Towards Systematic Discovery of Signaling Networks in Budding Yeast Filamentous Growth Stress Response Using Interventional Phosphorylation Data

PLoS Computational Biology

Volumn 9, Issue 6, 2013, Pages

  Zhang, Yan ^a   Kweon, Hye Kyong ^a   Shively, Christian ^b   Kumar, Anuj ^b   Andrews, Philip C ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; MOLECULAR BIOLOGY; PIPELINES; PROTEINS; SIGNAL TRANSDUCTION; SIGNALING; YEAST;

BUDDING YEASTS; FILAMENTOUS GROWTH; GROWTH STRESS; INTERVENTIONAL; META-ANALYSIS; PHOSPHOPROTEOMES; PHOSPHOPROTEOMICS; REVERSIBLE PHOSPHORYLATION; SIGNALING NETWORKS; STRESSES RESPONSE;

PHOSPHORYLATION;

FUNGAL PROTEIN; PROTEIN HSP42P; PROTEIN NTH1P; PROTEIN PBI2P; PROTEIN PDR12P; PROTEIN RCN2P; UNCLASSIFIED DRUG;

ARTICLE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; FUNGAL CELL; FUNGUS GROWTH; FUNGUS MUTANT; GENE MUTATION; GENE REGULATORY NETWORK; ISOTOPE LABELING; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; QUANTITATIVE STUDY; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 84879533104     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003077     Document Type: Article

References (99)

1. Ptacek J, Devgan G, Michaud G, Zhu H, Zhu X, et al. (2005) Global analysis of protein phosphorylation in yeast. Nature 438: 679-684 doi:10.1038/nature04187.
2. Manning G, Plowman GD, Hunter T, Sudarsanam S, (2002) Evolution of protein kinase signaling from yeast to man. Trends in biochemical sciences 27: 514-520.
3. Ficarro SB, McCleland ML, Stukenberg PT, Burke DJ, Ross MM, et al. (2002) Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae. Nature biotechnology 20: 301-305 doi:10.1038/nbt0302-301.
4. Cohen P, (2000) The regulation of protein function by multisite phosphorylation-a 25 year update. Trends in biochemical sciences 25: 596-601.
5. Bodenmiller B, Wanka S, Kraft C, Urban J, Campbell D, et al. (2010) Phosphoproteomic analysis reveals interconnected system-wide responses to perturbations of kinases and phosphatases in yeast. Science signaling 3: rs4 doi:10.1126/scisignal.2001182.
6. Breitkreutz A, Choi H, Sharom JR, Boucher L, Neduva V, et al. (2010) A global protein kinase and phosphatase interaction network in yeast. Science 328: 1043-1046 doi:10.1126/science.1176495.
7. Yachie N, Saito R, Sugiyama N, Tomita M, Ishihama Y, (2011) Integrative features of the yeast phosphoproteome and protein-protein interaction map. PLoS computational biology 7: e1001064 doi:10.1371/journal.pcbi.1001064.
8. Schmelzle K, White FM, (2006) Phosphoproteomic approaches to elucidate cellular signaling networks. Current opinion in biotechnology 17: 406-414 doi:10.1016/j.copbio.2006.06.004.
9. Macek B, Mann M, Olsen JV, (2009) Global and site-specific quantitative phosphoproteomics: principles and applications. Annual review of pharmacology and toxicology 49: 199-221 doi:10.1146/annurev.pharmtox.011008.145606.
10. Kosako H, Nagano K, (2011) Quantitative phosphoproteomics strategies for understanding protein kinase-mediated signal transduction pathways. Expert review of proteomics 8: 81-94 doi:10.1586/epr.10.104.
11. Bantscheff M, Schirle M, Sweetman G, Rick J, Kuster B, (2007) Quantitative mass spectrometry in proteomics: a critical review. Analytical and bioanalytical chemistry 389: 1017-1031 doi:10.1007/s00216-007-1486-6.
12. Ong S-E, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, et al. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Molecular & cellular proteomics: MCP 1: 376-386.
13. Mann M, (2006) Functional and quantitative proteomics using SILAC. Nature reviews Molecular cell biology 7: 952-958 doi:10.1038/nrm2067.
14. Gimeno CJ, Ljungdahl PO, Styles CA, Fink GR, (1992) Unipolar cell divisions in the yeast S. cerevisiae lead to filamentous growth: regulation by starvation and RAS. Cell 68: 1077-1090.
15. Palecek SP, Parikh AS, Kron SJ, (2002) Sensing, signalling and integrating physical processes during Saccharomyces cerevisiae invasive and filamentous growth. Microbiology (Reading, England) 148: 893-907.
16. Lorenz MC, Cutler NS, Heitman J, (2000) Characterization of alcohol-induced filamentous growth in Saccharomyces cerevisiae. Molecular biology of the cell 11: 183-199.
17. Cullen PJ, Sprague GF, (2000) Glucose depletion causes haploid invasive growth in yeast. Proceedings of the National Academy of Sciences of the United States of America 97: 13619-13624 doi:10.1073/pnas.240345197.
18. Kron SJ, Styles CA, Fink GR, (1994) Symmetric cell division in pseudohyphae of the yeast Saccharomyces cerevisiae. Molecular biology of the cell 5: 1003-1022.
19. Jin R, Dobry CJ, McCown PJ, Kumar A, (2008) Large-scale analysis of yeast filamentous growth by systematic gene disruption and overexpression. Molecular biology of the cell 19: 284-296 doi:10.1091/mbc.E07-05-0519.
20. Thorner J, Truckses D, Garrenton L, (2012) Filamentous Growth Pathway in Yeast. Science Signaling Database of Cell Signaling Available: http://stke.sciencemag.org/cgi/cm/stkecmCMP_14554. Accessed 3 February 1BC.
21. Ceccato-Antonini SR, Sudbery PE, (2004) Filamentous growth in Saccharomyces cerevisiae. Brazilian Journal of Microbiology 35: 173-181 doi:10.1590/S1517-83822004000200001.
22. Saito H, (2010) Regulation of cross-talk in yeast MAPK signaling pathways. Current opinion in microbiology 13: 677-683 doi:10.1016/j.mib.2010.09.001.
23. Pan X, Heitman J, (1999) Cyclic AMP-dependent protein kinase regulates pseudohyphal differentiation in Saccharomyces cerevisiae. Molecular and cellular biology 19: 4874-4887.
24. Robertson LS, Fink GR, (1998) The three yeast A kinases have specific signaling functions in pseudohyphal growth. Proceedings of the National Academy of Sciences of the United States of America 95: 13783-13787.
25. Batlle M, Lu A, Green DA, Xue Y, Hirsch JP, (2003) Krh1p and Krh2p act downstream of the Gpa2p G(alpha) subunit to negatively regulate haploid invasive growth. Journal of cell science 116: 701-710.
26. Bharucha N, Ma J, Dobry CJ, Lawson SK, Yang Z, et al. (2008) Analysis of the yeast kinome reveals a network of regulated protein localization during filamentous growth. Molecular biology of the cell 19: 2708-2717 doi:10.1091/mbc.E07-11-1199.
27. Kanehisa M, Goto S, (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic acids research 28: 27-30.
28. Edgington NP, Blacketer MJ, Bierwagen TA, Myers AM, (1999) Control of Saccharomyces cerevisiae filamentous growth by cyclin-dependent kinase Cdc28. Molecular and cellular biology 19: 1369-1380.
29. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS, (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20: 3551-3567 doi:;10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2.
30. Cox J, Mann M, (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature biotechnology 26: 1367-1372 doi:10.1038/nbt.1511.
31. Tseng GC, Wong WH, (2005) Tight clustering: a resampling-based approach for identifying stable and tight patterns in data. Biometrics 61: 10-16.
32. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature genetics 25: 25-29 doi:10.1038/75556.
33. Huang DW, Sherman BT, Lempicki RA, (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic acids research 37: 1-13 doi:10.1093/nar/gkn923.
34. Huang DW, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nature protocols 4: 44-57 doi:10.1038/nprot.2008.211.
35. Fisher RA (1925) Statistical methods for research workers. Boyd OA, editor. Edinburgh: Oliver and Boyd.
36. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B 57: 289-300.
37. Li J, Tseng GC, (2011) An adaptively weighted statistic for detecting differential gene expression when combining multiple transcriptomic studies. The Annals of Applied Statistics 5: 994-1019 doi:10.1214/10-AOAS393.
38. Zähringer H, Burgert M, Holzer H, Nwaka S, (1997) Neutral trehalase Nth1p of Saccharomyces cerevisiae encoded by the NTH1 gene is a multiple stress responsive protein. FEBS letters 412: 615-620.
39. François J, Parrou JL, (2001) Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiology Reviews 25: 125-145 doi:10.1016/S0168-6445(00)00059-0.
40. Galello F, Portela P, Moreno S, Rossi S, (2010) Characterization of substrates that have a differential effect on Saccharomyces cerevisiae protein kinase A holoenzyme activation. The Journal of biological chemistry 285: 29770-29779 doi:10.1074/jbc.M110.120378.
41. Panni S, Landgraf C, Volkmer-Engert R, Cesareni G, Castagnoli L, (2008) Role of 14-3-3 proteins in the regulation of neutral trehalase in the yeast Saccharomyces cerevisiae. FEMS yeast research 8: 53-63 doi:10.1111/j.1567-1364.2007.00312.x.
42. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, et al. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637-643 doi:10.1038/nature04670.
43. Santangelo GM, (2006) Glucose signaling in Saccharomyces cerevisiae. Microbiology and molecular biology reviews: MMBR 70: 253-282 doi:10.1128/MMBR.70.1.253-282.2006.
44. Estruch F, (2000) Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS microbiology reviews 24: 469-486.
45. Norbeck J, Blomberg A, (2000) The level of cAMP-dependent protein kinase A activity strongly affects osmotolerance and osmo-instigated gene expression changes in Saccharomyces cerevisiae. Yeast (Chichester, England) 16: 121-137 doi:;10.1002/(SICI)1097-0061(20000130)16:2<121::AID-YEA511>3.0.CO;2-A.
46. Barbieri M, Bonafè M, Franceschi C, Paolisso G, (2003) Insulin/IGF-I-signaling pathway: an evolutionarily conserved mechanism of longevity from yeast to humans. American journal of physiology Endocrinology and metabolism 285: E1064-71 doi:10.1152/ajpendo.00296.2003.
47. Roberts RL, Mösch HU, Fink GR, (1997) 14-3-3 proteins are essential for RAS/MAPK cascade signaling during pseudohyphal development in S. cerevisiae. Cell 89: 1055-1065.
48. Gancedo JM, (2001) Control of pseudohyphae formation in Saccharomyces cerevisiae. FEMS microbiology reviews 25: 107-123.
49. Bertram PG, Zeng C, Thorson J, Shaw AS, Zheng XF, (1998) The 14-3-3 proteins positively regulate rapamycin-sensitive signaling. Current biology: CB 8: 1259-1267.
50. Irie K, Gotoh Y, Yashar BM, Errede B, Nishida E, et al. (1994) Stimulatory effects of yeast and mammalian 14-3-3 proteins on the Raf protein kinase. Science (New York, NY) 265: 1716-1719.
51. Gelperin D, Weigle J, Nelson K, Roseboom P, Irie K, et al. (1995) 14-3-3 proteins: potential roles in vesicular transport and Ras signaling in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America 92: 11539-11543.
52. Wotton D, Freeman K, Shore D, (1996) Multimerization of Hsp42p, a novel heat shock protein of Saccharomyces cerevisiae, is dependent on a conserved carboxyl-terminal sequence. The Journal of biological chemistry 271: 2717-2723.
53. Von Mering C, Huynen M, Jaeggi D, Schmidt S, Bork P, et al. (2003) STRING: a database of predicted functional associations between proteins. Nucleic Acids Research 31: 258-261.
54. Szklarczyk D, Franceschini A, Kuhn M, Simonovic M, Roth A, et al. (2011) The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Research 39: D561-8 doi:10.1093/nar/gkq973.
55. Cherry JM, Hong EL, Amundsen C, Balakrishnan R, Binkley G, et al. (2011) Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic acids research doi:10.1093/nar/gkr1029.
56. SGD project (2012) Saccharomyces Genome Database. Available: http://www.yeastgenome.org/. Accessed 16 August 2012.
57. Nwaka S, Holzer H, (1998) Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Progress in nucleic acid research and molecular biology 58: 197-237.
58. Yoshikawa K, Tanaka T, Furusawa C, Nagahisa K, Hirasawa T, et al. (2009) Comprehensive phenotypic analysis for identification of genes affecting growth under ethanol stress in Saccharomyces cerevisiae. FEMS yeast research 9: 32-44 doi:10.1111/j.1567-1364.2008.00456.x.
59. Lee M-W, Kim B-J, Choi H-K, Ryu M-J, Kim S-B, et al. (2007) Global protein expression profiling of budding yeast in response to DNA damage. Yeast (Chichester, England) 24: 145-154 doi:10.1002/yea.1446.
60. Hatzixanthis K, Mollapour M, Seymour I, Bauer BE, Krapf G, et al. (2003) Moderately lipophilic carboxylate compounds are the selective inducers of the Saccharomyces cerevisiae Pdr12p ATP-binding cassette transporter. Yeast (Chichester, England) 20: 575-585 doi:10.1002/yea.981.
61. Schüller C, Mamnun YM, Mollapour M, Krapf G, Schuster M, et al. (2004) Global phenotypic analysis and transcriptional profiling defines the weak acid stress response regulon in Saccharomyces cerevisiae. Molecular biology of the cell 15: 706-720 doi:10.1091/mbc.E03-05-0322.
62. Kren A, Mamnun YM, Bauer BE, Schüller C, Wolfger H, et al. (2003) War1p, a novel transcription factor controlling weak acid stress response in yeast. Molecular and cellular biology 23: 1775-1785.
63. Holyoak CD, Thompson S, Ortiz Calderon C, Hatzixanthis K, Bauer B, et al. (2000) Loss of Cmk1 Ca(2+)-calmodulin-dependent protein kinase in yeast results in constitutive weak organic acid resistance, associated with a post-transcriptional activation of the Pdr12 ATP-binding cassette transporter. Molecular microbiology 37: 595-605.
64. Kopp M, Müller H, Holzer H, (1993) Molecular analysis of the neutral trehalase gene from Saccharomyces cerevisiae. The Journal of biological chemistry 268: 4766-4774.
65. Slusarewicz P, Xu Z, Seefeld K, Haas A, Wickner WT, (1997) I2B is a small cytosolic protein that participates in vacuole fusion. Proceedings of the National Academy of Sciences of the United States of America 94: 5582-5587.
66. Xu Z, Mayer A, Muller E, Wickner W, (1997) A heterodimer of thioredoxin and I(B)2 cooperates with Sec18p (NSF) to promote yeast vacuole inheritance. The Journal of cell biology 136: 299-306.
67. Elazar Z, Scherz-Shouval R, Shorer H, (2003) Involvement of LMA1 and GATE-16 family members in intracellular membrane dynamics. Biochimica et biophysica acta 1641: 145-156.
68. Betz H, (1975) Levels and turnover of the proteinase B inhibitors in yeast. Biochimica et biophysica acta 404: 142-151.
69. Schu P, Suarez Rendueles P, Wolf DH, (1991) The proteinase yscB inhibitor (PB12) gene of yeast and studies on the function of its protein product. European journal of biochemistry/FEBS 197: 1-7.
70. Mehta S, Li H, Hogan PG, Cunningham KW, (2009) Domain architecture of the regulators of calcineurin (RCANs) and identification of a divergent RCAN in yeast. Molecular and cellular biology 29: 2777-2793 doi:10.1128/MCB.01197-08.
71. Piper P, Mahé Y, Thompson S, Pandjaitan R, Holyoak C, et al. (1998) The pdr12 ABC transporter is required for the development of weak organic acid resistance in yeast. The EMBO journal 17: 4257-4265 doi:10.1093/emboj/17.15.4257.
72. Holyoak CD, Bracey D, Piper PW, Kuchler K, Coote PJ, (1999) The Saccharomyces cerevisiae weak-acid-inducible ABC transporter Pdr12 transports fluorescein and preservative anions from the cytosol by an energy-dependent mechanism. Journal of bacteriology 181: 4644-4652.
73. Kratchmarova I, Blagoev B, Haack-Sorensen M, Kassem M, Mann M, (2005) Mechanism of divergent growth factor effects in mesenchymal stem cell differentiation. Science (New York, NY) 308: 1472-1477 doi:10.1126/science.1107627.
74. Boersema PJ, Aye TT, Van Veen TAB, Heck AJR, Mohammed S, (2008) Triplex protein quantification based on stable isotope labeling by peptide dimethylation applied to cell and tissue lysates. Proteomics 8: 4624-4632 doi:10.1002/pmic.200800297.
75. Zhang G, Fenyö D, Neubert TA, (2008) Screening for EphB signaling effectors using SILAC with a linear ion trap-orbitrap mass spectrometer. Journal of Proteome Research 7: 4715-4726.
76. Seyfried NT, Gozal YM, Donovan LE, Herskowitz JH, Dammer EB, et al. (2012) Quantitative analysis of the detergent-insoluble brain proteome in frontotemporal lobar degeneration using SILAC internal standards. Journal of proteome research 11: 2721-2738 doi:10.1021/pr2010814.
77. Geiger T, Madden SF, Gallagher WM, Cox J, Mann M, (2012) Proteomic portrait of human breast cancer progression identifies novel prognostic markers. Cancer research 72: 2428-2439 doi:10.1158/0008-5472.CAN-11-3711.
78. Monetti M, Nagaraj N, Sharma K, Mann M, (2011) Large-scale phosphosite quantification in tissues by a spike-in SILAC method. Nature methods 8: 655-658 doi:10.1038/nmeth.1647.
79. Ivanov A, Lazarev A (2011) Sample preparation in biological mass spectrometry. New York: Springer.
80. Thorsell A, Portelius E, Blennow K, Westman-Brinkmalm A, (2007) Evaluation of sample fractionation using micro-scale liquid-phase isoelectric focusing on mass spectrometric identification and quantitation of proteins in a SILAC experiment. Rapid communications in mass spectrometry: RCM 21: 771-778 doi:10.1002/rcm.2898.
81. Emmott E, Rodgers MA, Macdonald A, McCrory S, Ajuh P, et al. (2010) Quantitative proteomics using stable isotope labeling with amino acids in cell culture reveals changes in the cytoplasmic, nuclear, and nucleolar proteomes in Vero cells infected with the coronavirus infectious bronchitis virus. Molecular & cellular proteomics: MCP 9: 1920-1936.
82. Larsen MR, Thingholm TE, Jensen ON, Roepstorff P, Jørgensen TJD, (2005) Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Molecular & cellular proteomics: MCP 4: 873-886 doi:10.1074/mcp.T500007-MCP200.
83. Thingholm TE, Jørgensen TJD, Jensen ON, Larsen MR, (2006) Highly selective enrichment of phosphorylated peptides using titanium dioxide. Nature protocols 1: 1929-1935 doi:10.1038/nprot.2006.185.
84. Hastie T, Tibshirani R, Sherlock G, Eisen M, Brown P, et al. (1999) Imputing missing data for gene expression arrays. Stanford University Statistics Department Technical report.
85. Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, et al. (2001) Missing value estimation methods for DNA microarrays. Bioinformatics (Oxford, England) 17: 520-525.
86. Ward JHJ, (1963) Hierarchical Grouping to Optimize an Objective Function 58: 236-244.
87. Theodoridis S, Koutroumbas K (2006) Pattern Recognition. Third edition. New York: Springer. 635pp.
88. Miller RG (1981) Simultaneous Statistical Inference. Second edition. New York: Springer-Verlag.
89. Stark C, Breitkreutz B-J, Reguly T, Boucher L, Breitkreutz A, et al. (2006) BioGRID: a general repository for interaction datasets. Nucleic acids research 34: D535-9 doi:10.1093/nar/gkj109.
90. Friedman N, Linial M, Nachman I, Pe'er D, (2000) Using Bayesian networks to analyze expression data. Journal of computational biology: a journal of computational molecular cell biology 7: 601-620 doi:10.1089/106652700750050961.
91. Yoo C, Thorsson V, Cooper G, (2002) Discovery of Causal Relationships in a Gene-regulation Pathway from a Mixture of Experimental and Observational DNA Microarray Data. Pacific Symposium on Biocomputing 7: 498-509.
92. Mani S, Cooper GF, (2004) Causal discovery using a Bayesian local causal discovery algorithm. Studies in health technology and informatics 107: 731-735.
93. Cooper GF, Herskovits E, (1992) A Bayesian Method for the Induction of Probabilistic Networks from Data. Machine Learning 9: 309-347 doi:10.1023/A:1022649401552.
94. David Heckerman DMC, (1995) Learning Bayesian networks: The combination of knowledge and statistical data. Machine Learning 20: 197-243.
95. Cooper G, Yoo C, (1999) Causal Discovery from a Mixture of Experimental and Observational Data. Proceedings of Uncertainty in Artificial Intelligence pp. 116-125.
96. Murphy K (2011) Bayes Net Toolbox for Matlab. Available: http://code.google.com/p/bnt/. Accessed 12 May 1BC.
97. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome research 13: 2498-2504 doi:10.1101/gr.1239303.
98. Smoot ME, Ono K, Ruscheinski J, Wang P-L, Ideker T, (2011) Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics (Oxford, England) 27: 431-432 doi:10.1093/bioinformatics/btq675.
99. Hubbard TJP, Aken BL, Beal K, Ballester B, Caccamo M, et al. (2007) Ensembl 2007. Nucleic acids research 35: D610-7.