Global analysis of phosphoproteome regulation by the Ser/Thr phosphatase Ppt1 in saccharomyces cerevisiae

Journal of Proteome Research

Volumn 11, Issue 4, 2012, Pages 2397-2408

  Schreiber, Thiemo B ^a   Mäusbacher, Nina ^a   Soroka, Joanna ^b   Wandinger, Sebastian K ^b   Buchner, Johannes ^b   Daub, Henrik ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

phosphoproteomics; Ppt1; Ser Thr phosphatase; SILAC; yeast

Indexed keywords

CELL PROTEIN; PHOSPHATASE; PHOSPHOPEPTIDE; PHOSPHOPROTEIN; SERINE; THREONINE;

ABLATION THERAPY; ARTICLE; CONTROLLED STUDY; FRACTIONATION; HEAT STRESS; IMMOBILIZED METAL AFFINITY CHROMATOGRAPHY; ION EXCHANGE CHROMATOGRAPHY; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; SACCHAROMYCES CEREVISIAE; UPREGULATION; WILD TYPE; YEAST CELL;

GENE DELETION; ISOTOPE LABELING; MASS SPECTROMETRY; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHOPROTEINS; PROTEOME; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

SACCHAROMYCES CEREVISIAE;

EID: 84859562238     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr201134p     Document Type: Article

References (96)

1. Shi, Y. Serine/threonine phosphatases: mechanism through structure Cell 2009, 139 (3) 468-484
2. Alonso, A.; Sasin, J.; Bottini, N.; Friedberg, I.; Friedberg, I.; Osterman, A.; Godzik, A.; Hunter, T.; Dixon, J.; Mustelin, T. Protein tyrosine phosphatases in the human genome Cell 2004, 117 (6) 699-711
3. Becker, W.; Kentrup, H.; Klumpp, S.; Schultz, J. E.; Joost, H. G. Molecular cloning of a protein serine/threonine phosphatase containing a putative regulatory tetratricopeptide repeat domain J. Biol. Chem. 1994, 269 (36) 22586-22592
4. Chen, M. X.; McPartlin, A. E.; Brown, L.; Chen, Y. H.; Barker, H. M.; Cohen, P. T. A novel human protein serine/threonine phosphatase, which possesses four tetratricopeptide repeat motifs and localizes to the nucleus EMBO J. 1994, 13 (18) 4278-4290
5. Chinkers, M. Targeting of a distinctive protein-serine phosphatase to the protein kinase-like domain of the atrial natriuretic peptide receptor Proc. Natl. Acad. Sci. U.S.A. 1994, 91 (23) 11075-11079
6. Kennelly, P. J. Protein phosphatases-a phylogenetic perspective Chem. Rev. 2001, 101 (8) 2291-2312
7. Stark, M. J. Yeast protein serine/threonine phosphatases: multiple roles and diverse regulation Yeast 1996, 12 (16) 1647-1675
8. Cohen, P.; Cohen, P. T. Protein phosphatases come of age J. Biol. Chem. 1989, 264 (36) 21435-21438
9. Chen, M. X.; Cohen, P. T. Activation of protein phosphatase 5 by limited proteolysis or the binding of polyunsaturated fatty acids to the TPR domain FEBS Lett. 1997, 400 (1) 136-140
10. Andreeva, A. V.; Kutuzov, M. A. RdgC/PP5-related phosphatases: novel components in signal transduction Cell Signal 1999, 11 (8) 555-562
11. Chinkers, M. Protein phosphatase 5 in signal transduction Trends Endocrinol. Metab. 2001, 12 (1) 28-32
12. Sinclair, C.; Borchers, C.; Parker, C.; Tomer, K.; Charbonneau, H.; Rossie, S. The tetratricopeptide repeat domain and a C-terminal region control the activity of Ser/Thr protein phosphatase 5 J. Biol. Chem. 1999, 274 (33) 23666-23672
13. Kang, H.; Sayner, S. L.; Gross, K. L.; Russell, L. C.; Chinkers, M. Identification of amino acids in the tetratricopeptide repeat and C-terminal domains of protein phosphatase 5 involved in autoinhibition and lipid activation Biochemistry 2001, 40 (35) 10485-90
14. Swingle, M. R.; Honkanen, R. E.; Ciszak, E. M. Structural basis for the catalytic activity of human serine/threonine protein phosphatase-5 J. Biol. Chem. 2004, 279 (32) 33992-9
15. Skinner, J.; Sinclair, C.; Romeo, C.; Armstrong, D.; Charbonneau, H.; Rossie, S. Purification of a fatty acid-stimulated protein-serine/threonine phosphatase from bovine brain and its identification as a homolog of protein phosphatase 5 J. Biol. Chem. 1997, 272 (36) 22464-22471
16. Ramsey, A. J.; Chinkers, M. Identification of potential physiological activators of protein phosphatase 5 Biochemistry 2002, 41 (17) 5625-5632
17. Jeong, J. Y.; Johns, J.; Sinclair, C.; Park, J. M.; Rossie, S. Characterization of Saccharomyces cerevisiae protein Ser/Thr phosphatase T1 and comparison to its mammalian homolog PP5 BMC Cell. Biol. 2003, 4, 3
18. Silverstein, A. M.; Galigniana, M. D.; Chen, M. S.; Owens-Grillo, J. K.; Chinkers, M.; Pratt, W. B. Protein phosphatase 5 is a major component of glucocorticoid receptor.hsp90 complexes with properties of an FK506-binding immunophilin J. Biol. Chem. 1997, 272 (26) 16224-16230
19. Scheufler, C.; Brinker, A.; Bourenkov, G.; Pegoraro, S.; Moroder, L.; Bartunik, H.; Hartl, F. U.; Moarefi, I. Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine Cell 2000, 101 (2) 199-210
20. Ramsey, A. J.; Russell, L. C.; Whitt, S. R.; Chinkers, M. Overlapping sites of tetratricopeptide repeat protein binding and chaperone activity in heat shock protein 90 J. Biol. Chem. 2000, 275 (23) 17857-17862
21. Yang, J.; Roe, S. M.; Cliff, M. J.; Williams, M. A.; Ladbury, J. E.; Cohen, P. T.; Barford, D. Molecular basis for TPR domain-mediated regulation of protein phosphatase 5 EMBO J. 2005, 24 (1) 1-10
22. Russell, L. C.; Whitt, S. R.; Chen, M. S.; Chinkers, M. Identification of conserved residues required for the binding of a tetratricopeptide repeat domain to heat shock protein 90 J. Biol. Chem. 1999, 274 (29) 20060-20063
23. Wandinger, S. K.; Suhre, M. H.; Wegele, H.; Buchner, J. The phosphatase Ppt1 is a dedicated regulator of the molecular chaperone Hsp90 EMBO J. 2006, 25 (2) 367-376
24. Gavin, A. C.; Bosche, M.; Krause, R.; Grandi, P.; Marzioch, M.; Bauer, A.; Schultz, J.; Rick, J. M.; Michon, A. M.; Cruciat, C. M.; Remor, M.; Hofert, C.; Schelder, M.; Brajenovic, M.; Ruffner, H.; Merino, A.; Klein, K.; Hudak, M.; Dickson, D.; Rudi, T.; Gnau, V.; Bauch, A.; Bastuck, S.; Huhse, B.; Leutwein, C.; Heurtier, M. A.; Copley, R. R.; Edelmann, A.; Querfurth, E.; Rybin, V.; Drewes, G.; Raida, M.; Bouwmeester, T.; Bork, P.; Seraphin, B.; Kuster, B.; Neubauer, G.; Superti-Furga, G. Functional organization of the yeast proteome by systematic analysis of protein complexes Nature 2002, 415 (6868) 141-147
25. Shao, J.; Hartson, S. D.; Matts, R. L. Evidence that protein phosphatase 5 functions to negatively modulate the maturation of the Hsp90-dependent heme-regulated eIF2alpha kinase Biochemistry 2002, 41 (21) 6770-6779
26. Chen, M. S.; Silverstein, A. M.; Pratt, W. B.; Chinkers, M. The tetratricopeptide repeat domain of protein phosphatase 5 mediates binding to glucocorticoid receptor heterocomplexes and acts as a dominant negative mutant J. Biol. Chem. 1996, 271 (50) 32315-32320
27. Vaughan, C. K.; Mollapour, M.; Smith, J. R.; Truman, A.; Hu, B.; Good, V. M.; Panaretou, B.; Neckers, L.; Clarke, P. A.; Workman, P.; Piper, P. W.; Prodromou, C.; Pearl, L. H. Hsp90-dependent activation of protein kinases is regulated by chaperone-targeted dephosphorylation of Cdc37 Mol. Cell 2008, 31 (6) 886-895
28. Gasch, A. P.; Spellman, P. T.; Kao, C. M.; Carmel-Harel, O.; Eisen, M. B.; Storz, G.; Botstein, D.; Brown, P. O. Genomic expression programs in the response of yeast cells to environmental changes Mol. Biol. Cell 2000, 11 (12) 4241-4257
29. Lyons, T. J.; Gasch, A. P.; Gaither, L. A.; Botstein, D.; Brown, P. O.; Eide, D. J. Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (14) 7957-7962
30. Roberts, C. J.; Nelson, B.; Marton, M. J.; Stoughton, R.; Meyer, M. R.; Bennett, H. A.; He, Y. D.; Dai, H.; Walker, W. L.; Hughes, T. R.; Tyers, M.; Boone, C.; Friend, S. H. Signaling and circuitry of multiple MAPK pathways revealed by a matrix of global gene expression profiles Science 2000, 287 (5454) 873-880
31. Reece, R. J. Molecular basis of nutrient-controlled gene expression in Saccharomyces cerevisiae Cell. Mol. Life Sci. 2000, 57 (8-9) 1161-1171
32. Cohen, P. T. Novel protein serine/threonine phosphatases: variety is the spice of life Trends Biochem. Sci. 1997, 22 (7) 245-251
33. Morita, K.; Saitoh, M.; Tobiume, K.; Matsuura, H.; Enomoto, S.; Nishitoh, H.; Ichijo, H. Negative feedback regulation of ASK1 by protein phosphatase 5 (PP5) in response to oxidative stress EMBO J. 2001, 20 (21) 6028-6036
34. Choudhary, C.; Olsen, J. V.; Brandts, C.; Cox, J.; Reddy, P. N.; Bohmer, F. D.; Gerke, V.; Schmidt-Arras, D. E.; Berdel, W. E.; Muller-Tidow, C.; Mann, M.; Serve, H. Mislocalized activation of oncogenic RTKs switches downstream signaling outcomes Mol. Cell 2009, 36 (2) 326-339
35. Holt, L. J.; Tuch, B. B.; Villen, J.; Johnson, A. D.; Gygi, S. P.; Morgan, D. O. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution Science 2009, 325 (5948) 1682-1686
36. Olsen, J. V.; Blagoev, B.; Gnad, F.; Macek, B.; Kumar, C.; Mortensen, P.; Mann, M. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks Cell 2006, 127 (3) 635-648
37. Olsen, J. V.; de Godoy, L. M.; Li, G.; Macek, B.; Mortensen, P.; Pesch, R.; Makarov, A.; Lange, O.; Horning, S.; Mann, M. Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap Mol. Cell. Proteomics 2005, 4 (12) 2010-2021
38. Olsen, J. V.; Vermeulen, M.; Santamaria, A.; Kumar, C.; Miller, M. L.; Jensen, L. J.; Gnad, F.; Cox, J.; Jensen, T. S.; Nigg, E. A.; Brunak, S.; Mann, M. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis Sci. Signal 2010, 3 (104) ra3
39. Ong, S. E.; Mann, M. Mass spectrometry-based proteomics turns quantitative Nat. Chem. Biol. 2005, 1 (5) 252-262
40. Schreiber, T. B.; Mausbacher, N.; Breitkopf, S. B.; Grundner-Culemann, K.; Daub, H. Quantitative phosphoproteomics - an emerging key technology in signal-transduction research Proteomics 2008, 8 (21) 4416-4432
41. Schreiber, T. B.; Mausbacher, N.; Keri, G.; Cox, J.; Daub, H. An integrated phosphoproteomics workflow reveals extensive network regulation in early lysophosphatidic acid signaling Mol. Cell. Proteomics 2010, 9 (6) 1047-1062
42. Dephoure, N.; Zhou, C.; Villen, J.; Beausoleil, S. A.; Bakalarski, C. E.; Elledge, S. J.; Gygi, S. P. A quantitative atlas of mitotic phosphorylation Proc. Natl. Acad. Sci. U.S.A. 2008, 105 (31) 10762-10767
43. Soufi, B.; Kelstrup, C. D.; Stoehr, G.; Frohlich, F.; Walther, T. C.; Olsen, J. V. Global analysis of the yeast osmotic stress response by quantitative proteomics Mol. Biosyst. 2009, 5 (11) 1337-1346
44. Cox, J.; Mann, M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat. Biotechnol. 2008, 26 (12) 1367-1372
45. Hilger, M.; Bonaldi, T.; Gnad, F.; Mann, M. Systems-wide analysis of a phosphatase knock-down by quantitative proteomics and phosphoproteomics Mol. Cell. Proteomics 2009, 8 (8) 1908-1920
46. Mertins, P.; Eberl, H. C.; Renkawitz, J.; Olsen, J. V.; Tremblay, M. L.; Mann, M.; Ullrich, A.; Daub, H. Investigation of protein-tyrosine phosphatase 1B function by quantitative proteomics Mol. Cell. Proteomics 2008, 7 (9) 1763-1777
47. Ham, B. M.; Jayachandran, H.; Yang, F.; Jaitly, N.; Polpitiya, A. D.; Monroe, M. E.; Wang, L.; Zhao, R.; Purvine, S. O.; Livesay, E. A.; Camp, D. G., 2nd; Rossie, S.; Smith, R. D. Novel Ser/Thr protein phosphatase 5 (PP5) regulated targets during DNA damage identified by proteomics analysis J. Proteome Res. 2010, 9 (2) 945-953
48. Bodenmiller, B.; Wanka, S.; Kraft, C.; Urban, J.; Campbell, D.; Pedrioli, P. G.; Gerrits, B.; Picotti, P.; Lam, H.; Vitek, O.; Brusniak, M. Y.; Roschitzki, B.; Zhang, C.; Shokat, K. M.; Schlapbach, R.; Colman-Lerner, A.; Nolan, G. P.; Nesvizhskii, A. I.; Peter, M.; Loewith, R.; von Mering, C.; Aebersold, R. Phosphoproteomic analysis reveals interconnected system-wide responses to perturbations of kinases and phosphatases in yeast Sci. Signal 2011, 3 (153) rs4
49. Albuquerque, C. P.; Smolka, M. B.; Payne, S. H.; Bafna, V.; Eng, J.; Zhou, H. A multidimensional chromatography technology for in-depth phosphoproteome analysis Mol. Cell. Proteomics 2008, 7 (7) 1389-1396
50. Gruhler, A.; Olsen, J. V.; Mohammed, S.; Mortensen, P.; Faergeman, N. J.; Mann, M.; Jensen, O. N. Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway Mol. Cell. Proteomics 2005, 4 (3) 310-327
51. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254
52. Wessel, D.; Flugge, U. I. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids Anal. Biochem. 1984, 138 (1) 141-143
53. Villen, J.; Gygi, S. P. The SCX/IMAC enrichment approach for global phosphorylation analysis by mass spectrometry Nat. Protoc. 2008, 3 (10) 1630-1638
54. Boersema, P. J.; Mohammed, S.; Heck, A. J. Hydrophilic interaction liquid chromatography (HILIC) in proteomics Anal. Bioanal. Chem. 2008, 391 (1) 151-159
55. Daub, H.; Olsen, J. V.; Bairlein, M.; Gnad, F.; Oppermann, F. S.; Korner, R.; Greff, Z.; Keri, G.; Stemmann, O.; Mann, M. Kinase-selective enrichment enables quantitative phosphoproteomics of the kinome across the cell cycle Mol. Cell 2008, 31 (3) 438-448
56. Schroeder, M. J.; Shabanowitz, J.; Schwartz, J. C.; Hunt, D. F.; Coon, J. J. A neutral loss activation method for improved phosphopeptide sequence analysis by quadrupole ion trap mass spectrometry Anal. Chem. 2004, 76 (13) 3590-3598
57. Gnad, F.; de Godoy, L. M.; Cox, J.; Neuhauser, N.; Ren, S.; Olsen, J. V.; Mann, M. High-accuracy identification and bioinformatic analysis of in vivo protein phosphorylation sites in yeast Proteomics 2009, 9 (20) 4642-4652
58. Elias, J. E.; Haas, W.; Faherty, B. K.; Gygi, S. P. Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations Nat. Methods 2005, 2 (9) 667-675
59. Huang da, W.; Sherman, B. T.; Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 2009, 4 (1) 44-57
60. Dennis, G., Jr.; Sherman, B. T.; Hosack, D. A.; Yang, J.; Gao, W.; Lane, H. C.; Lempicki, R. A. DAVID: Database for Annotation, Visualization, and Integrated Discovery Genome Biol. 2003, 4 (5) P3
61. Mann, M. Functional and quantitative proteomics using SILAC Nat. Rev. Mol. Cell. Biol. 2006, 7 (12) 952-958
62. Wandinger, S. K.; Richter, K.; Buchner, J. The Hsp90 chaperone machinery J. Biol. Chem. 2008, 283 (27) 18473-18477
63. Gaiser, A. M.; Kretzschmar, A.; Richter, K. Cdc37-Hsp90 complexes are responsive to nucleotide-induced conformational changes and binding of further cofactors J. Biol. Chem. 2010, 285 (52) 40921-40932
64. Vaughan, C. K.; Gohlke, U.; Sobott, F.; Good, V. M.; Ali, M. M.; Prodromou, C.; Robinson, C. V.; Saibil, H. R.; Pearl, L. H. Structure of an Hsp90-Cdc37-Cdk4 complex Mol. Cell 2006, 23 (5) 697-707
65. Roe, S. M.; Ali, M. M.; Meyer, P.; Vaughan, C. K.; Panaretou, B.; Piper, P. W.; Prodromou, C.; Pearl, L. H. The Mechanism of Hsp90 regulation by the protein kinase-specific cochaperone p50(cdc37) Cell 2004, 116 (1) 87-98
66. Stepanova, L.; Leng, X.; Parker, S. B.; Harper, J. W. Mammalian p50Cdc37 is a protein kinase-targeting subunit of Hsp90 that binds and stabilizes Cdk4 Genes Dev. 1996, 10 (12) 1491-1502
67. Brugge, J. S.; Erikson, E.; Erikson, R. L. The specific interaction of the Rous sarcoma virus transforming protein, pp60src, with two cellular proteins Cell 1981, 25 (2) 363-372
68. Shao, J.; Prince, T.; Hartson, S. D.; Matts, R. L. Phosphorylation of serine 13 is required for the proper function of the Hsp90 co-chaperone, Cdc37 J. Biol. Chem. 2003, 278 (40) 38117-38120
69. Bandhakavi, S.; McCann, R. O.; Hanna, D. E.; Glover, C. V. A positive feedback loop between protein kinase CKII and Cdc37 promotes the activity of multiple protein kinases J. Biol. Chem. 2003, 278 (5) 2829-2836
70. Ali, A.; Bharadwaj, S.; OCarroll, R.; Ovsenek, N. HSP90 interacts with and regulates the activity of heat shock factor 1 in Xenopus oocytes Mol. Cell. Biol. 1998, 18 (9) 4949-4960
71. Zou, J.; Guo, Y.; Guettouche, T.; Smith, D. F.; Voellmy, R. Repression of heat shock transcription factor HSF1 activation by HSP90 (HSP90 complex) that forms a stress-sensitive complex with HSF1 Cell 1998, 94 (4) 471-480
72. Guo, Y.; Guettouche, T.; Fenna, M.; Boellmann, F.; Pratt, W. B.; Toft, D. O.; Smith, D. F.; Voellmy, R. Evidence for a mechanism of repression of heat shock factor 1 transcriptional activity by a multichaperone complex J. Biol. Chem. 2001, 276 (49) 45791-45799
73. Xia, W.; Voellmy, R. Hyperphosphorylation of heat shock transcription factor 1 is correlated with transcriptional competence and slow dissociation of active factor trimers J. Biol. Chem. 1997, 272 (7) 4094-4102
74. Voellmy, R. On mechanisms that control heat shock transcription factor activity in metazoan cells Cell Stress Chaperones 2004, 9 (2) 122-133
75. Sorger, P. K.; Lewis, M. J.; Pelham, H. R. Heat shock factor is regulated differently in yeast and HeLa cells Nature 1987, 329 (6134) 81-84
76. Sorger, P. K.; Pelham, H. R. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation Cell 1988, 54 (6) 855-864
77. Larson, J. S.; Schuetz, T. J.; Kingston, R. E. Activation in vitro of sequence-specific DNA binding by a human regulatory factor Nature 1988, 335 (6188) 372-375
78. Sorger, P. K. Yeast heat shock factor contains separable transient and sustained response transcriptional activators Cell 1990, 62 (4) 793-805
79. Conde, R.; Xavier, J.; McLoughlin, C.; Chinkers, M.; Ovsenek, N. Protein phosphatase 5 is a negative modulator of heat shock factor 1 J. Biol. Chem. 2005, 280 (32) 28989-28996
80. de Godoy, L. M.; Olsen, J. V.; Cox, J.; Nielsen, M. L.; Hubner, N. C.; Frohlich, F.; Walther, T. C.; Mann, M. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast Nature 2008, 455 (7217) 1251-1254
81. Holmberg, C. I.; Hietakangas, V.; Mikhailov, A.; Rantanen, J. O.; Kallio, M.; Meinander, A.; Hellman, J.; Morrice, N.; MacKintosh, C.; Morimoto, R. I.; Eriksson, J. E.; Sistonen, L. Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1 EMBO J. 2001, 20 (14) 3800-3810
82. Crowe, J. H.; Crowe, L. M.; Oliver, A. E.; Tsvetkova, N.; Wolkers, W.; Tablin, F. The trehalose myth revisited: introduction to a symposium on stabilization of cells in the dry state Cryobiology 2001, 43 (2) 89-105
83. Singer, M. A.; Lindquist, S. Multiple effects of trehalose on protein folding in vitro and in vivo Mol. Cell 1998, 1 (5) 639-648
84. Singer, M. A.; Lindquist, S. Thermotolerance in Saccharomyces cerevisiae: the Yin and Yang of trehalose Trends Biotechnol. 1998, 16 (11) 460-468
85. Vuorio, O. E.; Kalkkinen, N.; Londesborough, J. Cloning of two related genes encoding the 56-kDa and 123-kDa subunits of trehalose synthase from the yeast Saccharomyces cerevisiae Eur. J. Biochem. 1993, 216 (3) 849-861
86. Vandercammen, A.; Francois, J.; Hers, H. G. Characterization of trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase of Saccharomyces cerevisiae Eur. J. Biochem. 1989, 182 (3) 613-620
87. Bell, W.; Sun, W.; Hohmann, S.; Wera, S.; Reinders, A.; De Virgilio, C.; Wiemken, A.; Thevelein, J. M. Composition and functional analysis of the Saccharomyces cerevisiae trehalose synthase complex J. Biol. Chem. 1998, 273 (50) 33311-33319
88. Neves, M. J.; Francois, J. On the mechanism by which a heat shock induces trehalose accumulation in Saccharomyces cerevisiae Biochem. J. 1992, 288 (Pt 3) 859-864
89. Hottiger, T.; Schmutz, P.; Wiemken, A. Heat-induced accumulation and futile cycling of trehalose in Saccharomyces cerevisiae J. Bacteriol. 1987, 169 (12) 5518-5522
90. Francois, J.; Neves, M. J.; Hers, H. G. The control of trehalose biosynthesis in Saccharomyces cerevisiae: evidence for a catabolite inactivation and repression of trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase Yeast 1991, 7 (6) 575-587
91. Panek, A. C.; de Araujo, P. S.; Moura Neto, V.; Panek, A. D. Regulation of the trehalose-6-phosphate synthase complex in Saccharomyces. I. Interconversion of forms by phosphorylation Curr. Genet. 1987, 11 (6-7) 459-465
92. Francois, J.; Eraso, P.; Gancedo, C. Changes in the concentration of cAMP, fructose 2,6-bisphosphate and related metabolites and enzymes in Saccharomyces cerevisiae during growth on glucose Eur. J. Biochem. 1987, 164 (2) 369-373
93. Clotet, J.; Posas, F.; Hu, G. Z.; Ronne, H.; Arino, J. Role of protein phosphatase 2A in the control of glycogen metabolism in yeast Eur. J. Biochem. 1995, 229 (1) 207-214
94. Swinnen, J. V.; Van Veldhoven, P. P.; Timmermans, L.; De Schrijver, E.; Brusselmans, K.; Vanderhoydonc, F.; Van de Sande, T.; Heemers, H.; Heyns, W.; Verhoeven, G. Fatty acid synthase drives the synthesis of phospholipids partitioning into detergent-resistant membrane microdomains Biochem. Biophys. Res. Commun. 2003, 302 (4) 898-903
95. Tehlivets, O.; Scheuringer, K.; Kohlwein, S. D. Fatty acid synthesis and elongation in yeast Biochim. Biophys. Acta 2007, 1771 (3) 255-270
96. Richter, K.; Haslbeck, M.; Buchner, J. The heat shock response: life on the verge of death Mol. Cell 2010, 40 (2) 253-266