Characterization of the reconstituted UTase/UR-PII-NRII-NRI bicyclic signal transduction system that controls the transcription of nitrogen-regulated (Ntr) genes in Escherichia coli

Biochemistry

Volumn 51, Issue 45, 2012, Pages 9045-9057

  Jiang, Peng ^a   Ventura, Alejandra C ^b   Ninfa, Alexander J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BICYCLIC SYSTEMS; GLUTAMINE LEVELS; PHYSIOLOGICAL RANGE; PROTEIN CONCENTRATIONS; PROTEIN LEVEL; SIGNAL TRANSDUCTION SYSTEM; STATE RESPONSE; SUBSTRATE INHIBITION;

AMINO ACIDS; ESCHERICHIA COLI; PHOSPHORYLATION; PHYSIOLOGY; PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION;

PHYSIOLOGICAL MODELS;

BACTERIAL ENZYME; GLUTAMINE; NITROGEN; UNCLASSIFIED DRUG; UTASE;

ABSOLUTE CONCENTRATION ROBUSTNESS; ARTICLE; BACTERIAL GENE; CONCENTRATION (PARAMETERS); ENZYME ACTIVITY; ESCHERICHIA COLI; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SIGNAL PROCESSING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; URIDYLATION;

BACTERIAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GLUTAMINE; MULTIENZYME COMPLEXES; NITROGEN; NUCLEOTIDYLTRANSFERASES; PHOSPHOPROTEIN PHOSPHATASES; PII NITROGEN REGULATORY PROTEINS; PROTEIN KINASES; PROTEIN MULTIMERIZATION; RNA POLYMERASE SIGMA 54; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

ESCHERICHIA COLI;

EID: 84869016171     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300575j     Document Type: Article

References (64)

1. Ninfa, A. J., Jiang, P., Atkinson, M. R., and Peliska, J. A. (2000) Integration of antagonistic signals in the regulation of nitrogen assimilation in Escherichia coli Curr. Top. Cell. Regul. 36, 31-75
2. Ninfa, A. J., Reitzer, L. J., and Magasanik, B. (1987) Initiation of transcription at the bacterial glnAp2 promoter by purified E. coli components is facilitated by enhancers Cell 50, 1039-1046
3. Su, W., Porter, S., Kustu, S., and Echols, H. (1990) DNA looping and enhancer activity: association between DNA-bound NtrC activator and RNA polymerase at the bacterial glnAp2 promoter Proc. Natl. Acad. Sci. U. S. A. 87, 5504-5508
4. Hoover, T. R., Santero, E., Porter, S., and Kustu, S. (1990) The integration host factor stimulates interaction of RNA polymerase with NIFA, the transcriptional activator for nitrogen fixation operons Cell 63, 11-22
5. Ueno-Nishio, S., Mango, S., Reitzer, L. J., and Magasanik, B. (1984) Identification and regulation of the glnL operator-promoter of the complex glnALG operon of Escherichia coli J. Bacteriol. 160, 379-384
6. Atkinson, M. R., Pattaramanon, N., and Ninfa, A. J. (2002) Governor of the glnAp2 promoter of Escherichia coli Mol. Microbiol. 46, 1247-1257
7. Ninfa, A. J. and Magasanik, B. (1986) Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 83, 5909-5913
8. Zimmer, D. P., Soupene, E., Lee, H. L., Wendisch, V. F., Khodursky, A. B., Peter, B. J., Bender, R. A., and Kustu, S. (2000) Nitrogen regulatory protein C-controlled genes of Escherichia coli: Scavenging as a defense against niotrogen limitation Proc. Natl. Acad. Sci. U. S. A. 97, 14674-14679
9. Porter, S. C., North, A. K., Wedel, A. B., and Kustu, S. (1993) Oligomerization of NTRC at the glnA enhancer is required for transcriptional activation Genes Dev. 7, 2258-2273
10. Popham, D. L., Szeto, D, Keener, J, and Kustu, S. (1989) Function of a bacterial activator protein that binds to transcriptional enhancers Science 243, 629-635
11. Weiss, V. and Magasanik, B. (1988) Phosphorylation of nitrogen regulator I of Escherichia coli Proc. Natl. Acad. Sci. U. S. A. 85, 8919-8923
12. Backman, K., Chen, Y. M., and Magasanik, B. (1981) Physical and genetic characterization of the glnA-glnG region of the Escherichia coli chromosome Proc. Natl. Acad. Sci. U. S. A. 78, 3743-3747
13. Reitzer, L. (2003) Nitrogen assimilation and global regulation in Escherichia coli Annu. Rev. Microbiol. 57, 155-176
14. Atkinson, M. R., Blauwkamp, T. A., Bondarenko, V., Studitsky, V, and Ninfa, A. J. (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
15. Atkinson, M. R., Blauwkamp, T. A., and Ninfa, A. J. (2002) Context-dependent functions of the PII and GlnK signal transduction protein in Escherichia coli J. Bacteriol. 184, 5364-5375
16. Keener, J and 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. U. S. A. 85, 4976-4980
17. Jiang, P., Atkinson, M. R., Srisawat, C., Sun, Q., and Ninfa, A. J. (2000) Functional dissection of the dimerization and enzymatic activities of Escherichia coli nitrogen regulator II and their regulation by the PII protein Biochemistry 39, 13433-13449
18. Jiang, P. and Ninfa, A. J. (1999) Regulation of he autophosphorylation of Escherichia coli nitrogen regulator II by the PII signal transduction protein J. Bacteriol. 181, 1906-1911
19. Pioszak, A. A. and Ninfa, A. J. (2003) Mechanism of the PII-activated phosphatase activity of Escherichia coli NRII (NtrB): how the different domains of NRII collaborate to act as a phoshatase Biochemistry 42, 8885-8899
20. Pioszak, A. A. and Ninfa, A. J. (2004) Mutations altering the N-terminal receiver domain of NRI (NtrC) that prevent dephosphorylation by the NRII-PII complex in Escherichia coli J. Bacteriol. 186, 5730-5740
21. Zhao, R., Collins, E. J., Bourret, R. B., and Silversmith, R. E. (2002) Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ Nat. Struct. Biol. 9, 570-575
22. Ninfa, A. J. and Jiang, P. (2005) PII signal transduction proteins: sensors of alpha-ketoglutarate that regulate nitrogen metabolism Curr. Opin Microbiol. 8, 168-173
23. Atkinson, M. R., Kamberov, E. S., Weiss, R. L., and Ninfa, A. J. (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
24. Jiang, P. and Ninfa, A. J. (2011) A source of ultrasensitivity in the glutamine response of the bicyclic cascade system controlling glutamine synthetase adenylylation state and activity in Escherichia coli Biochemistry 50, 10929-10940
25. Ventura, A. C., Jiang, P., Van Wassenhove, L., Del Vecchio, D., Merajver, S. D., and Ninfa, A. J. (2010) Signaling properties of a covalent modification cycle are altered by a downstream target Proc. Natl. Acad. Sci. U. S. A. 107, 10032-10037
26. Ikeda, T. P., Shauger, A. E., and Kustu, S. (1996) Salmonella typhimurium apparently perceives external nitrogen limitation as internal glutamine limitation J. Mol. Biol. 259, 589-607
27. Bennett, B. D., Kimball, E. H., Gao, M., Osterhout, R., Van Dien, S. J., and Rabinowitz, J. D. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli Nat. Chem Biol. 5, 593-599
28. Jiang, P., Peliska, J. A., and Ninfa, A. J. (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 proteins Biochemistry 37, 12782-12794
29. Zhang, Y., Pohlmann, E. L., Serate, J., Conrad, M. C., and Roberts, G. P. (2010) Mutagenesis and functional characterization of the four domains of GlnD, a bifunctional nitrogen sensor protein J. Bacteriol. 192, 2711-2721
30. Kamberov, E. S., Atkinson, M. R., and Ninfa, A. J. (1995) The Escherichia coli PII signal transduction protein is activated upon binding 2-ketoglutarate and ATP J. Biol. Chem. 270, 17797-17807
31. Jiang, P. and Ninfa, A. J. (2007) Escherichia coli PII signal transduction protein controlling nitrogen assimilation acts as a sensor of adenylylate energy charge in vitro Biochemistry 46, 12979-12996
32. Forchhammer, K. (2004) Global carbon/nitrogen control by PII signal transduction in cyanobacteria: from signals to targets FEMS Microbiol. Rev. 28, 319-333
33. Senior, P. J. (1975) Regulation of nitrogen metabolism in Escherichia coli and Klebsiella aerogenes: studies with the continuous culture technique J. Bacteriol. 123, 407-418
34. Taketa, K. and Pogell, B. M. (1965) Allosteric inhibition of rat liver fructose 1, 6-diphosphatase by Adenosine 5′-Monophosphate J. Biol. Chem. 240, 651-662
35. Goldbeter, A. and Koshland, D. E. (1981) An amplified sensitivity arising from covalent modification in biological systems Proc. Natl. Acad. Sci. U. S. A. 78, 6840-6844
36. Pomerening, J. R., Sontag, E. D., and Ferrell, J. E., Jr. (2003) Building a cell cycle oscillator: hysteresis and bistability in the activation of cdc2 Nat. Cell Biol. 5, 346-351
37. Angeli, D., Ferrell, J. E., Jr., and Sontag, E. D. (2004) Detection of multistability, bifurcations, and hysteresis in a large class of biological feedback systems Proc. Natl. Acad. Sci. U. S. A. 101, 1822-1827
38. Melen, G. J., Levy, S., Barkai, N., and Shilo, B. Z. (2005) Threshold responses to morphogen gradients by zero-order ultrasensitivity Mol. Syst. Biol. 1 2005.0028
39. Ferrell, J. E., Jr. (1996) Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs Trends Biochem. Sci. 21, 460-466
40. Savageau, M. A. (1971) Parameter sensitivity as a criterion for evaluating and comparing the performance of biochemical systems Nature 229, 542-544
41. Kitano, H. (2007) Towards a theory of biological robustness Mol. Syst. Biol. 3, 137
42. Alon, U., Surette, M. G., Barkai, N., and Leibler, S. (1999) Robustness in bacterial chemotaxis Nature 397, 168-171
43. Shinar, G., Milo, R., Martinez, M. R. T., and Alon, U. (2007) Input-output robustness in simple bacterial signaling systems Proc. Natl. Acad. Sci. U. S. A. 104, 19931-19935
44. Batchelor, E. and Goulian, M. (2003) Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system Proc. Natl. Acad. Sci. U. S. A. 100, 691-696
45. Siryaporn, A., Perchuk, B. S., and Goulian, M. (2010) Evolving a robust signal transduction pathway from weak cross talk Mol. Syst. Biol. 6, 452
46. Bornholdt, S. and Sneppen, K. (2000) Robustness as an evolutionary principle Proc. R. Soc. London B 267, 2281-2286
47. Soyer, O. S. and Pfeiffer, T. (2010) Evolution under fluctuating environments explains observed robustness in metabolic netwoorks PLoS Comp. Biol. 6, e10000907
48. van Heeswijk, W. C., Hoving, S., Molenaar, D., Stegeman, B., Kahn, D., and Westerhoff, H. V. (1996) An alternative PII protein in the regulation of glutamine synthetase in Escherichia coli Mol. Microbiol. 21, 133-146
49. Atkinson, M. R. and Ninfa, A. J. (1998) Role of the GlnK signal transduction protein in the regulation of nitrogen assimilation in Escherichia coli Mol. Microbiol. 29, 431-447
50. Goldbeter, A. and Koshland, D. E. (1982) Sensitivity amplification in biochemical systems Q. Rev. Biophys. 15, 555-591
51. Koshland, D. E., Jr, Goldbeter, A., and Stock, J. B. (1982) Amplification and adaptation in regulatory and sensory systems Science 217, 220-225
52. Goldbeter, A. and Koshland, D. E. (1984) Ultrasensitivity in biochemical systems controlled by covalent modification. Interplay between zero order and multistep effects J. Biol. Chem. 259, 14441-14447
53. Cardenas, M. L. and 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
54. Ortega, F., Acerenza, L., Westerhoff, H. V., Mas, F., and Cascante, M. (2002) Product dependence and bifunctionality compromise the ultraasensitivity of signal transduction cascades Proc. Natl. Acad. Sci. U. S. A. 99, 1170-1175
55. Mutalik, V. K., Shah, P., and Vankatesh, K. V. (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
56. Guidi, G. M., Carlier, M. F., and Goldbeter, A. (1998) Bistability in the isocitrate dehydrogenase reaction: an experimentally based theoretical study Biophys. J. 74, 1229-1240
57. Goulian, M. (2004) Robust control in bacterial regulatory circuits Curr. Opin. Microbiol. 7, 198-202
58. Shinar, G. and Feinberg, M. (2011) Design principles for robust biochemical reaction networks: what works, what cannot work, and what might almost work Math. Biosci. 231, 39-48
59. Pioszak, A. A. and Ninfa, A. J. (2003b) Genetic and Biochemical analysis of the phosphatase activity of Escherichia coli NRII (NtrB) and its regulation by the PII signal transduction protein J. Bacteriol. 185, 1299-131552
60. Chock, P. B. and Stadtman, E. R. (1977) Superiority of interconvertable enzyme cascades in metabolic regulation: analysis of multicyclic systems Proc. Natl. Acad. Sci. U. S. A. 74, 2766-2770
61. Gomez-Uribe, C., Verghese, G. C., and Mirny, L. A. (2007) Operating regimes of signaling cycles: statics, dynamics, and noise filtering PLoS Comp. Biol. 3, e246
62. Stadtman, E. R. and Chock, P. B. (1977) Superiority of interconvertable enzyme cascades in metabolic regulation: analysis of monocyclic systems Proc. Natl. Acad. Sci. U. S. A. 74, 2761-2765
63. Hart, Y., Madar, D., Yuan, J., Bren, A., Mayo, A. E., Rabinowitz, J. D., and Alon, U. (2011) Robust control of nitrogen assimilation by a bifunctional enzyme in E. coli Mol. Cell 41, 117-127
64. Doucette, C. D., Schwab, D. J., Wingreen, N. S., and Rabinowitz, J. D. (2011) α-Ketoglutarate coordinates carbon and nitrogen utilization via Enzyme I inhibition Nat. Chem. Biol. 7, 894-901