Discrimination between structurally related ligands nitrate and nitrite controls autokinase activity of the NarX transmembrane signal transducer of Escherichia coli K-12

Molecular Microbiology

Volumn 26, Issue 5, 1997, Pages 911-925

  Williams, Stanly B ^a,b   Stewart, Valley ^a,c  

^a Department of Obstetrics Gynecology   (United States)

^b TEXAS A AND M UNIVERSITY   (United States)

^c Section of Microbiology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; NITRATE; NITRITE; PHOSPHOTRANSFERASE;

ARTICLE; AUTOPHOSPHORYLATION; CONTROLLED STUDY; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSDUCER;

ESCHERICHIA; ESCHERICHIA COLI; ESCHERICHIA COLI K12; TRIXIS;

EID: 0030694514     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1997.6262002.x     Document Type: Article

References (55)

1. Baumgartner, J.W., Kim, C., Brissette, R.E., Inouye, M., Park, C., and Hazelbauer, G.L. (1994) Transmembrane signalling by a hybrid protein: communication from the domain of chemoreceptor Trg that recognizes sugar-binding proteins to the kinase/phosphatase domain of osmosensor EnvZ. J Bacteriol 176: 1157-1163.
2. Bordo, D., and Argos, P. (1991) Suggestions for 'safe' residue substitutions in site-directed mutagenesis. J Mol Biol 217: 721-729.
3. Cavicchioli, R., Chiang, R.C., Kalman, L.V., and Gunsalus, R.P. (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.
4. Chervitz, S.A., and Falke, J.J. (1996) Molecular mechanism of transmembrane signaling by the aspartate receptor: a model. Proc Natl Acad Sci USA 93: 2545-2550.
5. Chiang, R.C., Cavicchioli, R., and Gunsalus, R.P. (1992) Identification and characterization of narQ, a second nitrate sensor for nitrate-dependent gene regulation in Escherichia coli. Mol Microbiol 6: 1913-23.
6. Chiang, R.C., Cavicchioli, R., and Gunsalus, R.P. (1997) 'Locked-on' and 'locked-off' signal transduction mutations in the periplasmic domain of the Escherichia coli NarQ and NarX sensors affect nitrate- and nitrite-dependent regulation by NarL and NarP. Mol Microbiol 24: 1049-1060.
7. Darwin, A.J., and Stewart, V. (1996) The Nar modulon systems: nitrate and nitrite regulation of anaerobic gene expression. In Regulation of Gene Expression in Escherichia coli. Lin, E.C.C., and Lynch, A.S. (eds). Austin, TX: R.G. Landes, pp. 343-360.
8. Darwin, A.J., Li, J., and Stewart, V. (1996) Analysis of nitrate regulatory protein NarL binding sites in the fdnG and narG operon control regions of Escherichia coli K-12. Mol Microbiol 20: 621-632.
9. Darwin, A.J., Tyson, K.L., Busby, S.J.W., and Stewart, V. (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. Doty, S.L., Yu, M.C., Lundin, J.I., Heath, J., and Nester, E.W. (1996) Mutational analysis of the input domain of the VirA protein of Agrobacterium tumefaciens. J Bacteriol 178: 961-970.
11. Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., Bult, C.J., Tomb, J.-F., Dougherty, B.A., Merrick, J.M., McKenney, K., Sutton, G., FitzHugh, W., Fields, C., Gocayne, J.D., Scott, J., Shirley, R., Liu, L.-I., Glodek, A., Kelley, J.M., Weidman, J.F., Phillips, C.A., Spriggs, T., Hedblom, E., Cotton, M.D., Utterback, T.R., Hanna, M.C., Nguyen, D.T., Saudek, D.M., Brandon, R.C., Fine, L.D., Fritchman, J.L., Fuhrmann, J.L., Geoghagen, N.S.M., Gnehm, C.L., McDonald, L.A., Small, K.V., Fraser, C.M., Smith, H.O., and Venter, J.C. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512.
12. Futai, M. (1974) Orientation of membrane vesicles from Escherichia coli prepared by different procedures. J Membr Biol 15: 15-28.
13. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165-174.
14. García Véscovi, E., Ayala, Y.M., Di Cera, E., and Groisman, E.A. (1997) Characterization of the bacterial sensor protein PhoQ. J Biol Chem 272: 1440-1443.
15. Harlow, E., and Lane, D. (1988) Antibodies. A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
16. Hazelbauer, G.L., Yaghmai, Y., Burrows, G.G., Baumgartner, J.W., Dutton, D.P., and Morgan, D.G. (1990) Transducers: transmembrane receptor proteins involved in bacterial chemotaxis. Symp Soc Gen Microbiol 46: 107-134.
17. Hazes, B., Magnus, K.A., Kalk, K.H., Bonaventura, C., and Hol, W.G.J. (1996) Nitrate binding to Limulus polyphemus subunit type II hemocyanin and its functional implications. J Mol Biol 262: 532-542.
18. Hertzberg, E.L., and Hinkle, P.C. (1974) Oxidative phosphorylation and proton translocation in membrane vesicles prepared from Escherichia coli. Biochem Biophys Res Commun 58: 178-184.
19. Hoch, J.A., and Silhavy, T.J. (1995) Two-Component Signal Transduction. Washington, DC: American Society for Microbiology Press.
20. Hsing, W., and Silhavy, T.J. (1997) Function of conserved histidine-243 in phosphatase activity of EnvZ, the sensor for porin osmoregulation in Escherichia coli. J Bacteriol 179: 3729-3735.
21. Igo, M.M., and Silhavy, T.J. (1988) EnvZ, a Iransmembrane environmental sensor of Escherichia coli K-12, is phosphorylated in vitro. J Bacteriol 170: 5971-5973.
22. Igo, M.M., Ninfa, A.J., and Silhavy, T.S. (1989) A bacterial environmental sensor that functions as a protein kinase and stimulates transcriptional activation. Genes Dev 3: 598-605.
23. 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 USA 85: 4976-4980.
24. Liu, J., and Parkinson, J.S. (1989) Genetics and sequence analysis of the pcnB locus, an Escherichia coli gene involved in plasmid copy number control J Bacteriol 171: 1254-1261.
25. Lopilato, J., Bortner, S., and Beckwith, J. (1986) Mutations in a new chromosomal gene of Escherichia coli K-12, pcnB, reduce plasmid copy number of pBR322 and its derivatives. Mol Gen Genet 205: 285-290.
26. Milburn, M.V., Privé, G.C., Milligan, D.L., Scott, W.G., Yeh, J., Jancarik, J., Koshland, Jr, D.E., and Kim, S. (1991) Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand. Science 254: 1342-1347.
27. Miller, J.H. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
28. II, regulates the transcription of the glnALG operon in Escherichia coli. Proc Natl Acad Sci USA 83: 5909-5913.
29. II two-component system of enteric bacteria. In Two-Component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington DC: American Society for Microbiology Press, pp. 67-88.
30. Pan, S.Q., Charles, T., Jin, S., Wu, Z., and Nester, E.W. (1993) Preformed dimeric state of the sensor protein VirA is involved in plant-Agrobacterium signal transduction. Proc Natl Acad Sci USA 90: 9939-9943.
31. Parkinson, J.S. (1993) Signal transduction schemes of bacteria. Cell 73: 857-871.
32. Parkinson, J.S., and Kofoid, E.C. (1992) Communication modules in bacterial signaling proteins. Annu Rev Genet 26: 71-112.
33. Pratt, L.A., and Silhavy, T.J. (1995) Porin regulon of Escherichia coli. In Two-Component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds) Washington DC: American Society for Microbiology Press, pp. 105-127.
34. Rabin, R.S., and Stewart, V. (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.
35. Rabin, R.S., and Stewart, V. (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.
36. Roberts, D.L., Bennett, D.W., and Forst, S.A. (1994) Identification of the site of phosphorylation on the osmosensor, EnvZ, of Escherichia coli. J Biol Chem 269: 8728-8733.
37. Russo, F.D., and Silhavy, T.J. (1991) EnvZ controls the concentration of phosphorylated OmpR to mediate osmoregulation of the porin genes. J Mol Biol 222: 567-580.
38. Saiki, R.K., Gelfand, D.H., Stoffel, S., Scharf, S.J., Higuchi, R., Horn, G.T., Mullis, K.B., and Erlich, H.A. (1988) Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487-491.
39. Sanger, F., Nicklen, S., and Coulson, A.R. (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463-5467.
40. Schröder, I., Wolin, C.D., Cavicchioli, R., and Gunsalus, R.P. (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.
41. Stewart, G.S.A.B., Lubinsky-Mink, S., Jackson, C.G., Kassel, A., and Kuhn, J. (1986) pHG165: a pBR322 copy number derivative of pUC8 for cloning and expression. Plasmid 15: 172-181.
42. Stewart, V., and Parales, J. (1988) Identification and expression of genes narL and narX of the nar (nitrate reductase) locus in Escherichia coli K-12. J Bacteriol 170: 1589-1597.
43. Stewarl, V., and Rabin, R.S. (1995) Dual sensors and dual response regulators interact to control nitrate- and nitrite-responsive gene expression in Escherichia coli. In Two-Component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington DC: American Society for Microbiology Press, pp. 233-252.
44. Stock, J.B., and Surette, M.G. (1996) Chemotaxis. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtiss, III, R., Ingraham, J.L., Lin, E.C.C., Low, K.B., Magasanik, B., Reznikoff, W.S., Riley, M., Schaechter, M., and Umbarger, H.E. (eds). Washington, DC: American Society for Microbiology Press, pp. 1103-1129.
45. Stock, J.B., Surette, M.G., Levit, M., and Park, P. (1995) Two-component signal transduction systems: structure-function relationships and mechanisms of catalysis. In Two-Component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington DC: American Society for Microbiology Press, pp. 25-51.
46. Tabor, S., and Richardson, C.C. (1985) A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc Natl Acad Sci USA 82: 1074-1078.
47. Tokishita, S., Yamada, H., Aiba, H., and Mizuno, T. (1990) Transmembrane signal transduction and osmoregulation in Escherichia coli: II. The osmotic sensor, EnvZ, located in the isolated cytoplasmic membrane displays its phosphorylation and dephosphorylation abilities as to the activator protein, OmpR. J Biochem 108: 488-493.
48. Tyson, K.L., Cole, J.A., and Busby, S.J.W. (1994) Nitrite and nitrate regulation at the promoters of two Escherichia coli operons encoding nitrite reductase: identification of common target heptamers for both NarP- and NarL-dependent regulation. Mol Microbiol 13: 1045-1055.
49. Utsumi, R., Brissette, R.E., Rampersaud, A., Forst, S.A., Oosawa, K., and Inouye, M. (1989) Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate. Science 245: 1246-1249.
50. Waldburger, C.D., and Sauer, R.T. (1996) Signal detection by the PhoQ sensor-transmitter. Characterization of the sensor domain and a response-impaired mutant that identifies ligand-binding determinants. J Biol Chem 271: 26630-26636.
51. Walker, M.S., and DeMoss, J.A. (1993) Phosphorylation and dephosphorylation catalyzed in vitro by purified components of the nitrate sensing system, NarX and NarL. J Biol Chem 268: 8391-8393.
52. Wanner, B.L. (1995) Signal transduction and cross regulation in the Escherichia coli phosphate regulon by PhoR, CreC, and acetyl phosphate. In Two-Component Signal Transduction. Hoch, J.A., and Silhavy, T.J. (eds). Washington DC: American Society for Microbiology Press, pp. 203-221.
53. Williams, S.B., and Stewart, V. (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.
54. Yaghmai, R., and Hazelbauer, G.L. (1992) Ligand occupancy mimicked by single residue substitutions in a receptor: transmembrane signaling induced by mutation. Proc Natl Acad Sci USA 89: 7890-7894.
55. Yeh, J.I., Biemann, H., Privé, G.G., Pandit, J., Koshland, Jr, D.E., and Kim, S. (1996) High-resolution structures of the ligand binding domain of the wild-type bacterial aspartate receptor. J Mol Biol 262: 186-201.