UNR/CSDE1 Drives a Post-transcriptional Program to Promote Melanoma Invasion and Metastasis

Cancer Cell - Tập 30 - Trang 694-707 - 2016
Laurence Wurth1,2, Panagiotis Papasaikas1,2, David Olmeda3, Nadine Bley4, Guadalupe T. Calvo3, Santiago Guerrero1,2, Daniela Cerezo-Wallis3, Javier Martinez-Useros5, María García-Fernández3, Stefan Hüttelmaier4, Maria S. Soengas3, Fátima Gebauer1,2
1Gene Regulation, Stem Cells and Cancer Programme, Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, 08003 Barcelona, Spain
2Universitat Pompeu Fabra (UPF), 08003 Barcelona, Spain
3Molecular Oncology Programme, Spanish National Cancer Research Centre (CNIO), 28029 Madrid, Spain
4Section Molecular Cell Biology, Institute of Molecular Medicine (IMM), Martin-Luther-University (MLU), 06120 Halle, Germany
5Translational Oncology Division, Oncohealth Institute - Health Research Institute - University Hospital “Fundacion Jimenez Diaz”, 28040 Madrid, Spain

Tài liệu tham khảo

Abaza, 2006, Drosophila UNR is required for translational repression of male-specific lethal 2 mRNA during regulation of X-chromosome dosage compensation, Genes Dev., 20, 380, 10.1101/gad.371906 Athanasiadis, 2014, A Web-based database of genetic association studies in cutaneous melanoma enhanced with network-driven data exploration tools, Database (Oxford), 2014, 10.1093/database/bau101 Ayala, 2008, Multiple regulatory inputs converge on cortactin to control invadopodia biogenesis and extracellular matrix degradation, J. Cell Sci., 121, 369, 10.1242/jcs.008037 Bailey, 2011, DREME: motif discovery in transcription factor ChIP-seq data, Bioinformatics, 27, 1653, 10.1093/bioinformatics/btr261 Bathia, 2016, PD-1 blockade in melanoma: a promising start, but a long way to go, JAMA, 315, 1573, 10.1001/jama.2016.4012 Bid, 2013, RAC1: an emerging therapeutic option for targeting cancer angiogenesis and metastasis, Mol. Cancer Ther., 12, 1925, 10.1158/1535-7163.MCT-13-0164 Castello, 2013, RNA-binding proteins in Mendelian disease, Trends Genet., 29, 318, 10.1016/j.tig.2013.01.004 Cerami, 2011, Pathway Commons, a web resource for biological pathway data, Nucleic Acids Res., 39, D685, 10.1093/nar/gkq1039 Chang, 2004, UNR, a new partner of poly(A)-binding protein, plays a key role in translationally coupled mRNA turnover mediated by the c-fos major coding-region determinant, Genes Dev., 18, 2010, 10.1101/gad.1219104 Darnell, 2010, RNA regulation in neurologic disease and cancer, Cancer Res. Treat., 42, 125, 10.4143/crt.2010.42.3.125 Darnell, 2011, FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism, Cell, 146, 247, 10.1016/j.cell.2011.06.013 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 Duncan, 2006, Sex-lethal imparts a sex-specific function to UNR by recruiting it to the msl-2 mRNA 3' UTR: translational repression for dosage compensation, Genes Dev., 20, 368, 10.1101/gad.371406 Dutton-Regester, 2012, Reviewing the somatic genetics of melanoma: from current to future analytical approaches, Pigment Cell Melanoma Res., 25, 144, 10.1111/j.1755-148X.2012.00975.x Elatmani, 2011, The RNA-binding protein Unr prevents mouse embryonic stem cells differentiation toward the primitive endoderm lineage, Stem Cells, 29, 1504, 10.1002/stem.712 Elfenbein, 2013, Syndecan-4 signaling at a glance, J. Cell Sci., 126, 3799 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 Feng, 2014, Hippo-independent activation of YAP by the GNAQ uveal melanoma oncogene through a trio-regulated rho GTPase signaling circuitry, Cancer Cell, 25, 831, 10.1016/j.ccr.2014.04.016 Flaherty, 2012, From genes to drugs: targeted strategies for melanoma, Nat. Rev. Cancer, 12, 349, 10.1038/nrc3218 Friend, 2012, A conserved PUF-Ago-eEF1A complex attenuates translation elongation, Nat. Struct. Mol. Biol., 19, 176, 10.1038/nsmb.2214 Futreal, 2004, A census of human cancer genes, Nat. Rev. Cancer, 4, 177, 10.1038/nrc1299 Goroncy, 2010, The NMR solution structures of the five constituent cold-shock domains (CSD) of the human UNR (upstream of N-ras) protein, J. Struct. Funct. Genomics, 11, 181, 10.1007/s10969-010-9081-z Hennig, 2014, Structural basis for the assembly of the Sxl-Unr translation regulatory complex, Nature, 515, 287, 10.1038/nature13693 Hettinger, 2007, c-Jun promotes cellular survival by suppression of PTEN, Cell Death Differ, 14, 218, 10.1038/sj.cdd.4401946 Horos, 2012, Ribosomal deficiencies in Diamond-Blackfan anemia impair translation of transcripts essential for differentiation of murine and human erythroblasts, Blood, 119, 262, 10.1182/blood-2011-06-358200 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 Ingolia, 2009, Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling, Science, 324, 218, 10.1126/science.1168978 Ingolia, 2012, The ribosome profiling strategy for monitoring translation in vivo by deep sequencing of ribosome-protected mRNA fragments, Nature Protocols, 7, 1534, 10.1038/nprot.2012.086 Kanehisa, 2000, KEGG: Kyoto Encyclopedia of Genes and Genomes, Nucleic Acids Res., 28, 27, 10.1093/nar/28.1.27 Kanehisa, 2014, Data, information, knowledge and principle: back to metabolism in KEGG, Nucleic Acids Res., 42, D199, 10.1093/nar/gkt1076 Kappelmann, 2014, AP-1/c-Jun transcription factors: regulation and function in malignant melanoma, Eur. J. Cell Biol., 93, 76, 10.1016/j.ejcb.2013.10.003 Konig, 2011, iCLIP—transcriptome-wide mapping of protein-RNA interactions with individual nucleotide resolution, J. Vis. Exp., 10.3791/2638 Krauthammer, 2012, Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma, Nat. Genet., 44, 1006, 10.1038/ng.2359 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 Liu, 2013, Cotranslational response to proteotoxic stress by elongation pausing of ribosomes, Mol. Cell, 49, 453, 10.1016/j.molcel.2012.12.001 Mihailovic, 2012, Widespread generation of alternative UTRs contributes to sex-specific RNA binding by UNR, RNA, 18, 53, 10.1261/rna.029603.111 Mihailovich, 2010, Eukaryotic cold shock domain proteins: highly versatile regulators of gene expression, Bioessays, 32, 109, 10.1002/bies.200900122 Militti, 2014, UNR facilitates the interaction of MLE with the lncRNA roX2 during Drosophila dosage compensation, Nat. Commun., 5, 4762, 10.1038/ncomms5762 Mitchell, 2003, The Apaf-1 internal ribosome entry segment attains the correct structural conformation for function via interactions with PTB and unr, Mol. Cell, 11, 757, 10.1016/S1097-2765(03)00093-5 Morris, 2010, Systematic analysis of posttranscriptional gene expression, Wiley Interdiscip. Rev. Syst. Biol. Med., 2, 162, 10.1002/wsbm.54 Novak, 2015, Metastasis suppressor NME1 regulates melanoma cell morphology, self-adhesion and motility via induction of fibronectin expression, Exp. Dermatol., 24, 455, 10.1111/exd.12697 Patel, 2005, The autoregulatory translational control element of poly(A)-binding protein mRNA forms a heteromeric ribonucleoprotein complex, Nucleic Acids Res., 33, 7074, 10.1093/nar/gki1014 Qian, 2011, CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis, Nature, 475, 222, 10.1038/nature10138 Ridgway, 2010, Modulation of GEF-H1 induced signaling by heparanase in brain metastatic melanoma cells, J. Cell Biochem., 111, 1299, 10.1002/jcb.22854 Satelli, 2011, Vimentin in cancer and its potential as a molecular target for cancer therapy, Cell Mol. Life Sci., 68, 3033, 10.1007/s00018-011-0735-1 Schadendorf, 2015, Melanoma, Nat. Rev. Dis. Primers, 1, 15003, 10.1038/nrdp.2015.3 Schepens, 2007, A role for hnRNP C1/C2 and Unr in internal initiation of translation during mitosis, EMBO J., 26, 158, 10.1038/sj.emboj.7601468 Shalgi, 2013, Widespread regulation of translation by elongation pausing in heat shock, Mol. Cell, 49, 439, 10.1016/j.molcel.2012.11.028 Shannon, 2003, Cytoscape: a software environment for integrated models of biomolecular interaction networks, Genome Res., 13, 2498, 10.1101/gr.1239303 Shao, 2015, Tenascin-C signaling in melanoma, Cell Adh. Migr., 9, 125, 10.4161/19336918.2014.972781 Sonenberg, 2009, Regulation of translation initiation in eukaryotes: mechanisms and biological targets, Cell, 136, 731, 10.1016/j.cell.2009.01.042 Thompson, 2004, The history and future of melanoma staging, J. Surg. Oncol., 86, 224, 10.1002/jso.20082 Tinton, 2005, Regulation of the cell-cycle-dependent internal ribosome entry site of the PITSLRE protein kinase: roles of Unr (upstream of N-ras) protein and phosphorylated translation initiation factor eIF-2alpha, Biochem. J., 385, 155, 10.1042/BJ20040963 Trapnell, 2013, Differential analysis of gene regulation at transcript resolution with RNA-seq, Nat Biotechnol., 31, 46, 10.1038/nbt.2450 Triqueneaux, 1999, RNA binding specificity of Unr, a protein with five cold shock domains, Nucleic Acids Res., 27, 1926, 10.1093/nar/27.8.1926 Vaqué, 2013, A genome-wide RNAi screen reveals a Trio-regulated Rho GTPase circuitry transducing mitogenic signals initiated by G protein-coupled receptors, Mol. Cell, 49, 94, 10.1016/j.molcel.2012.10.018 Wan, 2014, Landscape and variation of RNA secondary structure across the human transcriptome, Nature, 505, 706, 10.1038/nature12946 Wolter, 2008, c-Jun controls histone modifications, NF-kappaB recruitment, and RNA polymerase II function to activate the ccl2 gene, Mol. Cell Biol., 28, 4407, 10.1128/MCB.00535-07 Wurth, 2015, RNA-binding proteins, multifaceted translational regulators in cancer, Biochim. Biophys. Acta, 1849, 881, 10.1016/j.bbagrm.2014.10.001