. A., 107, 1894, 10.1073/pnas.0914845107
David, 2010, HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer, Nature, 463, 364, 10.1038/nature08697
Kang, 2008, NF-kappaB activates transcription of the RNA-binding factor HuR, via PI3K–AKT signaling, to promote gastric tumorigenesis, Gastroenterology, 135, 2030, 10.1053/j.gastro.2008.08.009
Preca, 2015, A self-enforcing CD44s/ZEB1 feedback loop maintains EMT and stemness properties in cancer cells, Int. J. Cancer, 137, 2566, 10.1002/ijc.29642
Larsen, 2016, ZEB1 drives epithelial-to-mesenchymal transition in lung cancer, J. Clin. Invest., 126, 3219, 10.1172/JCI76725
Shu, 2006, RNPC1, an RNA-binding protein and a target of the p53 family, is required for maintaining the stability of the basal and stress-induced p21 transcript, Genes Dev., 20, 2961, 10.1101/gad.1463306
Zhang, 2014, Mice deficient in Rbm38, a target of the p53 family, are susceptible to accelerated aging and spontaneous tumors, Proc. Natl. Acad. Sci. U. S. A., 111, 18637, 10.1073/pnas.1415607112
Abdelmohsen, 2008, miR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels, Proc. Natl. Acad. Sci. U. S. A., 105, 20297, 10.1073/pnas.0809376106
Guo, 2009, MicroRNA-125a represses cell growth by targeting HuR in breast cancer, RNA Biol., 6, 575, 10.4161/rna.6.5.10079
Abdelmohsen, 2010, miR-519 suppresses tumor growth by reducing HuR levels, Cell Cycle, 9, 1354, 10.4161/cc.9.7.11164
Tokumaru, 2008, let-7 regulates Dicer expression and constitutes a negative feedback loop, Carcinogenesis, 29, 2073, 10.1093/carcin/bgn187
Martello, 2010, A microRNA targeting dicer for metastasis control, Cell, 141, 1195, 10.1016/j.cell.2010.05.017
Kumar, 2007, Impaired microRNA processing enhances cellular transformation and tumorigenesis, Nat. Genet., 39, 673, 10.1038/ng2003
Vo, 2011, The oncogenic RNA-binding protein Musashi1 is regulated by tumor suppressor miRNAs, RNA Biol., 8, 817, 10.4161/rna.8.5.16041
Vo, 2012, The oncogenic RNA-binding protein Musashi1 is regulated by HuR via mRNA translation and stability in glioblastoma cells, Mol. Cancer Res., 10, 143, 10.1158/1541-7786.MCR-11-0208
Babic, 2004, The RNA binding protein Sam68 is acetylated in tumor cell lines, and its acetylation correlates with enhanced RNA binding activity, Oncogene, 23, 3781, 10.1038/sj.onc.1207484
Nakka, 2015, Nuclear matrix-associated protein SMAR1 regulates alternative splicing via HDAC6-mediated deacetylation of Sam68, Proc. Natl. Acad. Sci. U. S. A., 112, E3374, 10.1073/pnas.1418603112
Chaudhury, 2010, TGF-beta-mediated phosphorylation of hnRNP E1 induces EMT via transcript-selective translational induction of Dab2 and ILEI, Nat. Cell Biol., 12, 286, 10.1038/ncb2029
Hussey, 2011, Identification of an mRNP complex regulating tumorigenesis at the translational elongation step, Mol. Cell, 41, 419, 10.1016/j.molcel.2011.02.003
Zhang, 2013, Glycogen synthase kinase 3 promotes p53 mRNA translation via phosphorylation of RNPC1, Genes Dev., 27, 2246, 10.1101/gad.221739.113
Fu, 2014, Context-dependent control of alternative splicing by RNA-binding proteins, Nat Rev. Genet., 15, 689, 10.1038/nrg3778
Gouble, 2002, A new player in oncogenesis: AUF1/hnRNPD overexpression leads to tumorigenesis in transgenic mice, Cancer Res., 62, 1489
Liao, 2007, Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation, Nat. Struct. Mol. Biol., 14, 511, 10.1038/nsmb1249
Vázquez-Chantada, 2010, HuR/methyl-HuR and AUF1 regulate the MAT expressed during liver proliferation, differentiation, and carcinogenesis, Gastroenterology, 138, 1943, 10.1053/j.gastro.2010.01.032
Tauler, 2010, hnRNP A2/B1 modulates epithelial-mesenchymal transition in lung cancer cell lines, Cancer Res., 70, 7137, 10.1158/0008-5472.CAN-10-0860
Golan-Gerstl, 2011, Splicing factor hnRNP A2/B1 regulates tumor suppressor gene splicing and is an oncogenic driver in glioblastoma, Cancer Res., 71, 4464, 10.1158/0008-5472.CAN-10-4410
Lefave, 2011, Splicing factor hnRNPH drives an oncogenic splicing switch in gliomas, EMBO J., 30, 4084, 10.1038/emboj.2011.259
Abdelmohsen, 2012, RNA-binding protein AUF1 represses Dicer expression, Nucleic Acids Res., 40, 11531, 10.1093/nar/gks930
Xu, 2014, Cell type-restricted activity of hnRNPM promotes breast cancer metastasis via regulating alternative splicing, Genes Dev., 28, 1191, 10.1101/gad.241968.114
Yoon, 2014, PAR-CLIP analysis uncovers AUF1 impact on target RNA fate and genome integrity, Nat. Commun., 5, 5248, 10.1038/ncomms6248
Pont, 2012, mRNA decay factor AUF1 maintains normal aging, telomere maintenance, and suppression of senescence by activation of telomerase transcription, Mol. Cell, 47, 5, 10.1016/j.molcel.2012.04.019
Gallardo, 2015, hnRNP K is a haploinsufficient tumor suppressor that regulates proliferation and differentiation programs in hematologic malignancies, Cancer Cell, 28, 486, 10.1016/j.ccell.2015.09.001
Gautrey, 2015, SRSF3 and hnRNP H1 regulate a splicing hotspot of HER2 in breast cancer cells, RNA Biol., 12, 1139, 10.1080/15476286.2015.1076610
Ghigna, 2005, Cell motility is controlled by SF2/ASF through alternative splicing of the Ron protooncogene, Mol. Cell., 20, 881, 10.1016/j.molcel.2005.10.026
Li, 2005, Loss of splicing factor ASF/SF2 induces G2 cell cycle arrest and apoptosis, but inhibits internucleosomal DNA fragmentation, Genes Dev., 19, 2705, 10.1101/gad.1359305
Karni, 2007, The gene encoding the splicing factor SF2/ASF is a proto-oncogene, Nat. Struct. Mol. Biol., 14, 185, 10.1038/nsmb1209
Gonçalves, 2009, Antagonistic SR proteins regulate alternative splicing of tumor-related Rac1b downstream of the PI3-kinase and Wnt pathways, Hum. Mol. Genet., 18, 3696, 10.1093/hmg/ddp317
Olshavsky, 2010, Identification of ASF/SF2 as a critical, allele-specific effector of the cyclin D1b oncogene, Cancer Res., 70, 3975, 10.1158/0008-5472.CAN-09-3468
Das, 2012, Oncogenic splicing factor SRSF1 is a critical transcriptional target of MYC, Cell Rep., 1, 110, 10.1016/j.celrep.2011.12.001
Anczuków, 2012, The splicing factor SRSF1 regulates apoptosis and proliferation to promote mammary epithelial cell transformation, Nat. Struct. Mol. Biol., 19, 220, 10.1038/nsmb.2207
Fregoso, 2013, Splicing-factor oncoprotein SRSF1 stabilizes p53 via RPL5 and induces cellular senescence, Mol. Cell, 50, 56, 10.1016/j.molcel.2013.02.001
Zong, 2014, The RNA-binding protein QKI suppresses cancer-associated aberrant splicing, PLoS Genet., 10, e1004289, 10.1371/journal.pgen.1004289
Bechara, 2013, RBM5, 6, and 10 differentially regulate NUMB alternative splicing to control cancer cell proliferation, Mol. Cell, 52, 720, 10.1016/j.molcel.2013.11.010
Hernández, 2016, Tumor suppressor properties of the splicing regulatory factor RBM10, RNA Biol., 13, 466, 10.1080/15476286.2016.1144004
Elkon, 2013, Alternative cleavage and polyadenylation: extent, regulation and function, Nat. Rev. Genet., 14, 496, 10.1038/nrg3482
Mayr, 2009, Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells, Cell, 138, 673, 10.1016/j.cell.2009.06.016
Singh, 2009, Global changes in processing of mRNA 3′ untranslated regions characterize clinically distinct cancer subtypes, Cancer Res., 69, 9422, 10.1158/0008-5472.CAN-09-2236
Gruber, 2012, Cleavage factor Im is a key regulator of 3′ UTR length, RNA Biol., 9, 1405, 10.4161/rna.22570
Martin, 2012, Genome-wide analysis of pre-mRNA 3′ end processing reveals a decisive role of human cleavage factor I in the regulation of 3′ UTR length, Cell Rep., 1, 753, 10.1016/j.celrep.2012.05.003
Masamha, 2014, CFIm25 links alternative polyadenylation to glioblastoma tumour suppression, Nature, 510, 412, 10.1038/nature13261
D'Ambrogio, 2013, Translational control of cell growth and malignancy by the CPEBs, Nat. Rev. Cancer, 13, 283, 10.1038/nrc3485
Bava, 2013, CPEB1 coordinates alternative 3′-UTR formation with translational regulation, Nature, 495, 121, 10.1038/nature11901
Pérez-Guijarro, 2016, Lineage-specific roles of the cytoplasmic polyadenylation factor CPEB4 in the regulation of melanoma drivers, Nat. Commun., 7, 13418, 10.1038/ncomms13418
Calderone, 2016, Sequential functions of CPEB1 and CPEB4 regulate pathologic expression of vascular endothelial growth factor and angiogenesis in chronic liver disease, Gastroenterology, 150, 982, 10.1053/j.gastro.2015.11.038
Garneau, 2007, The highways and byways of mRNA decay, Nat. Rev. Mol. Cell. Biol., 8, 113, 10.1038/nrm2104
Gruber, 2011, AREsite: a database for the comprehensive investigation of AU-rich elements, Nucleic Acids Res., 39, D66, 10.1093/nar/gkq990
Benjamin, 2007, mRNA stability and cancer: an emerging link?, Expert Opin. Biol. Ther., 7, 1515, 10.1517/14712598.7.10.1515
Wang, 2000, HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation, EMBO J., 19, 2340, 10.1093/emboj/19.10.2340
Lal, 2004, Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs, EMBO J., 23, 3092, 10.1038/sj.emboj.7600305
Guo, 2006, HuR contributes to cyclin E1 deregulation in MCF-7 breast cancer cells, Cancer Res., 66, 7948, 10.1158/0008-5472.CAN-05-4362
Moore, 2014, Physiological networks and disease functions of RNA-binding protein AUF1, Wiley Interdiscip. Rev. RNA, 5, 549, 10.1002/wrna.1230
Medioni, 2012, Principles and roles of mRNA localization in animal development, Development, 139, 3263, 10.1242/dev.078626
Hüttelmaier, 2005, Spatial regulation of beta-actin translation by Src-dependent phosphorylation of ZBP1, Nature, 438, 512, 10.1038/nature04115
Gu, 2009, Blocking beta-catenin binding to the ZBP1 promoter represses ZBP1 expression, leading to increased proliferation and migration of metastatic breast-cancer cells, J. Cell Sci., 122, 1895, 10.1242/jcs.045278
Gu, 2012, Regulation of local expression of cell adhesion and motility-related mRNAs in breast cancer cells by IMP1/ZBP1, J. Cell Sci., 125, 81, 10.1242/jcs.086132
Preitner, 2014, APC is an RNA-binding protein, and its interactome provides a link to neural development and microtubule assembly, Cell, 158, 368, 10.1016/j.cell.2014.05.042
Hsieh, 2010, Targeting eukaryotic translation initiation factor 4E (eIF4E) in cancer, Clin. Cancer Res., 16, 4914, 10.1158/1078-0432.CCR-10-0433
Ruggero, 2004, The translation factor eIF-4E promotes tumor formation and cooperates with c-Myc in lymphomagenesis, Nat. Med., 10, 484, 10.1038/nm1042
Furic, 2010, eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression, Proc. Natl. Acad. Sci. U. S. A., 107, 14134, 10.1073/pnas.1005320107
Truitt, 2015, Differential requirements for eIF4E dose in normal development and cancer, Cell, 162, 59, 10.1016/j.cell.2015.05.049
Holcik, 2000, Functional characterization of the X-linked inhibitor of apoptosis (XIAP) internal ribosome entry site element: role of La autoantigen in XIAP translation, Mol. Cell Biol., 20, 4648, 10.1128/MCB.20.13.4648-4657.2000
Petz, 2012, La enhances IRES-mediated translation of laminin B1 during malignant epithelial to mesenchymal transition, Nucleic Acids Res., 40, 290, 10.1093/nar/gkr717
Miles, 2012, Pumilio facilitates miRNA regulation of the E2F3 oncogene, Genes Dev., 26, 356, 10.1101/gad.182568.111
Miles, 2016, Alternative polyadenylation in triple-negative breast tumors allows NRAS and c-JUN to bypass PUMILIO posttranscriptional regulation, Cancer Res., 76, 7231, 10.1158/0008-5472.CAN-16-0844
Lee, 2016, Noncoding RNA NORAD regulates genomic stability by sequestering PUMILIO proteins, Cell, 164, 69, 10.1016/j.cell.2015.12.017
Tichon, 2016, A conserved abundant cytoplasmic long noncoding RNA modulates repression by Pumilio proteins in human cells, Nat. Commun., 7, 12209, 10.1038/ncomms12209
Beachy, 2012, Enforced expression of Lin28b leads to impaired T-cell development, release of inflammatory cytokines, and peripheral T-cell lymphoma, Blood, 120, 1048, 10.1182/blood-2012-01-401760
Molenaar, 2012, LIN28 B induces neuroblastoma and enhances MYCN levels via let-7 suppression, Nat. Genet., 44, 1199, 10.1038/ng.2436
Madison, 2013, LIN28B promotes growth and tumorigenesis of the intestinal epithelium via Let-7, Genes Dev., 27, 10.1101/gad.224659.113
Nguyen, 2014, Lin28b is sufficient to drive liver cancer and necessary for its maintenance in murine models, Cancer Cell, 26, 248, 10.1016/j.ccr.2014.06.018
Viswanathan, 2009, Lin28 promotes transformation and is associated with advanced human malignancies, Nat. Genet., 41, 843, 10.1038/ng.392
Piskounova, 2011, Lin28A and Lin28 B inhibit let-7 microRNA biogenesis by distinct mechanisms, Cell, 147, 1066, 10.1016/j.cell.2011.10.039
Yang, 2011, Double-negative feedback loop between reprogramming factor LIN28 and microRNA let-7 regulates aldehyde dehydrogenase 1-positive cancer stem cells, Cancer Res., 70, 9463, 10.1158/0008-5472.CAN-10-2388
Ma, 2014, Lin28/let-7 axis regulates aerobic glycolysis and cancer progression via PDK1, Nat. Commun., 5, 5212, 10.1038/ncomms6212
Tu, 2015, LIN28 cooperates with WNT signaling to drive invasive intestinal and colorectal adenocarcinoma in mice and humans, Genes Dev., 29, 1074, 10.1101/gad.256693.114
Matter, 2002, Signal-dependent regulation of splicing via phosphorylation of Sam68, Nature, 420, 691, 10.1038/nature01153
Paronetto, 2010, Alternative splicing of the cyclin D1 proto-oncogene is regulated by the RNA-binding protein Sam68, Cancer Res., 70, 229, 10.1158/0008-5472.CAN-09-2788
Song, 2010, Sam68 up-regulation correlates with, and its down-regulation inhibits, proliferation and tumourigenicity of breast cancer cells, J. Pathol., 222, 227, 10.1002/path.2751
Richard, 2008, Sam68 haploinsufficiency delays onset of mammary tumorigenesis and metastasis, Oncogene, 27, 548, 10.1038/sj.onc.1210652
Paronetto, 2007, The RNA-binding protein Sam68 modulates the alternative splicing of Bcl-x, J. Cell Biol., 176, 929, 10.1083/jcb.200701005
Mulholland, 2006, Genomic profiling identifies discrete deletions associated with translocations in glioblastoma multiforme, Cell Cycle, 5, 783, 10.4161/cc.5.7.2631
Chen, 2012, STAR RNA-binding protein Quaking suppresses cancer via stabilization of specific miRNA, Genes Dev., 26, 1459, 10.1101/gad.189001.112
Yang, 2011, E2F1 and RNA binding protein QKI comprise a negative feedback in the cell cycle regulation, Cell Cycle, 10, 2703, 10.4161/cc.10.16.15928
Ji, 2013, miR-574-5p negatively regulates Qki6/7 to impact β-catenin/Wnt signalling and the development of colorectal cancer, Gut, 62, 716, 10.1136/gutjnl-2011-301083
Tessier, 2004, Mammary tumor induction in transgenic mice expressing an RNA-binding protein, Cancer Res., 64, 209, 10.1158/0008-5472.CAN-03-2927
Vikesaa, 2006, RNA-binding IMPs promote cell adhesion and invadopodia formation, EMBO J., 25, 1456, 10.1038/sj.emboj.7601039
Mongroo, 2011, IMP-1 displays cross-talk with K-Ras and modulates colon cancer cell survival through the novel proapoptotic protein CYFIP2, Cancer Res., 71, 2172, 10.1158/0008-5472.CAN-10-3295
Kato, 2007, Increased expression of insulin-like growth factor-II messenger RNA-binding protein 1 is associated with tumor progression in patients with lung cancer, Clin. Cancer Res., 13, 434, 10.1158/1078-0432.CCR-06-1297
Hamilton, 2013, IMP1 promotes tumor growth, dissemination and a tumor-initiating cell phenotype in colorectal cancer cell xenografts, Carcinogenesis, 34, 2647, 10.1093/carcin/bgt217
Degrauwe, 2016, The RNA binding protein IMP2 preserves glioblastoma stem cells by preventing let-7 target gene silencing, Cell Rep., 15, 1634, 10.1016/j.celrep.2016.04.086
Jønson, 2014, IMP3 RNP safe houses prevent miRNA-directed HMGA2 mRNA decay in cancer and development, Cell Rep., 7, 539, 10.1016/j.celrep.2014.03.015
Rivera Vargas, 2014, Post-transcriptional regulation of cyclins D1, D3 and G1 and proliferation of human cancer cells depend on IMP-3 nuclear localization, Oncogene, 33, 2866, 10.1038/onc.2013.252
Hsu, 2015, Overexpression of the RNA-binding proteins Lin28 B and IGF2BP3 (IMP3) is associated with chemoresistance and poor disease outcome in ovarian cancer, Br. J. Cancer, 113, 414, 10.1038/bjc.2015.254
Palanichamy, 2016, RNA-binding protein IGF2BP3 targeting of oncogenic transcripts promotes hematopoietic progenitor proliferation, J. Clin. Invest., 126, 1495, 10.1172/JCI80046
Nabors, 2001, HuR, a RNA stability factor, is expressed in malignant brain tumors and binds to adenine- and uridine-rich elements within the 3′ untranslated regions of cytokine and angiogenic factor mRNAs, Cancer Res., 61, 2154
López de Silanes, 2003, Role of the RNA-binding protein HuR in colon carcinogenesis, Oncogene, 22, 7146, 10.1038/sj.onc.1206862
Dong, 2007, Stabilization of Snail by HuR in the process of hydrogen peroxide induced cell migration, Biochem. Biophys. Res. Commun., 356, 318, 10.1016/j.bbrc.2007.02.145
Mazan-Mamczarz, 2003, RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation, Proc. Natl. Acad. Sci. U. S. A., 100, 8354, 10.1073/pnas.1432104100
Lal, 2005, Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha, EMBO J., 24, 1852, 10.1038/sj.emboj.7600661
Abdelmohsen, 2007, Posttranscriptional orchestration of an anti-apoptotic program by HuR, Cell Cycle, 6, 1288, 10.4161/cc.6.11.4299
Abdelmohsen, 2007, Phosphorylation of HuR by Chk2 regulates SIRT1 expression, Mol. Cell, 25, 543, 10.1016/j.molcel.2007.01.011
Kim, 2009, HuR recruits let-7/RISC to repress c-Myc expression, Genes Dev., 23, 1743, 10.1101/gad.1812509
Durie, 2011, RNA-binding protein HuR mediates cytoprotection through stimulation of XIAP translation, Oncogene, 30, 1460, 10.1038/onc.2010.527
Ghosh, 2009, Essential role of the RNA-binding protein HuR in progenitor cell survival in mice, J. Clin. Invest., 119, 3530, 10.1172/JCI38263
Abdelmohsen, 2010, Posttranscriptional regulation of cancer traits by HuR, Wiley Interdiscip. Rev. RNA, 1, 214, 10.1002/wrna.4
Podszywalow-Bartnicka, 2014, Downregulation of BRCA1 protein in BCR-ABL1 leukemia cells depends on stress-triggered TIAR-mediated suppression of translation, Cell Cycle, 13, 3727, 10.4161/15384101.2014.965013
Förch, 2000, The apoptosis-promoting factor TIA-1 is a regulator of alternative pre-mRNA splicing, Mol. Cell, 6, 1089, 10.1016/S1097-2765(00)00107-6
Izquierdo, 2005, Regulation of Fas alternative splicing by antagonistic effects of TIA-1 and PTB on exon definition, Mol. Cell, 19, 475, 10.1016/j.molcel.2005.06.015
Yu, 2003, Translational repression of human matrix metalloproteinases-13 by an alternatively spliced form of T-cell-restricted intracellular antigen-related protein (TIAR), J. Biol. Chem., 278, 1579, 10.1074/jbc.M203526200
Mazan-Mamczarz, 2006, Translational repression by RNA-binding protein TIAR, Mol. Cell Biol., 26, 2716, 10.1128/MCB.26.7.2716-2727.2006
Izquierdo, 2011, Knockdown of T-cell intracellular antigens triggers cell proliferation, invasion and tumour growth, Biochem. J., 435, 337, 10.1042/BJ20101030
Lal, 2006, Posttranscriptional derepression of GADD45alpha by genotoxic stress, Mol. Cell, 22, 117, 10.1016/j.molcel.2006.03.016
Wigington, 2015, Post-transcriptional regulation of programmed cell death 4 (PDCD4) mRNA by the RNA-binding proteins human antigen R (HuR) and T-cell intracellular antigen 1 (TIA1), J. Biol. Chem., 290, 3468, 10.1074/jbc.M114.631937
Trotta, 2003, BCR/ABL activates mdm2 mRNA translation via the La antigen, Cancer Cell, 3, 145, 10.1016/S1535-6108(03)00020-5
Sommer, 2011, The RNA-binding protein La contributes to cell proliferation and CCND1 expression, Oncogene, 30, 434, 10.1038/onc.2010.425
Heise, 2016, The La protein counteracts cisplatin-induced cell death by stimulating protein synthesis of anti-apoptotic factor Bcl2, Oncotarget, 7, 29664, 10.18632/oncotarget.8819
Burrows, 2010, The RNA binding protein Larp1 regulates cell division, apoptosis and cell migration, Nucleic Acids Res., 38, 5542, 10.1093/nar/gkq294
Tcherkezian, 2014, Proteomic analysis of cap-dependent translation identifies LARP1 as a key regulator of 5′TOP mRNA translation, Genes Dev., 28, 357, 10.1101/gad.231407.113
Mura, 2015, LARP1 post-transcriptionally regulates mTOR and contributes to cancer progression, Oncogene, 34, 5025, 10.1038/onc.2014.428
Kato, 2015, MicroRNA-26a/b directly regulate La-related protein 1 and inhibit cancer cell invasion in prostate cancer, Int. J. Oncol., 47, 710, 10.3892/ijo.2015.3043
Shao, 2012, The novel lupus antigen related protein acheron enhances the development of human breast cancer, Int. J. Cancer, 130, 544, 10.1002/ijc.26015
Koso, 2016, Identification of RNA-binding protein LARP4 B as a tumor suppressor in glioma, Cancer Res., 76, 2254, 10.1158/0008-5472.CAN-15-2308
Seetharaman, 2016, The RNA-binding protein LARP4 regulates cancer cell migration and invasion, Cytoskeleton, 73, 680, 10.1002/cm.21336
He, 2008, A La-related protein modulates 7SK snRNP integrity to suppress P-TEFb-dependent transcriptional elongation and tumorigenesis, Mol. Cell, 29, 588, 10.1016/j.molcel.2008.01.003
Cheng, 2012, LARP7 is a potential tumor suppressor gene in gastric cancer, Lab. Invest., 92, 1013, 10.1038/labinvest.2012.59
Ji, 2014, LARP7 suppresses P-TEFb activity to inhibit breast cancer progression and metastasis, Elife, 3, e02907, 10.7554/eLife.02907
Leontieva, 2009, RNA-binding motif protein 35A is a novel tumor suppressor for colorectal cancer, Cell Cycle, 8, 490, 10.4161/cc.8.3.7679
Warzecha, 2009, ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing, Mol. Cell, 33, 591, 10.1016/j.molcel.2009.01.025
Warzecha, 2010, An ESRP-regulated splicing programme is abrogated during the epithelial–mesenchymal transition, EMBO J., 29, 3286, 10.1038/emboj.2010.195
Shapiro, 2011, An EMT-driven alternative splicing program occurs in human breast cancer and modulates cellular phenotype, PLoS Genet., 7, e1002218, 10.1371/journal.pgen.1002218
Zhao, 2013, Tumor-specific isoform switch of the fibroblast growth factor receptor 2 underlies the mesenchymal and malignant phenotypes of clear cell renal cell carcinomas, Clin. Cancer Res., 19, 2460, 10.1158/1078-0432.CCR-12-3708
Lu, 2013, Exo70 isoform switching upon epithelial–mesenchymal transition mediates cancer cell invasion, Dev. Cell, 27, 560, 10.1016/j.devcel.2013.10.020
Ueda, 2014, Epithelial splicing regulatory protein 1 is a favorable prognostic factor in pancreatic cancer that attenuates pancreatic metastases, Oncogene, 33, 4485, 10.1038/onc.2013.392
Deloria, 2016, Epithelial splicing regulatory protein 1 and 2 paralogues correlate with splice signatures and favorable outcome in human colorectal cancer, Oncotarget, 7, 73800, 10.18632/oncotarget.12070
Yae, 2012, Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell, Nat. Commun., 3, 883, 10.1038/ncomms1892
Yao, 2016, Altered expression and splicing of ESRP1 in malignant melanoma correlates with epithelial-mesenchymal status and tumor-associated immune cytolytic activity, Cancer Immunol. Res., 4, 552, 10.1158/2326-6066.CIR-15-0255
Fagoonee, 2017, The RNA-binding protein ESRP1 promotes human colorectal cancer progression, Oncotarget, 8, 10007, 10.18632/oncotarget.14318
Malz, 2009, Overexpression of far upstream element binding proteins: a mechanism regulating proliferation and migration in liver cancer cells, Hepatology, 50, 1130, 10.1002/hep.23051
Trabucchi, 2009, The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs, Nature, 459, 1010, 10.1038/nature08025
Zhang, 2011, The ATM kinase induces microRNA biogenesis in the DNA damage response, Mol. Cell, 371, 10.1016/j.molcel.2011.01.020
Yang, 2013, Genome-wide RNAi screening identifies genes inhibiting the migration of glioblastoma cells, PLoS One, 8, e61915, 10.1371/journal.pone.0061915
Puppo, 2016, miRNA-mediated KHSRP silencing rewires distinct post-transcriptional programs during TGF-β-induced epithelial-to-mesenchymal transition, Cell Rep., 16, 967, 10.1016/j.celrep.2016.06.055
Evans, 2003, Members of the poly (rC) binding protein family stimulate the activity of the c-myc internal ribosome entry segment in vitro and in vivo, Oncogene, 22, 8012, 10.1038/sj.onc.1206645
Dormoy-Raclet, 2007, Unr, a cytoplasmic RNA-binding protein with cold-shock domains, is involved in control of apoptosis in ES and HuH7 cells, Oncogene, 26, 2595, 10.1038/sj.onc.1210068
Yu, 2007, Induced pluripotent stem cell lines derived from human somatic cells, Science, 318, 1917, 10.1126/science.1151526
Ito, 2010, Regulation of myeloid leukaemia by the cell-fate determinant Musashi, Nature, 466, 765, 10.1038/nature09171
Kharas, 2010, Musashi-2 regulates normal hematopoiesis and promotes aggressive myeloid leukemia, Nat. Med., 2010, 903, 10.1038/nm.2187
Park, 2015, Musashi2 sustains the mixed-lineage leukemia-driven stem cell regulatory program, J. Clin. Invest., 125, 1286, 10.1172/JCI78440
Katz, 2014, Musashi proteins are post-transcriptional regulators of the epithelial-luminal cell state, Elife, 3, e03915, 10.7554/eLife.03915
Vo, 2012, The RNA-binding protein Musashi1 affects medulloblastoma growth via a network of cancer-related genes and is an indicator of poor prognosis, Am. J. Pathol., 181, 1762, 10.1016/j.ajpath.2012.07.031
Rezza, 2010, The overexpression of the putative gut stem cell marker Musashi-1 induces tumorigenesis through Wnt and Notch activation, J. Cell Sci., 123, 3256, 10.1242/jcs.065284
Li, 2015, The Msi family of RNA-binding proteins function redundantly as intestinal oncoproteins, Cell Rep., 13, 2440, 10.1016/j.celrep.2015.11.022
Wang, 2015, Transformation of the intestinal epithelium by the MSI2 RNA-binding protein, Nat. Commun., 6, 6517, 10.1038/ncomms7517
Ciosk, 2006, Translational regulators maintain totipotency in the Caenorhabditis elegans germline, Science, 311, 851, 10.1126/science.1122491
Buchet-Poyau, 2007, Identification and characterization of human Mex-3 proteins, a novel family of evolutionarily conserved RNA-binding proteins differentially localized to processing bodies, Nucleic Acids Res., 35, 1289, 10.1093/nar/gkm016
Burrell, 2013, Replication stress links structural and numerical cancer chromosomal instability, Nature, 494, 492, 10.1038/nature11935
Pereira, 2013, CDX2 regulation by the RNA-binding protein MEX3A: impact on intestinal differentiation and stemness, Nucleic Acids Res., 41, 3986, 10.1093/nar/gkt087
Barriga, 2017, Mex3a marks a slowly dividing subpopulation of Lgr5+ intestinal stem cells, Cell Stem Cell, 20, 10.1016/j.stem.2017.02.007
Castello, 2012, Insights into RNA biology from an atlas of mammalian mRNA-binding proteins, Cell, 149, 1393, 10.1016/j.cell.2012.04.031
Kafasla, 2014, Post-transcriptional coordination of immunological responses by RNA-binding proteins, Nat. Immunol., 15, 492, 10.1038/ni.2884
Kratochvill, 2015, Tristetraprolin limits inflammatory cytokine production in tumor-associated macrophages in an mRNA decay-independent manner, Cancer Res., 75, 3054, 10.1158/0008-5472.CAN-15-0205
Duewell, 2014, RIG-I-like helicases induce immunogenic cell death of pancreatic cancer cells and sensitize tumors toward killing by CD8+ T cells, Cell Death Differ., 21, 1825, 10.1038/cdd.2014.96
Wang, 2015, Design and bioinformatics analysis of genome-wide CLIP experiments, Nucleic Acids Res., 43, 5263, 10.1093/nar/gkv439
Sundararaman, 2016, Resources for the comprehensive discovery of functional RNA elements, Mol. Cell, 61, 903, 10.1016/j.molcel.2016.02.012
Blackinton, 2014, Post-transcriptional RNA regulons affecting cell cycle and proliferation, Semin. Cell Dev. Biol., 34, 44, 10.1016/j.semcdb.2014.05.014
Wu, 2015, Identification and validation of novel small molecule disruptors of HuR–mRNA interaction, ACS Chem. Biol., 10, 1476, 10.1021/cb500851u
Huang, 2016, Delivery of therapeutics targeting the mRNA-binding protein HuR using 3DNA nanocarriers suppresses ovarian tumor growth, Cancer Res., 76, 1549, 10.1158/0008-5472.CAN-15-2073
Roos, 2016, A small-molecule inhibitor of Lin28, ACS Chem. Biol., 11, 2773, 10.1021/acschembio.6b00232
Wang, 2009, Engineering splicing factors with designed specificities, Nat. Methods, 6, 825, 10.1038/nmeth.1379
Peritz, 2006, Immunoprecipitation of mRNA–protein complexes, Nat. Protoc., 1, 577, 10.1038/nprot.2006.82
Ule, 2005, CLIP: a method for identifying protein–RNA interaction sites in living cells, Methods, 37, 376, 10.1016/j.ymeth.2005.07.018
Licatalosi, 2008, HITS-CLIP yields genome-wide insights into brain alternative RNA processing, Nature, 456, 464, 10.1038/nature07488
Hafner, 2010, Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP, Cell, 141, 129, 10.1016/j.cell.2010.03.009
Jungkamp, 2011, In vivo and transcriptome-wide identification of RNA binding protein target sites, Mol. Cell, 44, 828, 10.1016/j.molcel.2011.11.009
König, 2010, iCLIP reveals the function of hnRNP particles in splicing at individual nucleotide resolution, Nat. Struct. Mol. Biol., 17, 909, 10.1038/nsmb.1838
Van Nostrand, 2016, Robust transcriptome-wide discovery of RNA-binding protein binding sites with enhanced CLIP (eCLIP), Nat. Methods, 13, 508, 10.1038/nmeth.3810
Zarnegar, 2016, irCLIP platform for efficient characterization of protein-RNA interactions, Nat. Methods, 13, 489, 10.1038/nmeth.3840
McMahon, 2016, TRIBE: hijacking an RNA-editing enzyme to identify cell-specific targets of RNA-binding proteins, Cell, 165, 742, 10.1016/j.cell.2016.03.007
Nagaoka, 2012, CPEB-mediated ZO-1 mRNA localization is required for epithelial tight-junction assembly and cell polarity, Nat. Commun., 3, 675, 10.1038/ncomms1678
Nagaoka, 2016, CPEB1 mediates epithelial-to-mesenchyme transition and breast cancer metastasis, Oncogene, 35, 2893, 10.1038/onc.2015.350
Wang, 2014, The splicing factor RBM4 controls apoptosis, proliferation, and migration to suppress tumor progression, Cancer Cell, 26, 374, 10.1016/j.ccr.2014.07.010
Qi, 2016, A splicing isoform of TEAD4 attenuates the Hippo–YAP signalling to inhibit tumour proliferation, Nat. Commun., 7, 10.1038/ncomms11840
Vanharanta, 2014, Loss of the multifunctional RNA-binding protein RBM47 as a source of selectable metastatic traits in breast cancer, Elife, 3, 02734, 10.7554/eLife.02734