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Science 320 (5882): 1465-1470
Copyright © 2008 by the American Association for the Advancement of Science
An in Vivo Map of the Yeast Protein Interactome
Kirill Tarassov,1*
Vincent Messier,1*
Christian R. Landry,1,2*
Stevo Radinovic,1*
Mercedes M. Serna Molina,1
Igor Shames,1
Yelena Malitskaya,1
Jackie Vogel,3
Howard Bussey,3
Stephen W. Michnick1,2
Abstract:
Protein interactions regulate the systems-level behavior of cells; thus, deciphering the structure and dynamics of protein interaction networks in their cellular context is a central goal in biology. We have performed a genome-wide in vivo screen for protein-protein interactions in Saccharomyces cerevisiae by means of a protein-fragment complementation assay (PCA). We identified 2770 interactions among 1124 endogenously expressed proteins. Comparison with previous studies confirmed known interactions, but most were not known, revealing a previously unexplored subspace of the yeast protein interactome. The PCA detected structural and topological relationships between proteins, providing an 8-nanometer–resolution map of dynamically interacting complexes in vivo and extended networks that provide insights into fundamental cellular processes, including cell polarization and autophagy, pathways that are evolutionarily conserved and central to both development and human health.
1 Département de Biochimie, Université de Montréal Casier postal 6128, Succursale Centre-ville, Montréal, Québec H3C 3J7, Canada.
2 Centre Robert-Cedergren, Bio-Informatique et Génomique, Université de Montréal, C.P. 6128, Succursale Centre-ville, Montréal, Québec H3C 3J7, Canada.
3 Department of Biology, McGill University, 1205 Avenue Dr. Penfield, Montréal, Québec H3A 1B1, Canada.
* These authors contributed equally to this work.
To whom correspondence should be addressed. E-mail: stephen.michnick{at}umontreal.ca
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- M.-K. Sung, G. Lim, D.-G. Yi, Y. J. Chang, E. B. Yang, K. Lee, and W.-K. Huh (2013)
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| Abstract »
| Full Text »
| PDF »
- A novel single-cell screening platform reveals proteome plasticity during yeast stress responses.
- M. Breker, M. Gymrek, and M. Schuldiner (2013)
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- D. Richmond, R. Rizkallah, F. Liang, M. M. Hurt, and Y. Wang (2013)
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| Abstract »
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| Abstract »
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| Abstract »
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- R. Ramanagoudr-Bhojappa, L. P. Blair, A. J. Tackett, and K. D. Raney (2013)
Nucleic Acids Res.
41, 1029-1046
| Abstract »
| Full Text »
| PDF »
- PrePPI: a structure-informed database of protein-protein interactions.
- Q. C. Zhang, D. Petrey, J. I. Garzon, L. Deng, and B. Honig (2013)
Nucleic Acids Res.
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| Abstract »
| Full Text »
| PDF »
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| PDF »
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| Abstract »
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- Integrative Proteomic Profiling of Protein Activity and Interactions Using Protein Arrays.
- S.-H. Jung, K. Lee, D.-H. Kong, W. J. Kim, Y.-M. Kim, and K.-S. Ha (2012)
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| Abstract »
| Full Text »
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- Proteomic Characterization of Phagosomal Membrane Microdomains During Phagolysosome Biogenesis and Evolution.
- G. Goyette, J. Boulais, N. J. Carruthers, C. R. Landry, I. Jutras, S. Duclos, J.-F. Dermine, S. W. Michnick, S. LaBoissiere, G. Lajoie, et al. (2012)
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| Abstract »
| Full Text »
| PDF »
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- A. M. C. Pittman, M. D. Lage, V. Poltoratsky, J. D. Vrana, A. Paiardini, A. Roncador, B. Cellini, R. M. Hughes, and C. L. Tucker (2012)
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| Abstract »
| Full Text »
| PDF »
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- J. Jakovljevic, U. Ohmayer, M. Gamalinda, J. Talkish, L. Alexander, J. Linnemann, P. Milkereit, and J. L. Woolford Jr. (2012)
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| Full Text »
| PDF »
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- Y. Wang, X. Zhang, H. Zhang, Y. Lu, H. Huang, X. Dong, J. Chen, J. Dong, X. Yang, H. Hang, et al. (2012)
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| Abstract »
| Full Text »
| PDF »
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- J. Talkish, J. Zhang, J. Jakovljevic, E. W. Horsey, and J. L. Woolford Jr (2012)
Nucleic Acids Res.
40, 8646-8661
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| Full Text »
| PDF »
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- A. Kamburov, U. Stelzl, and R. Herwig (2012)
Nucleic Acids Res.
40, W140-W146
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| Full Text »
| PDF »
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- U. Schlecht, M. Miranda, S. Suresh, R. W. Davis, and R. P. St.Onge (2012)
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| Full Text »
| PDF »
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- B. Stynen, H. Tournu, J. Tavernier, and P. Van Dijck (2012)
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- J.-P. Daniels, K. Gull, and B. Wickstead (2012)
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| Full Text »
| PDF »
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- Y. Zhang, L. Liu, X. Wu, X. An, J. Stubbe, and M. Huang (2011)
J. Biol. Chem.
286, 41499-41509
| Abstract »
| Full Text »
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- X. Yu, J. Ivanic, V. Memisevic, A. Wallqvist, and J. Reifman (2011)
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| Abstract »
| Full Text »
| PDF »
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27, 3024-3028
| Abstract »
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333, 532-533
| Abstract »
| Full Text »
| PDF »
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| Abstract »
| Full Text »
| PDF »
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| Abstract »
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124, 35-46
| Abstract »
| Full Text »
| PDF »
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- Y. V. Sun and S. L. R. Kardia (2010)
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19, 4345-4352
| Abstract »
| Full Text »
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| Abstract »
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| Abstract »
| Full Text »
| PDF »
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Nucleic Acids Res.
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| Abstract »
| Full Text »
| PDF »
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- E. Karaca, A. S. J. Melquiond, S. J. de Vries, P. L. Kastritis, and A. M. J. J. Bonvin (2010)
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| Abstract »
| Full Text »
| PDF »
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- K. Lasker, J. L. Phillips, D. Russel, J. Velazquez-Muriel, D. Schneidman-Duhovny, E. Tjioe, B. Webb, A. Schlessinger, and A. Sali (2010)
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9, 1689-1702
| Abstract »
| Full Text »
| PDF »
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- C. Stark, T.-C. Su, A. Breitkreutz, P. Lourenco, M. Dahabieh, B.-J. Breitkreutz, M. Tyers, and I. Sadowski (2010)
Database
2010, bap026
| Abstract »
| Full Text »
| PDF »
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- P. Q. Nguyen and J. J. Silberg (2010)
Protein Eng. Des. Sel.
23, 529-536
| Abstract »
| Full Text »
| PDF »
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- A. B. Mak, Z. Ni, J. A. Hewel, G. I. Chen, G. Zhong, K. Karamboulas, K. Blakely, S. Smiley, E. Marcon, D. Roudeva, et al. (2010)
Mol. Cell. Proteomics
9, 811-823
| Abstract »
| Full Text »
| PDF »
- Orm1 and Orm2 are conserved endoplasmic reticulum membrane proteins regulating lipid homeostasis and protein quality control.
- S. Han, M. A. Lone, R. Schneiter, and A. Chang (2010)
PNAS
107, 5851-5856
| Abstract »
| Full Text »
| PDF »
- The Genetic Landscape of a Cell.
- M. Costanzo, A. Baryshnikova, J. Bellay, Y. Kim, E. D. Spear, C. S. Sevier, H. Ding, J. L.Y. Koh, K. Toufighi, S. Mostafavi, et al. (2010)
Science
327, 425-431
| Abstract »
| Full Text »
| PDF »
- Toward the dynamic interactome: it's about time.
- T. M. Przytycka, M. Singh, and D. K. Slonim (2010)
Brief Bioinform
| Abstract »
| Full Text »
| PDF »
- Powering through ribosome assembly.
- B. S. Strunk and K. Karbstein (2009)
RNA
15, 2083-2104
| Abstract »
| Full Text »
| PDF »
- Stu1 inversely regulates kinetochore capture and spindle stability.
- J. Ortiz, C. Funk, A. Schafer, and J. Lechner (2009)
Genes & Dev.
23, 2778-2791
| Abstract »
| Full Text »
| PDF »
- Proteome Organization in a Genome-Reduced Bacterium.
- S. Kuhner, V. van Noort, M. J. Betts, A. Leo-Macias, C. Batisse, M. Rode, T. Yamada, T. Maier, S. Bader, P. Beltran-Alvarez, et al. (2009)
Science
326, 1235-1240
| Abstract »
| Full Text »
| PDF »
- Early-Arriving Syp1p and Ede1p Function in Endocytic Site Placement and Formation in Budding Yeast.
- H. E. M. Stimpson, C. P. Toret, A. T. Cheng, B. S. Pauly, and D. G. Drubin (2009)
Mol. Biol. Cell
20, 4640-4651
| Abstract »
| Full Text »
| PDF »
- An analytical platform for mass spectrometry-based identification and chemical analysis of RNA in ribonucleoprotein complexes.
- M. Taoka, Y. Yamauchi, Y. Nobe, S. Masaki, H. Nakayama, H. Ishikawa, N. Takahashi, and T. Isobe (2009)
Nucleic Acids Res.
37, e140
| Abstract »
| Full Text »
| PDF »
- Ribosome stalk assembly requires the dual-specificity phosphatase Yvh1 for the exchange of Mrt4 with P0.
- K.-Y. Lo, Z. Li, F. Wang, E. M. Marcotte, and A. W. Johnson (2009)
J. Cell Biol.
186, 849-862
| Abstract »
| Full Text »
| PDF »
- Mutations in the Saccharomyces cerevisiae Kinase Cbk1p Lead to a Fertility Defect That Can Be Suppressed by the Absence of Brr1p or Mpt5p (Puf5p), Proteins Involved in RNA Metabolism.
- M. Bourens, C. Panozzo, A. Nowacka, S. Imbeaud, M.-H. Mucchielli, and C. J. Herbert (2009)
Genetics
183, 161-173
| Abstract »
| Full Text »
| PDF »
- Budding Yeast SSD1-V Regulates Transcript Levels of Many Longevity Genes and Extends Chronological Life Span in Purified Quiescent Cells.
- L. Li, Y. Lu, L.-X. Qin, Z. Bar-Joseph, M. Werner-Washburne, and L. L. Breeden (2009)
Mol. Biol. Cell
20, 3851-3864
| Abstract »
| Full Text »
| PDF »
- A Rab escort protein integrates the secretion system with TOR signaling and ribosome biogenesis.
- J. Singh and M. Tyers (2009)
Genes & Dev.
23, 1944-1958
| Abstract »
| Full Text »
| PDF »
- The Ccr4-Pop2-NOT mRNA Deadenylase Contributes to Septin Organization in Saccharomyces cerevisiae.
- A. Traven, T. H. Beilharz, T. L. Lo, F. Lueder, T. Preiss, and J. Heierhorst (2009)
Genetics
182, 955-966
| Abstract »
| Full Text »
| PDF »
- Yeast Surface Two-hybrid for Quantitative in Vivo Detection of Protein-Protein Interactions via the Secretory Pathway.
- X. Hu, S. Kang, X. Chen, C. B. Shoemaker, and M. M. Jin (2009)
J. Biol. Chem.
284, 16369-16376
| Abstract »
| Full Text »
| PDF »
- A survey of available tools and web servers for analysis of protein-protein interactions and interfaces.
- N. Tuncbag, G. Kar, O. Keskin, A. Gursoy, and R. Nussinov (2009)
Brief Bioinform
10, 217-232
| Abstract »
| Full Text »
| PDF »
- Detection of Protein-Protein Interactions Through Vesicle Targeting.
- J. H. Boysen, S. Fanning, J. Newberg, R. F. Murphy, and A. P. Mitchell (2009)
Genetics
182, 33-39
| Abstract »
| Full Text »
| PDF »
- A Novel Hybrid Yeast-Human Network Analysis Reveals an Essential Role for FNBP1L in Antibacterial Autophagy.
- A. Huett, A. Ng, Z. Cao, P. Kuballa, M. Komatsu, M. J. Daly, D. K. Podolsky, and R. J. Xavier (2009)
J. Immunol.
182, 4917-4930
| Abstract »
| Full Text »
| PDF »
- A Novel Proteomics Approach for the Discovery of Chromatin-associated Protein Networks.
- J.-P. Lambert, L. Mitchell, A. Rudner, K. Baetz, and D. Figeys (2009)
Mol. Cell. Proteomics
8, 870-882
| Abstract »
| Full Text »
| PDF »
- The WASP Homologue Las17 Activates the Novel Actin-regulatory Activity of Ysc84 to Promote Endocytosis in Yeast.
- A. S. Robertson, E. G. Allwood, A. P.C. Smith, F. C. Gardiner, R. Costa, S. J. Winder, and K. R. Ayscough (2009)
Mol. Biol. Cell
20, 1618-1628
| Abstract »
| Full Text »
| PDF »
- The Cartographers toolbox: building bigger and better human protein interaction networks.
- C. M. Sanderson (2009)
Briefings in Functional Genomics
| Abstract »
| Full Text »
| PDF »
- How Perfect Can Protein Interactomes Be?.
- E. D. Levy, C. R. Landry, and S. W. Michnick (2009)
Science Signaling
2, pe11
| Abstract »
| Full Text »
| PDF »
- A Mutant Plasma Membrane Protein Is Stabilized Upon Loss of Yvh1, a Novel Ribosome Assembly Factor.
- Y. Liu and A. Chang (2009)
Genetics
181, 907-915
| Abstract »
| Full Text »
| PDF »
- Up-to-date catalogues of yeast protein complexes.
- S. Pu, J. Wong, B. Turner, E. Cho, and S. J. Wodak (2009)
Nucleic Acids Res.
37, 825-831
| Abstract »
| Full Text »
| PDF »
- The Yeast Vacuolar Membrane Proteome.
- E. Wiederhold, T. Gandhi, H. P. Permentier, R. Breitling, B. Poolman, and D. J. Slotboom (2009)
Mol. Cell. Proteomics
8, 380-392
| Abstract »
| Full Text »
| PDF »
- Precision and recall estimates for two-hybrid screens.
- H. Huang and J. S. Bader (2009)
Bioinformatics
25, 372-378
| Abstract »
| Full Text »
| PDF »
- Challenges and Rewards of Interaction Proteomics.
- S. J. Wodak, S. Pu, J. Vlasblom, and B. Seraphin (2009)
Mol. Cell. Proteomics
8, 3-18
| Abstract »
| Full Text »
| PDF »
- Combining multiple positive training sets to generate confidence scores for protein-protein interactions.
- J. Yu and R. L. Finley Jr (2009)
Bioinformatics
25, 105-111
| Abstract »
| Full Text »
| PDF »
- Assembly of the PtdIns 4-kinase Stt4 complex at the plasma membrane requires Ypp1 and Efr3.
- D. Baird, C. Stefan, A. Audhya, S. Weys, and S. D. Emr (2008)
J. Cell Biol.
183, 1061-1074
| Abstract »
| Full Text »
| PDF »
- Discovery of Cellular Regulation by Protein Degradation.
- A. Varshavsky (2008)
J. Biol. Chem.
283, 34469-34489
| Full Text »
| PDF »
- Voa1p Functions in V-ATPase Assembly in the Yeast Endoplasmic Reticulum.
- M. Ryan, L. A. Graham, and T. H. Stevens (2008)
Mol. Biol. Cell
19, 5131-5142
| Abstract »
| Full Text »
| PDF »
- Defining a Candidate Lung Cancer Gene.
- F. J. Kaye (2008)
J Natl Cancer Inst
100, 1564-1565
| Full Text »
| PDF »
- BIOCHEMISTRY: Not Comparable, But Complementary.
- L. J. Jensen and P. Bork (2008)
Science
322, 56-57
| Abstract »
| Full Text »
| PDF »
|
|