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Exploration of the Function and Organization of the Yeast Early Secretory Pathway through an Epistatic Miniarray Profile
Open accessAbstract
We present a strategy for generating and analyzing comprehensive genetic-interaction maps, termed E-MAPs (epistatic miniarray profiles), comprising quantitative measures of aggravating or alleviating interactions between gene pairs. Crucial to the interpretation of E-MAPs is their high-density nature made possible by focusing on logically connected gene subsets and including essential genes. Described here is the analysis of an E-MAP of genes acting in the yeast early secretory pathway. Hierarchical clustering, together with novel analytical strategies and experimental verification, revealed or clarified the role of many proteins involved in extensively studied processes such as sphingolipid metabolism and retention of HDEL proteins. At a broader level, analysis of the E-MAP delineated pathway organization and components of physical complexes and illustrated the interconnection between the various secretory processes. Extension of this strategy to other logically connected gene subsets in yeast and higher eukaryotes should provide critical insights into the functional/organizational principles of biological systems.
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“positive interactions were also enriched between genes involved in mRNA decay and essential gene DAmP alleles (13)”
From A global genetic interaction network maps a wiring diagram of cellular function (2016) · cites this paper as [13]
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“However, comprehensive SGA analysis has been the most extensively used method for GI studies (for example, Collins et al., 2007; Schuldiner et al., 2005; Tong et al., 2004) and its large-scale application enabled mapping of a global GI network for budding yeast (Costanzo et al.”
InfluentialSelf-citationWilmes, 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 263
“E-MAP Analysis Strains were constructed and E-MAP experiments were performed as previously described (Collins et al., 2006, 2007b; Schuldiner et al., 2005).”
MethodInfluentialSelf-citationFunctions and metabolism of sphingolipids in Saccharomyces cerevisiae
Dickson, R. C., Sumanasekera, C., & Lester, R. L. (2006) · Progress in Lipid Research · doi:10.1016/j.plipres.2006.03.004 · Cited by 262
Bach, L., Michaelson, L. V., Haslam, R. P., Bellec, Y., Gissot, L., Marion, J., Costa, M. D., Boutin, J., Miquel, M., Tellier, F., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0805089105 · Cited by 263
“PHS1 had the strongest epistatic interaction in yeast with the LCB phosphatase LCB3 (6).”
BackgroundTail-anchored membrane protein insertion into the endoplasmic reticulum
Hegde, R. S., & Keenan, R. J. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3226 · Cited by 258
“, and mutant phenotypes in other organisms were related to processes that involved TA protein”
Cyclic changes in metabolic state during the life of a yeast cell
Tu, B. P., Mohler, R. E., Liu, J. C., Dombek, K. M., Young, E. T., Synovec, R. E., & McKnight, S. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0708365104 · Cited by 260
Functional Organization of the S. cerevisiae Phosphorylation Network
Fiedler, D., Braberg, H., Mehta, M., Chechik, G., Cagney, G., Mukherjee, P., Silva, A. C., Shales, M., Collins, S. R., van Wageningen, S., et al. (2009) · Cell · doi:10.1016/j.cell.2008.12.039 · Cited by 254
“Abovedashedline:Theptonratiosofpreviouslypublisheddatasets (early secretory pathway [ESP] [Schuldiner et al., 2005] and chromosome function [Collins et al., 2007b]), the signaling E-MAP, only protein kinases and protein phosphatases (K versus K or P versus P), and protein kinases versus protein…”
InfluentialSelf-citationInhibition of RNA lariat debranching enzyme suppresses TDP-43 toxicity in ALS disease models
Armakola, M., Higgins, M., Figley, M. D., Barmada, S. J., Scarborough, E. A., Diaz, Z., Fang, X., Shorter, J., Krogan, N. J., Finkbeiner, S. M., et al. (2012) · Nature Genetics · doi:10.1038/ng.2434 · Cited by 253
Self-citationEvolution of protein phosphatases in plants and animals
Moorhead, G. B. G., Wever, V. D., Templeton, G. W., & Kerk, D. (2008) · Biochemical Journal · doi:10.1042/bj20081986 · Cited by 260
Interaction landscape of membrane-protein complexes in Saccharomyces cerevisiae
Babu, M., Vlasblom, J., Pu, S., Guo, X., Graham, C., Bean, B. D. M., Burston, H. E., Vizeacoumar, F. J., Snider, J. D., Phanse, S., et al. (2012) · Nature · doi:10.1038/nature11354 · Cited by 258
Self-citationDefenouillère, Q., Yao, Y., Mouaikel, J., Namane, A., Galopier, A., Decourty, L., Doyen, A., Malabat, C., Saveanu, C., Jacquier, A., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1221724110 · Cited by 246
High-throughput, quantitative analyses of genetic interactions in E. coli
Typas, A., Nichols, R. J., Siegele, D. A., Shales, M., Collins, S. R., Lim, B., Braberg, H., Yamamoto, N., Takeuchi, R., Wanner, B. L., et al. (2008) · Nature Methods · doi:10.1038/nmeth.1240 · Cited by 239
Self-citationBhamidipati, A., Denic, V., Toyama, E. Q., & Weissman, J. S. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.07.027 · Cited by 234
Self-citationHierarchical 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 238
“Frameworks for modeling and scoring genetic interactions are normally centered at zero (i.e., a neutral gene pair) (Schuldiner et al., 2005; Collins et al., 2006, 2010; Baryshnikova et al., 2010; Horn et al., 2011) and have been developed to capture a continuous spectrum of phenotype strengths.”
InfluentialSelf-citationWyce, A., Xiao, T., Whelan, K. A., Kosman, C., Walter, W., Eick, D., Hughes, T. R., Krogan, N. J., Strahl, B. D., & Berger, S. L. (2007) · Molecular Cell · doi:10.1016/j.molcel.2007.01.035 · Cited by 229
“Images were taken after 2 days of growth at 30 C. Genetic Interaction and Gene Expression Profiling Genetic interaction profiles using E-MAP technology (Schuldiner et al., 2005) and effects of deletions on gene expression were identified as previously described (Keogh et al., 2005).”
MethodSelf-citationProbing Nucleosome Function: A Highly Versatile Library of Synthetic Histone H3 and H4 Mutants
Dai, J., Hyland, E. M., Yuan, D., Huang, H., Bader, J. S., & Boeke, J. D. (2008) · Cell · doi:10.1016/j.cell.2008.07.019 · Cited by 231
A fine scale phenotype–genotype virulence map of a bacterial pathogenPreprint
van Opijnen, T., & Camilli, A. (2012) · Genome Research · doi:10.1101/gr.137430.112 · Cited by 220
“A reverse genetics approach based on genome-wide ordered arrays of single gene knockouts (Tong et al. 2001; Schuldiner et al. 2005) has been applied to several model organisms (Giaever et al.”
BackgroundMethodThe KDEL receptor: New functions for an old protein
Capitani, M., & Sallese, M. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.10.053 · Cited by 215
“pathway in yeast, another study reported that two subunits of the co-chaperone complex involved in the folding of microtubules (GIM3 and GIM4) have epistatic relationships with the KDEL receptor [72].”
BackgroundDickson, R. C. (2008) · Journal of Lipid Research · doi:10.1194/jlr.r800003-jlr200 · Cited by 227
Ben‐Aroya, S., Coombes, C. E., Kwok, T., O’Donnell, K. A., Boeke, J. D., & Hieter, P. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.02.021 · Cited by 213
“…by the yeast community for the study of essential genes, which resulted in a few collections that are already available to the community: DAmP alleles (Schuldiner et al., 2005), the N-degron (Kanemaki et al., 2003; Labib et al., 2000), and the tet promoter collections (Mnaimneh et al., 2004).”
BackgroundInfluentialPitre, S., Dehne, F., Chan, A., Cheetham, J., Duong, A., Emili, A., Gebbia, M., Greenblatt, J. F., Jessulat, M. G., Krogan, N. J., et al. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-365 · Cited by 216
Self-citationIntegrating 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
“Conversely, alleviating interactions have been thought to indicate genes within the same pathwa”
BackgroundGenome-wide analysis of barcoded Saccharomyces cerevisiae gene-deletion mutants in pooled cultures
Pierce, S. E., Davis, R. W., Nislow, C., & Giaever, G. N. (2007) · Nature Protocols · doi:10.1038/nprot.2007.427 · Cited by 213
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 212
Self-citationGreen, R. A., Kao, H.-L., Audhya, A., Arur, S., Mayers, J. R., Fridolfsson, H. N., Schulman, M., Schloissnig, S., Niessen, S., Laband, K., et al. (2011) · Cell · doi:10.1016/j.cell.2011.03.037 · Cited by 206
“, 2010), and maps have also been generated for subsets of gene implicated in specific processes—such as RNA processing, chromosome biology, proteasome function, and the secretory pathway (Breslow et al., 2008; Collins et al., 2007; Schuldiner et al., 2005; Wilmes et al., 2008).”
An integrated approach to characterize genetic interaction networks in yeast metabolism
Szappanos, B., Kovács, K., Szamecz, B., Honti, F., Costanzo, M., Baryshnikova, A., Gelius‐Dietrich, G., Lercher, M. J., Jelasity, M., Myers, C. L., et al. (2011) · Nature Genetics · doi:10.1038/ng.846 · Cited by 213
“as well as genetic networks underlying specific biological processe”
Self-citationTargeting pathways of C-tail-anchored proteins
Borgese, N., & Fasana, E. (2010) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2010.07.010 · Cited by 203
One library to make them all: streamlining the creation of yeast libraries via a SWAp-Tag strategy
Yofe, I., Weill, U., Meurer, M., Chuartzman, S. G., Zalckvar, E., Goldman, O., Ben‐Dor, S., Schütze, C., Wiedemann, N., Knop, M., et al. (2016) · Nature Methods · doi:10.1038/nmeth.3795 · Cited by 211
Self-citationA Network of Cytosolic Factors Targets SRP-Independent Proteins to the Endoplasmic Reticulum
Ast, T., Cohen, G., & Schuldiner, M. (2013) · Cell · doi:10.1016/j.cell.2013.02.003 · Cited by 193
“Genetic interaction studies (Costanzo et al., 2010; Jonikas et al., 2009; Schuldiner et al., 2005) revealed that the deletion of Ydj1 was synthetically lethal when combined with deletions of the GET pathway (Figure S5), hinting that the two might have parallel cellular functions.”
BackgroundSelf-citationLearning a Prior on Regulatory Potential from eQTL Data
Lee, S., Dudley, A. M., Drubin, D. A., Silver, P. A., Krogan, N. J., Pe’er, D., & Koller, D. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000358 · Cited by 195
“In particular, all of the data sets that we used to produce our benchmark set of regulator-target interactions (such as differential expression subject to regulator deletion or over-expression) can also be used as meta-features, as can other high-throughput data such as signaling interactions [50,51] or genetic intera…”
MethodSelf-citationSpokoini, R., Moldavski, O., Nahmias, Y., England, J. L., Schuldiner, M., & Kaganovich, D. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.08.024 · Cited by 191
Self-citationPaumi, C. M., Chuk, M., Snider, J. D., Štagljar, I., & Michaelis, S. (2009) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00020-09 · Cited by 194
“and for defining cellular pathways (12, 45, 67, 87, 140, 152).”
A gene ontology inferred from molecular networks
Dutkowski, J., Kramer, M., Surma, M. A., Balakrishnan, R., Cherry, J. M., Krogan, N. J., & Ideker, T. (2013) · Nature Biotechnology · doi:10.1038/nbt.2463 · Cited by 184
Exploring genetic suppression interactions on a global scale
van Leeuwen, J. S., Pons, C., Mellor, J. C., Yamaguchi, T. N., Friesen, H., Koschwanez, J. H., Ušaj, M. M., Pechlaner, M., Takar, M., Ušaj, M., et al. (2016) · Science · doi:10.1126/science.aag0839 · Cited by 182
“Although no significant functional enrichment was found for genes involved in RNA processing, nonsense-mediatedmRNA decay genes suppressed several DAmP alleles of essential genes (generated by decreased abundance by mRNA perturbation, DAmP) (22), which affect mRNA stability throughdisruption of their 3′untranslated re…”
BackgroundSelf-citationEvolution of phosphoregulation: comparison of phosphorylation patterns across yeast species
Beltrao, P., Trinidad, J. C., Fiedler, D., Roguev, A., Lim, W. A., Shokat, K. M., Burlingame, A. L., & Krogan, N. J. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000134 · Cited by 188
“using the E-MAP method as previously described, adding an additional 2,000 genetic interactions to the dataset”
Self-citationZhao, R., Kakihara, Y., Gribun, A., Huen, J., Yang, G., Khanna, M., Costanzo, M., Brost, R. L., Boone, C. M., Hughes, T. R., et al. (2008) · The Journal of Cell Biology · doi:10.1083/jcb.200709061 · Cited by 185
“When both Tah1 and Pih1 were mixed with the Rvb1/2 complex, coelution of Rvb1, Rvb2, Tah1, and Pih1 was observed over several fractions, indicating that the complex might be dynamic ( Fig.”
BackgroundMethodSelf-citationExposing the fitness contribution of duplicated genes
DeLuna, A., Vetsigian, K., Shoresh, N., Hegreness, M., Colón‐González, M., Chao, S., & Kishony, R. (2008) · Nature Genetics · doi:10.1038/ng.123 · Cited by 177
“The functional overlap between members of duplicate pairs manifests as deviations of the fitness cost of double deletions from the additive expectation based on the effects of single deletion”
BackgroundNetwork Inference, Analysis, and Modeling in Systems Biology
Albert, R. (2007) · The Plant Cell · doi:10.1105/tpc.107.054700 · Cited by 183
“Most applications derive biological insight through ‘‘guilt by association;’’ that is, they predict the function of unknown gene products by their association with recognized clusters (Schuldiner et al., 2005; Bjorklund et al., 2006).”
BackgroundCharacterization of mycobacterial virulence genes through genetic interaction mapping
Joshi, S. M., Pandey, A. K., Capite, N., Fortune, S. M., Rubin, E. J., & Sassetti, C. M. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0603179103 · Cited by 177
Arsenic Metabolism in Prokaryotic and Eukaryotic Microbes
Bhattacharjee, H., & Rosen, B. P. (2007) · Springer eBooks · doi:10.1007/7171_2006_086 · Cited by 177
A global analysis of genetic interactions in Caenorhabditis elegans
Byrne, A. B., Weirauch, M. T., Wong, V., Koeva, M., Dixon, S. J., Stuart, J. M., & Roy, P. J. (2007) · Journal of Biology · doi:10.1186/jbiol58 · Cited by 174
Metadata
- Authors
- Schuldiner, M., Collins, S. R., Thompson, N. J., Denic, V., Bhamidipati, A., Punna, T., Ihmels, J., Andrews, B., Boone, C., Greenblatt, J. F., Weissman, J. S., & Krogan, N. J.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of Toronto (CA)
- Corresponding author
- Weissman, Jonathan S.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2005-11
- Volume
- 123
- Issue
- 3
- Pages
- 507-519
- ISSN
- 0092-8674 (ISSN-L)
- OpenAlex
- W2042688172
- Cited by
- 870
- References
- 45
- Citations by year
- 2026: 12 · 2025: 12 · 2024: 15 · 2023: 19 · 2022: 23 · 2021: 30 · 2020: 34 · 2019: 30 · 2018: 36 · 2017: 41 · 2016: 25 · 2015: 47 · 2014: 54 · 2013: 57 · 2012: 61
- FWCI
- 20.53
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- genetic interaction mapping, sphingolipid metabolism, protein complex formation, essential genes, hierarchical clustering, Saccharomyces cerevisiae
- MeSH terms
- Endoplasmic Reticulum, Epistasis, Genetic, Glycosylation, Membrane Proteins, Mutation, Saccharomyces cerevisiae, Cluster Analysis, Receptors, Peptide, Computational Biology, Gene Expression Profiling, Protein Transport, Protein Interaction Mapping, Saccharomyces cerevisiae Proteins
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