The self-inhibitory nature of metabolic networks and its alleviation through compartmentalization

Nature Communications

Volumn 8, Issue , 2017, Pages

  Alam, Mohammad Tauqeer ^a,b   Olin Sandoval, Viridiana ^a,c   Stincone, Anna ^a,g   Keller, Markus A ^a,d   Zelezniak, Aleksej ^a,e,f   Luisi, Ben F ^a   Ralser, Markus ^a,e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c INSTITUTO NACIONAL DE CIENCIAS MÉDICAS Y NUTRICIÓN SALVADOR ZUBIRÁN   (Mexico)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^e THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^f CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

^g SUMMIT PLC   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROLASE; ISOMERASE; LACTATE DEHYDROGENASE; LIGASE; LYASE; MALONIC ACID; OXALOACETIC ACID; OXIDOREDUCTASE; PYRUVIC ACID; TRANSFERASE; ENZYME;

BIOCHEMICAL COMPOSITION; COMPARTMENTALIZATION; ENZYME; ENZYME ACTIVITY; INHIBITION; INHIBITOR; METABOLISM; METABOLITE; SUBSTRATE;

ARTICLE; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; EUKARYOTIC CELL; METABOLIC INHIBITION; PROTEIN LOCALIZATION; ALLOSTERISM; BIOLOGICAL MODEL; CELL COMPARTMENTALIZATION; EVOLUTION; HUMAN; METABOLISM; METABOLOME; PHYSIOLOGICAL FEEDBACK;

EUKARYOTA;

ALLOSTERIC REGULATION; BIOLOGICAL EVOLUTION; CELL COMPARTMENTATION; ENZYMES; FEEDBACK, PHYSIOLOGICAL; HUMANS; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; MODELS, BIOLOGICAL;

EID: 85023208659     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms16018     Document Type: Article

References (64)

1. Lindsley, J. E. & Rutter, J. Whence cometh the allosterome? Proc. Natl Acad. Sci. USA. 103, 10533-10535 (2006).
2. Li, X., Gianoulis, T. A., Yip, K. Y., Gerstein, M. & Snyder, M. Extensive in vivo metabolite-protein interactions revealed by large-scale systematic analyses. Cell 143, 639-650 (2010).
3. Kochanowski, K. et al. Functioning of a metabolic flux sensor in Escherichia coli. Proc. Natl Acad. Sci. USA 110, 1130-1135 (2013).
4. Gerosa, L. & Sauer, U. Regulation and control of metabolic fluxes in microbes. Curr. Opin. Biotechnol. 22, 566-575 (2011).
5. Grüning, N.-M., Du, D., Keller, M. A., Luisi, B. F. & Ralser, M. Inhibition of triosephosphate isomerase by phosphoenolpyruvate in the feedback-regulation of glycolysis. Open Biol. 4, 130232 (2014).
6. Rose, I. A. Regulation of human red cell glycolysis: a review. Exp. Eye Res. 11, 264-272 (1971).
7. Hers, H. G. & Van Schaftingen, E. Fructose 2,6-bisphosphate 2 years after its discovery. Biochem. J. 206, 1-12 (1982).
8. Van Schaftingen, E. & Hers, H. G. Inhibition of fructose-1,6-bisphosphatase by fructose 2,6-biphosphate. Proc. Natl Acad. Sci. USA 78, 2861-2863 (1981)
9. Jurica, M. S. et al. The allosteric regulation of pyruvate kinase by fructose-1,6-bisphosphate. Structure 6, 195-210 (1998).
10. Murray, D. S. et al. Structures of the Bacillus subtilis glutamine synthetase dodecamer reveal large intersubunit catalytic conformational changes linked to a unique feedback inhibition mechanism. J. Biol. Chem. 288, 35801-35811 (2013).
11. Grüning, N.-M. et al. Pyruvate kinase triggers a metabolic feedback loop that controls redox metabolism in respiring cells. Cell Metab. 14, 415-427 (2011).
12. Smallbone, K. et al. A model of yeast glycolysis based on a consistent kinetic characterisation of all its enzymes. FEBS Lett. 587, 2832-2841 (2013)
13. Link, H., Christodoulou, D. & Sauer, U. Advancing metabolic models with kinetic information. Curr. Opin. Biotechnol. 29, 8-14 (2014).
14. Teusink, B. et al. Can yeast glycolysis be understood in terms of in vitro kinetics of the constituent enzymes? Testing biochemistry. Eur. J. Biochem. 267, 5313-5329 (2000).
15. Machado, D., Herrgard, M. J. & Rocha, I. Modeling the contribution of allosteric regulation for flux control in the central carbon metabolism of E. coli. Front. Bioeng. Biotechnol. 3, 154 (2015).
16. Schomburg, I. et al. BRENDA in 2013: integrated reactions, kinetic data, enzyme function data, improved disease classification: new options and contents in BRENDA. Nucleic Acids Res. 41, D764-D772 (2013).
17. Thiele, I. et al. A community-driven global reconstruction of human metabolism. Nat. Biotechnol. 31, 419-425 (2013).
18. Atkinson, D. E. & Walton, G. M. Adenosine triphosphate conservation in metabolic regulation. Rat liver citrate cleavage enzyme. J. Biol. Chem. 242, 3239-3241 (1967).
19. Rawlings, N. D., Tolle, D. P. & Barrett, A. J. Evolutionary families of peptidase inhibitors. Biochem. J. 378, 705-716 (2004).
20. Hudson, J. W., Brian, G. G. & Crerar, M. M. Evolution of allosteric control in glycogen phosphorylase. J. Mol. Biol. 234, 700-721 (1993).
21. Shen, Q. et al. ASD v3.0: unraveling allosteric regulation with structural mechanisms and biological networks. Nucleic Acids Res. 44, D527-D535 (2015).
22. Wishart, D. S. et al. HMDB: the human metabolome database. Nucleic Acids Res. 35, D521-D526 (2007).
23. Michaelis, L. & Menten, M. L. Die Kinetik der Invertinwirkung. Biochem. Z. 49, 333-369 (1913).
24. Lineweaver, H. & Burk, D. The determination of enzyme dissociation constants. J. Am. Chem. Soc. 56, 658-666 (1934).
25. Jogl, G., Rozovsky, S., McDermott, A. E. & Tong, L. Optimal alignment for enzymatic proton transfer: structure of the Michaelis complex of triosephosphate isomerase at 1.2-A resolution. Proc. Natl Acad. Sci. USA 100, 50-55 (2003).
26. Zhong, W. et al. 'In crystallo ' substrate binding triggers major domain movements and reveals magnesium as a co-activator of Trypanosoma brucei pyruvate kinase. Acta Crystallogr. D Biol. Crystallogr. 69, 1768-1779 (2013).
27. Holyoak, T. et al. Energetic coupling between an oxidizable cysteine and the phosphorylatable N-terminus of human liver pyruvate kinase. Biochemistry 52, 466-476 (2013).
28. Lloyd, S. J., Lauble, H., Prasad, G. S. & Stout, C. D. The mechanism of aconitase: 1.8A resolution crystal structure of the S642a:citrate complex. Protein Sci. 8, 2655-2662 (1999).
29. Lauble, H., Kennedy, M. C., Beinert, H. & Stout, C. D. Crystal structures of aconitase with trans-aconitate and nitrocitrate bound. J. Mol. Biol. 237, 437-451 (1994).
30. Cao, Y., Charisi, A., Cheng, L.-C., Jiang, T. & Girke, T. ChemmineR: a compound mining framework for R. Bioinformatics 24, 1733-1734 (2008)
31. Cao, D.-S., Xiao, N., Xu, Q.-S. & Chen, A. F. Rcpi: R/Bioconductor package to generate various descriptors of proteins, compounds and their interactions. Bioinformatics 31, 279-281 (2015).
32. Wang, Y., Backman, T. W. H., Horan, K. & Girke, T. fmcsR: mismatch tolerant maximum common substructure searching in R. Bioinformatics 29, 2792-2794 (2013).
33. Stambaugh, R. & Post, D. Substrate and product inhibition of rabbit muscle lactic dehydrogenase heart (H4) and muscle (M4) isozymes. J. Biol. Chem. 241, 1462-1467 (1966).
34. Wang, C. S. Inhibition of human erythrocyte lactate dehydrogenase by high concentrations of pyruvate. Evidence for the competitive substrate inhibition. Eur. J. Biochem. 78, 569-574 (1977).
35. Ottolenghi, P. & Denstedt, O. F. Mechanism of action of the lactic dehydrogenase of the mammalian erythrocyte. I. Influence of inhibitors. Biochem. Cell Biol. 36, 1075-1083 (1958).
36. Fritz, P. J. Rabbit muscle lactate dehydrogenase 5; a regulatory enzyme. Science 150, 364-366 (1965).
37. Yoshida, A. Enzymic properties of lactate dehydrogenase of Bacillus subtilis. Biochim. Biophys. Acta 99, 66-77 (1965).
38. Steinbüchel, A. & Schlegel, H. G. NAD-linked L())-lactate dehydrogenase from the strict aerobe alcaligenes eutrophus.2. Kinetic properties and inhibition by oxaloacetate. Eur. J. Biochem. 130, 329-334 (1983)
39. Alam, M. T., Medema, M. H., Takano, E. & Breitling, R. Comparative genomescale metabolic modeling of actinomycetes: the topology of essential core metabolism. FEBS Lett. 585, 2389-2394 (2011).
40. Zecchin, A., Stapor, P. C., Goveia, J. & Carmeliet, P. Metabolic pathway compartmentalization: an underappreciated opportunity? Curr. Opin. Biotechnol. 34, 73-81 (2015).
41. Collard, F. et al. A conserved phosphatase destroys toxic glycolytic side-products in mammals and yeasts. Nat. Chem. Biol. 12, 601-607 (2016)
42. Linster, C. L., Van Schaftingen, E. & Hanson, A. D. Metabolite damage and its repair or pre-emption. Nat. Chem. Biol. 9, 72-80 (2013).
43. Albery, W. J., John Albery, W. & Knowles, J. R. Free-energy profile for the reaction catalyzed by triosephosphate isomerase. Biochemistry 15, 5627-5631 (1976).
44. Ralser, M. et al. Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J. Biol. 6, 10 (2007).
45. Schaftingen, E. V., Van Schaftingen, E. & Henri-Géry, H. Phosphofructokinase 2 the enzyme that forms fructose 2,6-bisphosphate from fructose 6-phosphate and ATP. Biochem. Biophys. Res. Commun. 101, 1078-1084 (1981).
46. Van Schaftingen, E. & Henri-Géry, H. Formation of fructose 2,6-bisphosphate from fructose 1,6-bisphosphate by intramolecular cyclisation followed by alkaline hydrolysis. Eur. J. Biochem. 117, 319-323 (1981).
47. Kim, J. & Copley, S. D. Inhibitory cross-talk upon introduction of a new metabolic pathway into an existing metabolic network. Proc. Natl Acad. Sci. USA 109, E2856-E2864 (2012).
48. Orth, J. D. et al. A comprehensive genome-scale reconstruction of Escherichia coli metabolism - 2011. Mol. Syst. Biol. 7, 535 (2011).
49. Yoshikuni, Y., Ferrin, T. E. & Keasling, J. D. Designed divergent evolution of enzyme function. Nature 440, 1078-1082 (2006).
50. Nielsen, J. & Keasling, J. D. Engineering cellular metabolism. Cell 164, 1185-1197 (2016).
51. Ro, D.-K. et al. Production of the antimalarial drug precursor artemisinic acid in engineered yeast. Nature 440, 940-943 (2006).
52. Mayer, M. J. et al. Effect of bio-engineering on size, shape, composition and rigidity of bacterial microcompartments. Sci. Rep. 6, 36899 (2016).
53. Tu, B. P., Kudlicki, A., Rowicka, M. & McKnight, S. L. Logic of the yeast metabolic cycle: temporal compartmentalization of cellular processes. Science 310, 1152-1158 (2005).
54. Zelezniak, A. et al. Metabolic dependencies drive species co-occurrence in diverse microbial communities. Proc. Natl Acad. Sci. USA 112, 6449-6454 (2015).
55. Xu, P., Ranganathan, S., Fowler, Z. L., Maranas, C. D. & Koffas, M. A. G. Genome-scale metabolic network modeling results in minimal interventions that cooperatively force carbon flux towards malonyl-CoA. Metab. Eng. 13, 578-587 (2011).
56. Liu, Y., Beer, L. L. & Whitman, W. B. Methanogens: a window into ancient sulfur metabolism. Trends Microbiol. 20, 251-258 (2012).
57. Kanehisa, M. & Goto, S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27-30 (2000).
58. Wohlgemuth, G., Haldiya, P. K., Willighagen, E., Kind, T. & Fiehn, O. The Chemical Translation Service - a web-based tool to improve standardization of metabolomic reports. Bioinformatics 26, 2647-2648 (2010).
59. Degtyarenko, K. et al. ChEBI: a database and ontology for chemical entities of biological interest. Nucleic Acids Res. 36, D344-D350 (2008).
60. Sud, M. et al. LMSD: LIPID MAPS structure database. Nucleic Acids Res. 35, D527-D532 (2007).
61. Wang, T. et al. Identification and characterization of essential genes in the human genome. Science 350, 1096-1101 (2015).
62. Swiderek, K., Panczakiewicz, A., Bujacz, A., Bujacz, G. & Paneth, P. Modeling of isotope effects on binding oxamate to lactic dehydrogenase. J. Phys. Chem. B 113, 12782-12789 (2009).
63. Bell, M. J., Gillespie, C. S., Swan, D. & Lord, P. An approach to describing and analysing bulk biological annotation quality: a case study using UniProtKB. Bioinformatics 28, i562-i568 (2012).
64. Csárdi, G. & Nepusz, T. The igraph software package for complex network research. InterJournal Complex Systems 1695 (2006) http://igraph.org.