Post-translational modifications on yeast carbon metabolism: Regulatory mechanisms beyond transcriptional control

Biochimica et Biophysica Acta - General Subjects

Volumn 1850, Issue 4, 2015, Pages 620-627

  Tripodi, Farida ^a,b   Nicastro, Raffaele ^a,b   Reghellin, Veronica ^a,b   Coccetti, Paola ^a,b  

^a SYSBIO Centre of Systems Biology ^*  (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

Acetylation; Glycolysis; Phosphorylation; PKA; Saccharomyces cerevisiae; Ubiquitination

Indexed keywords

6 PHOSPHOFRUCTO 2 KINASE; 6 PHOSPHOFRUCTOKINASE; LYSINE; PYRUVATE KINASE; CARBON;

CARBOHYDRATE METABOLISM; CARBON METABOLISM; FERMENTATION; FUNGAL METABOLISM; GENETIC ANALYSIS; GLYCOLYSIS; METABOLIC REGULATION; NONHUMAN; PROTEIN ACETYLATION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REGULATORY MECHANISM; REVIEW; TRANSCRIPTION REGULATION; UBIQUITINATION; YEAST CELL; ALLOSTERISM; GENETIC TRANSCRIPTION; GLUCONEOGENESIS; METABOLISM; PHOSPHORYLATION; RNA STABILITY; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

ALLOSTERIC REGULATION; CARBON; FERMENTATION; GLUCONEOGENESIS; GLYCOLYSIS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA STABILITY; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION, GENETIC;

EID: 84921033338     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.12.010     Document Type: Review

References (94)

1. B. Turcotte, X.B. Liang, F. Robert, and N. Soontorngun Transcriptional regulation of nonfermentable carbon utilization in budding yeast FEMS Yeast Res. 10 2010 2 13
2. H.-J. Schüller Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae Curr. Genet. 43 2003 139 160
3. E. Fernández, F. Moreno, and R. Rodicio The ICL1 gene from Saccharomyces cerevisiae Eur. J. Biochem. 204 1992 983 990
4. K.M. Taylor, C.P. Kaplan, X. Gao, and A. Baker Localization and targeting of isocitrate lyases in Saccharomyces cerevisiae Biochem. J. 319 Pt 1 1996 255 262
5. W.H. Kunau, and A. Hartig Peroxisome Biogenesis in Saccharomyces cerevisiae 62 1992 Antonie Van Leeuwenhoek 63 78
6. M. Kunze, F. Kragler, M. Binder, A. Hartig, and A. Gurvitz Targeting of malate synthase 1 to the peroxisomes of Saccharomyces cerevisiae cells depends on growth on oleic acid medium Eur. J. Biochem. 269 2002 915 922
7. W.W. Wells, Y. Yang, T.L. Deits, and Z.R. Gan Thioltransferases Adv. Enzymol. Relat. Areas Mol. Biol. 66 1993 149 201
8. B. Halliwell Free radicals and antioxidants: a personal view Nutr. Rev. 52 1994 253 265
9. J. François, and J.L. Parrou Reserve carbohydrates metabolism in the yeast Saccharomyces cerevisiae FEMS Microbiol. Rev. 25 2001 125 145
10. D. Brisson, M.C. Vohl, J. St-Pierre, T.J. Hudson, and D. Gaudet Glycerol: a neglected variable in metabolic processes? Bioessays 23 2001 534 542
11. S. Hohmann, M. Krantz, and B. Nordlander Yeast osmoregulation Methods Enzymol. 428 2007 29 45
12. G. Winter, and J.O. Krömer Fluxomics - connecting 'omics analysis and phenotypes Environ. Microbiol. 15 2013 1901 1916
13. A. Lombardo, G.P. Cereghino, and I.E. Scheffler Control of mRNA turnover as a mechanism of glucose repression in Saccharomyces cerevisiae Mol. Cell. Biol. 12 1992 2941 2948
14. G.P. Cereghino, D.P. Atencio, M. Saghbini, J. Beiner, and I.E. Scheffler Glucose-dependent turnover of the mRNAs encoding succinate dehydrogenase peptides in Saccharomyces cerevisiae: sequence elements in the 5′ untranslated region of the Ip mRNA play a dominant role Mol. Biol. Cell 6 1995 1125 1143
15. G.P. Cereghino, and I.E. Scheffler Genetic analysis of glucose regulation in Saccharomyces cerevisiae: control of transcription versus mRNA turnover EMBO J. 15 1996 363 374
16. J.J. Mercado, R. Smith, F.A. Sagliocco, A.J. Brown, and J.M. Gancedo The levels of yeast gluconeogenic mRNAs respond to environmental factors Eur. J. Biochem. 224 1994 473 481
17. B.J. de la Cruz, S. Prieto, and I.E. Scheffler The role of the 5′ untranslated region (UTR) in glucose-dependent mRNA decay Yeast 19 2002 887 902
18. Z. Yin, L. Hatton, and A.J. Brown Differential post-transcriptional regulation of yeast mRNAs in response to high and low glucose concentrations Mol. Microbiol. 35 2000 553 565
19. E.T. Young, C. Zhang, K.M. Shokat, P.K. Parua, and K.A. Braun The AMP-activated protein kinase Snf1 regulates transcription factor binding, RNA polymerase II activity, and mRNA stability of glucose-repressed genes in Saccharomyces cerevisiae J. Biol. Chem. 287 2012 29021 29034
20. K. Hedbacker, and M. Carlson SNF1/AMPK pathways in yeast Front. Biosci. 13 2008 2408 2420
21. D.G. Hardie Sensing of energy and nutrients by AMP-activated protein kinase Am. J. Clin. Nutr. 93 2011 891S 896S
22. S. Pessina, V. Tsiarentsyeva, S. Busnelli, M. Vanoni, L. Alberghina, and P. Coccetti Snf1/AMPK promotes S-phase entrance by controlling CLB5 transcription in budding yeast Cell Cycle 9 2010 2189 2200
23. S. Busnelli, F. Tripodi, R. Nicastro, C. Cirulli, G. Tedeschi, and R. Pagliarin Snf1/AMPK promotes SBF and MBF-dependent transcription in budding yeast Biochim. Biophys. Acta 1833 2013 3254 3264
24. K.A. Braun, S. Vaga, K.M. Dombek, F. Fang, S. Palmisano, and R. Aebersold Phosphoproteomic analysis identifies proteins involved in transcription-coupled mRNA decay as targets of Snf1 signaling Sci. Signal. 7 2014 ra64
25. E. Boles, F. Schulte, T. Miosga, K. Freidel, E. Schlüter, and F.K. Zimmermann Characterization of a glucose-repressed pyruvate kinase (Pyk2p) in Saccharomyces cerevisiae that is catalytically insensitive to fructose-1,6-bisphosphate J. Bacteriol. 179 1997 2987 2993
26. G.F. Sprague Isolation and characterization of a Saccharomyces cerevisiae mutant deficient in pyruvate kinase activity J. Bacteriol. 130 1977 232 241
27. C.N. Morris, S. Ainsworth, and J. Kinderlerer The regulatory properties of yeast pyruvate kinase. Effect of fructose 1,6-bisphosphate Biochem. J. 234 1986 691 698
28. M.S. Jurica, A. Mesecar, P.J. Heath, W. Shi, T. Nowak, and B.L. Stoddard The allosteric regulation of pyruvate kinase by fructose-1,6-bisphosphate Structure 6 1998 195 210
29. M.A. Blázquez, R. Lagunas, C. Gancedo, and J.M. Gancedo Trehalose-6-phosphate, a new regulator of yeast glycolysis that inhibits hexokinases FEBS Lett. 329 1993 51 54
30. A.P. Oliveira, C. Ludwig, P. Picotti, M. Kogadeeva, R. Aebersold, and U. Sauer Regulation of yeast central metabolism by enzyme phosphorylation Mol. Syst. Biol. 8 2012 623
31. S. Sharifpoor, A.N. Nguyen Ba, J.-Y. Youn, J.-Y. Young, D. van Dyk, and H. Friesen A quantitative literature-curated gold standard for kinase-substrate pairs Genome Biol. 12 2011 R39
32. D. Huang, H. Friesen, and B. Andrews Pho85, a multifunctional cyclin-dependent protein kinase in budding yeast Mol. Microbiol. 66 2007 303 314
33. S. Busti, P. Coccetti, L. Alberghina, and M. Vanoni Glucose signaling-mediated coordination of cell growth and cell cycle in Saccharomyces cerevisiae Sensors 10 2010 6195 6240
34. S. Zaman, S.I. Lippman, X. Zhao, and J.R. Broach How Saccharomyces responds to nutrients Annu. Rev. Genet. 42 2008 27 81
35. J.M. Thevelein, B.M. Bonini, D. Castermans, S. Haesendonckx, J. Kriel, and W. Louwet Novel mechanisms in nutrient activation of the yeast protein kinase A pathway Acta Microbiol. Immunol. Hung. 55 2008 75 89
36. T. Nozaki, K. Nishimura, A.J. Michael, T. Maruyama, Y. Kakinuma, and K. Igarashi A second gene encoding a putative serine/threonine protein kinase which enhances spermine uptake in Saccharomyces cerevisiae Biochem. Biophys. Res. Commun. 228 1996 452 458
37. E. Gobbini, D. Cesena, A. Galbiati, A. Lockhart, and M.P. Longhese Interplays between ATM/Tel1 and ATR/Mec1 in sensing and signaling DNA double-strand breaks DNA Repair (Amst) 12 2013 791 799
38. M. Hochstrasser Ubiquitin-dependent protein degradation Annu. Rev. Genet. 30 1996 405 439
39. A. Varshavsky The ubiquitin system Trends Biochem. Sci. 22 1997 383 387
40. X.-J. Yang, and E. Seto HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention Oncogene 26 2007 5310 5318
41. J.K. Hiltunen, A.M. Mursula, H. Rottensteiner, R.K. Wierenga, A.J. Kastaniotis, and A. Gurvitz The biochemistry of peroxisomal beta-oxidation in the yeast Saccharomyces cerevisiae FEMS Microbiol. Rev. 27 2003 35 64
42. B.T. Weinert, V. Iesmantavicius, T. Moustafa, C. Schölz, S.A. Wagner, and C. Magnes Acetylation dynamics and stoichiometry in Saccharomyces cerevisiae Mol. Syst. Biol. 10 2014 716
43. J.C. Newman, W. He, and E. Verdin Mitochondrial protein acylation and intermediary metabolism: regulation by sirtuins and implications for metabolic disease J. Biol. Chem. 287 2012 42436 42443
44. K.K. Lee, and J.L. Workman Histone acetyltransferase complexes: one size doesn't fit all Nat. Rev. Mol. Cell Biol. 8 2007 284 295
45. C.F. Kurat, J. Recht, E. Radovani, T. Durbic, B. Andrews, and J. Fillingham Regulation of histone gene transcription in yeast Cell. Mol. Life Sci. 71 2014 599 613
46. Z. Liu, J. Cao, X. Gao, Y. Zhou, L. Wen, and X. Yang CPLA 1.0: an integrated database of protein lysine acetylation Nucleic Acids Res. 39 2011 D1029 D1034
47. Z. Liu, Y. Wang, T. Gao, Z. Pan, H. Cheng, and Q. Yang CPLM: a database of protein lysine modifications Nucleic Acids Res. 42 2014 D531 D536
48. M. Cytryńska, M. Frajnt, and T. Jakubowicz Saccharomyces cerevisiae pyruvate kinase Pyk1 is PKA phosphorylation substrate in vitro FEMS Microbiol. Lett. 203 2001 223 227
49. P. Portela, S. Howell, S. Moreno, and S. Rossi In vivo and in vitro phosphorylation of two isoforms of yeast pyruvate kinase by protein kinase A J. Biol. Chem. 277 2002 30477 30487
50. P. Portela, S. Moreno, and S. Rossi Characterization of yeast pyruvate kinase 1 as a protein kinase A substrate, and specificity of the phosphorylation site sequence in the whole protein Biochem. J. 396 2006 117 126
51. J. François, E. Van Schaftigen, and H.G. Hers Characterization of phosphofructokinase 2 and of enzymes involved in the degradation of fructose 2,6-bisphosphate in yeast Eur. J. Biochem. 171 1988 599 608
52. S. Müller, F.K. Zimmermann, and E. Boles Mutant studies of phosphofructo-2-kinases do not reveal an essential role of fructose-2,6-bisphosphate in the regulation of carbon fluxes in yeast cells Microbiology 143 Pt 9 1997 3055 3061
53. H. Dihazi, R. Kessler, and K. Eschrich Glucose-induced stimulation of the Ras-cAMP pathway in yeast leads to multiple phosphorylations and activation of 6-phosphofructo-2-kinase Biochemistry 42 2003 6275 6282
54. D.E. Levin Cell wall integrity signaling in Saccharomyces cerevisiae Microbiol. Mol. Biol. Rev. 69 2005 262 291
55. K.R. Davenport, M. Sohaskey, Y. Kamada, D.E. Levin, and M.C. Gustin A second osmosensing signal transduction pathway in yeast. Hypotonic shock activates the PKC1 protein kinase-regulated cell integrity pathway J. Biol. Chem. 270 1995 30157 30161
56. H. Dihazi, R. Kessler, and K. Eschrich Phosphorylation and inactivation of yeast 6-phosphofructo-2-kinase contribute to the regulation of glycolysis under hypotonic stress Biochemistry 40 2001 14669 14678
57. S. Shahinian, and H. Bussey Beta-1,6-glucan synthesis in Saccharomyces cerevisiae Mol. Microbiol. 35 2000 477 489
58. H. Dihazi, R. Kessler, G.A. Müller, and K. Eschrich Lysine 3 acetylation regulates the phosphorylation of yeast 6-phosphofructo-2-kinase under hypo-osmotic stress Biol. Chem. 386 2005 895 900
59. H. Saito, and F. Posas Response to hyperosmotic stress Genetics 192 2012 289 318
60. H. Dihazi, R. Kessler, and K. Eschrich High osmolarity glycerol (HOG) pathway-induced phosphorylation and activation of 6-phosphofructo-2-kinase are essential for glycerol accumulation and yeast cell proliferation under hyperosmotic stress J. Biol. Chem. 279 2004 23961 23968
61. E. Petelenz-Kurdziel, C. Kuehn, B. Nordlander, D. Klein, K.-K. Hong, and T. Jacobson Quantitative analysis of glycerol accumulation, glycolysis and growth under hyper osmotic stress PLoS Comput. Biol. 9 2013 e1003084
62. J.A. Benanti, S.K. Cheung, M.C. Brady, and D.P. Toczyski A proteomic screen reveals SCFGrr1 targets that regulate the glycolytic-gluconeogenic switch Nat. Cell Biol. 9 2007 1184 1191
63. M.J. Mazón, J.M. Gancedo, and C. Gancedo Phosphorylation and inactivation of yeast fructose-bisphosphatase in vivo by glucose and by proton ionophores. A possible role for cAMP Eur. J. Biochem. 127 1982 605 608
64. J.M. Gancedo, M.J. Mazón, and C. Gancedo Fructose 2,6-bisphosphate activates the cAMP-dependent phosphorylation of yeast fructose-1,6-bisphosphatase in vitro J. Biol. Chem. 258 1983 5998 5999
65. J. Rittenhouse, L. Moberly, and F. Marcus Phosphorylation in vivo of yeast (Saccharomyces cerevisiae) fructose-1,6-bisphosphatase at the cyclic AMP-dependent site J. Biol. Chem. 262 1987 10114 10119
66. G.-C. Hung, C.R. Brown, A.B. Wolfe, J. Liu, and H.-L. Chiang Degradation of the gluconeogenic enzymes fructose-1,6-bisphosphatase and malate dehydrogenase is mediated by distinct proteolytic pathways and signaling events J. Biol. Chem. 279 2004 49138 49150
67. P. Tortora, N. Burlini, G. Caspani, and A. Guerritore Studies on glucose-induced inactivation of gluconeogenetic enzymes in adenylate cyclase and cAMP-dependent protein kinase yeast mutants Eur. J. Biochem. 145 1984 543 548
68. S.M. Schork, G. Bee, M. Thumm, and D.H. Wolf Catabolite inactivation of fructose-1,6-bisphosphatase in yeast is mediated by the proteasome FEBS Lett. 349 1994 270 274
69. Y. Jiang, C. Davis, and J.R. Broach Efficient transition to growth on fermentable carbon sources in Saccharomyces cerevisiae requires signaling through the Ras pathway EMBO J. 17 1998 6942 6951
70. J. Regelmann, T. Schüle, F.S. Josupeit, J. Horak, M. Rose, and K.-D. Entian Catabolite degradation of fructose-1,6-bisphosphatase in the yeast Saccharomyces cerevisiae: a genome-wide screen identifies eight novel GID genes and indicates the existence of two degradation pathways Mol. Biol. Cell 14 2003 1652 1663
71. B. Braun, T. Pfirrmann, R. Menssen, K. Hofmann, H. Scheel, and D.H. Wolf Gid9, a second RING finger protein contributes to the ubiquitin ligase activity of the Gid complex required for catabolite degradation FEBS Lett. 585 2011 3856 3861
72. Y. Lin, J. Lu, J. Zhang, W. Walter, W. Dang, and J. Wan Protein acetylation microarray reveals that NuA4 controls key metabolic target regulating gluconeogenesis Cell 136 2009 1073 1084
73. T.A. Hardy, and P.J. Roach Control of yeast glycogen synthase-2 by COOH-terminal phosphorylation J. Biol. Chem. 268 1993 23799 23805
74. I. Farkas, T.A. Hardy, M.G. Goebl, and P.J. Roach Two glycogen synthase isoforms in Saccharomyces cerevisiae are coded by distinct genes that are differentially controlled J. Biol. Chem. 266 1991 15602 15607
75. J. Rutter, B.L. Probst, and S.L. McKnight Coordinate regulation of sugar flux and translation by PAS kinase Cell 111 2002 17 28
76. D. Huang, I. Farkas, and P.J. Roach Pho85p, a cyclin-dependent protein kinase, and the Snf1p protein kinase act antagonistically to control glycogen accumulation in Saccharomyces cerevisiae Mol. Cell. Biol. 16 1996 4357 4365
77. D. Huang, J. Moffat, W.A. Wilson, L. Moore, C. Cheng, and P.J. Roach Cyclin partners determine Pho85 protein kinase substrate specificity in vitro and in vivo: control of glycogen biosynthesis by Pcl8 and Pcl10 Mol. Cell. Biol. 18 1998 3289 3299
78. W.A. Wilson, A.M. Mahrenholz, and P.J. Roach Substrate targeting of the yeast cyclin-dependent kinase Pho85p by the cyclin Pcl10p Mol. Cell. Biol. 19 1999 7020 7030
79. C.P. Albuquerque, M.B. Smolka, S.H. Payne, V. Bafna, J. Eng, and H. Zhou A multidimensional chromatography technology for in-depth phosphoproteome analysis Mol. Cell. Proteomics 7 2008 1389 1396
80. L.J. Holt, B.B. Tuch, J. Villén, A.D. Johnson, S.P. Gygi, and D.O. Morgan Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution Science 325 2009 1682 1686
81. S. Wera, E. De Schrijver, I. Geyskens, S. Nwaka, and J.M. Thevelein Opposite roles of trehalase activity in heat-shock recovery and heat-shock survival in Saccharomyces cerevisiae Biochem. J. 343 Pt 3 1999 621 626
82. C.M. Cardon, and J. Rutter PAS kinase: integrating nutrient sensing with nutrient partitioning Semin. Cell Dev. Biol. 23 2012 626 630
83. D. DeMille, and J.H. Grose PAS kinase: a nutrient sensing regulator of glucose homeostasis IUBMB Life. 65 2013 921 929
84. J.M. Daran, N. Dallies, D. Thines-Sempoux, V. Paquet, and J. François Genetic and biochemical characterization of the UGP1 gene encoding the UDP-glucose pyrophosphorylase from Saccharomyces cerevisiae Eur. J. Biochem. 233 1995 520 530
85. J.H. Grose, T.L. Smith, H. Sabic, and J. Rutter Yeast PAS kinase coordinates glucose partitioning in response to metabolic and cell integrity signaling EMBO J. 26 2007 4824 4830
86. T.L. Smith, and J. Rutter Regulation of glucose partitioning by PAS kinase and Ugp1 phosphorylation Mol. Cell 26 2007 491 499
87. Y.J. Lee, G.R. Jeschke, F.M. Roelants, J. Thorner, and B.E. Turk Reciprocal phosphorylation of yeast glycerol-3-phosphate dehydrogenases in adaptation to distinct types of stress Mol. Cell. Biol. 32 2012 4705 4717
88. K.I. Minard, and L. McAlister-Henn Glucose-induced degradation of the MDH2 isozyme of malate dehydrogenase in yeast J. Biol. Chem. 267 1992 17458 17464
89. I. Ordiz, P. Herrero, R. Rodicio, and F. Moreno Glucose-induced inactivation of isocitrate lyase in Saccharomyces cerevisiae is mediated by an internal decapeptide sequence FEBS Lett. 367 1995 219 222
90. I. Ordiz, P. Herrero, R. Rodicio, and F. Moreno Glucose-induced inactivation of isocitrate lyase in Saccharomyces cerevisiae is mediated by the cAMP-dependent protein kinase catalytic subunits Tpk1 and Tpk2 FEBS Lett. 385 1996 43 46
91. J. Jeffery, L. Hobbs, and H. Jörnvall Glucose-6-phosphate dehydrogenase from Saccharomyces cerevisiae: characterization of a reactive lysine residue labeled with acetylsalicylic acid Biochemistry 24 1985 666 671
92. S.R. Ande, G.P. Padilla-Meier, and S. Mishra Mutually exclusive acetylation and ubiquitylation among enzymes involved in glucose metabolism Adipocyte. 2 2013 256 261
93. L. Alberghina, P. Coccetti, and I. Orlandi Systems biology of the cell cycle of Saccharomyces cerevisiae: from network mining to system-level properties Biotechnol. Adv. 27 2009 960 978
94. M.S. Cline, M. Smoot, E. Cerami, A. Kuchinsky, N. Landys, and C. Workman Integration of biological networks and gene expression data using Cytoscape Nat. Protoc. 2 2007 2366 2382