Functional Maps of Protein Complexes from Quantitative Genetic Interaction Data
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Recently, a number of advanced screening technologies have allowed for the comprehensive quantification of aggravating and alleviating genetic interactions among gene pairs. In parallel, TAP-MS studies (tandem affinity purification followed by mass spectroscopy) have been successful at identifying physical protein interactions that can indicate proteins participating in the same molecular complex. Here, we propose a method for the joint learning of protein complexes and their functional relationships by integration of quantitative genetic interactions and TAP-MS data. Using 3 independent benchmark datasets, we demonstrate that this method is >50% more accurate at identifying functionally related protein pairs than previous approaches. Application to genes involved in yeast chromosome organization identifies a functional map of 91 multimeric complexes, a number of which are novel or have been substantially expanded by addition of new subunits. Interestingly, we find that complexes that are enriched for aggravating genetic interactions (i.e., synthetic lethality) are more likely to contain essential genes, linking each of these interactions to an underlying mechanism. These results demonstrate the importance of both large-scale genetic and physical interaction data in mapping pathway architecture and function.
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Protein complexes exhibited highly organized patterns of genetic interactions.
“Consistent with previous findings (1, 5, 28, 29), we found that protein complexes exhibited highly organized patterns of genetic interactions.”
From A global genetic interaction network maps a wiring diagram of cellular function (2016) · cites this paper as [29]
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Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
Cytoscape: A software Environment for integrated models of biomolecular interaction networks
Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., & Ideker, T. (2003) · Genome Research · doi:10.1101/gr.1239303 · Cited by 51,888 · see citing works
Self-citationA Statistical Method for Evaluating Systematic Relationships
Sokal, R. R., & Michener, C. D. (1958) · Biodiversity Heritage Library (Smithsonian Institution) · doi:10.5281/zenodo.16435756 · Cited by 4,432 · see citing works
The Role of Chromatin during Transcription
Li, B., Carey, M., & Workman, J. L. (2007) · Cell · doi:10.1016/j.cell.2007.01.015 · Cited by 3,503 · see citing works
Integration of biological networks and gene expression data using Cytoscape
Cline, M. S., Smoot, M., Cerami, E., Kuchinsky, A., Landys, N., Workman, C., Christmas, R., Avila-Campilo, I., Creech, M., Gross, B., et al. (2007) · Nature Protocols · doi:10.1038/nprot.2007.324 · Cited by 2,507 · see citing works
Self-citationSystematic Genetic Analysis with Ordered Arrays of Yeast Deletion Mutants
Tong, A. H. Y., Evangelista, M., Parsons, A. B., Xu, H., Bader, G. D., Pagé, N., Robinson, M., Raghibizadeh, S., Hogue, C. W. V., Bussey, H., et al. (2001) · Science · doi:10.1126/science.1065810 · Cited by 2,138 · see citing works
Transcriptional regulatory code of a eukaryotic genome
Harbison, C. T., Gordon, D. B., Lee, T. I., Rinaldi, N. J., MacIsaac, K. D., Danford, T., Hannett, N. M., Tagne, J., Reynolds, D. B., Yoo, J. Y., et al. (2004) · Nature · doi:10.1038/nature02800 · Cited by 2,116 · see citing works
ATP-Driven Exchange of Histone H2AZ Variant Catalyzed by SWR1 Chromatin Remodeling Complex
Mizuguchi, G., Shen, X., Landry, J., Wu, W.-H., Sen, S., & Wu, C. (2003) · Science · doi:10.1126/science.1090701 · Cited by 1,312 · see citing works
Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast
Sun, Z., & Allis, C. D. (2002) · Nature · doi:10.1038/nature00883 · Cited by 1,076 · see citing works
Global analysis of protein phosphorylation in yeast
Ptacek, J., Devgan, G., Michaud, G. A., Zhu, H., Zhu, X., Fasolo, J., Guo, H., Jona, G., Breitkreutz, A., Sopko, R., et al. (2005) · Nature · doi:10.1038/nature04187 · Cited by 970 · see citing works
Mitchell, P., Petfalski, E., Shevchenko, A., Mann, M., & Tollervey, D. W. (1997) · Cell · doi:10.1016/s0092-8674(00)80432-8 · Cited by 947 · see citing works
Schuldiner, M., Collins, S. R., Thompson, N. J., Denic, V., Bhamidipati, A., Punna, T., Ihmels, J., Andrews, B., Boone, C., Greenblatt, J. F., et al. (2005) · Cell · doi:10.1016/j.cell.2005.08.031 · Cited by 870 · cited 2× · see citing works
“This approach has been applied to several largescale genetic interaction screens in yeast including genes involved in the secretory pathway [8] and chromosome organization [6].”
MethodSelf-citationCollins, S. R., Miller, K. M., Maas, N. L., Roguev, A., Fillingham, J., Chu, C. S., Schuldiner, M., Gebbia, M., Recht, J., Shales, M., et al. (2007) · Nature · doi:10.1038/nature05649 · Cited by 869 · see citing works
Self-citationToward a Comprehensive Atlas of the Physical Interactome of Saccharomyces cerevisiae
Collins, S. R., Kemmeren, P., Zhao, X.-C., Greenblatt, J. F., Spencer, F., Holstege, F. C. P., Weissman, J. S., & Krogan, N. J. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600381-mcp200 · Cited by 795 · see citing works
Self-citationKrogan, N. J., Dover, J., Wood, A., Schneider, J., Heidt, J. W., Boateng, M. A., Dean, K., Ryan, O. W., Golshani, A., Johnston, M., et al. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00091-1 · Cited by 706 · see citing works
Self-citationBerger, M. F., Philippakis, A., Qureshi, A. M., He, F. S., Estep, P. W., & Bulyk, M. L. (2006) · Nature Biotechnology · doi:10.1038/nbt1246 · Cited by 685 · see citing works
Exploring genetic interactions and networks with yeast
Boone, C., Bussey, H., & Andrews, B. J. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2085 · Cited by 661 · see citing works
Kobor, M. S., Venkatasubrahmanyam, S., Meneghini, M. D., Gin, J., Jennings, J. L., Link, A. J., Madhani, H. D., & Rine, J. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020131 · Cited by 607 · see citing works
Modular epistasis in yeast metabolism
Segrè, D., DeLuna, A., Church, G. M., & Kishony, R. (2005) · Nature Genetics · doi:10.1038/ng1489 · Cited by 575 · see citing works
Methylation of Histone H3 by COMPASS Requires Ubiquitination of Histone H2B by Rad6
Dover, J., Schneider, J., Tawiah-Boateng, M. A., Wood, A., Dean, K., Johnston, M., & Shilatifard, A. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c200348200 · Cited by 554 · see citing works
Bre1, an E3 Ubiquitin Ligase Required for Recruitment and Substrate Selection of Rad6 at a Promoter
Wood, A., Krogan, N. J., Dover, J., Schneider, J., Heidt, J. W., Boateng, M. A., Dean, K., Golshani, A., Zhang, Y., Greenblatt, J., et al. (2003) · Molecular Cell · doi:10.1016/s1097-2765(02)00802-x · Cited by 530 · see citing works
Self-citationOtero, G., Fellows, J., Li, Y., de Bizemont, T., Dirac, A. M. G., Gustafsson, C. M., Erdjument‐Bromage, H., Tempst, P., & Svejstrup, J. Q. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80179-3 · Cited by 482 · see citing works
A Conserved RING Finger Protein Required for Histone H2B Monoubiquitination and Cell Size Control
Hwang, W. W., Venkatasubrahmanyam, S., Ianculescu, A. G., Tong, A. H. Y., Boone, C. M., & Madhani, H. D. (2003) · Molecular Cell · doi:10.1016/s1097-2765(02)00826-2 · Cited by 439 · see citing works
Yeast Rtt109 Promotes Genome Stability by Acetylating Histone H3 on Lysine 56
Driscoll, R., Hudson, A., & Jackson, S. P. (2007) · Science · doi:10.1126/science.1135862 · Cited by 439 · see citing works
Systematic interpretation of genetic interactions using protein networks
Kelley, R., & Ideker, T. (2005) · Nature Biotechnology · doi:10.1038/nbt1096 · Cited by 437 · see citing works
Self-citationRtt109 Acetylates Histone H3 Lysine 56 and Functions in DNA Replication
Han, J., Zhou, H., Horazdovsky, B. F., Zhang, K., Xu, R.-M., & Zhang, Z. (2007) · Science · doi:10.1126/science.1133234 · Cited by 421 · see citing works
Sequential gene function in the initiation of Saccharomyces cerevisiae DNA synthesis
Hereford, L. M., & Hartwell, L. H. (1974) · Journal of Molecular Biology · doi:10.1016/0022-2836(74)90451-3 · Cited by 395 · see citing works
MPact: the MIPS protein interaction resource on yeast
Güldener, U. (2005) · Nucleic Acids Research · doi:10.1093/nar/gkj003 · Cited by 353 · see citing works
Systematic pathway analysis using high-resolution fitness profiling of combinatorial gene deletions
St.Onge, R. P., Mani, R., Oh, J., Proctor, M. J., Fung, E., Davis, R. W., Nislow, C., Roth, F. P., & Giaever, G. N. (2007) · Nature Genetics · doi:10.1038/ng1948 · Cited by 306 · see citing works
A strategy for extracting and analyzing large-scale quantitative epistatic interaction data
Collins, S. R., Schuldiner, M., Krogan, N. J., & Weissman, J. S. (2006) · Genome biology · doi:10.1186/gb-2006-7-7-r63 · Cited by 300 · see citing works
Self-citationGenetic interactions between polymorphisms that affect gene expression in yeast
Brem, R. B., Storey, J. D., Whittle, J., & Kruglyak, L. (2005) · Nature · doi:10.1038/nature03865 · Cited by 298 · see citing works
Winkler, G. S., Kristjuhan, A., Erdjument‐Bromage, H., Tempst, P., & Svejstrup, J. Q. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.022042899 · Cited by 276 · see citing works
Ordering gene function: the interpretation of epistasis in regulatory hierarchies
Avery, L., & Wasserman, S. A. (1992) · Trends in Genetics · doi:10.1016/0168-9525(92)90263-4 · Cited by 247 · see citing works
Integrating physical and genetic maps: from genomes to interaction networks
Beyer, A., Bandyopadhyay, S., & Ideker, T. (2007) · Nature Reviews Genetics · doi:10.1038/nrg2144 · Cited by 207 · cited 1× · see citing works
“Another set of methods has sought to interpret genetic relationships using physical protein-protein interactions [13].”
BackgroundSelf-citationDNA helicase gene interaction network defined using synthetic lethality analyzed by microarray
Ooi, S. L., Shoemaker, D. D., & Boeke, J. D. (2003) · Nature Genetics · doi:10.1038/ng1258 · Cited by 194 · see citing works
Motifs, themes and thematic maps of an integrated Saccharomyces cerevisiaeinteraction network
Zhang, L. V., King, O. D., Wong, S. L., Goldberg, D. S., Tong, A. H., Lesage, G., Andrews, B., Bussey, H., Boone, C. M., & Roth, F. P. (2005) · Journal of Biology · doi:10.1186/jbiol23 · Cited by 190 · see citing works
Demeter, J., Beauheim, C. C., Gollub, J., Hernandez‐Boussard, T., Jin, H., Maier, D., Matese, J. C., Nitzberg, M., Wymore, F., Zachariah, Z. K., et al. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl1019 · Cited by 172 · see citing works
Derivation of genetic interaction networks from quantitative phenotype data
Drees, B., Thórsson, V., Carter, G. W., Rives, A. W., Raymond, M. Z., Avila-Campillo, I., Shannon, P. T., & Galitski, T. (2005) · Genome biology · doi:10.1186/gb-2005-6-4-r38 · Cited by 122 · see citing works
Ulitsky, I., & Ron Shamir, A. (2007) · Molecular Systems Biology · doi:10.1038/msb4100144 · Cited by 98 · see citing works
Schuldiner, M., Collins, S. R., Weissman, J. S., & Krogan, N. J. (2006) · Methods · doi:10.1016/j.ymeth.2006.07.034 · Cited by 83 · see citing works
Self-citationPrediction of phenotype and gene expression for combinations of mutations
Carter, G. W., Prinz, S., Neou, C., Shelby, J. P., Marzolf, B., Thórsson, V., & Galitski, T. (2007) · Molecular Systems Biology · doi:10.1038/msb4100137 · Cited by 47 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [17]Phillips PC Otto SP Whitlock MC 2000 Beyond the average: the evolutionary importance of gene interactions and variability of epistatic effects in epistasis and evolutionary process New York Oxford University Press
Cited by
Sorted by citations
A global genetic interaction network maps a wiring diagram of cellular function
Costanzo, M., VanderSluis, B., Koch, E. N., Baryshnikova, A., Pons, C., Tan, G., Wang, W., Usaj, M., Hanchard, J., Lee, S. D., et al. (2016) · Science · doi:10.1126/science.aaf1420 · Cited by 1,240 · see citing works
The Notch signalling system: recent insights into the complexity of a conserved pathway
Guruharsha, K. G., Kankel, M. W., & Artavanis‐Tsakonas, S. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3272 · Cited by 700 · see citing works
Up-to-date catalogues of yeast protein complexes
Pu, S., Wong, J., Turner, B., Cho, E., & Wodak, S. J. (2008) · Nucleic Acids Research · doi:10.1093/nar/gkn1005 · Cited by 606 · see citing works
Integrative approaches for finding modular structure in biological networks
Mitra, K., Carvunis, A.-R., Ramesh, S. K., & Ideker, T. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3552 · Cited by 535 · see citing works
Self-citationRewiring of Genetic Networks in Response to DNA Damage
Bandyopadhyay, S., Mehta, M., Kuo, D., Sung, M.-K., Chuang, R., Jaehnig, E. J., Bodenmiller, B., Licon, K., Copeland, W., Shales, M., et al. (2010) · Science · doi:10.1126/science.1195618 · Cited by 447 · see citing works
Self-citationGlobal Functional Atlas of Escherichia coli Encompassing Previously Uncharacterized Proteins
Hu, P., Janga, S. C., Babu, M., Díaz-Mejía, J. J., Butland, G., Yang, W., Pogoutse, O., Guo, X., Phanse, S., Wong, P., et al. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000096 · Cited by 387 · see citing works
Quantitative analysis of fitness and genetic interactions in yeast on a genome scale
Baryshnikova, A., Costanzo, M., Kim, Y., Ding, H., Koh, J., Toufighi, K., Youn, J.-Y., Ou, J., San Luis, B.-J., Bandyopadhyay, S., et al. (2010) · Nature Methods · doi:10.1038/nmeth.1534 · Cited by 364 · see citing works
Self-citationConservation and Rewiring of Functional Modules Revealed by an Epistasis Map in Fission Yeast
Roguev, A., Bandyopadhyay, S., Zofall, M., Zhang, K., Fischer, T., Collins, S. R., Qu, H., Shales, M., Park, H.-O., Hayles, J., et al. (2008) · Science · doi:10.1126/science.1162609 · Cited by 352 · see citing works
Self-citationDrug interactions and the evolution of antibiotic resistance
Yeh, P. J., Hegreness, M. J., Aiden, A. P., & Kishony, R. (2009) · Nature Reviews Microbiology · doi:10.1038/nrmicro2133 · Cited by 350 · see citing works
Molecular mechanisms of epistasis within and between genes
Lehner, B. (2011) · Trends in Genetics · doi:10.1016/j.tig.2011.05.007 · Cited by 325 · see citing works
Chuang, H., Hofree, M., & Ideker, T. (2010) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100109-104122 · Cited by 316 · see citing works
Self-citationHistory of protein–protein interactions: From egg‐white to complex networks
Falter‐Braun, P., & Gingras, A. (2012) · PROTEOMICS · doi:10.1002/pmic.201100563 · Cited by 308 · see citing works
Systematic Mapping of Genetic Interaction Networks
Dixon, S. J., Costanzo, M., Baryshnikova, A., Andrews, B., & Boone, C. M. (2008) · Annual Review of Genetics · doi:10.1146/annurev.genet.39.073003.114751 · Cited by 290 · see citing works
Global Genetic Networks and the Genotype-to-Phenotype Relationship
Costanzo, M., Kuzmin, E., van Leeuwen, J., Mair, B., Moffat, J., Boone, C., & Andrews, B. (2019) · Cell · doi:10.1016/j.cell.2019.01.033 · Cited by 241 · see citing works
Wilmes, G. M., Bergkessel, M., Bandyopadhyay, S., Shales, M., Braberg, H., Cagney, G., Collins, S. R., Whitworth, G. B., Kress, T. L., Weissman, J. S., et al. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.11.012 · Cited by 265 · see citing works
Self-citationThe binary protein-protein interaction landscape of Escherichia coli
Rajagopala, S. V., Sikorski, P., Kumar, A., Mosca, R., Vlasblom, J., Arnold, R., Franca-Koh, J., Pakala, S. B., Phanse, S., Ceol, A., et al. (2014) · Nature Biotechnology · doi:10.1038/nbt.2831 · Cited by 233 · see citing works
Toward the dynamic interactome: it's about time
Przytycka, T. M., Singh, M., & Slonim, D. K. (2010) · Briefings in Bioinformatics · doi:10.1093/bib/bbp057 · Cited by 252 · see citing works
Hierarchical Modularity and the Evolution of Genetic Interactomes across Species
Ryan, C. J., Roguev, A., Patrick, K. L., Xu, J., Jahari, H., Tong, Z., Beltrão, P., Shales, M., Qu, H., Collins, S. R., et al. (2012) · Molecular Cell · doi:10.1016/j.molcel.2012.05.028 · Cited by 230 · see citing works
Self-citationGenotype to phenotype: lessons from model organisms for human genetics
Lehner, B. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3404 · Cited by 228 · see citing works
Synthetic Genetic Array (SGA) Analysis in Saccharomyces cerevisiae and Schizosaccharomyces pombe
Baryshnikova, A., Costanzo, M., Dixon, S. J., Vizeacoumar, F. J., Myers, C. L., Andrews, B., & Boone, C. M. (2010) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(10)70007-0 · Cited by 201 · see citing works
Shadows of complexity: what biological networks reveal about epistasis and pleiotropy
Tyler, A. L., Asselbergs, F. W., Williams, S. M., & Moore, J. H. (2009) · BioEssays · doi:10.1002/bies.200800022 · Cited by 185 · see citing works
Quantitative Genetic Interactions Reveal Biological Modularity
Beltrão, P., Cagney, G., & Krogan, N. J. (2010) · Cell · doi:10.1016/j.cell.2010.05.019 · Cited by 156 · see citing works
Self-citationThe Cancer Cell Map Initiative: Defining the Hallmark Networks of Cancer
Krogan, N. J., Lippman, S. M., Agard, D. A., Ashworth, A., & Ideker, T. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.05.008 · Cited by 151 · see citing works
Self-citationBabu, M., Arnold, R. R., Bundalovic-Torma, C., Gagarinova, A. G., Wong, K. S., Kumar, A., Stewart, G., Samanfar, B., Aoki, H., Wagih, O., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004120 · Cited by 133 · see citing works
Babu, M., Díaz-Mejía, J. J., Vlasblom, J., Gagarinova, A. G., Phanse, S., Graham, C., Yousif, F., Ding, H., Xiong, X., Nazarians-Armavil, A., et al. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002377 · Cited by 121 · see citing works
Towards genome-scale signalling-network reconstructions
Hyduke, D. R., & Palsson, B. Ø. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2750 · Cited by 124 · see citing works
Charting the genetic interaction map of a cell
Costanzo, M., Baryshnikova, A., Myers, C. L., Andrews, B., & Boone, C. M. (2010) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2010.11.001 · Cited by 114 · see citing works
Genetic Interaction Networks: Toward an Understanding of Heritability
Baryshnikova, A., Costanzo, M., Myers, C. L., Andrews, B., & Boone, C. M. (2013) · Annual Review of Genomics and Human Genetics · doi:10.1146/annurev-genom-082509-141730 · Cited by 108 · see citing works
Genetic interaction networks: better understand to better predict
Boucher, B., & Jenna, S. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00290 · Cited by 105 · see citing works
Quantitative genetic-interaction mapping in mammalian cells
Roguev, A., Talbot, D., Negri, G. L., Shales, M., Cagney, G., Bandyopadhyay, S., Panning, B., & Krogan, N. J. (2013) · Nature Methods · doi:10.1038/nmeth.2398 · Cited by 103 · see citing works
Self-citationVizeacoumar, F. J., van Dyk, N., Vizeacoumar, F. S., Cheung, V., Li, J., Sydorskyy, Y., Case, N., Li, Z., Datti, A., Nislow, C., et al. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.200909013 · Cited by 105 · see citing works
Aguilar, P. S., Fröhlich, F., Rehman, M., Shales, M., Ulitsky, I., Olivera-Couto, A., Braberg, H., Ron Shamir, A., Walter, P., Mann, M., et al. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1829 · Cited by 103 · see citing works
Self-citationHigh-resolution network biology: connecting sequence with function
Ryan, C. J., Cimermančič, P., Szpiech, Z. A., Šali, A., Hernandez, R. D., & Krogan, N. J. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3574 · Cited by 98 · see citing works
Self-citationRegulation of Recombination and Genomic MaintenancePreprint
Heyer, W. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a016501 · Cited by 94 · see citing works
Qi, Y., Suhail, Y., Lin, Y.-Y., Boeke, J. D., & Bader, J. S. (2008) · Genome Research · doi:10.1101/gr.077693.108 · Cited by 94 · see citing works
DRYGIN: a database of quantitative genetic interaction networks in yeast
Koh, J. L. Y., Ding, H., Costanzo, M., Baryshnikova, A., Toufighi, K., Bader, G. D., Myers, C. L., Andrews, B., & Boone, C. M. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp820 · Cited by 92 · see citing works
Translation of Genotype to Phenotype by a Hierarchy of Cell Subsystems
Yu, M., Kramer, M. H., Dutkowski, J., Srivas, R., Licon, K., Kreisberg, J. F., Ng, C. T., Krogan, N. J., Sharan, R., & Ideker, T. (2016) · Cell Systems · doi:10.1016/j.cels.2016.02.003 · Cited by 78 · see citing works
Self-citationDetection of Composite Communities in Multiplex Biological Networks
Bennett, L., Kittas, A., Muirhead, G., Papageorgiou, L. G., & Tsoka, S. (2015) · Scientific Reports · doi:10.1038/srep10345 · Cited by 80 · see citing works
Putting genetic interactions in context through a global modular decompositionPreprint
Bellay, J., Atluri, G., Sing, T. L., Toufighi, K., Costanzo, M., Ribeiro, P. S. M., Pandey, G. S., Baller, J. A., VanderSluis, B., Michaut, M., et al. (2011) · Genome Research · doi:10.1101/gr.117176.110 · Cited by 71 · see citing works
From E-MAPs to module maps: dissecting quantitative genetic interactions using physical interactions
Ulitsky, I., Shlomi, T., Kupiec, M., & Shamir, R. (2008) · Molecular Systems Biology · doi:10.1038/msb.2008.42 · Cited by 80 · see citing works
Comprehensive prediction of robust synthetic lethality between paralog pairs in cancer cell lines
Kegel, B. D., Quinn, N., Thompson, N., Adams, D. J., & Ryan, C. J. (2021) · Cell Systems · doi:10.1016/j.cels.2021.08.006 · Cited by 65 · see citing works
Dynamics of and on complex networks
Halu, A. (2014) · doi:10.17760/d20004937 · Cited by 75 · see citing works
Brochado, A. R., & Typas, A. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.01.008 · Cited by 61 · see citing works
Predicting genetic interactions with random walks on biological networks
Chipman, K. C., & Singh, A. K. (2009) · BMC Bioinformatics · doi:10.1186/1471-2105-10-17 · Cited by 63 · see citing works
Protein Complexes are Central in the Yeast Genetic Landscape
Michaut, M., Baryshnikova, A., Costanzo, M., Myers, C. L., Andrews, B., Boone, C. M., & Bader, G. D. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1001092 · Cited by 57 · see citing works
Hosur, R., Xu, J., Bienkowska, J. R., & Berger, B. (2010) · Journal of Molecular Biology · doi:10.1016/j.jmb.2010.11.025 · Cited by 56 · see citing works
Network Analysis Identifies an HSP90-Central Hub Susceptible in Ovarian Cancer
Liu, H., Xiao, F., Serebriiskii, I. G., O’Brien, S. W., Maglaty, M. A., Astsaturov, I. A., Litwin, S., Martin, L. P., Proia, D. A., Golemis, E. A., et al. (2013) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-1115 · Cited by 52 · see citing works
VanderSluis, B., Costanzo, M., Billmann, M., Ward, H. N., Myers, C. L., Andrews, B., & Boone, C. M. (2018) · Current Opinion in Microbiology · doi:10.1016/j.mib.2018.06.004 · Cited by 49 · see citing works
A Systematic Approach for the Genetic Dissection of Protein Complexes in Living Cells
Diss, G., Dubé, A. K., Boutin, J., Gagnon‐Arsenault, I., & Landry, C. R. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.05.004 · Cited by 44 · see citing works
Somasekharan, S. P., Stoynov, N., Rotblat, B., Leprivier, G., Galpin, J. D., Ahern, C. A., Foster, L. J., & Sorensen, P. H. B. (2012) · Journal of Proteomics · doi:10.1016/j.jprot.2012.08.019 · Cited by 46 · see citing works
Revealing and avoiding bias in semantic similarity scores for protein pairs
Wang, J., Zhou, X., Zhu, J., Zhou, C., & Guo, Z. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-290 · Cited by 46 · see citing works
Lim, D., Kim, N.-K., Park, H., Lee, S. H., Cho, Y.-M., Oh, S. J., Kim, T.-H., & Kim, H. (2011) · International Journal of Biological Sciences · doi:10.7150/ijbs.7.992 · Cited by 45 · see citing works
A Compendium of Co-regulated Protein Complexes in Breast Cancer Reveals Collateral Loss Events
Ryan, C. J., Kennedy, S. A., Bajrami, I., Matallanas, D., & Lord, C. J. (2017) · Cell Systems · doi:10.1016/j.cels.2017.09.011 · Cited by 44 · see citing works
Analysing Network Models to Make Discoveries about Biological Mechanisms
Bechtel, W. (2017) · The British Journal for the Philosophy of Science · doi:10.1093/bjps/axx051 · Cited by 42 · see citing works
Putnam, C. D., Srivatsan, A., Nene, R. V., Martinez, S. L., Clotfelter, S. P., Bell, S., Somach, S. B., de Souza, J. E. S., Fonseca, A. F., SOUZA, S. J. D., et al. (2016) · Nature Communications · doi:10.1038/ncomms11256 · Cited by 41 · see citing works
Walhout, A. J. M., Vidal, M., & Dekker, J. (2013) · Elsevier eBooks · doi:10.1016/c2010-0-67190-2 · Cited by 45 · see citing works
Iyaswamy, A., & Sheeladevi, R. (2015) · Journal of Food and Drug Analysis · doi:10.1016/j.jfda.2014.07.011 · Cited by 39 · see citing works
Fault Tolerance in Protein Interaction Networks: Stable Bipartite Subgraphs and Redundant Pathways
Brady, A., Maxwell, K., Daniels, N. M., & Cowen, L. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005364 · Cited by 38 · see citing works
All or Nothing: Protein Complexes Flip Essentiality between Distantly Related Eukaryotes
Ryan, C. J., Krogan, N. J., Cunningham, P., & Cagney, G. (2013) · Genome Biology and Evolution · doi:10.1093/gbe/evt074 · Cited by 35 · see citing works
Self-citationModularity and directionality in genetic interaction maps
Jaimovich, A., Rinott, R., Schuldiner, M., Margalit, H., & Friedman, N. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq197 · Cited by 32 · see citing works
Constructing module maps for integrated analysis of heterogeneous biological networks
Amar, D., & Ron Shamir, A. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku102 · Cited by 32 · see citing works
Babu, M., Musso, G. A., Díaz-Mejía, J. J., Butland, G. P., Greenblatt, J. F., & Emili, A. (2009) · Molecular BioSystems · doi:10.1039/b907407d · Cited by 32 · see citing works
Zinovyev, A. Y., Kuperstein, I., Barillot, E., & Heyer, W. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003016 · Cited by 32 · see citing works
A Novel Scoring Approach for Protein Co-Purification Data Reveals High Interaction Specificity
Yu, X., Ivanic, J., Wallqvist, A., & Jaques Reifman, A. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000515 · Cited by 30 · see citing works
Patrick, K. L., Ryan, C. J., Xu, J., Lipp, J., Nissen, K. E., Roguev, A., Shales, M., Krogan, N. J., & Guthrie, C. (2015) · PLoS Genetics · doi:10.1371/journal.pgen.1005074 · Cited by 28 · see citing works
Self-citationLocal coherence in genetic interaction patterns reveals prevalent functional versatility
Pu, S., Ronen, K., Vlasblom, J., Greenblatt, J. F., & Wodak, S. J. (2008) · Bioinformatics · doi:10.1093/bioinformatics/btn440 · Cited by 28 · see citing works
Network-based functional modeling of genomics, transcriptomics and metabolism in bacteria
Cloots, L., & Marchal, K. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2011.09.003 · Cited by 27 · see citing works
Towards accurate imputation of quantitative genetic interactions
Ulitsky, I., Krogan, N. J., & Ron Shamir, A. (2009) · Genome biology · doi:10.1186/gb-2009-10-12-r140 · Cited by 25 · see citing works
Self-citationMissing value imputation for epistatic MAPs
Ryan, C. J., Greene, D., Cagney, G., & Cunningham, P. (2010) · BMC Bioinformatics · doi:10.1186/1471-2105-11-197 · Cited by 25 · see citing works
Comparative evolutionary analysis of protein complexes in E. coli and yeast
Reid, A. J., Ranea, J. A. G., & Orengo, C. A. (2010) · BMC Genomics · doi:10.1186/1471-2164-11-79 · Cited by 24 · see citing works
Srivas, R., Hannum, G., Ruscheinski, J., Ono, K., Wang, P., Smoot, M. E., & Ideker, T. (2011) · Nature Protocols · doi:10.1038/nprot.2011.368 · Cited by 23 · see citing works
Self-citationCharles, G. M., Chen, C., Shih, S. C., Collins, S. R., Beltrão, P., Zhang, X., Sharma, T., Tan, S., Burlingame, A. L., Krogan, N. J., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019735108 · Cited by 23 · see citing works
Self-citationSystematic Planning of Genome-Scale Experiments in Poorly Studied Species
Guan, Y., Dunham, M. J., Caudy, A. A., & Troyanskaya, O. G. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000698 · Cited by 21 · see citing works
Srivas, R., Costelloe, T., Carvunis, A., Sarkar, S., Malta, E., Sun, S. M., Pool, M., Licon, K., van Welsem, T., van Leeuwen, F., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.11.035 · Cited by 21 · see citing works
Self-citationGu, Y., Wang, H., Qin, Y., Zhang, Y., Zhao, W., Qi, L., Zhang, Y., Wang, C., & Guo, Z. (2013) · Molecular BioSystems · doi:10.1039/c2mb25528f · Cited by 20 · see citing works
Atias, N., Kupiec, M., & Sharan, R. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv1284 · Cited by 20 · see citing works
Differential analysis of high-throughput quantitative genetic interaction data
Bean, G. J., & Ideker, T. E. (2012) · Genome biology · doi:10.1186/gb-2012-13-12-r123 · Cited by 19 · see citing works
Self-citationJin, K., Musso, G. A., Vlasblom, J., Jessulat, M., Deineko, V., Negroni, J., Mosca, R., Malty, R. H., Nguyen‐Tran, D., Aoki, H., et al. (2014) · Journal of Proteome Research · doi:10.1021/pr501148q · Cited by 19 · see citing works
Quantitative maps of genetic interactions in yeast - Comparative evaluation and integrative analysis
Lindén, R., Eronen, V.-P., & Aittokallio, T. A. (2011) · BMC Systems Biology · doi:10.1186/1752-0509-5-45 · Cited by 18 · see citing works
Ma, W., Yang, D., Gu, Y., Guo, X., Zhao, W., & Guo, Z. (2009) · Genomics · doi:10.1016/j.ygeno.2009.05.001 · Cited by 18 · see citing works
Babu, M., Gagarinova, A. G., Greenblatt, J. F., & Emili, A. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-197-0_9 · Cited by 16 · see citing works
Jafari, M., Mirzaie, M., & Sadeghi, M. (2015) · BMC Bioinformatics · doi:10.1186/s12859-015-0755-1 · Cited by 15 · see citing works
Babu, M., Gagarinova, A. G., & Emili, A. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-276-2_7 · Cited by 15 · see citing works
Data Imputation in Epistatic MAPs by Network-Guided Matrix Completion
Žitnik, M., & Zupan, B. (2015) · Journal of Computational Biology · doi:10.1089/cmb.2014.0158 · Cited by 14 · see citing works
Exploring mitochondrial system properties of neurodegenerative diseases through interactome mapping
Vlasblom, J., Jin, K., Kassir, S., & Babu, M. (2013) · Journal of Proteomics · doi:10.1016/j.jprot.2013.11.008 · Cited by 14 · see citing works
Carvunis, A., Roth, F. P., Calderwood, M. A., Cusick, M. E., Superti‐Furga, G., & Vidal, M. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-385944-0.00003-4 · Cited by 12 · see citing works
The Role of Protein Interactions in Mediating Essentiality and Synthetic Lethality
Talavera, D., Robertson, D. L., & Lovell, S. C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062866 · Cited by 12 · see citing works
Explorations in topology–delving underneath the surface of genetic interaction maps
Breker, M., & Schuldiner, M. (2009) · Molecular BioSystems · doi:10.1039/b907076c · Cited by 12 · see citing works
Modular analysis of the probabilistic genetic interaction network
Hou, L., Wang, L., Qian, M., Li, D., Tang, C., Zhu, Y., Deng, M., & Li, F. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr031 · Cited by 11 · see citing works
Leiserson, M. D. M., Tatar, D., Cowen, L., & Hescott, B. J. (2011) · Journal of Computational Biology · doi:10.1089/cmb.2011.0191 · Cited by 10 · see citing works
Predicting Quantitative Genetic Interactions by Means of Sequential Matrix Approximation
Järvinen, A. P., Hiissa, J., Elo, L. L., & Aittokallio, T. A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003284 · Cited by 10 · see citing works
Genetic interaction mapping with microfluidic-based single cell sequencing
Haliburton, J. R., Shao, W., Deutschbauer, A. M., Arkin, A. P., & Abate, A. R. (2017) · PLoS ONE · doi:10.1371/journal.pone.0171302 · Cited by 10 · see citing works
Interaction networks: Lessons from large‐scale studies in yeast
Cagney, G. (2009) · PROTEOMICS · doi:10.1002/pmic.200900177 · Cited by 10 · see citing works
Braberg, H., Moehle, E. A., Shales, M., Guthrie, C., & Krogan, N. J. (2014) · BioEssays · doi:10.1002/bies.201400044 · Cited by 9 · see citing works
Self-citationA quantitative analysis of monochromaticity in genetic interaction networks
Hsu, C.-H., Wang, T., Chu, H., Kao, C., & Chen, K.-C. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-s13-s16 · Cited by 9 · see citing works
Data Journeys Beyond Databases in Systems Biology: Cytoscape and NDEx
Bechtel, W. (2020) · Springer eBooks · doi:10.1007/978-3-030-37177-7_7 · Cited by 8 · see citing works
Genecentric: a package to uncover graph-theoretic structure in high-throughput epistasis data
Gallant, A., Leiserson, M. D. M., Kachalov, M., Cowen, L., & Hescott, B. J. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-23 · Cited by 8 · see citing works
Roguev, A., Ryan, C. J., Hartsuiker, E., & Krogan, N. J. (2017) · Cold Spring Harbor Protocols · doi:10.1101/pdb.top079905 · Cited by 8 · see citing works
Self-citationAcar, O., Zhang, S., Bahar, İ., & Carvunis, A. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1010181 · Cited by 7 · see citing works
Extracting Between-Pathway Models from E-MAP Interactions Using Expected Graph Compression
Kelley, D. R., & Kingsford, C. (2011) · Journal of Computational Biology · doi:10.1089/cmb.2010.0268 · Cited by 7 · see citing works
- Authors
- Bandyopadhyay, S., Kelley, R., Krogan, N. J., & Ideker, T.
- Affiliations
- University of California San Diego (US)
- University of California, San Francisco (US)
- Corresponding author
- Ideker, Trey
- Venue
- PLoS Computational Biology
- Publisher
- Public Library of Science (PLoS)
- Published
- 2008-04-18
- Volume
- 4
- Issue
- 4
- Pages
- e1000065
- ISSN
- 1553-734X (ISSN-L)
- 1553-7358
- PMC
- PMC2289880
- OpenAlex
- W2037225069
- Cited by
- 141
- References
- 41
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 1 · 2022: 4 · 2021: 2 · 2020: 3 · 2019: 4 · 2018: 3 · 2017: 4 · 2016: 3 · 2015: 10 · 2014: 7 · 2013: 19 · 2012: 14
- FWCI
- 8.77
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Computational Biology (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion, cc-by)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institute of General Medical Sciences (GM 070743, R01GM070743)
- National Institute of Environmental Health Sciences (ES14811, R01ES014811)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene Regulatory Network Analysis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Keywords
- protein complexes, genetic interactions, synthetic lethality, tandem affinity purification, protein-protein interaction, functional maps, essential genes, multimeric complexes, data integration
- MeSH terms
- Binding Sites, Chromosome Mapping, Computer Simulation, Models, Biological, Protein Binding, Signal Transduction, Proteome, Protein Interaction Mapping
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