Highly Combinatorial Genetic Interaction Analysis Reveals a Multi-Drug Transporter Influence Network

Angeles-Albores, 2018, Reconstructing a metazoan genetic pathway with transcriptome-wide epistasis measurements, Proc. Natl. Acad. Sci. USA, 115, E2930, 10.1073/pnas.1712387115 Baeza-Centurion, 2019, Combinatorial genetics reveals a scaling law for the effects of mutations on splicing, Cell, 176, 549, 10.1016/j.cell.2018.12.010 Beh, 2001, Overlapping functions of the yeast oxysterol-binding protein homologues, Genetics, 157, 1117, 10.1093/genetics/157.3.1117 Bloom, 2013, Finding the sources of missing heritability in a yeast cross, Nature, 494, 234, 10.1038/nature11867 Boettcher, 2018, Dual gene activation and knockout screen reveals directional dependencies in genetic networks, Nat. Biotechnol., 36, 170, 10.1038/nbt.4062 Braun, 2009, An experimentally derived confidence score for binary protein-protein interactions, Nat. Methods, 6, 91, 10.1038/nmeth.1281 Costanzo, 2010, The genetic landscape of a cell, Science, 327, 425, 10.1126/science.1180823 Costanzo, 2016, A global genetic interaction network maps a wiring diagram of cellular function, Science, 353, aaf1420, 10.1126/science.aaf1420 Díaz-Mejía, 2018, Mapping DNA damage-dependent genetic interactions in yeast via party mating and barcode fusion genetics, Mol. Syst. Biol., 14, e7985, 10.15252/msb.20177985 DiCarlo, 2013, Yeast oligo-mediated genome engineering (YOGE), ACS Synth. Biol., 2, 741, 10.1021/sb400117c Diss, 2018, The genetic landscape of a physical interaction, Elife, 7, e32472, 10.7554/eLife.32472 Dixit, 2016, Perturb-seq: dissecting molecular circuits with scalable single-cell RNA profiling of pooled genetic screens, Cell, 167, 1853, 10.1016/j.cell.2016.11.038 Domingo, 2018, Pairwise and higher-order genetic interactions during the evolution of a tRNA, Nature, 558, 117, 10.1038/s41586-018-0170-7 Donner, 2001, Up-regulation of basolateral multidrug resistance protein 3 (Mrp3) in cholestatic rat liver, Hepatology, 34, 351, 10.1053/jhep.2001.26213 Ferretti, 2018, Evolutionary constraints in fitness landscapes, Heredity (Edinb), 121, 466, 10.1038/s41437-018-0110-1 Fu, 2013, ABCA12 regulates ABCA1-dependent cholesterol efflux from macrophages and the development of atherosclerosis, Cell Metab., 18, 225, 10.1016/j.cmet.2013.07.003 Giaever, 2002, Functional profiling of the Saccharomyces cerevisiae genome, Nature, 418, 387, 10.1038/nature00935 Gibson, 2009, Enzymatic assembly of DNA molecules up to several hundred kilobases, Nat. Methods, 6, 343, 10.1038/nmeth.1318 Gietz, 2007, High-efficiency yeast transformation using the LiAc/SS carrier DNA/PEG method, Nat. Protoc., 2, 31, 10.1038/nprot.2007.13 Graf, 2003, ABCG5 and ABCG8 Are obligate heterodimers for protein trafficking and biliary cholesterol excretion, J. Biol. Chem., 278, 48275, 10.1074/jbc.M310223200 Haber, 2013, Systematic triple-mutant analysis uncovers functional connectivity between pathways involved in chromosome regulation, Cell Rep., 3, 2168, 10.1016/j.celrep.2013.05.007 Hartman, 2001, Principles for the buffering of genetic variation, Science, 291, 1001, 10.1126/science.291.5506.1001 Horlbeck, 2018, Mapping the genetic landscape of human cells, Cell, 174, 953, 10.1016/j.cell.2018.06.010 Huls, 2008, The breast cancer resistance protein transporter ABCG2 is expressed in the human kidney proximal tubule apical membrane, Kidney Int., 73, 220, 10.1038/sj.ki.5002645 Jakočiūnas, 2015, Multiplex metabolic pathway engineering using CRISPR/Cas9 in Saccharomyces cerevisiae, Metab. Eng., 28, 213, 10.1016/j.ymben.2015.01.008 Jao, 2013, Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system, Proc. Natl. Acad. Sci. USA, 110, 13904, 10.1073/pnas.1308335110 Kebschull, 2018, Cellular barcoding: lineage tracing, screening and beyond, Nat. Methods, 15, 871, 10.1038/s41592-018-0185-x Khakhina, 2015, Control of plasma membrane permeability by ABC transporters, Eukaryot. Cell, 14, 442, 10.1128/EC.00021-15 Kolaczkowska, 2008, Compensatory activation of the multidrug transporters Pdr5p, Snq2p, and Yor1p by Pdr1p in Saccharomyces cerevisiae, FEBS Lett., 582, 977, 10.1016/j.febslet.2008.02.045 König, 1999, Characterization of the human multidrug resistance protein isoform MRP3 localized to the basolateral hepatocyte membrane, Hepatology, 29, 1156, 10.1002/hep.510290404 Kuzmin, 2018, Systematic analysis of complex genetic interactions, Science, 360, eaao1729, 10.1126/science.aao1729 Lee, 2014, Mapping the cellular response to small molecules using chemogenomic fitness signatures, Science, 344, 208, 10.1126/science.1250217 Ma, 2018, Using deep learning to model the hierarchical structure and function of a cell, Nat. Methods, 15, 290, 10.1038/nmeth.4627 Mani, 2008, Defining genetic interaction, Proc. Natl. Acad. Sci. USA, 105, 3461, 10.1073/pnas.0712255105 Najm, 2018, Orthologous CRISPR–Cas9 enzymes for combinatorial genetic screens, Nat. Biotechnol., 36, 179, 10.1038/nbt.4048 Nawrocki, 2001, The effects of transcription regulating genes PDR1,pdr1-3 and PDR3 in pleiotropic drug resistance, Proteomics, 1, 1022, 10.1002/1615-9861(200108)1:8<1022::AID-PROT1022>3.0.CO;2-7 Paumi, 2008, Negative regulation of the yeast ABC transporter Ycf1p by phosphorylation within its N-terminal extension, J. Biol. Chem., 283, 27079, 10.1074/jbc.M802569200 Paumi, 2009, ABC transporters in Saccharomyces cerevisiae and their interactors: new technology advances the biology of the ABCC (MRP) subfamily, Microbiol. Mol. Biol. Rev., 73, 577, 10.1128/MMBR.00020-09 Sadhu, 2016, CRISPR-directed mitotic recombination enables genetic mapping without crosses, Science, 352, 1113, 10.1126/science.aaf5124 Sarkisyan, 2016, Local fitness landscape of the green fluorescent protein, Nature, 533, 397, 10.1038/nature17995 Shaw, 2019, Engineering a model cell for rational tuning of GPCR signaling, Cell, 177, 782, 10.1016/j.cell.2019.02.023 Shekhar-Guturja, 2016, Beauvericin Potentiates Azole Activity via Inhibition of Multidrug Efflux, Blocks Candida albicans Morphogenesis, and Is Effluxed via Yor1 and Circuitry Controlled by Zcf29, Antimicrob. Agents Chemother., 60, 7468, 10.1128/AAC.01959-16 Shen, 2018, Synthetic lethal networks for precision oncology: promises and pitfalls, J. Mol. Biol., 430, 2900, 10.1016/j.jmb.2018.06.026 Shen, 2017, Combinatorial CRISPR–Cas9 screens for de novo mapping of genetic interactions, Nat. Methods, 14, 573, 10.1038/nmeth.4225 Snider, 2013, Mapping the functional yeast ABC transporter interactome, Nat. Chem. Biol., 9, 565, 10.1038/nchembio.1293 Snider, 2010, Split-ubiquitin based membrane yeast two-hybrid (MYTH) system: a powerful tool for identifying protein-protein interactions, J. Vis. Exp., 10.3791/1698 St Onge, 2007, Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions, Nat. Genet., 39, 199, 10.1038/ng1948 Suzuki, 2011, Knocking out multigene redundancies via cycles of sexual assortment and fluorescence selection, Nat. Methods, 8, 159, 10.1038/nmeth.1550 Takahashi, 2006, Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors, Cell, 126, 663, 10.1016/j.cell.2006.07.024 Tarassov, 2008, An in vivo map of the yeast protein interactome, Science, 320, 1465, 10.1126/science.1153878 Taylor, 2014, Genetic interactions involving five or more genes contribute to a complex trait in yeast, PLoS Genet., 10, e1004324, 10.1371/journal.pgen.1004324 Wang, 2013, One-step generation of mice carrying mutations in multiple genes by CRISPR/cas-mediated genome engineering, Cell, 153, 910, 10.1016/j.cell.2013.04.025 Wang, 2009, Programming cells by multiplex genome engineering and accelerated evolution, Nature, 460, 894, 10.1038/nature08187 Wieczorke, 1999, Concurrent knock-out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae, FEBS Lett., 464, 123, 10.1016/S0014-5793(99)01698-1 Wong, 2016, Multiplexed barcoded CRISPR-Cas9 screening enabled by CombiGEM, Proc. Natl. Acad. Sci. USA, 113, 2544, 10.1073/pnas.1517883113 Xu, 2016, Targeted mutagenesis of duplicated genes in Caenorhabditis elegans using CRISPR-Cas9, J. Genet. Genomics, 43, 103, 10.1016/j.jgg.2015.11.004 Yachie, 2016, Pooled-matrix protein interaction screens using Barcode Fusion Genetics, Mol. Syst. Biol., 12, 863, 10.15252/msb.20156660 Zeitoun, 2015, Multiplexed tracking of combinatorial genomic mutations in engineered cell populations, Nat. Biotechnol., 33, 631, 10.1038/nbt.3177 Zeitoun, 2017, Quantitative tracking of combinatorially engineered populations with multiplexed binary assemblies, ACS Synth. Biol., 6, 619, 10.1021/acssynbio.6b00376 Zhang, 2016, A multiplex CRISPR/Cas9 platform for fast and efficient editing of multiple genes in Arabidopsis, Plant Cell Rep, 35, 1519, 10.1007/s00299-015-1900-z