Comprehensive quantitative analysis of central carbon and amino-acid metabolism in Saccharomyces cerevisiae under multiple conditions by targeted proteomics

Molecular Systems Biology

Volumn 7, Issue , 2011, Pages

  Costenoble, Roeland ^a   Picotti, Paola ^a   Reiter, Lukas ^a,b   Stallmach, Robert ^a   Heinemann, Matthias ^a,c   Sauer, Uwe ^a   Aebersold, Ruedi ^a,b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

metabolism; S. cerevisiae; SRM; targeted proteomics

Indexed keywords

AMINO ACID METABOLISM; ARTICLE; CARBON METABOLISM; ENZYME ANALYSIS; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEOMICS; QUANTITATIVE ANALYSIS; SACCHAROMYCES CEREVISIAE; BIOLOGICAL MODEL; CHEMISTRY; CLUSTER ANALYSIS; ENZYMOLOGY; METABOLISM; METHODOLOGY; SYSTEMS BIOLOGY;

SACCHAROMYCES CEREVISIAE;

AMINO ACID; CARBON; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO ACIDS; CARBON; CLUSTER ANALYSIS; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; PROTEOMICS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SYSTEMS BIOLOGY;

EID: 79551600149     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2010.122     Document Type: Article

References (51)

1. Addona TA, Abbatiello SE, Schilling B, Skates SJ, Mani DR, Bunk DM, Spiegelman CH, Zimmerman LJ, Ham AJ, Keshishian H, Hall SC, Allen S, Blackman RK, Borchers CH, Buck C, Cardasis HL, Cusack MP, Dodder NG, Gibson BW, Held JM et al (2009) Multi-site assessment of the precision and reproducibility of multiple reaction monitoring-based measurements of proteins in plasma. Nat Biotechnol 27: 633-641
2. Aldridge BB, Burke JM, Lauffenburger DA, Sorger PK (2006) Physicochemical modelling of cell signalling pathways. Nat Cell Biol 8: 1195-1203
3. Anderson L, Hunter CL (2006) Quantitative mass spectrometric multiple reaction monitoring assays for major plasma proteins. Mol Cell Proteomics 5: 573-588
4. Baty JD, Robinson PR (1977) Single and multiple ion recording techniques for the analysis of diphenylhydantoin and its major metabolite in plasma. Biomed Mass Spectrom 4: 36-41
5. Bell AW, Deutsch EW, Au CE, Kearney RE, Beavis R, Sechi S, Nilsson T, Bergeron JJ (2009) A HUPO test sample study reveals common problems in mass spectrometry-based proteomics. Nat Methods 6: 423-430
6. 13C-flux analysis reveals mechanistic principles of metabolic network robustness to null mutations in yeast. Genome Biol 6: R49
7. Chin CS, Chubukov V, Jolly ER, DeRisi J, Li H (2008) Dynamics and design principles of a basic regulatory architecture controlling metabolic pathways. PLoS Biol 6: e146
8. Daran-Lapujade P, Rossell S, van Gulik WM, Luttik MA, de Groot MJ, Slijper M, Heck AJ, Daran JM, de Winde JH, Westerhoff HV, Pronk JT, Bakker BM (2007) The fluxes through glycolytic enzymes in Saccharomyces cerevisiae are predominantly regulated at posttranscriptional levels. Proc Natl Acad Sci USA 104: 15753-15758
9. De Godoy LM, Olsen JV, Cox J, Nielsen ML, Hubner NC, Frohlich F, Walther TC, Mann M (2008) Comprehensive mass-spectrometrybased proteome quantification of haploid versus diploid yeast. Nature 455: 1251-1254
10. De Groot MJ, Daran-Lapujade P, van Breukelen B, Knijnenburg TA, de Hulster EA, Reinders MJ, Pronk JT, Heck AJ, Slijper M (2007) Quantitative proteomics and transcriptomics of anaerobic and aerobic yeast cultures reveals post-transcriptional regulation of key cellular processes. Microbiology 153: 3864-3878
11. Dekel E, Alon U (2005) Optimality and evolutionary tuning of the expression level of a protein. Nature 436: 588-592
12. Deutsch EW, Lam H, Aebersold R (2008) PeptideAtlas: a resource for target selection for emerging targeted proteomics workflows. EMBO Rep 9: 429-434
13. Duarte NC, Becker SA, Jamshidi N, Thiele I, Mo ML, Vo TD, Srivas R, Palsson B (2007) Global reconstruction of the human metabolic network based on genomic and bibliomic data. Proc Natl Acad Sci USA 104: 1777-1782
14. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95: 14863-14868
15. Feist AM, Herrgard MJ, Thiele I, Reed JL, Palsson B (2009) Reconstruction of biochemical networks in microorganisms. Nat RevMicrobiol 7: 129-143
16. Fell DA, Small JR (1986) Fat synthesis in adipose tissue. An examination of stoichiometric constraints. Biochem J 238: 781-786
17. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O'Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425: 737-741
18. Gutteridge A, Pir P, Castrillo JI, Charles PD, Lilley KS, Oliver SG (2010) Nutrient control of eukaryote cell growth: a systems biology study in yeast. BMC Biol 8: 68
19. Heer D, Sauer U (2008) Identification of furfural as a key toxin in lignocellulosic hydrolysates and evolution of a tolerant yeast strain. Microb Biotechnol 1: 497-506
20. Heinemann M, Sauer U (2010) Systems biology of microbial metabolism. Curr Opin Microbiol 13: 337-343
21. Herrgard MJ, Swainston N, Dobson P, Dunn WB, Arga KY, Arvas M, Büthgen N, Borger S, Costenoble R, Heinemann M, Hucka M, Le Novère N, Li P, Liebermeister W, Mo ML, Oliveira AP, Petranovic D, Pettifer S, Simeonidis E, Smallbone K et al (2008) A consensus yeast metabolic network reconstruction obtained from a community approach to systems biology Nat Biotechnol 26: 1155-1160
22. Hua H, Hui R, Xu L, Shuilong T, Zhiqiang Z, Liwen N, Maikun T (2008) The crystal structure and identification of NQM1/YGR043C, a transaldolase from Saccharomyces cerevisiae. Proteins 73: 1076-1081
23. Ihmels J, Collins SR, Schuldiner M, Krogan NJ, Weissman JS (2007) Backup without redundancy: genetic interactions reveal the cost of duplicate gene loss. Mol Syst Biol 3: 86
24. Ihmels J, Levy R, Barkai N (2004) Principles of transcriptional control in the metabolic network of Saccharomyces cerevisiae. Nat Biotechnol 22: 86-92
25. Kitano H (2002a) Computational systems biology. Nature 420: 206-210
26. Kitano H (2002b) Systems biology: a brief overview. Science 295: 1662-1664
27. Kolkman A, Daran-Lapujade P, Fullaondo A, Olsthoorn MM, Pronk JT, Slijper M, Heck AJ (2006) Proteome analysis of yeast response to various nutrient limitations. Mol Syst Biol 2: 26
28. Kotte O, Heinemann M (2009) A divide-and-conquer approach to analyze underdetermined biochemical models. Bioinformatics 25: 519-525
29. Kotte O, Zaugg JB, Heinemann M (2010) Bacterial adaptation through distributed sensing of metabolic fluxes. Mol Syst Biol 6: 355
30. Kuepfer L, Sauer U, Blank LM (2005) Metabolic functions of duplicate genes in Saccharomyces cerevisiae. Genome Res 15: 1421-1430
31. Lange V, Malmstrom JA, Didion J, King NL, Johansson BP, Schafer J, Rameseder J, Wong CH, Deutsch EW, Brusniak MY, Buhlmann P, Bjorck L, Domon B, Aebersold R (2008a) Targeted quantitative analysis of Streptococcus pyogenes virulence factors by multiple reaction monitoring. Mol Cell Proteomics 7: 1489-1500
32. Lange V, Picotti P, Domon B, Aebersold R (2008b) Selected reaction monitoring for quantitative proteomics: a tutorial. Mol Syst Biol 4: 222
33. MacLean B, Tomazela DM, Shulman N, Chambers M, Finney GL, Frewen B, Kern R, Tabb DL, Liebler DC, MacCoss MJ (2010) Skyline: an open source document editor for creating and analyzing targeted proteomics experiments. Bioinformatics 26: 966-968
34. Mallick P, Schirle M, Chen SS, Flory MR, Lee H, Martin D, Ranish J, Raught B, Schmitt R, Werner T, Kuster B, Aebersold R (2007) Computational prediction of proteotypic peptides for quantitative proteomics. Nat Biotechnol 25: 125-131
35. Minard KI, McAlister-Henn L (2005) Sources of NADPH in yeast vary with carbon source. JBiol Chem 280: 39890-39896
36. Oberhardt MA, Palsson BO, Papin JA (2009) Applications of genome-scale metabolic reconstructions. Mol Syst Biol 5: 320
37. Oyedotun KS, Lemire BD (2004) The quaternary structure of the Saccharomyces cerevisiae succinate dehydrogenase: homology modeling, cofactor docking, and molecular dynamics simulation studies. JBiol Chem 279: 9424-9431
38. Picotti P, Bodenmiller B, Mueller LN, Domon B, Aebersold R (2009) Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 138: 795-806
39. Picotti P, Lam H, Campbell D, Deutsch EW, Mirzaei H, Ranish J, Domon B, Aebersold R (2008) A database of mass spectrometric assays for the yeast proteome. Nat Methods 5: 913-914
40. Picotti P, Rinner O, Stallmach R, Dautel F, Farrah T, Domon B, Wenschuh H, Aebersold R (2010) High-throughput generation of selected reaction-monitoring assays for proteins and proteomes. Nat Methods 7: 43-46
41. 13C-based flux analysis. Mol Syst Biol 2: 62
42. Sauer U, Heinemann M, Zamboni N (2007) Genetics: getting closer to the whole picture. Science 316: 550-551
43. Schellenberger J, Palsson B (2009) Use of randomized sampling for analysis of metabolic networks. JBiol Chem 284: 5457-5461
44. Shachrai I, Zaslaver A, Alon U, Dekel E (2010) Cost of unneeded proteins in E. coli is reduced after several generations in exponential growth. Mol Cell 38: 758-767
45. Stahl-Zeng J, Lange V, Ossola R, Eckhardt K, Krek W, Aebersold R, Domon B (2007) High sensitivity detection of plasma proteins by multiple reaction monitoring of N-glycosites. Mol Cell Proteomics 6: 1809-1817
46. Tabb DL, Vega-Montoto L, Rudnick PA, Variyath AM, Ham AJ, Bunk DM, Kilpatrick LE, Billheimer DD, Blackman RK, Cardasis HL, Carr SA, Clauser KR, Jaffe JD, Kowalski KA, Neubert TA, Regnier FE, Schilling B, Tegeler TJ, Wang M, Wang P et al (2010) Repeatability and reproducibility in proteomic identifications by liquid chromatographytandem mass spectrometry. J Proteome Res 9: 761-776
47. Verduyn C, Postma E, Scheffers WA, van Dijken JP (1990) Physiology of Saccharomyces cerevisiae in anaerobic glucose-limited chemostat cultures. J Gen Microbiol 136: 395-403
48. Wagner A (2008) Gene duplications, robustness and evolutionary innovations. Bioessays 30: 367-373
49. Wilson JE (2003) Isozymes of mammalian hexokinase: structure, subcellular localization and metabolic function. J Exp Biol 206: 2049-2057
50. Winston F, Dollard C, Ricupero-Hovasse SL (1995) Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11: 53-55
51. Zaslaver A, Mayo AE, Rosenberg R, Bashkin P, Sberro H, Tsalyuk M, Surette MG, Alon U (2004) Just-in-time transcription program in metabolic pathways. Nat Genet 36: 486-491