Autophosphorylation and dephosphorylation by soluble forms of the nitrate-responsive sensors NarX and NarQ from Escherichia coli K-12

Journal of Bacteriology

Volumn 190, Issue 11, 2008, Pages 3869-3876

  Noriega, Chris E ^a   Schmidt, Radomir ^a   Gray, Michael J ^a,b   Chen, Li Ling ^a   Stewart, Valley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; MALTOSE BINDING PROTEIN; NITRATE; PROTEIN NARQ; PROTEIN NARX;

AMINO TERMINAL SEQUENCE; ARTICLE; AUTOPHOSPHORYLATION; BINDING AFFINITY; CONCENTRATION (PARAMETERS); ESCHERICHIA COLI K 12; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SOLUBILITY;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; KINETICS; MEMBRANE PROTEINS; NITRATES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; TIME FACTORS;

ESCHERICHIA COLI; ESCHERICHIA COLI K12;

EID: 44349144008     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00092-08     Document Type: Article

References (44)

1. Anantharaman, V., S. Balaji, and L. Aravind. 2006. The signaling helix: a common functional theme in diverse signaling proteins. Biol. Direct. 1:25.
2. Appleman, J. A., L. L. Chen, and V. Stewart. 2003. Probing conservation of HAMP linker structure and signal transduction mechanism through analysis of hybrid sensor kinases. J. Bacteriol. 185:4872-4882.
3. Appleman, J. A., and V. Stewart. 2003. Mutational analysis of a conserved signal-transducing element: the HAMP linker of the Escherichia coli nitrate sensor NarX. J. Bacteriol. 185:89-97.
4. Bilwes, A. M., C. M. Quezada, L. R. Croal, B. R. Crane, and M. I. Simon. 2001. Nucleotide binding by the histidine kinase CheA. Nat. Struct. Biol. 8:353-360.
5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
6. Buckstein, M. H., J. He, and H. Rubin. 2008. Characterization of nucleotide pools as a function of physiological state in Escherichia coli. J. Bacteriol. 190:718-726.
7. Cavicchioli, R., R. C. Chiang, L. V. Kaiman, and R. P. Gunsalus. 1996. Role of the periplasmic domain of the Escherichia coli NarX sensor-transmitter protein in nitrate-dependent signal transduction and gene regulation. Mol. Microbiol. 21:901-911.
8. Cavicchioli, R., I. Schröder, M. Constanti, and R. P. Gunsalus. 1995. The NarX and NarQ sensor-transmitter proteins of Escherichia coli each require two conserved histidines for nitrate-dependent signal transduction to NarL. J. Bacteriol. 177:2416-2424.
9. Darwin, A. J., K. L. Tyson, S. J. Busby, and V. Stewart. 1997. Differential regulation by the homologous response regulators NarL and NarP of Escherichia coli K-12 depends on DNA binding site arrangement. Mol. Microbiol. 25:583-595.
10. Dutta, R., and M. Inouye. 2000. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 25:24-28.
11. Dutta, R., L. Qin, and M. Inouye. 1999. Histidine kinases: diversity of domain organization. Mol. Microbiol. 34:633-640.
12. Foster, J. E., Q. Sheng, J. R. McClain, M. Bures, T. I. Nicas, K. Henry, M. E. Winkler, and R. Gilmour. 2004. Kinetic and mechanistic analyses of new classes of inhibitors of two-component signal transduction systems using a coupled assay containing HpkA-DrrA from Thermotoga maritima. Microbiology 150:885-896.
13. Goh, E. B., P. J. Bledsoe, L. L. Chen, P. Gyaneshwar, V. Stewart, and M. M. Igo. 2005. Hierarchical control of anaerobic gene expression in Escherichia coli K-12: the nitrate-responsive NarX-NarL regulatory system represses synthesis of the fumarate-responsive DcuS-DcuR regulatory system. J. Bacteriol. 187:4890-4899.
14. Grebe, T. W., and J. B. Stock. 1999. The histidine protein kinase superfamily. Adv. Microb. Physiol. 41:139-227.
15. Grimshaw, C. E., S. Huang, C. G. Hanstein, M. A. Strauch, D. Burbulys, L. Wang, J. A. Hoch, and J. M. Whiteley. 1998. Synergistic kinetic interactions between components of the phosphorelay controlling sporulation in Bacillus subtilis. Biochemistry 37:1365-1375.
16. Jiang, P., J. A. Peliska, and A. J. Ninfa. 2000. Asymmetry in the autophosphorylation of the two-component regulatory system transmitter protein nitrogen regulator 11 of Escherichia coli. Biochemistry 39:5057-5065.
17. Kenney, L. J. 1997. Kinase activity of EnvZ, an osmoregulatory signal transducing protein of Escherichia coli. Arch. Biochem. Biophys. 346:303-311.
18. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
19. Lee, A. I., A. Delgado, and R. P. Gunsalus. 1999. Signal-dependent phosphorylation of the membrane-bound NarX two-component sensor-transmitter protein of Escherichia coli: nitrate elicits a superior anion ligand response compared to nitrite. J. Bacteriol. 181:5309-5316.
20. Lukat, G. S., B. H. Lee, J. M. Mottonen, A. M. Stock, and J. B. Stock. 1991. Roles of the highly conserved aspartate and lysine residues in the response regulator of bacterial chemotaxis. J. Biol. Chem. 266:8348-8354.
21. Marina, A., C. Mott, A. Auyzenberg, W. A. Hendrickson, and C. D. Waldburger. 2001. Structural and mutational analysis of the PhoQ histidine kinase catalytic domain. Insight into the reaction mechanism. J. Biol. Chem. 276:41182-41190.
22. Mukai, K., M. Kawata, and T. Tanaka. 1990. Isolation and phosphorylation of the Bacillus subtilis degS and degU gene products. J. Biol. Chem. 265:20000-20006.
23. Ninfa, E. G., A. Stock, S. Mowbray, and J. Stock. 1991. Reconstitution of the bacterial chemotaxis signal transduction system from purified components. J. Biol. Chem. 266:9764-9770.
24. +-ATPase activity. Methods Enzymol. 156:116-119.
25. Nowak, E., S. Panjikar, J. P. Morth, R. Jordanova, D. I. Svergun, and P. A. Tucker. 2006. Structural and functional aspects of the sensor histidine kinase PrrB from Mycobacterium tuberculosis. Structure 14:275-285.
26. Parkinson, J. S., and E. C. Kofoid. 1992. Communication modules in bacterial signaling proteins. Annu. Rev. Genet. 26:71-112.
27. Rabin, R. S., and V. Stewart. 1993. Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. J. Bacteriol. 175:3259-3268.
28. Rabin, R. S., and V. Stewart. 1992. Either of two functionally redundant sensor proteins, NarX and NarQ, is sufficient for nitrate regulation in Escherichia coli K-12. Proc. Natl. Acad. Sci. USA 89:8419-8423.
29. Schneider, D. A., and R. L. Gourse. 2004. Relationship between growth rate and ATP concentration in Escherichia coli: a bioassay for available cellular ATP. J. Biol. Chem. 279:8262-8268.
30. Schröder. I., C. D. Wolin, R. Cavicchioli, and R. P. Gunsalus. 1994. phosphorylation and dephosphorylation of the NarQ, NarX, and NarL proteins of the nitrate-dependent two-component regulatory system of Escherichia coli. J. Bacteriol. 176:4985-4992.
31. Stewart, R. C. 2005. Analysis of ATP binding to CheA containing tryptophan substitutions near the active site. Biochemistry 44:4375-4385.
32. Stewart, V. 2003. Nitrate- and nitrite-responsive sensors NarX and NarQ of proteobacteria. Biochem. Soc. Trans. 31:1-10.
33. Stewart, V., L. L. Chen, and H. C. Wu. 2003. Response to culture aeration mediated by the nitrate and nitrite sensor NarQ of Escherichia coli K-12. Mol. Microbiol. 50:1391-1399.
34. Stock, J. B., M. G. Surette, M. Levit, and P. Park. 1995. Two-component signal transduction systems: structure-function relationships and mechanisms of catalysis, p. 25-51. In J. A. Hoch and T. J. Silhavy (ed.), Two-component signal transduction. ASM Press, Washington, DC.
35. Tawa, P., and R. C. Stewart. 1994. Kinetics of CheA autophosphorylation and dephosphorylation reactions. Biochemistry 33:7917-7924.
36. Verhamme, D. T., J. C. Arents, P. W. Postma, W. Crielaard, and K. J. Hellingwerf. 2001. Glucose-6-phosphate-dependent phosphoryl flow through the Uhp two-component regulatory system. Microbiology 147:3345-3352.
37. Walker, M. S., and J. A. DeMoss. 1993. phosphorylation and dephosphorylation catalyzed in vitro by purified components of the nitrate sensing system, NarX and NarL. J. Biol. Chem. 268:8391-8393.
38. Waugh, D. S. 2005. Making the most of affinity tags. Trends Biotechnol. 23:316-320.
39. Williams, S. B. 1997. Ph.D. thesis. Cornell University, Ithaca, NY.
40. Williams, S. B., and V. Stewart. 1997. Discrimination between structurally related ligands nitrate and nitrite controls autokinase activity of the NarX transmembrane signal transducer of Escherichia coli K-12. Mol. Microbiol. 26:911-925.
41. Williams, S. B., and V. Stewart. 1997. Nitrate- and nitrite-sensing protein NarX of Escherichia coli K-12: mutational analysis of the amino-terminal tail and first transmembrane segment. J. Bacteriol. 179:721-729.
42. Wolanin, P. M., P. A. Thomason, and J. B. Stock. 2002. Histidine protein kinases: key signal transducers outside the animal kingdom. Genome. Biol. 3:REVIEWS3013.
43. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
44. Zhu, Y., and M. Inouye. 2002. The role of the G2 box, a conserved motif in the histidine kinase superfamily, in modulating the function of EnvZ. Mol. Microbiol. 45:653-663.