Pseudo-transition Analysis Identifies the Key Regulators of Dynamic Metabolic Adaptations from Steady-State Data

Cell Systems

Volumn 1, Issue 4, 2015, Pages 270-282

  Gerosa, Luca ^a,b,c   Haverkorn Van Rijsewijk, Bart R B ^a,b   Christodoulou, Dimitris ^a,b   Kochanowski, Karl ^a,b   Schmidt, Thomas S B ^a   Noor, Elad ^a   Sauer, Uwe ^a  

^a ETH ZURICH   (Switzerland)

^b PhD Program in Molecular Life Sciences Zurich   (Switzerland)

^c HARVARD UNIVERSITY   (United States)

Author keywords

computational biology; metabolism; metabolomics; regulation network; transcription factor

Indexed keywords

GLUCOSE; SUCCINIC ACID; TRICARBOXYLIC ACID;

ARTICLE; BACTERIAL GROWTH; CALCULATION; CARBON METABOLISM; CARBON SOURCE; CELL FUNCTION; CITRIC ACID CYCLE; ESCHERICHIA COLI; GENE EXPRESSION; GENETIC TRANSCRIPTION; METABOLITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; STEADY STATE; UPREGULATION;

EID: 84951061481     PISSN: None     EISSN: 24054712     Source Type: Journal    
DOI: 10.1016/j.cels.2015.09.008     Document Type: Article

References (43)

1. M.J. Brauer, C. Huttenhower, E.M. Airoldi, R. Rosenstein, J.C. Matese, D. Gresham, V.M. Boer, O.G. Troyanskaya, and D. Botstein Coordination of growth rate, cell cycle, stress response, and metabolic activity in yeast Mol. Biol. Cell 19 2008 352 367
2. J.M. Buescher, S. Moco, U. Sauer, and N. Zamboni Ultrahigh performance liquid chromatography-tandem mass spectrometry method for fast and robust quantification of anionic and aromatic metabolites Anal. Chem. 82 2010 4403 4412
3. J.M. Buescher, W. Liebermeister, M. Jules, M. Uhr, J. Muntel, E. Botella, B. Hessling, R.J. Kleijn, L. Le Chat, F. Lecointe, and et al. Global network reorganization during dynamic adaptations of Bacillus subtilis metabolism Science 335 2012 1099 1103
4. V. Chubukov, M. Uhr, L. Le Chat, R.J. Kleijn, M. Jules, H. Link, S. Aymerich, J. Stelling, and U. Sauer Transcriptional regulation is insufficient to explain substrate-induced flux changes in Bacillus subtilis Mol. Syst. Biol. 9 2013 709
5. V. Chubukov, L. Gerosa, K. Kochanowski, and U. Sauer Coordination of microbial metabolism Nat. Rev. Microbiol. 12 2014 327 340
6. M.W. Covert, E.M. Knight, J.L. Reed, M.J. Herrgard, and B.O. Palsson Integrating high-throughput and computational data elucidates bacterial networks Nature 429 2004 92 96
7. P. Daran-Lapujade, S. Rossell, W.M. van Gulik, M.A.H. Luttik, M.J.L. de Groot, M. Slijper, A.J.R. Heck, J.-M. Daran, J.H. de Winde, H.V. Westerhoff, and et al. The fluxes through glycolytic enzymes in Saccharomyces cerevisiae are predominantly regulated at posttranscriptional levels Proc. Natl. Acad. Sci. USA 104 2007 15753 15758
8. S.-M. Fendt, A.P. Oliveira, S. Christen, P. Picotti, R.C. Dechant, and U. Sauer Unraveling condition-dependent networks of transcription factors that control metabolic pathway activity in yeast Mol. Syst. Biol. 6 2010 432
9. A.P. Gasch, P.T. Spellman, C.M. Kao, O. Carmel-Harel, M.B. Eisen, G. Storz, D. Botstein, and P.O. Brown Genomic expression programs in the response of yeast cells to environmental changes Mol. Biol. Cell 11 2000 4241 4257
10. L. Gerosa, and U. Sauer Regulation and control of metabolic fluxes in microbes Curr. Opin. Biotechnol. 22 2011 566 575
11. L. Gerosa, K. Kochanowski, M. Heinemann, and U. Sauer Dissecting specific and global transcriptional regulation of bacterial gene expression Mol. Syst. Biol. 9 2013 658
12. N. Geva-Zatorsky, E. Dekel, A.A. Cohen, T. Danon, L. Cohen, and U. Alon Protein dynamics in drug combinations: a linear superposition of individual-drug responses Cell 140 2010 643 651
13. B. Görke, and J. Stülke Carbon catabolite repression in bacteria: many ways to make the most out of nutrients Nat. Rev. Microbiol. 6 2008 613 624
14. S. Goyal, J. Yuan, T. Chen, J.D. Rabinowitz, and N.S. Wingreen Achieving optimal growth through product feedback inhibition in metabolism PLoS Comput. Biol. 6 2010 e1000802
15. 13C-flux analysis reveals distinct transcriptional control of respiratory and fermentative metabolism in Escherichia coli Mol. Syst. Biol. 7 2011 477
16. M. Heinemann, and U. Sauer Systems biology of microbial metabolism Curr. Opin. Microbiol. 13 2010 337 343
17. S. Hui, J.M. Silverman, S.S. Chen, D.W. Erickson, M. Basan, J. Wang, T. Hwa, and J.R. Williamson Quantitative proteomic analysis reveals a simple strategy of global resource allocation in bacteria Mol. Syst. Biol. 11 2015 784
18. N. Ishii, K. Nakahigashi, T. Baba, M. Robert, T. Soga, A. Kanai, T. Hirasawa, M. Naba, K. Hirai, A. Hoque, and et al. Multiple high-throughput analyses monitor the response of E. coli to perturbations Science 316 2007 593 597
19. K.C. Kao, Y.-L. Yang, R. Boscolo, C. Sabatti, V. Roychowdhury, and J.C. Liao Transcriptome-based determination of multiple transcription regulator activities in Escherichia coli by using network component analysis Proc. Natl. Acad. Sci. USA 101 2004 641 646
20. S. Kaplan, A. Bren, A. Zaslaver, E. Dekel, and U. Alon Diverse two-dimensional input functions control bacterial sugar genes Mol. Cell 29 2008 786 792
21. L. Keren, O. Zackay, M. Lotan-Pompan, U. Barenholz, E. Dekel, V. Sasson, G. Aidelberg, A. Bren, D. Zeevi, A. Weinberger, and et al. Promoters maintain their relative activity levels under different growth conditions Mol. Syst. Biol. 9 2013 701
22. R.J. Kleijn, J.M. Buescher, L. Le Chat, M. Jules, S. Aymerich, and U. Sauer Metabolic fluxes during strong carbon catabolite repression by malate in Bacillus subtilis J. Biol. Chem. 285 2010 1587 1596
23. K. Kochanowski, B. Volkmer, L. Gerosa, B.R. Haverkorn van Rijsewijk, A. Schmidt, and M. Heinemann Functioning of a metabolic flux sensor in Escherichia coli Proc. Natl. Acad. Sci. USA 110 2013 1130 1135
24. N.J. Kruger, and R.G. Ratcliffe Fluxes through plant metabolic networks: measurements, predictions, insights and challenges Biochem. J. 465 2015 27 38
25. J.C. Liao, R. Boscolo, Y.-L. Yang, L.M. Tran, C. Sabatti, and V.P. Roychowdhury Network component analysis: reconstruction of regulatory signals in biological systems Proc. Natl. Acad. Sci. USA 100 2003 15522 15527
26. H. Link, K. Kochanowski, and U. Sauer Systematic identification of allosteric protein-metabolite interactions that control enzyme activity in vivo Nat. Biotechnol. 31 2013 357 361
27. H. Link, D. Christodoulou, and U. Sauer Advancing metabolic models with kinetic information Curr. Opin. Biotechnol. 29 2014 8 14
28. F.I.C. Mensonides, B.M. Bakker, F. Cremazy, H.L. Messiha, P. Mendes, F.C. Boogerd, and H.V. Westerhoff A new regulatory principle for in vivo biochemistry: pleiotropic low affinity regulation by the adenine nucleotides - illustrated for the glycolytic enzymes of Saccharomyces cerevisiae FEBS Lett. 587 2013 2860 2867
29. E. Noor, A. Flamholz, W. Liebermeister, A. Bar-Even, and R. Milo A note on the kinetics of enzyme action: a decomposition that highlights thermodynamic effects FEBS Lett. 587 2013 2772 2777
30. E. Noor, A. Bar-Even, A. Flamholz, E. Reznik, W. Liebermeister, and R. Milo Pathway thermodynamics highlights kinetic obstacles in central metabolism PLoS Comput. Biol. 10 2014 e1003483
31. 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
32. K.R. Patil, and J. Nielsen Uncovering transcriptional regulation of metabolism by using metabolic network topology Proc. Natl. Acad. Sci. USA 102 2005 2685 2689
33. T. Pisithkul, N.M. Patel, and D. Amador-Noguez Post-translational modifications as key regulators of bacterial metabolic fluxes Curr. Opin. Microbiol. 24 2015 29 37
34. M.N. Price, A.M. Deutschbauer, J.M. Skerker, K.M. Wetmore, T. Ruths, J.S. Mar, J.V. Kuehl, W. Shao, and A.P. Arkin Indirect and suboptimal control of gene expression is widespread in bacteria Mol. Syst. Biol. 9 2013 660
35. S. Rossell, C.C. van der Weijden, A. Lindenbergh, A. van Tuijl, C. Francke, B.M. Bakker, and H.V. Westerhoff Unraveling the complexity of flux regulation: a new method demonstrated for nutrient starvation in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. USA 103 2006 2166 2171
36. D. Rothschild, E. Dekel, J. Hausser, A. Bren, G. Aidelberg, P. Szekely, and U. Alon Linear superposition and prediction of bacterial promoter activity dynamics in complex conditions PLoS Comput. Biol. 10 2014 e1003602
37. H. Salgado, M. Peralta-Gil, S. Gama-Castro, A. Santos-Zavaleta, L. Muñiz-Rascado, J.S. García-Sotelo, V. Weiss, H. Solano-Lira, I. Martínez-Flores, A. Medina-Rivera, and et al. RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more Nucleic Acids Res. 41 2013 D203 D213
38. 13C-based flux analysis Mol. Syst. Biol. 2 2006 62
39. J. Schellenberger, R. Que, R.M.T. Fleming, I. Thiele, J.D. Orth, A.M. Feist, D.C. Zielinski, A. Bordbar, N.E. Lewis, S. Rahmanian, and et al. Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2.0 Nat. Protoc. 6 2011 1290 1307
40. Y.-F. Xu, X. Zhao, D.S. Glass, F. Absalan, D.H. Perlman, J.R. Broach, and J.D. Rabinowitz Regulation of yeast pyruvate kinase by ultrasensitive allostery independent of phosphorylation Mol. Cell 48 2012 52 62
41. C. You, H. Okano, S. Hui, Z. Zhang, M. Kim, C.W. Gunderson, Y.-P. Wang, P. Lenz, D. Yan, and T. Hwa Coordination of bacterial proteome with metabolism by cyclic AMP signalling Nature 500 2013 301 306
42. N. Zamboni, S.-M. Fendt, M. Rühl, and U. Sauer (13)C-based metabolic flux analysis Nat. Protoc. 4 2009 878 892
43. A. Zaslaver, A. Bren, M. Ronen, S. Itzkovitz, I. Kikoin, S. Shavit, W. Liebermeister, M.G. Surette, and U. Alon A comprehensive library of fluorescent transcriptional reporters for Escherichia coli Nat. Methods 3 2006 623 628