Predicting the fission yeast protein interaction network

G3: Genes, Genomes, Genetics

Volumn 2, Issue 4, 2012, Pages 453-467

  Pancaldi, Vera ^a,b   Saraç, Ömer S ^c   Rallis, Charalampos ^a,b   McLean, Janel R ^d   Převorovský, Martin ^a,b   Gould, Kathleen ^d   Beyer, Andreas ^c   Bähler, Jürg ^a,b  

^a Department of Genetics Evolution and Environment ^*  (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cbf11; Mak1 2 3 support vector machine random forest; TOR

Indexed keywords

EID: 84878883764     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.111.001560     Document Type: Article

References (96)

1. Aloy, P., and R. B. Russell, 2002 The third dimension for protein interactions and complexes. Trends Biochem. Sci. 27: 633-638.
2. Aoyama, K., H. Aiba, and T. Mizuno, 2001 Genetic analysis of the His-to- Asp phosphorelay implicated in mitotic cell cycle control: involvement of histidine-kinase genes of Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 65: 2347-2352.
3. Ashburner, M., C. Ball, J. Blake, D. Botstein, H. Butler et al., 2000 Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25: 25-29.
4. Babar, I. A., F. J. Slack, and J. B. Weidhaas, 2008 miRNA modulation of the cellular stress response. Future Oncol. 4: 289-298.
5. Bayne, E. H., S. A. White, A. Kagansky, D. A. Bijos, L. Sanchez-Pulido et al., 2010 Stc1: a critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140: 666-677.
6. Ben-Hur, A., and W. Noble, 2005 Kernel methods for predicting proteinprotein interactions. Bioinformatics 21: i38-i46.
7. Ben-Hur, A., and W. Noble, 2006 Choosing negative examples for the prediction of protein-protein interactions. BMC Bioinformatics 7: S2.
8. Bjornsti, M.-A., and P. J. Houghton, 2004 The TOR pathway: a target for cancer therapy. Nat. Rev. Cancer 4: 335-348.
9. Bonawitz, N. D., M. Chatenay-Lapointe, Y. Pan, and G. S. Shadel, 2007 Reduced TOR signaling extends chronological life span via increased respiration and upregulation of mitochondrial gene expression. Cell Metab. 5: 265-277.
10. Boyle, E. I., S. Weng, J. Gollub, H. Jin, D. Botstein et al., 2004 GO::Term- Finder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20: 3710-3715.
11. Braun, P., M. Tasan, M. Dreze, M. Barrios-Rodiles, I. Lemmens et al., 2009 An experimentally derived confidence score for binary proteinprotein interactions. Nat. Methods 6: 91-97.
12. Breiman, L., 2001 Random Forests. Mach. Learn. 45: 5-32.
13. Breitkreutz, A., H. Choi, J. R. Sharom, L. Boucher, V. Neduva et al., 2010 A global protein kinase and phosphatase interaction network in yeast. Science 328: 1043-1046.
14. Buck, V., J. Quinn, T. Soto Pino, H. Martin, J. Saldanha et al., 2001 Peroxide sensors for the fission yeast stress-activated mitogenactivated protein kinase pathway. Mol. Biol. Cell 12: 407-419.
15. Bühler, M., N. Spies, D. P. Bartel, and D. Moazed, 2008 TRAMP-mediated RNA surveillance prevents spurious entry of RNAs into the Schizosaccharomyces pombe siRNA pathway. Nat. Struct. Mol. Biol. 15: 1015-1023.
16. Burger, L., and E. van Nimwegen, 2008 Accurate prediction of proteinprotein interactions from sequence alignments using a Bayesian method. Mol. Syst. Biol. 4: 165.
17. Burguete, A. S., T. D. Fenn, A. T. Brunger, and S. R. Pfeffer, 2008 Rab and Arl GTPase family members cooperate in the localization of the golgin GCC185. Cell 132: 286-298.
18. Cao, Y., J. A. Espinola, E. Fossale, A. C. Massey, A. M. Cuervo et al., 2006 Autophagy is disrupted in a knock-in mouse model of juvenile neuronal ceroid lipofuscinosis. J. Biol. Chem. 281: 20483-20493.
19. Chen, D., W. M. Toone, J. Mata, R. Lyne, G. Burns et al., 2003 Global transcriptional responses of fission yeast to environmental stress. Mol. Biol. Cell 14: 214-229.
20. Chen, D., C. R. Wilkinson, S. Watt, C. J. Penkett, W. M. Toone et al., 2008 Multiple pathways differentially regulate global oxidative stress responses in fission yeast. Mol. Biol. Cell 19: 308-317.
21. Cortes, C., and V. Vapnik, 1995 Support-vector networks. Mach. Learn. 20: 273-297.
22. Cuenca-Bono, B., V. Garcia-Molinero, P. Pascual-Garcia, E. Garcia-Oliver, A. Llopis et al., 2010 A novel link between Sus1 and the cytoplasmic mRNA decay machinery suggests a broad role in mRNA metabolism. BMC Cell Biol. 11: 19.
23. De Bodt, S., S. Proost, K. Vandepoele, P. Rouze, and Y. Van de Peer, 2009 Predicting protein-protein interactions in Arabidopsis thaliana through integration of orthology, gene ontology and co-expression. BMC Genomics 10: 288.
24. Desikan, R., J. Horak, C. Chaban, V. Mira-Rodado, J. Witthoft et al., 2008 The histidine kinase AHK5 integrates endogenous and environmental signals in Arabidopsis guard cells. PLoS ONE 3: e2491.
25. Dixon, S. J., Y. Fedyshyn, J. L. Koh, T. S. Prasad, C. Chahwan et al., 2008 Significant conservation of synthetic lethal genetic interaction networks between distantly related eukaryotes. Proc. Natl. Acad. Sci. USA 105: 16653-16658.
26. Fernandes, L. P., A. Annibale, J. Kleinjung, A. C. C. Coolen, and F. Fraternali, 2010 Protein networks reveal detection bias and species consistency when analysed by information-theoretic methods. PLoS ONE 5: e12083.
27. Formstecher, E., S. Aresta, V. Collura, A. Hamburger, A. Meil et al., 2005 Protein interaction mapping: a Drosophila case study. Genome Res. 15: 376-384.
28. Freeman-Cook, L. L., E. B. Gomez, E. J. Spedale, J. Marlett, S. L. Forsburg et al., 2005 Conserved locus-specific silencing functions of Schizosaccharomyces pombe sir2+. Genetics 169: 1243-1260.
29. Gan, B. Q., and B. L. Tang, 2010 Sirt1's beneficial roles in neurodegenerative diseases - a chaperonin containing TCP-1 (CCT) connection?. Aging Cell 9: 924-929.
30. Gavin, A.-C., M. Bosche, R. Krause, P. Grandi, M. Marzioch et al., 2002 Functional organization of the yeast proteome by systematic analysis of protein complexes. Nature 415: 141-147.
31. Gavin, A.-C., K. Maeda, and S. Kühner, 2011 Recent advances in charting protein-protein interaction: mass spectrometry-based approaches. Curr. Opin. Biotechnol. 22: 42-49.
32. Hart, G., A. Ramani, and E. Marcotte, 2006 How complete are current yeast and human protein-interaction networks? Genome Biol. 7: 120.
33. Hayashi, A., D. Da-Qiao, C. Tsutsumi, Y. Chikashige, H. Masuda et al., 2009 Localization of gene products using a chromosomally tagged GFPfusion library in the fission yeast Schizosaccharomyces pombe. Genes Cells 14: 217-225.
34. Helmlinger, D., S. Marguerat, J. Villén, S. P. Gygi, J. Bähler et al., 2008 The S. pombe SAGA complex controls the switch from proliferation to sexual differentiation through the opposing roles of its subunits Gcn5 and Spt8. Genes Dev. 22: 3184-3195.
35. Helmlinger, D., S. Marguerat, J. Villen, D. L. Swaney, S. P. Gygi et al., 2011 Tra1 has specific regulatory roles, rather than global functions, within the SAGA co-activator complex. EMBO J. 30: 2843-2852.
36. Ingvarsdottir, K., N. J. Krogan, N. C. T. Emre, A. Wyce, N. J. Thompson et al., 2005 H2B ubiquitin protease Ubp8 and Sgf11 constitute a discrete functional module within the Saccharomyces cerevisiae SAGA complex. Mol. Cell. Biol. 25: 1162-1172.
37. Ito, T., T. Chiba, R. Ozawa, M. Yoshida, M. Hattori et al., 2001 A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98: 4569-4574.
38. Jansen, R., H. Yu, D. Greenbaum, Y. Kluger, N. J. Krogan et al., 2003 A Bayesian networks approach for predicting protein-protein interactions from genomic data. Science 302: 449-453.
39. Jensen, L. J., M. Kuhn, M. Stark, S. Chaffron, C. Creevey et al., 2009 STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37: D412-D416.
40. Koutelou, E., C. L. Hirsch, and S. Y. R. Dent, 2010 Multiple faces of the SAGA complex. Curr. Opin. Cell Biol. 22: 374-382.
41. Krell, T., J. Lacal, A. Busch, H. Silva-Jimenez, M. E. Guazzaroni et al., 2010 Bacterial sensor kinases: diversity in the recognition of environmental signals. Annu. Rev. Microbiol. 64: 539-559.
42. Krogan, N. J., G. Cagney, H. Yu, G. Zhong, X. Guo et al., 2006 Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637-643.
43. Lackner, D. H., T. H. Beilharz, S. Marguerat, J. Mata, S. Watt et al., 2007 A network of multiple regulatory layers shapes gene expression in fission yeast. Mol. Cell 26: 145-155.
44. Lee, C. H., K. Inoki, M. Karbowniczek, E. Petroulakis, N. Sonenberg et al., 2007 Constitutive mTOR activation in TSC mutants sensitizes cells to energy starvation and genomic damage via p53. EMBO J. 26: 4812-4823.
45. Li, S., C.M. Armstrong, N. Bertin, H. Ge, S.Milstein et al., 2004 Amap of the interactome network of the metazoan C. elegans. Science 303: 540-543.
46. Liu, B., L. Larsson, A. Caballero, X. Hao, D. Öling et al., 2010 The polarisome is required for segregation and retrograde transport of protein aggregates. Cell 140: 257-267.
47. Lopez-Maury, L., S. Marguerat, and J. Bahler, 2008 Tuning gene expression to changing environments: from rapid responses to evolutionary adaptation. Nat. Rev. Genet. 9: 583-593.
48. Ma, Z.-Q., S. Dasari, M. C. Chambers, M. D. Litton, S. M. Sobecki et al., 2009 IDPicker 2.0: improved protein assembly with high discrimination peptide identification filtering. J. Proteome Res. 8: 3872-3881.
49. Martienssen, R. A., M. Zaratiegui, and D. B. Goto, 2005 RNA interference and heterochromatin in the fission yeast Schizosaccharomyces pombe. Trends Genet. 21: 450-456.
50. Matsuyama, A., R. Arai, Y. Yashiroda, A. Shirai, A. Kamata et al., 2006 ORFeome cloning and global analysis of protein localization in the fission yeast Schizosaccharomyces pombe. Nat. Biotechnol. 24: 841-847.
51. McDonald, W. H., R. Ohi, D. T.Miyamoto, T. J. Mitchison, and J. R. Yates, 2002 Comparison of three directly coupled HPLC MS/MS strategies for identification of proteins from complex mixtures: single-dimension LC-MS/MS, 2-phase MudPIT, and 3-phase MudPIT. Int. J. Mass Spectrom. 219: 245-251.
52. Motoyama, T., K. Kadokura, T. Ohira, A. Ichiishi, M. Fujimura et al., 2005 A two-component histidine kinase of the rice blast fungus is involved in osmotic stress response and fungicide action. Fungal Genet. Biol. 42: 200-212.
53. Mukaiyama, H., M. Nakase, T. Nakamura, Y. Kakinuma, and K. Takegawa, 2010 Autophagy in the fission yeast Schizosaccharomyces pombe. FEBS Lett. 584: 1327-1334.
54. Nakamichi, N., H. Yanada, H. Aiba, K. Aoyama, R. Ohmiya et al., 2003 Characterization of the Prr1 response regulator with special reference to sexual development in Schizosaccharomyces pombe. Biosci. Biotechnol. Biochem. 67: 547-555.
55. Pan, Y., and G. S. Shadel, 2009 Extension of chronological life span by reduced TOR signaling requires down-regulation of Sch9p and involves increased mitochondrial OXPHOS complex density. Aging (Albany NY) 1: 131-145.
56. Pancaldi, V., F. Schubert, and J. Bahler, 2010 Meta-analysis of genome regulation and expression variability across hundreds of environmental and genetic perturbations in fission yeast. Mol. Biosyst. 6: 543-552.
57. Patrick Walton, S., M. Wu, J. A. Gredell, and C. Chan, 2010 Designing highly active siRNAs for therapeutic applications. FEBS J. 277: 4806-4813.
58. Perez, P., and S. A. Rincón, 2010 Rho GTPases: regulation of cell polarity and growth in yeasts. Biochem. J. 426: 243-253.
59. Petersen, J., 2009 TOR signalling regulates mitotic commitment through stress-activated MAPK and Polo kinase in response to nutrient stress. Biochem. Soc. Trans. 37: 273-277.
60. Pitre, S., M. Alamgir, J. R. Green, M. Dumontier, F. Dehne et al., 2008 Computational methods for predicting protein-protein interactions, pp. 247-267 in Protein-Protein Interaction, edited by M. Werther and H. Seitz. Springer, Berlin/Heidelberg.
61. Posas, F., S. M. Wurgler-Murphy, T. Maeda, E. A. Witten, T. C. Thai et al., 1996 Yeast HOG1 MAP kinase cascade is regulated by a multistep phosphorelay mechanism in the SLN1-YPD1-SSK1 "two-component" osmosensor. Cell 86: 865-875.
62. Prevorovský, M., T. Grousl, J. Stanurová, J. Rynes, W. Nellen et al., 2009 Cbf11 and Cbf12, the fission yeast CSL proteins, play opposing roles in cell adhesion and coordination of cell and nuclear division. Exp. Cell Res. 315: 1533-1547.
63. Qi, Y., Z. Bar-Joseph, and J. Klein-Seetharaman, 2006 Evaluation of different biological data and computational classification methods for use in protein interaction prediction. Proteins 63: 490-500.
64. Rakheja, D., S. B. Narayan, and M. J. Bennett, 2008 The function of CLN3P, the Batten disease protein. Mol. Genet. Metab. 93: 269-274.
65. Rigaut, G., A. Schevchenko, B. Rutz, M. Wilm, M. Mann et al., 1999 A generic purification method for protein complex characterization and proteome exploration. Nat. Biotech. 17: 1030-1032.
66. Risson, V., L. Mazelin, M. Roceri, H. Sanchez, V. Moncollin et al., 2009 Muscle inactivation of mTOR causes metabolic and dystrophin defects leading to severe myopathy. J. Cell Biol. 187: 859-874.
67. Roberts-Galbraith, R. H., J.-S. Chen, J. Wang, and K. L. Gould, 2009 The SH3 domains of two PCH family members cooperate in assembly of the Schizosaccharomyces pombe contractile ring. J. Cell Biol. 184: 113-127.
68. Roguev, A., A. Shevchenko, D. Schaft, H. Thomas, A. F. Stewart et al., 2004 A comparative analysis of an orthologous proteomic environment in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Mol. Cell. Proteomics 3: 125-132.
69. Roguev, A., S. Bandyopadhyay, M. Zofall, K. Zhang, T. Fischer et al., 2008 Conservation and rewiring of functional modules revealed by an epistasis map in fission yeast. Science 322: 405-410.
70. Rowland, S. L., and G. F. King, 2007 Histidine kinases as antimicrobial targets: prospects and pitfalls. Mini Rev. Med. Chem. 7: 1144-1154.
71. Rual, J.-F., K. Venkatesan, T. Hao, T. Hirozane-Kishikawa, A. Dricot et al., 2005 Towards a proteome-scale map of the human protein-protein interaction network. Nature 437: 1173-1178.
72. Santos, J. L., and K. Shiozaki, 2001 Fungal histidine kinases. Sci. STKE 2001: re1.
73. Schreiber, M., I. Res, and A. Matter, 2009 Protein kinases as antibacterial targets. Curr. Opin. Cell Biol. 21: 325-330.
74. Shen, J., J. Zhang, X. Luo, W. Zhu, K. Yu et al., 2007 Predicting proteinprotein interactions based only on sequences information. Proc. Natl. Acad. Sci. USA 104: 4337-4341.
75. Shevchenko, A., A. Roguev, D. Schaft, L. Buchanan, B. Habermann et al., 2008 Chromatin Central: towards the comparative proteome by accurate mapping of the yeast proteomic environment. Genome Biol. 9(11): R167.
76. Singh, R., D. Park, J. Xu, R. Hosur, and B. Berger, 2010 Struct2Net: a web service to predict protein-protein interactions using a structure-based approach. Nucleic Acids Res. 38: W508-W515.
77. Smoot, M. E., K. Ono, J. Ruscheinski, P.-L. Wang, and T. Ideker, 2011 Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 27: 431-432.
78. Song, K., K. E. Mach, C.-Y. Chen, T. Reynolds, and C. F. Albright, 1996 A novel suppressor of ras1 in fission yeast, byr4, is a dosage-dependent inhibitor of cytokinesis. J. Cell Biol. 133: 1307-1319.
79. Stark, C., B.-J. Breitkreutz, A. Chatr-aryamontri, L. Boucher, R. Oughtred et al., 2011 The BioGRID Interaction Database: 2011 update. Nucleic Acids Res. 39: D698-D704.
80. Stelzl, U., U. Worm, M. Lalowski, C. Haenig, F. Brembeck et al., 2005 A human protein-protein interaction network: a resource for annotating the proteome. Cell 122: 957-968.
81. Stephenson, K., and J. A. Hoch, 2002 Two-component and phosphorelay signal-transduction systems as therapeutic targets. Curr. Opin. Pharmacol. 2: 507-512.
82. Stephenson, K., and J. A. Hoch, 2004 Developing inhibitors to selectively target two-component and phosphorelay signal transduction systems of pathogenic microorganisms. Curr. Med. Chem. 11: 765-773.
83. Strobl, C., A.-L. Boulesteix, T. Kneib, T. Augustin, and A. Zeileis, 2008 Conditional variable importance for random forests. BMC Bioinformatics 9: 307.
84. Szklarczyk, D., A. Franceschini, M. Kuhn, M. Simonovic, A. Roth et al., 2011 The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res. 39: D561-D568.
85. Tabb, D. L., C. G. Fernando, and M. C. Chambers, 2007 MyriMatch: highly accurate tandem mass spectral peptide identification by multivariate hypergeometric analysis. J. Proteome Res. 6: 654-661.
86. Tatebe, H., S. Morigasaki, S. Murayama, C. T. Zeng, and K. Shiozaki, 2010 Rab-Family GTPase regulates TOR complex 2 signaling in fission yeast. Curr. Biol. 20: 1975-1982.
87. Tuxworth, R. I., H. Chen, V. Vivancos, N. Carvajal, X. Huang et al., 2011 The Batten disease gene CLN3 is required for the response to oxidative stress. Hum. Mol. Genet. 20: 2037-2047.
88. Uetz, P., L. Giot, G. Cagney, T. Mansfield, R. Judson et al., 2000 A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403: 623-627.
89. Urao, T., K. Yamaguchi-Shinozaki, and K. Shinozaki, 2001 Plant histidine kinases: an emerging picture of two-component signal transduction in hormone and environmental responses. Sci. STKE 2001: re18.
90. Wang, J., C. Li, E. Wang, and X. Wang, 2009a Uncovering the rules for protein-protein interactions from yeast genomic data. Proc. Natl. Acad. Sci. USA 106: 3752-3757.
91. Wang, T., U. Lao, and B. A. Edgar, 2009b TOR-mediated autophagy regulates cell death in Drosophila neurodegenerative disease. J. Cell Biol. 186: 703-711.
92. Wedaman, K. P., A. Reinke, S. Anderson, J. Yates 3rd, J. M. McCaffery et al., 2003 Tor kinases are in distinct membrane-associated protein complexes in Saccharomyces cerevisiae. Mol. Biol. Cell 14: 1204-1220.
93. Wood, V., 2006 Schizosaccharomyces pombe comparative genomics; from sequence to systems, pp. 233-285 in Comparative Genomics: Using Fungi as Models, edited by P. Sunnerhagen and J. Piskur. Springer, Berlin/Heidelberg.
94. Yu, H., P. Braun, M. A. Yildirim, I. Lemmens, K. Venkatesan et al., 2008 High-quality binary protein interaction map of the yeast interactome network. Science 322: 104-110.
95. Yu, J., M. Guo, C. J. Needham, Y. Huang, L. Cai et al., 2010 Simple sequencebased kernels do not predict protein-protein interactions. Bioinformatics 26: 2610-2614.
96. Zhang, B., M. C. Chambers, and D. L. Tabb, 2007 Proteomic parsimony through bipartite graph analysis improves accuracy and transparency. J. Proteome Res. 6: 3549-3557.