An Integrated Genome-wide CRISPRa Approach to Functionalize lncRNAs in Drug Resistance

Cell - Tập 173 - Trang 649-664.e20 - 2018
Assaf C. Bester1,2, Jonathan D. Lee1,2, Alejandro Chavez3,4,5, Yu-Ru Lee1,2, Daphna Nachmani1,2, Suhani Vora3, Joshua Victor1,2, Martin Sauvageau6,7,8, Emanuele Monteleone9, John L. Rinn6, Paolo Provero9,10, George M. Church3, John G. Clohessy1,2,11, Pier Paolo Pandolfi1,2
1Cancer Research Institute, Beth Israel Deaconess Cancer Center, Department of Medicine and Pathology, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA
2Ludwig Center at Harvard, Harvard Medical School, Boston, MA, USA
3Wyss Institute for Biologically Inspired Engineering, Harvard University, Cambridge, MA, USA
4Department of Pathology and Cell Biology, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA
5Taub Institute for Research on Alzheimer’s Disease and the Aging Brain, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA
6Department of Stem Cell and Regenerative Biology, Harvard University, The Broad Institute of MIT and Harvard, Cambridge, MA, USA
7Functional Genomics and Noncoding RNAs Research Unit, Institut de Recherches Cliniques de Montréal (IRCM), Montréal, QC, Canada
8Department of Biochemistry and Molecular Medicine, Université de Montréal, Montréal, QC, Canada
9Department of Molecular Biotechnology and Health Sciences, and GenoBiToUS, Genomics and Bioinformatics Service, University of Turin, Turin, Italy
10Center for Translational Genomics and Bioinformatics, San Raffaele Scientific Institute IRCCS, Milan, Italy
11Preclinical Murine Pharmacogenetics Facility and Mouse Hospital, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, MA, USA

Tài liệu tham khảo

Abraham, 2015, RNA expression of genes involved in cytarabine metabolism and transport predicts cytarabine response in acute myeloid leukemia, Pharmacogenomics, 16, 877, 10.2217/pgs.15.44 Aken, 2016, The Ensembl gene annotation system, Database (Oxford), 2016, baw093, 10.1093/database/baw093 Barretina, 2012, The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity, Nature, 483, 603, 10.1038/nature11003 Basu, 2013, An interactive resource to identify cancer genetic and lineage dependencies targeted by small molecules, Cell, 154, 1151, 10.1016/j.cell.2013.08.003 Cabili, 2011, Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses, Genes Dev., 25, 1915, 10.1101/gad.17446611 Chavez, 2015, Highly efficient Cas9-mediated transcriptional programming, Nat. Methods, 12, 326, 10.1038/nmeth.3312 Chavez, 2016, Comparison of Cas9 activators in multiple species, Nat. Methods, 13, 563, 10.1038/nmeth.3871 Chen, 2007, Improved human disease candidate gene prioritization using mouse phenotype, BMC Bioinformatics, 8, 392, 10.1186/1471-2105-8-392 Cheng, 2013, Inhibition of BET bromodomain targets genetically diverse glioblastoma, Clin. Cancer Res., 19, 1748, 10.1158/1078-0432.CCR-12-3066 Colaprico, 2016, TCGAbiolinks: an R/Bioconductor package for integrative analysis of TCGA data, Nucleic Acids Res., 44, e71, 10.1093/nar/gkv1507 Di Ruscio, 2013, DNMT1-interacting RNAs block gene-specific DNA methylation, Nature, 503, 371, 10.1038/nature12598 Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15, 10.1093/bioinformatics/bts635 Durinck, 2005, BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis, Bioinformatics, 21, 3439, 10.1093/bioinformatics/bti525 Farge, 2017, Chemotherapy-resistant human acute myeloid leukemia cells are not enriched for leukemic stem cells but require oxidative metabolism, Cancer Discov., 7, 716, 10.1158/2159-8290.CD-16-0441 Garnett, 2012, Systematic identification of genomic markers of drug sensitivity in cancer cells, Nature, 483, 570, 10.1038/nature11005 Garzon, 2014, Expression and prognostic impact of lncRNAs in acute myeloid leukemia, Proc. Natl. Acad. Sci. USA, 111, 18679, 10.1073/pnas.1422050112 Gilbert, 2014, Genome-scale CRISPR-mediated control of gene repression and activation, Cell, 159, 647, 10.1016/j.cell.2014.09.029 Herold, 2017, Targeting SAMHD1 with the Vpx protein to improve cytarabine therapy for hematological malignancies, Nat. Med., 23, 256, 10.1038/nm.4265 Hon, 2017, An atlas of human long non-coding RNAs with accurate 5‘ ends, Nature, 543, 199, 10.1038/nature21374 Hong, 2008, Receptor tyrosine kinase AXL is induced by chemotherapy drugs and overexpression of AXL confers drug resistance in acute myeloid leukemia, Cancer Lett., 268, 314, 10.1016/j.canlet.2008.04.017 Hu, 2014, A functional genomic approach identifies FAL1 as an oncogenic long noncoding RNA that associates with BMI1 and represses p21 expression in cancer, Cancer Cell, 26, 344, 10.1016/j.ccr.2014.07.009 Huarte, 2015, The emerging role of lncRNAs in cancer, Nat. Med., 21, 1253, 10.1038/nm.3981 Imielinski, 2012, Mapping the hallmarks of lung adenocarcinoma with massively parallel sequencing, Cell, 150, 1107, 10.1016/j.cell.2012.08.029 Iyer, 2015, The landscape of long noncoding RNAs in the human transcriptome, Nat. Genet., 47, 199, 10.1038/ng.3192 Joung, 2017, Genome-scale activation screen identifies a lncRNA locus regulating a gene neighbourhood, Nature, 548, 343, 10.1038/nature23451 Joung, 2017, Genome-scale CRISPR-Cas9 knockout and transcriptional activation screening, Nat. Protoc., 12, 828, 10.1038/nprot.2017.016 Kaimal, 2010, ToppCluster: a multiple gene list feature analyzer for comparative enrichment clustering and network-based dissection of biological systems, Nucleic Acids Res., 38, 10.1093/nar/gkq418 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 Kassambara, A., and Kosinski, M. (2017). Survminer: drawing survival curves using ’Ggplot2’. https://CRAN.R-project.org/package=survminer. Konermann, 2015, Genome-scale transcriptional activation by an engineered CRISPR-Cas9 complex, Nature, 517, 583, 10.1038/nature14136 Lamba, 2009, Genetic factors influencing cytarabine therapy, Pharmacogenomics, 10, 1657, 10.2217/pgs.09.118 Ley, 2013, Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia, N. Engl. J. Med., 368, 2059, 10.1056/NEJMoa1301689 Li, 2009, The sequence alignment/map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 Li, 2014, MAGeCK enables robust identification of essential genes from genome-scale CRISPR/Cas9 knockout screens, Genome Biol., 15, 554, 10.1186/s13059-014-0554-4 Li, 2015, TANRIC: An Interactive Open Platform to Explore the Function of lncRNAs in Cancer, Cancer Res., 75, 3728, 10.1158/0008-5472.CAN-15-0273 Liao, 2014, featureCounts: an efficient general purpose program for assigning sequence reads to genomic features, Bioinformatics, 30, 923, 10.1093/bioinformatics/btt656 Liu, 2017, CRISPRi-based genome-scale identification of functional long noncoding RNA loci in human cells, Science, 355, eaah7111, 10.1126/science.aah7111 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Martin, 2011, Cutadapt removes adapter sequences from high-throughput sequencing reads, EMBnet.journal, 17, 10, 10.14806/ej.17.1.200 Mudduluru, 2008, The human receptor tyrosine kinase Axl gene--promoter characterization and regulation of constitutive expression by Sp1, Sp3 and CpG methylation, Biosci. Rep., 28, 161, 10.1042/BSR20080046 Perron, 2017, In silico prediction of lncRNA function using tissue specific and evolutionary conserved expression, BMC Bioinformatics, 18, 144, 10.1186/s12859-017-1535-x Quinn, 2016, Unique features of long non-coding RNA biogenesis and function, Nat. Rev. Genet., 17, 47, 10.1038/nrg.2015.10 Ramos, 2015, Current approaches in the treatment of relapsed and refractory acute myeloid leukemia, J. Clin. Med., 4, 665, 10.3390/jcm4040665 Rees, 2016, Correlating chemical sensitivity and basal gene expression reveals mechanism of action, Nat. Chem. Biol., 12, 109, 10.1038/nchembio.1986 Reimand, 2016, g:Profiler-a web server for functional interpretation of gene lists (2016 update), Nucleic Acids Res., 44, 10.1093/nar/gkw199 Rinn, 2012, Genome regulation by long noncoding RNAs, Annu. Rev. Biochem., 81, 145, 10.1146/annurev-biochem-051410-092902 Saland, 2015, A robust and rapid xenograft model to assess efficacy of chemotherapeutic agents for human acute myeloid leukemia, Blood Cancer J., 5, e297, 10.1038/bcj.2015.19 Schindelin, 2012, Fiji: an open-source platform for biological-image analysis, Nat. Methods, 9, 676, 10.1038/nmeth.2019 Schmitt, 2016, Long noncoding RNAs in cancer pathways, Cancer Cell, 29, 452, 10.1016/j.ccell.2016.03.010 Schneider, 2012, NIH Image to ImageJ: 25 years of image analysis, Nat. Methods, 9, 671, 10.1038/nmeth.2089 Schneider, 2017, SAMHD1 is a biomarker for cytarabine response and a therapeutic target in acute myeloid leukemia, Nat. Med., 23, 250, 10.1038/nm.4255 Schoumacher, 2017, Key roles of AXL and MER receptor tyrosine kinases in resistance to multiple anticancer therapies, Curr. Oncol. Rep., 19, 19, 10.1007/s11912-017-0579-4 Sergushichev, 2016, An algorithm for fast preranked gene set enrichment analysis using cumulative statistic calculation, bioRxiv Shechner, 2015, Multiplexable, locus-specific targeting of long RNAs with CRISPR-Display, Nat. Methods, 12, 664, 10.1038/nmeth.3433 Smoot, 2011, Cytoscape 2.8: new features for data integration and network visualization, Bioinformatics, 27, 431, 10.1093/bioinformatics/btq675 Stavropoulou, 2016, MLL-AF9 expression in hematopoietic stem cells drives a highly invasive AML expressing EMT-related genes linked to poor outcome, Cancer Cell, 30, 43, 10.1016/j.ccell.2016.05.011 Steelman, 2004, JAK/STAT, Raf/MEK/ERK, PI3K/Akt and BCR-ABL in cell cycle progression and leukemogenesis, Leukemia, 18, 189, 10.1038/sj.leu.2403241 Subramanian, 2005, Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles, Proc. Natl. Acad. Sci. USA, 102, 15545, 10.1073/pnas.0506580102 Therneau, T. (2015). A package for survival analysis in S. version 2.38. https://CRAN.R-project.org/package=survival. Wang, 2014, Genetic screens in human cells using the CRISPR-Cas9 system, Science, 343, 80, 10.1126/science.1246981 Wu, 2017, Molecular insights of Gas6/TAM in cancer development and therapy, Cell Death Dis., 8, e2700, 10.1038/cddis.2017.113 Xu, 2017, BCL6 promotes glioma and serves as a therapeutic target, Proc. Natl. Acad. Sci. USA, 114, 3981, 10.1073/pnas.1609758114 Yang, 2013, Genomics of Drug Sensitivity in Cancer (GDSC): a resource for therapeutic biomarker discovery in cancer cells, Nucleic Acids Res., 41, D955, 10.1093/nar/gks1111