Why in vivo may not equal in vitro - New effectors revealed by measurement of enzymatic activities under the same in vivo-like assay conditions

FEBS Journal

Volumn 279, Issue 22, 2012, Pages 4145-4159

  García Contreras, Rodolfo ^a,b   Vos, Paul ^a   Westerhoff, Hans V ^a,c,d   Boogerd, Fred C ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b INSTITUTO NACIONAL DE CARDIOLOGÍA IGNACIO CHÁVEZ   (Mexico)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

enzyme capacities; glycolysis; in vitro; in vivo; nitrogen assimilation

Indexed keywords

6 PHOSPHOFRUCTOKINASE; CHLORIDE; ENOLASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUCOSE 6 PHOSPHATE ISOMERASE; GLUTAMATE AMMONIA LIGASE; GLUTAMATE DEHYDROGENASE; GLUTAMATE SYNTHASE; GLUTAMIC ACID; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOLYTIC ENZYME; MAGNESIUM; NITROGEN; PHOSPHATE; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE MUTASE; POTASSIUM; SODIUM; SULFATE; TRIOSEPHOSPHATE ISOMERASE;

ARTICLE; CHEMICAL ANALYSIS; CYTOSOL; DYNAMICS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME INHIBITION; ENZYME KINETICS; ESCHERICHIA COLI; EXTRACTION; IN VITRO STUDY; IN VIVO STUDY; MEASUREMENT; NITROGEN FIXATION; NONHUMAN; PRIORITY JOURNAL;

BIOLOGICAL ASSAY; CARBON; CYTOSOL; FRUCTOSE-BISPHOSPHATE ALDOLASE; GLUCOSE-6-PHOSPHATE ISOMERASE; GLYCERALDEHYDE 3-PHOSPHATE; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; GLYCOLYSIS; HUMANS; NITROGEN; PHOSPHATES; PHOSPHOFRUCTOKINASE-1; PHOSPHOGLYCERATE KINASE; PHOSPHOGLYCERATE MUTASE; PHOSPHOPYRUVATE HYDRATASE; POTASSIUM; PYRUVATE KINASE; TRIOSE-PHOSPHATE ISOMERASE;

ESCHERICHIA COLI;

EID: 84868194895     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12007     Document Type: Article

References (84)

1. Sauer U, Lasko DR, Fiaux J, Hochuli M, Glaser R, Szyperski T, Wüthrich K, &, Bailey JE, (1999) Metabolic flux ratio analysis of genetic and environmental modulations of Escherichia coli central carbon metabolism. J Bacteriol 181, 6679-6688. (Pubitemid 29517982)
2. Reitzer L, (2003) Nitrogen assimilation and global regulation in Escherichia coli. Annu Rev Microbiol 57, 155-176. (Pubitemid 37392939)
3. Ingraham JL, &, Neidhardt FC, (1996) Escherichia coli & Salmonella typhimurium: Cellular & Molecular Biology, 2nd edn. ASM press, Washington DC.
4. Teusink B, Walsh MC, van Dam K, &, Westerhoff HV, (1998) The danger of metabolic pathways with turbo design. Trends Biochem Sci 23, 162-169. (Pubitemid 28261032)
5. Haanstra JR, van Tuijl A, Kessler P, Reijnders W, Michels PA, Westerhoff HV, Parsons M, &, Bakker BM, (2008) Compartmentation prevents a lethal turbo-explosion of glycolysis in trypanosomes. Proc Natl Acad Sci USA 105, 17718-17723.
6. Haanstra JR, Kerkhoven EJ, van Tuijl A, Blits M, Wurst M, van Nuland R, Albert MA, Michels PA, Bouwman J, Clayton C, et al,. (2011) A domino effect in drug action: from metabolic assault towards parasite differentiation. Mol Microbiol 79, 94-108.
7. Bruggeman FJ, van Heeswijk WC, Boogerd FC, &, Westerhoff HV, (2000) Macromolecular intelligence in microorganisms. Biol Chem 381, 965-972.
8. Bruggeman FJ, Boogerd FC, &, Westerhoff HV, (2005) The multifarious short-term regulation of ammonium assimilation of Escherichia coli: dissection using an in silico replica. FEBS J 272, 1965-1985. (Pubitemid 40547252)
9. Lodeiro A, &, Melgarejo A, (2008) Robustness in Escherichia coli glutamate and glutamine synthesis studied by a kinetic model. J Biol Phys 34, 91-106.
10. Hart Y, Madar D, Yuan J, Bren A, Mayo AE, Rabinowitz JD, &, Alon U, (2011) Robust control of nitrogen assimilation by a bifunctional enzyme in E. coli. Mol Cell 41, 117-127.
11. Masaki K, Maeda K, &, Kurata H, (2012) Biological design principles of complex feedback modules in the E. coli ammonia assimilation system. Artif Life 18, 53-90.
12. Chang A, Scheer M, Grote A, Schomburg I, &, Schomburg D, (2009) BRENDA, AMENDA and FRENDA the enzyme information system: new content and tools in 2009. Nucleic Acids Res 37, D588-D592.
13. Scheer M, Grote A, Chang A, Schomburg I, Munaretto C, Rother M, Söhngen C, Stelzer M, Thiele J, &, Schomburg D, (2011) BRENDA, the enzyme information system in 2011. Nucleic Acids Res 39, D670-D676.
14. Snoep JL, (2005) The Silicon Cell initiative: working towards a detailed kinetic description at the cellular level. Curr Opin Biotechnol 16, 336-343. (Pubitemid 40806472)
15. Visser D, Schmid JW, Mauch K, Reuss M, &, Heijnen JJ, (2004) Optimal re-design of primary metabolism in Escherichia coli using linlog kinetics. Metab Eng 6, 378-390. (Pubitemid 39379472)
16. Strand R, (1999) Towards a useful philosophy of biochemistry: sketches and examples. Found Chem 1, 269-292.
17. Jacob C, (2002) Philosophy and biochemistry: research at the interface between chemistry and biology. Found Chem 4, 97-125.
18. Srivastava DK, &, Bernhard SA, (1986) Metabolite transfer via enzyme-enzyme complexes. Science 234, 1081-1086. (Pubitemid 17206186)
19. Westerhoff HV, Melandri BA, Venturoli G, Azzone GF, &, Kell DB, (1984) A minimal hypothesis for membrane-linked free-energy transduction. The role of independent, small coupling units. Biochim Biophys Acta 768, 257-292. (Pubitemid 15194363)
20. Arakawa K, Yamada Y, Shinoda K, Nakayama Y, &, Tomita M, (2006) GEM System: automatic prototyping of cell-wide metabolic pathway models from genomes. BMC Bioinformatics 7, 168.
21. Slonczewski JL, Rosen BP, Alger JR, &, Macnab RM, (1981) pH homeostasis in Escherichia coli: measurement by 31P nuclear magnetic resonance of methylphosphonate and phosphate. Proc Natl Acad Sci USA 78, 6271-6275. (Pubitemid 12174865)
22. Booth IR, (1985) Regulation of cytoplasmic pH in bacteria. Microbiol Rev 49, 359-378. (Pubitemid 16209979)
23. Castle AM, Macnab RM, &, Shulman RG, (1986) Coupling between the sodium and proton gradients in respiring Escherichia coli cells measured by 23Na and 31P nuclear magnetic resonance. J Biol Chem 261, 7797-7806. (Pubitemid 17208704)
24. Slonczewski JL, Fujisawa M, Dopson M, &, Krulwich TA, (2009) Cytoplasmic pH measurement and homeostasis in bacteria and archaea. Adv Microb Physiol 55, 1-79, 317.
25. van Eunen K, Bouwman J, Daran-Lapujade P, Postmus J, Canelas AB, Mensonides FI, Orij R, Tuzun I, van den Brink J, Smits GJ, et al,. (2010) Measuring enzyme activities under standardized in vivo-like conditions for systems biology. FEBS J 277, 749-760.
26. Goel A, Santos F, de Vos WM, Teusink B, &, Molenaar D, (2011) Standardized assay medium to measure Lactococcus lactis enzyme activities while mimicking intracellular conditions. Appl Environ Microbiol 78, 134-143.
27. Ogawa T, Mori H, Tomita M, &, Yoshino M, (2007) Inhibitory effect of phosphoenolpyruvate on glycolytic enzymes in Escherichia coli. Res Microbiol 158, 159-163. (Pubitemid 46341719)
28. Chassagnole C, Noisommit-Rizzi N, Schmid JW, Mauch K, &, Reuss M, (2002) Dynamic modeling of the central carbon metabolism of Escherichia coli. Biotechnol Bioeng 79, 53-73. (Pubitemid 34746765)
29. Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ, &, Rabinowitz JD, (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5, 593-599.
30. Hoque MA, Ushiyama H, Tomita M, &, Shimizu K, (2005) Dynamic responses of the intracellular metabolite concentrations of the wild type and pykA mutant Escherichia coli against pulse addition of glucose or NH3 under those limiting continuous cultures. Biochem Eng J 26, 38-49. (Pubitemid 41219796)
31. Minton AP, (2001) The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276, 10577-10580. (Pubitemid 38089223)
32. Rohwer JM, Postma PW, Kholodenko BN, &, Westerhoff HV, (1998) Implications of macromolecular crowding for signal transduction and metabolite channeling. Proc Natl Acad Sci USA 95, 10547-10552. (Pubitemid 28413104)
33. Mason PW, Carbone DP, Cushman RA, &, Waggoner AS, (1981) The importance of inorganic phosphate in regulation of energy metabolism of Streptococcus lactis. J Biol Chem 256, 1861-1866. (Pubitemid 11106698)
34. Brauer MJ, Yuan J, Bennett BD, Lu W, Kimball E, Botstein D, &, Rabinowitz JD, (2006) Conservation of the metabolomic response to starvation across two divergent microbes. Proc Natl Acad Sci USA 103, 19302-19307. (Pubitemid 46026027)
35. Peterkofsky A, (1988) Redistribution of phosphate pools and the regulation of Escherichia coli adenylate cyclase activity. Arch Biochem Biophys 265, 227-233.
36. Lee CR, Cho SH, Yoon MJ, Peterkofsky A, &, Seok YJ, (2007) Escherichia coli enzyme IIANtr regulates the K+ transporter TrkA. Proc Natl Acad Sci USA 104, 4124-4129. (Pubitemid 47181589)
37. Dinnbier U, Limpinsel E, Schmid R, &, Bakker EP, (1988) Transient accumulation of potassium glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations. Arch Microbiol 150, 348-357.
38. Roe AJ, McLaggan D, Davidson I, O'Byrne C, &, Booth IR, (1998) Perturbation of anion balance during inhibition of growth of Escherichia coli by weak acids. J Bacteriol 180, 767-772. (Pubitemid 28084199)
39. Foster JW, (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2, 898-907. (Pubitemid 39561806)
40. Yuan J, Doucette CD, Fowler WU, Feng XJ, Piazza M, Rabitz HA, Wingreen NS, &, Rabinowitz JD, (2009) Metabolomics-driven quantitative analysis of ammonia assimilation in E. coli. Mol Syst Biol 5, 302.
41. Miller RE, &, Stadtman ER, (1972) Glutamate synthase from Escherichia coli. An iron-sulfide flavoprotein. J Biol Chem 247, 7407-7419.
42. Rendina AR, &, Orme-Johnson WH, (1978) Glutamate synthase: on the kinetic mechanism of the enzyme from Escherichia coli W. Biochemistry 17, 5388-5393. (Pubitemid 9096417)
43. van Hoek P, van Dijken JP, &, Pronk JT, (2000) Regulation of fermentative capacity and levels of glycolytic enzymes in chemostat cultures of Saccharomyces cerevisiae. Enzyme Microb Technol 26, 724-736. (Pubitemid 30345539)
44. Spring TG, &, Wold F, (1971) The purification and characterization of Escherichia coli enolase. J Biol Chem 246, 6797-6802.
45. Ohashi Y, Hirayama A, Ishikawa T, Nakamura S, Shimizu K, Ueno Y, Tomita M, &, Soga T, (2008) Depiction of metabolome changes in histidine-starved Escherichia coli by CE-TOFMS. Mol BioSyst 4, 135-147.
46. Feist AM, Henry CS, Reed JL, Krummenacker M, Joyce AR, Karp PD, Broadbelt LJ, Hatzimanikatis V, &, Palsson BO, (2007) A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol Syst Biol 3, 121.
47. Reaves ML, &, Rabinowitz JD, (2011) Metabolomics in systems microbiology. Curr Opin Biotechnol 22, 17-25.
48. van der Werf MJ, Overkamp KM, Muilwijk B, Coulier L, &, Hankemeier T, (2007) Microbial metabolomics: toward a platform with full metabolome coverage. Anal Biochem 370, 17-25. (Pubitemid 47404495)
49. Feist AM, &, Palsson BO, (2008) The growing scope of applications of genome-scale metabolic reconstructions using Escherichia coli. Nat Biotechnol 26, 659-667. (Pubitemid 351824691)
50. Keseler IM, Bonavides-Martínez C, Collado-Vides J, Gama-Castro S, Gunsalus RP, Johnson DA, Krummenacker M, Nolan LM, Paley S, Paulsen IT, et al,. (2009) EcoCyc: a comprehensive view of Escherichia coli biology. Nucleic Acids Res 37, D464-D470.
51. Keseler IM, Collado-Vides J, Santos-Zavaleta A, Peralta-Gil M, Gama-Castro S, Muñiz-Rascado L, Bonavides-Martinez C, Paley S, Krummenacker M, Altman T, et al,. (2011) EcoCyc: a comprehensive database of Escherichia coli biology. Nucleic Acids Res 39, D583-D590.
52. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, Aach J, Ansorge W, Ball CA, Causton HC, et al,. (2001) Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 29, 365-371. (Pubitemid 34326681)
53. Fiehn O, Kristal B, van Ommen B, Sumner LW, Sansone SA, Taylor C, Hardy N, &, Kaddurah-Daouk R, (2006) Establishing reporting standards for metabolomic and metabonomic studies: a call for participation. OMICS 10, 158-163. (Pubitemid 44298603)
54. MSI Board Members, Sansone SA, Fan T, Goodacre R, Griffin JL, Hardy NW, Kaddurah-Daouk R, Kristal BS, Lindon J, Mendes P, et al,. (2007) The metabolomics standards initiative. Nat Biotechnol 25, 846-848.
55. Sansone SA, Fan T, Goodacre R, Griffin JL, Hardy NW, Kaddurah-Daouk R, Kristal BS, Lindon J, Mendes P, Morrison N, et al,. (2007) The metabolomics standards initiative. Nat Biotechnol 25, 846-848.
56. Hucka M, Finney A, Sauro HM, Bolouri H, Doyle JC, Kitano H, Arkin AP, Bornstein BJ, Bray D, Cornish-Bowden A, et al,. (2003) The systems biology markup language (SBML): a medium for representation and exchange of biochemical network models. Bioinformatics 19, 524-531. (Pubitemid 36336519)
57. Krulwich TA, Sachs G, &, Padan E, (2011) Molecular aspects of bacterial pH sensing and homeostasis. Nat Rev Microbiol 9, 330-343.
58. Diez-Gonzalez F, &, Russell JB, (1997) The ability of Escherichia coli O157:H7 to decrease its intracellular pH and resist the toxicity of acetic acid. Microbiology 143 (Pt 4), 1175-1180. (Pubitemid 27207786)
59. Measures JC, (1975) Role of amino acids in osmoregulation of non-halophilic bacteria. Nature 257, 398-400.
60. Wen Z, &, Morrison M, (1997) Glutamate dehydrogenase activity profiles for type strains of ruminal Prevotella spp. Appl Environ Microbiol 63, 3314-3317. (Pubitemid 27337837)
61. Schultz SG, Wilson NL, &, Epstein W, (1962) Cation transport in Escherichia coli. II. Intracellular chloride concentration. J Gen Physiol 46, 159-166.
62. Cayley S, Lewis BA, Guttman HJ, &, Record MT Jr, (1991) Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity. Implications for protein-DNA interactions in vivo. J Mol Biol 222, 281-300. (Pubitemid 121004007)
63. Richey B, Cayley DS, Mossing MC, Kolka C, Anderson CF, Farrar TC, &, Record MT Jr, (1987) Variability of the intracellular ionic environment of Escherichia coli. Differences between in vitro and in vivo effects of ion concentrations on protein-DNA interactions and gene expression. J Biol Chem 262, 7157-7164.
64. Booth IR, &, Higgins CF, (1990) Enteric bacteria and osmotic stress: intracellular potassium glutamate as a secondary signal of osmotic stress? FEMS Microbiol Rev 6, 239-246. (Pubitemid 20211797)
65. McLaggan D, Naprstek J, Buurman ET, &, Epstein W, (1994) Interdependence of K+ and glutamate accumulation during osmotic adaptation of Escherichia coli. J Biol Chem 269, 1911-1917. (Pubitemid 24035392)
66. Yan D, Ikeda TP, Shauger AE, &, Kustu S, (1996) Glutamate is required to maintain the steady-state potassium pool in Salmonella typhimurium. Proc Natl Acad Sci USA 93, 6527-6531. (Pubitemid 26230340)
67. Stribling D, &, Perham RN, (1973) Purification and characterization of two fructose diphosphate aldolases from Escherichia coli (Crookes' strain). Biochem J 131, 833-841.
68. Baldwin SA, &, Perham RN, (1978) Novel kinetic and structural properties of the class-I D-fructose 1,6-bisphosphate aldolase from Escherichia coli (Crookes' strain). Biochem J 169, 643-652. (Pubitemid 8281769)
69. + -dependent and -independent enzymes. J Biol Chem 281, 30717-30724. (Pubitemid 44582127)
70. Prasad S, Wright KJ, Banerjee Roy D, Bush LA, Cantwell AM, &, Di Cera E, (2003) Redesigning the monovalent cation specificity of an enzyme. Proc Natl Acad Sci USA 100, 13785-13790. (Pubitemid 37499144)
71. 2+ ion and effect of phosphate on the activity of Escherichia coli phosphofructokinase-2: regulatory properties of a ribokinase family member. Biochemistry 45, 9291-9299. (Pubitemid 44156392)
72. Waygood EB, Rayman MK, &, Sanwal BD, (1975) The control of pyruvate kinases of Escherichia coli. II. Effectors and regulatory properties of the enzyme activated by ribose 5-phosphate. Can J Biochem 53, 444-454.
73. Somani BL, Valentini G, &, Malcovati M, (1977) Purification and molecular properties of the AMP-activated pyruvate kinase from Escherichia coli. Biochim Biophys Acta 482, 52-63. (Pubitemid 8087906)
74. Booth IR, Ferguson GP, Miller S, Li C, Gunasekera B, &, Kinghorn S, (2003) Bacterial production of methylglyoxal: a survival strategy or death by misadventure? Biochem Soc Trans 31, 1406-1408. (Pubitemid 38030987)
75. Westerhoff HV, &, Palsson BO, (2004) The evolution of molecular biology into systems biology. Nat Biotechnol 22, 1249-1252. (Pubitemid 39336777)
76. Bruggeman FJ, &, Westerhoff HV, (2007) The nature of systems biology. Trends Microbiol 15, 45-50. (Pubitemid 46043550)
77. Teusink B, Passarge J, Reijenga CA, Esgalhado E, van der Weijden CC, Schepper M, Walsh MC, Bakker BM, van Dam K, Westerhoff HV, et al,. (2000) Can yeast glycolysis be understood in terms of in vitro kinetics of the constituent enzymes? Testing biochemistry. Eur J Biochem 267, 5313-5329.
78. Pritchard L, &, Kell DB, (2002) Schemes of flux control in a model of Saccharomyces cerevisiae glycolysis. Eur J Biochem 269, 3894-3904. (Pubitemid 34994884)
79. Westerhoff HV, Winder C, Messiha H, Simeonidis E, Adamczyk M, Verma M, Bruggeman FJ, &, Dunn W, (2009) Systems biology: the elements and principles of life. FEBS Lett 583, 3882-3890.
80. Teusink B, &, Westerhoff HV, (2000) 'Slave' metabolites and enzymes. A rapid way of delineating metabolic control. Eur J Biochem 267, 1889-1893. (Pubitemid 30185274)
81. Bakker BM, Mensonides FI, Teusink B, van Hoek P, Michels PA, &, Westerhoff HV, (2000) Compartmentation protects trypanosomes from the dangerous design of glycolysis. Proc Natl Acad Sci USA 97, 2087-2092. (Pubitemid 30134026)
82. Olah J, Klivenyi P, Gardian G, Vecsei L, Orosz F, Kovacs GG, Westerhoff HV, &, Ovádi J, (2008) Increased glucose metabolism and ATP level in brain tissue of Huntington's disease transgenic mice. FEBS J 275, 4740-4755.
83. Backman K, Chen YM, &, Magasanik B, (1981) Physical and genetic characterization of the glnA-glnG region of the Escherichia coli chromosome. Proc Natl Acad Sci USA 78, 3743-3747.
84. Evans GCT, Herbert D, &, Tempest DW, (1970) The continuous cultivation of microorganisms-construction of a chemostat. In Methods in Microbiology (, Norris JR, &, Ribbons DW, eds), pp. 277-327. Academic Press, London.