Multi-tasking of biosynthetic and energetic functions of glycolysis explained by supply and demand logic

BioEssays

Volumn 37, Issue 1, 2015, Pages 34-45

  van Heerden, Johan H ^a,b   Bruggeman, Frank J ^a   Teusink, Bas ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Design principles; Energy metabolism; Glycolysis; Regulation; Supply and demand; Systems biology

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ADENOSINE TRIPHOSPHATE; FRUCTOSE 2,6 BISPHOSPHATE;

ALLOSTERISM; ARTICLE; BIOENERGY; BIOSYNTHESIS; ENERGY METABOLISM; ENVIRONMENT; GLUCOSE TRANSPORT; GLYCOLYSIS; HUMAN; METABOLIC REGULATION; NONHUMAN; SYSTEMS BIOLOGY; ANIMAL; METABOLISM;

ADENOSINE TRIPHOSPHATE; ANIMALS; BIOSYNTHETIC PATHWAYS; ENERGY METABOLISM; GLYCOLYSIS; HUMANS;

EID: 84919430359     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400108     Document Type: Article

References (86)

1. Buijs NA, Siewers V, Nielsen J. 2013. Advanced biofuel production by the yeast Saccharomyces cerevisiae. Curr Opin Chem Biol 17: 480-8.
2. Li H, Liao JC. 2013. Engineering a cyanobacterium as the catalyst for the photosynthetic conversion of CO2 to 1, 2-propanediol. Microb Cell Fact 12: 4.
3. Bogorad IW, Lin T-S, Liao JC. 2013. Synthetic non-oxidative glycolysis enables complete carbon conservation. Nature 502: 693-7.
4. Vander Heiden MG, Cantley LC, Thompson CB. 2009. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-33.
5. Zhao Y, Butler EB, Tan M. 2013. Targeting cellular metabolism to improve cancer therapeutics. Cell Death Dis 4: e532.
6. Schrauwen P, Timmers S, Hesselink MKC. 2013. Blocking the entrance to open the gate. Diabetes 62: 703-5.
7. Bénéteau M, Zunino B, Jacquin MA, Meynet O, et al. 2012. Combination of glycolysis inhibition with chemotherapy results in an antitumor immune response. Proc Natl Acad Sci USA 109: 20071-6.
8. Pearce EL, Poffenberger MC, Chang C-H, Jones RG. 2013. Fueling immunity: insights into metabolism and lymphocyte function. Science 342: 1242454.
9. Bar-Even A, Flamholz A, Noor E, Milo R. 2012. Rethinking glycolysis: on the biochemical logic of metabolic pathways. Nat Chem Biol 8: 509-17.
10. Keller MA, Turchyn AV, Ralser M. 2014. Non-enzymatic glycolysis and pentose phosphate pathway-like reactions in a plausible Archean ocean. Mol Syst Biol 10: 725.
11. Smallbone K, Messiha HL, Carroll KM, Winder CL, et al. 2013. A model of yeast glycolysis based on a consistent kinetic characterisation of all its enzymes. FEBS Lett 587: 2832-41.
12. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144: 646-74.
13. Van Heerden JH, Wortel MT, Bruggeman FJ, Heijnen JJ, et al. 2014. Lost in transition: start-up of glycolysis yields subpopulations of nongrowing cells. Science 343: 1245114.
14. Gancedo JM. 2008. The early steps of glucose signalling in yeast. FEMS Microbiol Rev 32: 673-704.
15. Ma H, Botstein D. 1986. Effects of null mutations in the hexokinase genes of Saccharomyces cerevisiae on catabolite repression. Mol Cell Biol 6: 4046-52.
16. Link H, Kochanowski K, Sauer U. 2013. Systematic identification of allosteric protein-metabolite interactions that control enzyme activity in vivo. Nat Biotechnol 31: 357-61.
17. Noor E, Eden E, Milo R, Alon U. 2010. Central carbon metabolism as a minimal biochemical walk between precursors for biomass and energy. Mol Cell 39: 809-20.
18. Tepper N, Noor E, Amador-Noguez D, Haraldsdóttir HS, et al. 2013. Steady-state metabolite concentrations reflect a balance between maximizing enzyme efficiency and minimizing total metabolite load. PLoS One 8: e75370.
19. Chubukov V, Gerosa L, Kochanowski K, Sauer U. 2014. Coordination of microbial metabolism. Nat Rev Microbiol 12: 327-40.
20. Hofmeyr JS, Cornish-Bowden A. 2000. Regulating the cellular economy of supply and demand. FEBS Lett 476: 47-51.
21. Magnusson LU, Farewell A, Nyström T. 2005. ppGpp: a global regulator in Escherichia coli. Trends Microbiol 13: 236-42.
22. Chubukov V, Zuleta IA, Li H. 2012. Regulatory architecture determines optimal regulation of gene expression in metabolic pathways. Proc Natl Acad Sci USA 109: 5127-32.
23. Hofmeyr J-HS, Rohwer JM. 2011. Supply-demand analysis a framework for exploring the regulatory design of metabolism. Methods Enzymol 500: 533-54.
24. Fendt S-M, Sauer U. 2010. Transcriptional regulation of respiration in yeast metabolizing differently repressive carbon substrates. BMC Syst Biol 4: 12.
25. Daran-Lapujade P, Rossell S, van Gulik WM, Luttik MAH, et al. 2007. The fluxes through glycolytic enzymes in Saccharomyces cerevisiae are predominantly regulated at posttranscriptional levels. Proc Natl Acad Sci USA 104: 15753-8.
26. Daran-Lapujade P, Jansen MLA, Daran J-M, van Gulik W, et al. 2004. Role of transcriptional regulation in controlling fluxes in central carbon metabolism of Saccharomyces cerevisiae. A chemostat culture study. J Biol Chem 279: 9125-38.
27. Even S, Lindley ND, Cocaign-Bousquet M. 2003. Transcriptional, translational and metabolic regulation of glycolysis in Lactococcus lactis subsp. cremoris MG 1363 grown in continuous acidic cultures. Microbiology 149: 1935-44.
28. Chubukov V, Uhr M, Le Chat L, Kleijn RJ, et al. 2013. Transcriptional regulation is insufficient to explain substrate-induced flux changes in Bacillus subtilis. Mol Syst Biol 9: 709.
29. Christofk HR, Vander Heiden MG, Wu N, Asara JM, et al. 2008. Pyruvate kinase M2 is a phosphotyrosine-binding protein. Nature 452: 181-6.
30. Warmoes MO, Locasale JW. 2014. Heterogeneity of glycolysis in cancers and therapeutic opportunities. Biochem Pharmocol, in press, doi: 10.1016/j.bcp.2014.07.019
31. Morgan HP, O'Reilly FJ, Wear MA, O'Neill JR, et al. 2013. M2 pyruvate kinase provides a mechanism for nutrient sensing and regulation of cell proliferation. Proc Natl Acad Sci USA 110: 5881-6.
32. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, et al. 2008. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452: 230-3.
33. Iqbal MA, Gupta V, Gopinath P, Mazurek S, et al. 2014. Pyruvate kinase M2 and cancer: an updated assessment. FEBS Lett 588: 2685-92.
34. Grüning N-M, Rinnerthaler M, Bluemlein K, Mülleder M, et al. 2011. Pyruvate kinase triggers a metabolic feedback loop that controls redox metabolism in respiring cells. Cell Metab 14: 415-27.
35. Boles E, Schulte F, Miosga T, Freidel K, et al. 1997. Characterization of a glucose-repressed pyruvate kinase (Pyk2p) in Saccharomyces cerevisiae that is catalytically insensitive to fructose-1, 6-bisphosphate. J Bacteriol 179: 2987-93.
36. Pearce AK, Crimmins K, Groussac E, Hewlins MJ, et al. 2001. Pyruvate kinase (Pyk1) levels influence both the rate and direction of carbon flux in yeast under fermentative conditions. Microbiology 147: 391-401.
37. Ralser M, Wamelink MM, Kowald A, Gerisch B, et al. 2007. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J Biol 6: 10.
38. Grüning NN-M, Du D, Keller MA, Luisi BF, et al. 2014. Inhibition of triosephosphate isomerase by phosphoenolpyruvate in the feedback-regulation of glycolysis. Open Biol 4: 130232.
39. Messiha HL, Kent E, Malys N, Carroll KM, et al. 2014. Enzyme characterisation and kinetic modelling of the pentose phosphate pathway in yeast. Peer J Prepr 2: e146v4.
40. Hauf J, Zimmermann FK, Müller S. 2000. Simultaneous genomic overexpression of seven glycolytic enzymes in the yeast Saccharomyces cerevisiae. Enzyme Microb Technol 26: 688-98.
41. Pritchard L, Kell DB. 2002. Schemes of flux control in a model of Saccharomyces cerevisiae glycolysis. Eur J Biochem 269: 3894-904.
42. Teusink B, Passarge J, Reijenga CA, Esgalhado E, et al. 2000. Can yeast glycolysis be understood in terms of in vitro kinetics of the constituent enzymes? Testing biochemistry. Eur J Biochem 267: 5313-29.
43. Teusink B, Diderich JA, Westerhoff HV, van Dam K, et al. 1998. Intracellular glucose concentration in derepressed yeast cells consuming glucose is high enough to reduce the glucose transport rate by 50%. J Bacteriol 180: 556-62.
44. Diderich JA, Teusink B, Valkier J, Anjos J, et al. 1999. Strategies to determine the extent of control exerted by glucose transport on glycolytic flux in the yeast Saccharomyces bayanus. Microbiology 145: 3447-54.
45. Reijenga KA, Snoep JL, Diderich JA, van Verseveld HW, et al. 2001. Control of glycolytic dynamics by hexose transport in Saccharomyces cerevisiae. Biophys J 80: 626-34.
46. Elbing K, Larsson C, Bill RM, Albers E, et al. 2004. Role of hexose transport in control of glycolytic flux in Saccharomyces cerevisiae. Appl Environ Microbiol 70: 5323-30.
47. Youk H, van Oudenaarden A. 2009. Growth landscape formed by perception and import of glucose in yeast. Nature 462: 875-9.
48. Larsson C, Nilsson A, Blomberg A, Gustafsson L. 1997. Glycolytic flux is conditionally correlated with ATP concentration in Saccharomyces cerevisiae: a chemostat study under carbon- or nitrogen-limiting conditions. J Bacteriol 179: 7243-50.
49. Koebmann BJ, Westerhoff HV, Snoep JL, Solem C, et al. 2002. The extent to which ATP demand controls the glycolytic flux depends strongly on the organism and conditions for growth. Mol Biol Rep 29: 41-5.
50. Koebmann B, Westerhoff H. 2002. The glycolytic flux in Escherichia coli is controlled by the demand for ATP. J Bacteriol 184: 3909-16.
51. Mensonides FIC, Bakker BM, Cremazy F, Messiha HL, et al. 2013. 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: 2860-7.
52. Larsson C, Påhlman I, Gustafsson L. 2000. The importance of ATP as a regulator of glycolytic flux in Saccharomyces cerevisiae. Yeast 16: 797-809.
53. Müller S, Zimmermann FK, Boles E. 1997. 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: 3055-61.
54. Canelas AB, Ras C, ten Pierick A, van Gulik WM, et al. 2011. An in vivo data-driven framework for classification and quantification of enzyme kinetics and determination of apparent thermodynamic data. Metab Eng 13: 294-306.
55. Schmitz JPJ, van Riel NAW, Nicolay K, Hilbers PAJ, et al. 2010. Silencing of glycolysis in muscle: experimental observation and numerical analysis. Exp Physiol 95: 380-97.
56. Gancedo C, Flores C. 2004. The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res 4: 351-9.
57. Agius L. 2008. Glucokinase and molecular aspects of liver glycogen metabolism. Biochem J 414: 1-18.
58. Wu C, Khan SA, Peng L-J, Lange AJ. 2006. Roles for fructose-2, 6-bisphosphate in the control of fuel metabolism: beyond its allosteric effects on glycolytic and gluconeogenic enzymes. Adv Enzyme Regul 46: 72-88.
59. Raamsdonk LM, Teusink B, Broadhurst D, Zhang N, et al. 2001. A functional genomics strategy that uses metabolome data to reveal the phenotype of silent mutations. Nat Biotechnol 19: 45-50.
60. Boles EM, Göhlmann HWH, Zimmermann FK. 1996. Cloning of a second gene encoding 6-phosphofructo-2-kinase in yeast, and characterization of mutant strains without fructose-2, 6-bisphosphate. Mol Microbiol 20: 65-76.
61. Navas MA, Gancedo JM. 1996. The regulatory characteristics of yeast fructose-1, 6-bisphosphatase confer only a small selective advantage. J Bacteriol 178: 1809-12.
62. Zaragoza O, Gancedo JM. 2001. Elements from the cAMP signaling pathway are involved in the control of expression of the yeast gluconeogenic gene FBP1. FEBS Lett 506: 262-6.
63. Schmitz JPJ, Groenendaal W, Wessels B, Wiseman RW, et al. 2013. Combined in vivo and in silico investigations of activation of glycolysis in contracting skeletal muscle. Am J Physiol Cell Physiol 304: C180-93.
64. Krause U, Wegener G. 1996. Control of glycolysis in vertebrate skeletal muscle during exercise. Am J Physiol Regul Integr Comp Physiol 270: R821-9.
65. Wu C, Khan SA, Peng L-J, Li H, et al. 2006. Perturbation of glucose flux in the liver by decreasing F26P2 levels causes hepatic insulin resistance and hyperglycemia. Am J Physiol Endocrinol Metab 291: E536-43.
66. Fell DA. 1997. Understanding the Control of Metabolim. London: Portland Press Ltd.
67. Kochanowski K, Volkmer B, Gerosa L, Haverkorn van Rijsewijk BR, et al. 2013. Functioning of a metabolic flux sensor in Escherichia coli. Proc Natl Acad Sci USA 110: 1130-5.
68. Kotte O, Zaugg JB, Heinemann M. 2010. Bacterial adaptation through distributed sensing of metabolic fluxes. Mol Syst Biol 6: 355.
69. Huberts DHEW, Niebel B, Heinemann M. 2012. A flux-sensing mechanism could regulate the switch between respiration and fermentation. FEMS Yeast Res 12: 118-28.
70. Shestov AA, Liu X, Ser Z, Cluntun AA, et al. 2014. Quantitative determinants of aerobic glycolysis identify flux through the enzyme GAPDH as a limiting step. elife 3: e03342.
71. Díaz-Ruiz R, Avéret N, Araiza D, Pinson B, et al. 2008. Mitochondrial oxidative phosphorylation is regulated by fructose 1, 6-bisphosphate. A possible role in Crabtree effect induction? J Biol Chem 283: 26948-55.
72. Ramseier TM, Nègre D, Cortay JC, Scarabel M, et al. 1993. In vitro binding of the pleiotropic transcriptional regulatory protein, FruR, to the fru, pps, ace, pts and icd operons of Escherichia coli and Salmonella typhimurium. J Mol Biol 234: 28-44.
73. Ramseier TM. 1996. Cra and the control of carbon flux via metabolic pathways. Res Microbiol 147: 489-93.
74. Meijer MM, Boonstra J, Verkleij AJ, Verrips CT. 1998. Glucose repression in Saccharomyces cerevisiae is related to the glucose concentration rather than the glucose flux. J Biol Chem 273: 24102-7.
75. Walther T, Mtimet N, Alkim C, Vax A, et al. 2013. Metabolic phenotypes of Saccharomyces cerevisiae mutants with altered trehalose 6-phosphate dynamics. Biochem J 454: 227-37.
76. You C, Okano H, Hui S, Zhang Z, et al. 2013. Coordination of bacterial proteome with metabolism by cyclic AMP signalling. Nature 500: 301-6.
77. Bluemlein K, Glückmann M, Grüning N-M, Feichtinger R, et al. 2012. Pyruvate kinase is a dosage-dependent regulator of cellular amino acid homeostasis. Oncotarget 3: 1356-69.
78. Argaud D, Lange AJ, Becker TC, Okar DA, et al. 1995. Adenovirus-mediated overexpression of liver 6-phosphofructo-2-kinase/fructose-2, 6-bisphosphatase in gluconeogenic rat hepatoma cells. Paradoxical effect on Fru-2, 6-P2 levels. J Biol Chem 270: 24229-36.
79. Yalcin A, Clem BF, Imbert-Fernandez Y, Ozcan SC, et al. 2014. 6-Phosphofructo-2-kinase (PFKFB3) promotes cell cycle progression and suppresses apoptosis via Cdk1-mediated phosphorylation of p27. Cell Death Dis 5: e1337.
80. Yang W, Zheng Y, Xia Y, Ji H, et al. 2012. ERK1/2-dependent phosphorylation and nuclear translocation of PKM2 promotes the Warburg effect. Nat Cell Biol 14: 1295-304.
81. Pilkis SJ, Claus TH, Kurland IJ, Lange AJ. 1995. 6-Phosphofructo-2-kinase/fructose-2, 6-bisphosphatase: a metabolic signaling enzyme. Annu Rev Biochem 64: 799-835.
82. Tyson JJ, Chen KC, Novak B. 2003. Sniffers, buzzers, toggles and blinkers: dynamics of regulatory and signaling pathways in the cell. Curr Opin Cell Biol 15: 221-31.
83. Alon U. 2006. An introduction to systems biology: design principles of biological circuits. Chapman and Hall/CRC.
84. Oliveira AP, Ludwig C, Picotti P, Kogadeeva M, et al. 2012. Regulation of yeast central metabolism by enzyme phosphorylation. Mol Syst Biol 8: 623.
85. Lin R, Zhou X, Huang W, Zhao D, et al. 2014. Acetylation control of cancer cell metabolism. Curr Pharm Des 20: 2627-33.
86. Johnson C, Warmoes MO, Shen X, Locasale JW. 2013. Epigenetics and cancer metabolism. Cancer Lett, in press, doi: 10.1016/j.canlet.2013.09.043