Exploring genetic suppression interactions on a global scale

Science

Volumn 354, Issue 6312, 2016, Pages

  Van Leeuwen, Jolanda ^a   Pons, Carles ^b,c   Mellor, Joseph C ^a,d   Yamaguchi, Takafumi N ^a,d   Friesen, Helena ^a   Koschwanez, John ^e   Ušaj, Mojca Mattiazzi ^a   Pechlaner, Maria ^f   Takar, Mehmet ^g   Ušaj, Matej ^a   Vander Sluis, Benjamin ^b,l   Andrusiak, Kerry ^a   Bansal, Pritpal ^a,d   Baryshnikova, Anastasia ^h   Boone, Claire E ^a   Cao, Jessica ^a   Cote, Atina ^a,d   Gebbia, Marinella ^a,d   Horecka, Gene ^a   Horecka, Ira ^a   Kuzmin, Elena ^a   Legro, Nicole ^a   Liang, Wendy ^a   Van Lieshout, Natascha ^a,d   McNee, Margaret ^a   San Luis, Bryan Joseph ^a   Shaeri, Fatemeh ^a,d   Shuteriqi, Ermira ^a   Sun, Song ^a   Yang, Lu ^a   Youn, Ji Young ^d   Yuen, Michael ^a   Costanzo, Michael ^a   Gingras, Anne Claude ^a,d   Aloy, Patrick ^c,i   Oostenbrink, Chris ^f   Murray, Andrew ^e   Graham, Todd R ^g   Myers, Chad L ^b,j   Andrews, Brenda J ^a   Roth, Frederick P ^a,d,j,k   Boone, Charles ^a   more..

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF MINNESOTA   (United States)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^d MOUNT SINAI HOSPITAL   (Canada)

^e HARVARD UNIVERSITY   (United States)

^f UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^g VANDERBILT UNIVERSITY   (United States)

^h PRINCETON UNIVERSITY   (United States)

ⁱ INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^j CANADIAN INSTITUTE FOR ADVANCED RESEARCH   (Canada)

^k UNIVERSITY OF TORONTO   (Canada)

^l Simons Center for Data Analysis   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; SACCHAROMYCES CEREVISIAE PROTEIN;

CELLS AND CELL COMPONENTS; CYTOGENETICS; EXPERIMENTAL STUDY; GENE; GENETIC ANALYSIS; GENETIC STRUCTURE; GENOME; MUTATION; YEAST;

ARTICLE; DNA END JOINING REPAIR; DNA REPAIR; DNA REPLICATION; GENE EXPRESSION; GENE INTERACTION; GENE MAPPING; GENE REPRESSION; GENE SEQUENCE; GENETIC ANALYSIS; GENETIC TRAIT; HOMOLOGOUS RECOMBINATION; LOSS OF FUNCTION MUTATION; MODIFIER GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; SACCHAROMYCES CEREVISIAE; SUPPRESSOR GENE; CELL FUNCTION; CHROMOSOMAL MAPPING; FUNGAL GENE; GENE REGULATORY NETWORK; GENETICS;

CELL PHYSIOLOGICAL PHENOMENA; CHROMOSOME MAPPING; GENE REGULATORY NETWORKS; GENES, FUNGAL; GENES, SUPPRESSOR; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUPPRESSION, GENETIC;

EID: 84995444658     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.aag0839     Document Type: Article

References (47)

1. S. J. Dixon, M. Costanzo, A. Baryshnikova, B. Andrews, C. Boone, Systematic mapping of genetic interaction networks. Annu. Rev. Genet. 43, 601-625 (2009). doi: 10.1146/annurev. genet.39.073003.114751; pmid: 19712041
2. M. Costanzo et al., The genetic landscape of a cell. Science 327, 425-431 (2010). doi: 10.1126/science.1180823; pmid: 20093466
3. R. Chen et al., Analysis of 589,306 genomes identifies individuals resilient to severe Mendelian childhood diseases. Nat. Biotechnol. 34, 531-538 (2016). doi: 10.1038/nbt.3514; pmid: 27065010
4. R. P. St Onge et al., Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions. Nat. Genet. 39, 199-206 (2007). doi: 10.1038/ng1948; pmid: 17206143
5. D. K. Breslow et al., A comprehensive strategy enabling high-resolution functional analysis of the yeast genome. Nat. Methods 5, 711-718 (2008). doi: 10.1038/nmeth.1234; pmid: 18622397
6. M. Costanzo et al., A global genetic interaction network maps a wiring diagram of cellular function. Science 353, aaf1420 (2016). doi: 10.1126/science.aaf1420; pmid: 27708008
7. A. Baryshnikova et al., Quantitative analysis of fitness and genetic interactions in yeast on a genome scale. Nat. Methods 7, 1017-1024 (2010). doi: 10.1038/nmeth.1534; pmid: 21076421
8. D. Botstein, Decoding the Language of Genetics (Cold Spring Harbor Laboratory Press, 2015).
9. C. Stark et al., BioGRID: A general repository for interaction datasets. Nucleic Acids Res. 34, D535-D539 (2006). doi: 10.1093/nar/gkj109; pmid: 16381927
10. P. Shannon et al., Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504 (2003). doi: 10.1101/gr.1239303; pmid: 14597658
11. M. Valencia-Burton et al., Different mating-type-regulated genes affect the DNA repair defects of Saccharomyces RAD51, RAD52 and RAD55 mutants. Genetics 174, 41-55 (2006). doi: 10.1534/genetics.106.058685; pmid: 16782999
12. L. Peiró-Chova, F. Estruch, Specific defects in different transcription complexes compensate for the requirement of the negative cofactor 2 repressor in Saccharomyces cerevisiae. Genetics 176, 125-138 (2007). doi: 10.1534/genetics.106.066829; pmid: 17339209
13. L. Magtanong et al., Dosage suppression genetic interaction networks enhance functional wiring diagrams of the cell. Nat. Biotechnol. 29, 505-511 (2011). doi: 10.1038/nbt.1855; pmid: 21572441
14. E. L. Huttlin et al., The BioPlex network: A systematic exploration of the human interactome. Cell 162, 425-440 (2015). doi: 10.1016/j.cell.2015.06.043; pmid: 26186194
15. T. Rolland et al., A proteome-scale map of the human interactome network. Cell 159, 1212-1226 (2014). doi: 10.1016/j.cell.2014.10.050; pmid: 25416956
16. R. Sopko et al., Mapping pathways and phenotypes by systematic gene overexpression. Mol. Cell 21, 319-330 (2006). doi: 10.1016/j.molcel.2005.12.011; pmid: 16455487
17. M. E. Cusick et al., Literature-curated protein interaction datasets. Nat. Methods 6, 39-46 (2009). doi: 10.1038/nmeth.1284; pmid: 19116613
18. A. H. Tong et al., Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294, 2364-2368 (2001). doi: 10.1126/science.1065810; pmid: 11743205
19. A. H. Tong et al., Global mapping of the yeast genetic interaction network. Science 303, 808-813 (2004). doi: 10.1126/science.1091317; pmid: 14764870
20. P. Jorgensen et al., High-resolution genetic mapping with ordered arrays of Saccharomyces cerevisiae deletion mutants. Genetics 162, 1091-1099 (2002). pmid: 12454058
21. Detailed materials and methods are available as supplementary materials in Science Online.
22. M. Schuldiner et al., Exploration of the function and organization of the yeast early secretory pathway through an epistatic miniarray profile. Cell 123, 507-519 (2005). doi: 10.1016/j.cell.2005.08.031; pmid: 16269340
23. C. D. Dunn, R. E. Jensen, Suppression of a defect in mitochondrial protein import identifies cytosolic proteins required for viability of yeast cells lacking mitochondrial DNA. Genetics 165, 35-45 (2003). pmid: 14504216
24. G. D. Clark-Walker, Kinetic properties of F1-ATPase influence the ability of yeasts to grow in anoxia or absence of mtDNA. Mitochondrion 2, 257-265 (2003). doi: 10.1016/S1567-7249 (02)00107-1; pmid: 16120326
25. A. Jézégou et al., Heptahelical protein PQLC2 is a lysosomal cationic amino acid exporter underlying the action of cysteamine in cystinosis therapy. Proc. Natl. Acad. Sci. U.S.A. 109, E3434-E3443 (2012). doi: 10.1073/pnas.1211198109; pmid: 23169667
26. A. K. Gillingham, J. R. Whyte, B. Panic, S. Munro, Mon2, a relative of large Arf exchange factors, recruits Dop1 to the Golgi apparatus. J. Biol. Chem. 281, 2273-2280 (2006). doi: 10.1074/jbc.M510176200; pmid: 16301316
27. S. Barbosa, D. Pratte, H. Schwarz, R. Pipkorn, B. Singer-Krüger, Oligomeric Dop1p is part of the endosomal Neo1p-Ysl2p-Arl1p membrane remodeling complex. Traffic 11, 1092-1106 (2010). doi: 10.1111/j.1600-0854.2010.01079.x; pmid: 20477991
28. M. Takar, Y. Wu, T. R. Graham, The essential Neo1 protein from budding yeast plays a role in establishing aminophospholipid asymmetry of the plasma membrane. J. Biol. Chem. 291, 15727-15739 (2016). doi: 10.1074/jbc.M115.686253; pmid: 27235400
29. A. B. Parsons et al., Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell 126, 611-625 (2006). doi: 10.1016/j.cell.2006.06.040; pmid: 16901791
30. K. Iwamoto et al., Curvature-dependent recognition of ethanolamine phospholipids by duramycin and cinnamycin. Biophys. J. 93, 1608-1619 (2007). doi: 10.1529/biophysj.106.101584; pmid: 17483159
31. G. D. Fairn, M. Hermansson, P. Somerharju, S. Grinstein, Phosphatidylserine is polarized and required for proper Cdc42 localization and for development of cell polarity. Nat. Cell Biol. 13, 1424-1430 (2011). doi: 10.1038/ncb2351; pmid: 21964439
32. X. Teng et al., Genome-wide consequences of deleting any single gene. Mol. Cell 52, 485-494 (2013). doi: 10.1016/j. molcel.2013.09.026; pmid: 24211263
33. G. I. Lang et al., Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500, 571-574 (2013). doi: 10.1038/nature12344; pmid: 23873039
34. S. Kryazhimskiy, D. P. Rice, E. R. Jerison, M. M. Desai, Global epistasis makes adaptation predictable despite sequence-level stochasticity. Science 344, 1519-1522 (2014). doi: 10.1126/science.1250939; pmid: 24970088
35. D. J. Kvitek, G. Sherlock, Whole genome, whole population sequencing reveals that loss of signaling networks is the major adaptive strategy in a constant environment. PLOS Genet. 9, e1003972 (2013). doi: 10.1371/journal.pgen.1003972; pmid: 24278038
36. E. Cameroni, N. Hulo, J. Roosen, J. Winderickx, C. De Virgilio, The novel yeast PAS kinase Rim 15 orchestrates G0-associated antioxidant defense mechanisms. Cell Cycle 3, 462-468 (2004). doi: 10.4161/cc.3.4.791; pmid: 15300954
37. A. Smith, M. P. Ward, S. Garrett, Yeast PKA represses Msn2p/Msn4p-dependent gene expression to regulate growth, stress response and glycogen accumulation. EMBO J. 17, 3556-3564 (1998). doi: 10.1093/emboj/17.13.3556; pmid: 9649426
38. D. Kaida, H. Yashiroda, A. Tohe, Y. Kikuchi, Yeast Whi2 and Psr1-phosphatase form a complex and regulate STRE-mediated gene expression. Genes Cells 7, 543-552 (2002). doi: 10.1046/j.1365-2443.2002.00538.x; pmid: 12090248
39. K. Tanaka et al., S. cerevisiae genes IRA1 and IRA2 encode proteins that may be functionally equivalent to mammalian ras GTPase activating protein. Cell 60, 803-807 (1990). doi: 10.1016/0092-8674(90)90094-U; pmid: 2178777
40. T. Hart et al., High-resolution CRISPR screens reveal fitness genes and genotype-specific cancer liabilities. Cell 163, 1515-1526 (2015). doi: 10.1016/j.cell.2015.11.015; pmid: 26627737
41. T. Wang et al., Identification and characterization of essential genes in the human genome. Science 350, 1096-1101 (2015). doi: 10.1126/science.aac7041; pmid: 26472758
42. V. A. Blomen et al., Gene essentiality and synthetic lethality in haploid human cells. Science 350, 1092-1096 (2015). doi: 10.1126/science.aac7557; pmid: 26472760
43. E. M. Torres et al., Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317, 916-924 (2007). doi: 10.1126/science.1142210; pmid: 17702937
44. A. B. Sunshine et al., The fitness consequences of aneuploidy are driven by condition-dependent gene effects. PLOS Biol. 13, e1002155 (2015). doi: 10.1371/journal. pbio.1002155; pmid: 26011532
45. L. M. Wahl, A. D. Zhu, Survival probability of beneficial mutations in bacterial batch culture. Genetics 200, 309-320 (2015). doi: 10.1534/genetics.114.172890; pmid: 25758382
46. C. M. Buchovecky et al., A suppressor screen in Mecp2 mutant mice implicates cholesterol metabolism in Rett syndrome. Nat. Genet. 45, 1013-1020 (2013). doi: 10.1038/ng.2714; pmid: 23892605
47. D. M. Jordan et al., Identification of cis-suppression of human disease mutations by comparative genomics. Nature 524, 225-229 (2015). doi: 10.1038/nature14497; pmid: 26123021