Ultrasensitive regulation of anapleurosis via allosteric activation of PEP carboxylase

Nature Chemical Biology

Volumn 8, Issue 6, 2012, Pages 562-568

  Xu, Yi Fan ^a   Amador Noguez, Daniel ^a   Reaves, Marshall Louis ^a   Feng, Xiao Jiang ^a   Rabinowitz, Joshua D ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRUCTOSE 1,6 BISPHOSPHATE; GLUCOSE; PHOSPHOENOLPYRUVATE CARBOXYLASE;

ALLOSTERISM; ANAPLEUROSIS; ARTICLE; CARBON METABOLISM; ENZYME ACTIVATION; ESCHERICHIA COLI; GLUCONEOGENESIS; GLUCOSE TRANSPORT; METABOLISM; NONHUMAN; OSCILLATION; PRIORITY JOURNAL;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 84861455370     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.941     Document Type: Article

References (50)

1. Kotte, O., Zaugg, J.B. & Heinemann, M. Bacterial adaptation through distributed sensing of metabolic fluxes. Mol. Syst. Biol. 6, 355 (2010).
2. Christofk, H.R. et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452, 230-233 (2008). (Pubitemid 351380249)
3. Sauer, U. & Eikmanns, B.J. The PEP-pyruvate-oxaloacetate node as the switch point for carbon flux distribution in bacteria. FEMS Microbiol. Rev. 29, 765-794 (2005). (Pubitemid 41149049)
4. Feist, A.M. et al. A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol. Syst. Biol. 3, 121 (2007).
5. Siddiquee, K.A., Arauzo-Bravo, M.J. & Shimizu, K. Effect of a pyruvate kinase (pykF-gene) knockout mutation on the control of gene expression and metabolic fluxes in Escherichia coli. FEMS Microbiol. Lett. 235, 25-33 (2004). (Pubitemid 38668633)
6. Ishii, N. et al. Multiple high-throughput analyses monitor the response of E. coli to perturbations. Science 316, 593-597 (2007). (Pubitemid 46683144)
7. Fiehn, O. Metabolomics-the link between genotypes and phenotypes. Plant Mol. Biol. 48, 155-171 (2002).
8. Brauer, M.J. et al. Conservation of the metabolomic response to starvation across two divergent microbes. Proc. Natl. Acad. Sci. USA 103, 19302-19307 (2006). (Pubitemid 46026027)
9. Rabinowitz, J.D. & Kimball, E. Acidic acetonitrile for cellular metabolome extraction from Escherichia coli. Anal. Chem. 79, 6167-6173 (2007). (Pubitemid 47282327)
10. Fischer, E. & Sauer, U. A novel metabolic cycle catalyzes glucose oxidation and anaplerosis in hungry Escherichia coli. J. Biol. Chem. 278, 46446-46451 (2003). (Pubitemid 37452216)
11. Salleh, H.M., Patel, M.A. & Woodard, R.W. Essential cysteines in 3-deoxy-D-manno-octulosonic acid 8-phosphate synthase from Escherichia coli: analysis by chemical modification and site-directed mutagenesis. Biochemistry 35, 8942-8947 (1996). (Pubitemid 26243735)
12. Kim, D.H. et al. Characterization of a Cys115 to Asp substitution in the Escherichia coli cell wall biosynthetic enzyme UDP-GlcNAc enolpyruvyl transferase (MurA) that confers resistance to inactivation by the antibiotic fosfomycin. Biochemistry 35, 4923-4928 (1996).
13. Al Zaid Siddiquee, K., Arauzo-Bravo, M.J. & Shimizu, K. Metabolic flux analysis of pykF gene knockout Escherichia coli based on C-13-labeling experiments together with measurements of enzyme activities and intracellular metabolite concentrations. Appl. Microbiol. Biotechnol. 63, 407-417 (2004). (Pubitemid 38134779)
14. Haverkorn van Rijsewijk, B.R., Nanchen, A., Nallet, S., Kleijn, R.J. & Sauer, U. Large-scale 13C-flux analysis reveals distinct transcriptional control of respiratory and fermentative metabolism in Escherichia coli. Mol. Syst. Biol. 7, 477 (2011).
15. Peng, L. & Shimizu, K. Global metabolic regulation analysis for Escherichia coli K12 based on protein expression by 2-dimensional electrophoresis and enzyme activity measurement. Appl. Microbiol. Biotechnol. 61, 163-178 (2003). (Pubitemid 36470198)
16. Herrmann, K.M. The Shikimate pathway as an entry to aromatic secondary metabolism. Plant Physiol. 107, 7-12 (1995).
17. Sanwal, B.D. & Maeba, P. Regulation of activity of phosphoenolypyruvate carboxylase by fructose diphosphate. Biochem. Biophys. Res. Commun. 22, 194-199 (1966).
18. Izui, K., Matsumura, H., Furumoto, T. & Kai, Y. Phosphoenolpyruvate carboxylase: a new era of structural biology. Annu. Rev. Plant Biol. 55, 69-84 (2004). (Pubitemid 38940926)
19. Morikawa, M., Izui, K., Taguchi, M. & Katsuki, H. Regulation of Escherichia coli phosphoenolpyruvate carboxylase by multiple effectors in vivo. 1. Estimation of the activities in the cells grown on various compounds. J. Biochem. 87, 441-449 (1980). (Pubitemid 10045366)
20. Izui, K., Taguchi, M., Morikawa, M. & Katsuki, H. Regulation of Escherichia coli phosphoenolpyruvate carboxylase by multiple effectors in vivo. 2. Kinetic studies with a reaction system containing physiological concentrations of ligands. J. Biochem. 90, 1321-1331 (1981). (Pubitemid 12220926)
21. Yuan, J. & Rabinowitz, J.D. Differentiating metabolites formed from de novo synthesis versus macromolecule decomposition. J. Am. Chem. Soc. 129, 9294-9295 (2007). (Pubitemid 47218792)
22. Kodaki, T., Fujita, N., Kameshita, I., Izui, K. & Katsuki, H. Phosphoenolpyruvate carboxylase of Escherichia coli-specificity of some compounds as activators at the site for fructose-1,6-bisphosphate, one of the allosteric effectors. J. Biochem. 95, 637-642 (1984).
23. Garnak, M. & Reeves, H.C. Phosphorylation of isocitrate dehydrogenase of Escherichia coli. Science 203, 1111-1112 (1979). (Pubitemid 9148085)
24. Wohl, R.C. & Markus, G. Phosphoenolpyruvate carboxylase of Escherichia coli-purification and some properties. J. Biol. Chem. 247, 5785-5792 (1972).
25. Silverstein, R. & Willis, M.S. Concerted regulation in vitro of phosphoenolpyruvate carboxylase from Escherichia coli. J. Biol. Chem. 248, 8402-8407 (1973).
26. Takahashi-Terada, A. et al. Maize phosphoenolpyruvate carboxylase-mutations at the putative binding site for glucose 6-phosphate caused desensitization and abolished responsiveness to regulatory phosphorylation. J. Biol. Chem. 280, 11798-11806 (2005). (Pubitemid 40418494)
27. Oh, M.K., Rohlin, L., Kao, K.C. & Liao, J.C. Global expression profiling of acetate-grown Escherichia coli. J. Biol. Chem. 277, 13175-13183 (2002). (Pubitemid 34952688)
28. Bennett, B.D. et al. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5, 593-599 (2009).
29. Zhao, J., Baba, T., Mori, H. & Shimizu, K. Effect of zwf gene knockout on the metabolism of Escherichia coli grown on glucose or acetate. Metab. Eng. 6, 164-174 (2004). (Pubitemid 38601069)
30. Schaub, J. & Reuss, M. In vivo dynamics of glycolysis in Escherichia coli shows need for growth-rate dependent metabolome analysis. Biotechnol. Prog. 24, 1402-1407 (2008).
31. Theobald, U., Mailinger, W., Baltes, M., Rizzi, M. & Reuss, M. In vivo analysis of metabolic dynamics in Saccharomyces cerevisiae. 1. Experimental observations. Biotechnol. Bioeng. 55, 305-316 (1997). (Pubitemid 27291199)
32. Zhu, T., Bailey, M.F., Angley, L.M., Cooper, T.F. & Dobson, R.C.J. The quaternary structure of pyruvate kinase type 1 from Escherichia coli at low nanomolar concentrations. Biochimie 92, 116-120 (2010).
33. Ogawa, T., Mori, H., Tomita, M. & Yoshino, M. Inhibitory effect of phosphoenolpyruvate on glycolytic enzymes in Escherichia coli. Res. Microbiol. 158, 159-163 (2007). (Pubitemid 46341719)
34. Kern, D. & Zuiderweg, E.R. The role of dynamics in allosteric regulation. Curr. Opin. Struct. Biol. 13, 748-757 (2003). (Pubitemid 37522151)
35. Walsh, K. & Koshland, D.E. Branch point control by the phosphorylation state of isocitrate dehydrogenase-a quantitative examination of fluxes during a regulatory transition. J. Biol. Chem. 260, 8430-8437 (1985). (Pubitemid 15011813)
36. Stadtman, E.R. The story of glutamine synthetase regulation. J. Biol. Chem. 276, 44357-44364 (2001). (Pubitemid 37391202)
37. Kai, Y., Matsumura, H. & Izui, K. Phosphoenolpyruvate carboxylase: three-dimensional structure and molecular mechanisms. Arch. Biochem. Biophys. 414, 170-179 (2003). (Pubitemid 36627349)
38. Gonzalez, C.F. et al. Molecular basis of formaldehyde detoxification characterization of two S-formylglutathione hydrolases from Escherichia coli, Frmb and Yeig. J. Biol. Chem. 281, 14514-14522 (2006). (Pubitemid 43848382)
39. Brown, G. et al. Structural and biochemical characterization of the type II fructose-1,6-bisphosphatase GlpX from Escherichia coli. J. Biol. Chem. 284, 3784-3792 (2009).
40. Lee, M., Chan, C.W., Guss, J.M., Christopherson, R.I. & Maher, M.J. Dihydroorotase from Escherichia coli: loop movement and cooperativity between subunits. J. Mol. Biol. 348, 523-533 (2005). (Pubitemid 40515667)
41. Song, W.J. & Jackowski, S. Kinetics and regulation of pantothenate kinase from Escherichia coli. J. Biol. Chem. 269, 27051-27058 (1994). (Pubitemid 24332909)
42. Bhasin, M., Billinsky, J.L. & Palmer, D.R.J. Steady-state kinetics and molecular evolution of Escherichia coli MenD [(1R,6R)-2-succinyl-6-hydroxy- 2,4-cyclohexadiene-1-carboxylate synthase], an anomalous thiamin diphosphate-dependent decarboxylase-carboligase. Biochemistry 42, 13496-13504 (2003). (Pubitemid 37444899)
43. Broglie, K.E. & Takahashi, M. Fluorescence studies of threonine-promoted conformational transitions in aspartokinase I using the substrate analogue 2′(3′)-O-(2,4,6-trinitrophenyl)adenosine 5′-triphosphate. J. Biol. Chem. 258, 12940-12946 (1983).
44. Eisenstein, E., Yu, H.D. & Schwarz, F.P. Cooperative binding of the feedback modifiers isoleucine and valine to biosynthetic threonine deaminase from Escherichia coli. J. Biol. Chem. 269, 29423-29429 (1994). (Pubitemid 24365087)
45. Yuan, J., Bennett, B.D. & Rabinowitz, J.D. Kinetic flux profiling for quantitation of cellular metabolic fluxes. Nat. Protoc. 3, 1328-1340 (2008).
46. Gutnick, D., Calvo, J.M., Klopotow, T. & Ames, B.N. Compounds which serve as sole source of carbon or nitrogen for Salmonella typhimurium LT-2. J. Bacteriol. 100, 215-219 (1969).
47. Lu, W., Bennett, B.D. & Rabinowitz, J.D. Analytical strategies for LC-MS-based targeted metabolomics. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 871, 236-242 (2008).
48. Lu, W. et al. Metabolomic analysis via reversed-phase ion-pairing liquid chromatography coupled to a stand alone orbitrap mass spectrometer. Anal. Chem. 82, 3212-3221 (2010).
49. Kitagawa, M. et al. Complete set of ORF clones of Escherichia coli ASKA library (a complete Set of E. coli K-12 ORF archive): unique resources for biological research. DNA Res. 12, 291-299 (2005).
50. Baba, T. et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2, 2006.0008 (2006).