The pivotal regulator GlnB of Escherichia coli is engaged in subtle and context-dependent control

FEBS Journal

Volumn 276, Issue 12, 2009, Pages 3324-3340

  Van Heeswijk, Wally C ^a   Molenaar, Douwe ^a   Hoving, Sjouke ^a,c   Westerhoff, Hans V ^a,b  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Glutamine synthetase; Metabolic control analysis; PII; Signal transduction cascades; Ultrasensitivity

Indexed keywords

AMMONIA; GLUTAMATE AMMONIA LIGASE; PROTEIN GLNB; PROTEIN GLNK; REGULATOR PROTEIN; UNCLASSIFIED DRUG;

ADENYLATION; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE EXPRESSION; IN VIVO STUDY; METABOLIC REGULATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STEADY STATE; WILD TYPE;

ADENOSINE MONOPHOSPHATE; ALGORITHMS; AMMONIA; BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; GLUTAMATE-AMMONIA LIGASE; ISOPROPYL THIOGALACTOSIDE; MODELS, BIOLOGICAL; MUTATION; NUCLEOTIDYLTRANSFERASES; PII NITROGEN REGULATORY PROTEINS; URIDINE MONOPHOSPHATE;

ESCHERICHIA COLI;

EID: 66249140236     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07058.x     Document Type: Article

References (72)

1. Chock PB Stadtman ER (1977) Superiority of interconvertible enzyme cascades in metabolite regulation: analysis of multicyclic systems. Proc Natl Acad Sci USA 74, 2766 2770. (Pubitemid 8150817)
2. Stadtman ER Chock PB (1977) Superiority of interconvertible enzyme cascades in metabolic regulation: analysis of monocyclic systems. Proc Natl Acad Sci USA 74, 2761 2765. (Pubitemid 8150816)
3. Goldbeter A Koshland DE Jr. (1981) An amplified sensitivity arising from covalent modification in biological systems. Proc Natl Acad Sci USA 78, 6840 6844. (Pubitemid 12216857)
4. Goldbeter A Koshland DE Jr. (1984) Ultrasensitivity in biochemical systems controlled by covalent modification. Interplay between zero-order and multistep effects. J Biol Chem 259, 14441 14447. (Pubitemid 15222262)
5. Cárdenas ML Cornish-Bowden A (1989) Characteristics necessary for an interconvertible enzyme cascade to generate a highly sensitive response to an effector. Biochem J 257, 339 345. (Pubitemid 19040902)
6. Small JR Fell DA (1990) Covalent modification and metabolic control analysis. Modification to the theorems and their application to metabolic systems containing covalently modifiable enzymes. Eur J Biochem 191, 405 411. (Pubitemid 20233755)
7. Szedlacsek SE, Cárdenas ML Cornish-Bowden A (1992) Response coefficients of interconvertible enzyme cascades towards effectors that act on one or both modifier enzymes. Eur J Biochem 204, 807 813.
8. Ortega F, Ehrenberg M, Acerenza L, Westerhoff HV, Mas F Cascante M (2002) Sensitivity analysis of metabolic cascades catalyzed by bifunctional enzymes. Mol Biol Rep 29, 211 215.
9. Ortega F, Acerenza L, Westerhoff HV, Mas F Cascante M (2002) Product dependence and bifunctionality compromise the ultrasensitivity of signal transduction cascades. Proc Natl Acad Sci USA 99, 1170 1175. (Pubitemid 34136465)
10. Kacser H Burns JA (1973) The control of flux. Symp Soc Exp Biol 27, 65 104.
11. Heinrich R Rapoport TA (1974) A linear steady-state treatment of enzymatic chains. General properties, control and effector strength. Eur J Biochem 42, 89 95.
12. Fell DA (1992) Metabolic control analysis: a survey of its theoretical and experimental development. Biochem J 286, 313 330.
13. Groen AK, Wanders RJ, Westerhoff HV, van der Meer R Tager JM (1982) Quantification of the contribution of various steps to the control of mitochondrial respiration. J Biol Chem 257, 2754 2757.
14. +-ATPase. Proc Natl Acad Sci USA 90, 8068 8072. (Pubitemid 23260856)
15. +-ATPase and inverse respiratory control in Escherichia coli. EMBO J 12, 1277 1282. (Pubitemid 23112782)
16. Kahn D Westerhoff HV (1991) Control theory of regulatory cascades. J Theor Biol 153, 255 285.
17. Ninfa AJ, Jiang P, Atkinson MR Peliska JA (2000) Integration of antagonistic signals in the regulation of nitrogen assimilation in Escherichia coli. Curr Top Cell Regul 36, 31 75.
18. Ninfa AJ Jiang P (2005) PII signal transduction proteins: sensors of alpha-ketoglutarate that regulate nitrogen metabolism. Curr Opin Microbiol 8, 168 173. (Pubitemid 40417958)
19. Reitzer LJ (1996) Ammonia assimilation and the biosynthesis of glutamine, glutamate, aspartate, asparagine, l-alanine, and d-alanine. In Escherichia coli and Salmonella. Cellular and Molecular Biology (Neidhardt FC, Curtiss R III., Ingraham JL, Lin ECC, Low KB, Magasanik B, Reznikoff WS, Riley M, Schaechter M Umbarger HE, eds), pp. 391 407. American Society for Microbiology, Washington, DC.
20. Prusiner S Stadtman ER (eds 1973) The Enzymes of Glutamine Metabolism. Academic Press, New York, NY.
21. Almassy RJ, Janson CA, Hamlin R, Xuong NH Eisenberg D (1986) Novel subunit-subunit interactions in the structure of glutamine synthetase. Nature 323, 304 309. (Pubitemid 16033127)
22. Jiang P, Mayo AE Ninfa AJ (2007) Escherichia coli glutamine synthetase adenylyltransferase (ATase, EC 2.7.7.49): kinetic characterization of regulation by PII, PII-UMP, glutamine, and α-ketoglutarate. Biochemistry 46, 4133 4146. (Pubitemid 46536075)
23. Jaggi R, van Heeswijk WC, Westerhoff HV, Ollis DL Vasudevan SG (1997) The two opposing activities of adenylyl transferase reside in distinct homologous domains, with intramolecular signal transduction. EMBO J 16, 5562 5571. (Pubitemid 27399848)
24. Jiang P, Pioszak AA Ninfa AJ (2007) Structure-function analysis of glutamine synthetase adenylyltransferase (ATase, EC 2.7.7.49) of Escherichia coli. Biochemistry 46, 4117 4132. (Pubitemid 46536074)
25. Clancy P, Xu Y, van Heeswijk WC, Vasudevan SG Ollis DL (2007) The domains carrying the opposing activities in adenylyltransferase are separated by a central regulatory domain. FEBS J 274, 2865 2877. (Pubitemid 46800553)
26. Jiang P, Peliska JA Ninfa AJ (1998) Enzymological characterization of the signal-transducing uridylyltransferase/uridylyl-removing enzyme (EC 2.7.7.59) of Escherichia coli and its interaction with the PII protein. Biochemistry 37, 12782 12794. (Pubitemid 28433509)
27. II protein: purification, crystallization and oligomeric structure. FEBS Lett 337, 255 258. (Pubitemid 2036854)
28. II. Structure 2, 981 990. (Pubitemid 2154317)
29. Kamberov ES, Atkinson MR Ninfa AJ (1995) The Escherichia coli PII signal transduction protein is activated upon binding 2-ketoglutarate and ATP. J Biol Chem 270, 17797 17807.
30. Keener J Kustu S (1988) Protein kinase and phosphoprotein phosphatase activities of nitrogen regulatory proteins NTRB and NTRC of enteric bacteria: roles of the conserved amino-terminal domain of NTRC. Proc Natl Acad Sci USA 85, 4976 4980.
31. Jiang P, Peliska JA Ninfa AJ (1998) Reconstitution of the signal-transduction bicyclic cascade responsible for the regulation of Ntr gene transcription in Escherichia coli. Biochemistry 37, 12795 12801. (Pubitemid 28433510)
32. II in Escherichia coli: a new regulatory protein in the glutamine synthetase cascade. FEMS Microbiol Lett 132, 153 157.
33. II protein in the regulation of glutamine synthetase in Escherichia coli. Mol Microbiol 21, 133 146. (Pubitemid 26233088)
34. Atkinson MR Ninfa AJ (1999) Characterization of the GlnK protein of Escherichia coli. Mol Microbiol 32, 301 313. (Pubitemid 29178697)
35. Xu Y, Cheah E, Carr PD, van Heeswijk WC, Westerhoff HV, Vasudevan SG Ollis DL (1998) GlnK, a PII-homologue: structure reveals ATP binding site and indicates how the T-loops may be involved in molecular recognition. J Mol Biol 282, 149 165. (Pubitemid 28418666)
36. Atkinson MR, Blauwkamp TA, Bondarenko V, Studitsky V Ninfa AJ (2002) Activation of the glnA, glnK, and nac promoters as Escherichia coli undergoes the transition from nitrogen excess growth to nitrogen starvation. J Bacteriol 184, 5358 5363.
37. 2 regulatory elements. Nucleic Acids Res 25, 1203 1210. (Pubitemid 27303212)
38. Müller-Hill B (1975) Lac repressor and lac operator. Prog Biophys Mol Biol 30, 227 252.
39. Calos MP Miller JH (1981) The DNA sequence change resulting from the IQ1 mutation, which greatly increases promoter strength. Mol Gen Genet 183, 559 560. (Pubitemid 12216647)
40. Jensen PR, Westerhoff HV Michelsen O (1993) The use of lac-type promoters in control analysis. Eur J Biochem 211, 181 191. (Pubitemid 23039512)
41. Maheswaran M Forchhammer K (2003) Carbon-source-dependent nitrogen regulation in Escherichia coli is mediated through glutamine-dependent GlnB signalling. Microbiology 149, 2163 2172. (Pubitemid 37038422)
42. van Heeswijk WC, Rabenberg M, Westerhoff HV Kahn D (1993) The genes of the glutamine synthetase adenylylation cascade are not regulated by nitrogen in Escherichia coli. Mol Microbiol 9, 443 457. (Pubitemid 23248757)
43. Javelle A, Severi E, Thornton J Merrick M (2004) Ammonium sensing in Escherichia coli. Role of the ammonium transporter AmtB and AmtB-GlnK complex formation. J Biol Chem 279, 8530 8538. (Pubitemid 38295906)
44. Senior PJ (1975) Regulation of nitrogen metabolism in Escherichia coli and Klebsiella aerogenes: studies with the continuous-culture technique. J Bacteriol 123, 407 418.
45. Atkinson MR, Kamberov ES, Weiss RL Ninfa AJ (1994) Reversible uridylylation of the Escherichia coli PII signal transduction protein regulates its ability to stimulate the dephosphorylation of the transcription factor nitrogen regulator I (NRI or NtrC). J Biol Chem 269, 28288 28293. (Pubitemid 24354569)
46. Mutalik VK, Shah P Venkatesh KV (2003) Allosteric interactions and bifunctionality make the response of glutamine synthetase cascade system of Escherichia coli robust and ultrasensitive. J Biol Chem 278, 26327 26332. (Pubitemid 36876770)
47. Oliver SG (1996) From DNA sequence to biological function. Nature 379, 597 600. (Pubitemid 26052817)
48. Teusink B, Baganz F, Westerhoff HV Oliver S (1998) Metabolic control analysis as a tool in the elucidation of the function of novel genes. In Yeast Genome Analysis. Methods in Microbiology, Vol. 26 (Tuite M Brown C, eds Academic Press, New York, NY.
49. van Heeswijk WC, Wen D, Clancy P, Jaggi R, Ollis DL, Westerhoff HV Vasudevan SG (2000) The Escherichia coli signal transducers PII (GlnB) and GlnK form heterotrimers in vivo: fine tuning the nitrogen signal cascade. Proc Natl Acad Sci USA 97, 3942 3947. (Pubitemid 30226066)
50. Rhee SG, Chock PB Stadtman ER (1989) Regulation of Escherichia coli glutamine synthetase. Adv Enzymol Relat Areas Mol Biol 62, 37 92.
51. Jiang P Ninfa AJ (2007) Escherichia coli PII signal transduction protein controlling nitrogen assimilation acts as a sensor of adenylate energy charge in vitro. Biochemistry 46, 12979 12996. (Pubitemid 350086218)
52. Ninfa AJ Atkinson MR (2000) PII signal transduction proteins. Trends Microbiol 8, 172 179. (Pubitemid 30224753)
53. Commichau FM, Forchhammer K Stülke J (2006) Regulatory links between carbon and nitrogen metabolism. Curr Opin Microbiol 9, 167 172.
54. Forchhammer K, Hedler A, Strobel H Weiss V (1999) Heterotrimerization of PII-like signalling proteins: implications for PII-mediated signal transduction systems. Mol Microbiol 33, 338 349. (Pubitemid 29322520)
55. Son HS Rhee SG (1987) Cascade control of Escherichia coli glutamine synthetase. Purification and properties of PII protein and nucleotide sequence of its structural gene. J Biol Chem 262, 8690 8695.
56. van der Vlag J, van't Hof R, van Dam K Postma PW (1995) Control of glucose metabolism by the enzymes of the glucose phosphotransferase system in Salmonella typhimurium. Eur J Biochem 230, 170 182.
57. Brenchley JE Magasanik B (1974) Mutants of Klebsiella aerogenes lacking glutamate dehydrogenase. J Bacteriol 117, 544 550.
58. Neidhardt FC, Bloch PL Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119, 736 747.
59. Chang AC Cohen SN (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134, 1141 1156. (Pubitemid 8354538)
60. Christie GE, Farnham PJ Platt T (1981) Synthetic sites for transcription termination and a functional comparison with tryptophan operon termination sites in vitro. Proc Natl Acad Sci USA 78, 4180 4184.
61. Jensen LB (1992) Biological containment of bacteria designed for deliberate release. PhD Thesis, Technical University of Denmark, Lyngby, Denmark.
62. Jensen LB, Ramos JL, Kaneva Z Molin S (1993) A substrate-dependent biological containment system for Pseudomonas putida based on the Escherichia coli gef gene. Appl Environ Microbiol 59, 3713 3717. (Pubitemid 23327573)
63. Herrero M, De Lorenzo V Timmis KN (1990) Transposon vectors containing non-antibiotic resistance selection markers for cloning and stable chromosomal insertion of foreign genes in Gram-negative bacteria. J Bacteriol 172, 6557 6567. (Pubitemid 20372801)
64. Liu J Magasanik B (1993) The glnB region of the Escherichia coli chromosome. J Bacteriol 175, 7441 7449. (Pubitemid 23339324)
65. He B, Choi KY Zalkin H (1993) Regulation of Escherichia coli glnB, prsA, and speA by the purine repressor. J Bacteriol 175, 3598 3606. (Pubitemid 23163406)
66. Cornet F, Mortier I, Patte J Louarn JM (1994) Plasmid pSC101 harbors a recombination site, psi, which is able to resolve plasmid multimers and to substitute for the analogous chromosomal Escherichia coli site dif. J Bacteriol 176, 3188 3195. (Pubitemid 24166708)
67. Hamilton CM, Aldea M, Washburn BK, Babitzke P Kushner SR (1989) New method for generating deletions and gene replacements in Escherichia coli. J Bacteriol 171, 4617 4622. (Pubitemid 19209055)
68. Blomfield IC, Vaughn V, Rest RF Eisenstein BI (1991) Allelic exchange in Escherichia coli using the Bacillus subtilis sacB gene and a temperature-sensitive pSC101 replicon. Mol Microbiol 5, 1447 1457. (Pubitemid 21896171)
69. Stadtman ER, Smyrniotis PZ, Davis JN Wittenberger ME (1979) Enzymic procedures for determining the average state of adenylylation of Escherichia coli glutamine synthetase. Anal Biochem 95, 275 285. (Pubitemid 9194293)
70. Markwell MA, Haas SM, Bieber LL Tolbert NE (1978) A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. Anal Biochem 87, 206 210. (Pubitemid 9050428)
71. Chen YM, Backman K Magasanik B (1982) Characterization of a gene, glnL, the product of which is involved in the regulation of nitrogen utilization in Escherichia coli. J Bacteriol 150, 214 220.
72. Bueno R, Pahel G Magasanik B (1985) Role of glnB and glnD gene products in regulation of the glnALG operon of Escherichia coli. J Bacteriol 164, 816 822. (Pubitemid 16191857)