Conserved mechanism for sensor phosphatase control of two-component signaling revealed in the nitrate sensor NarX

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 49, 2010, Pages 21140-21145

  Huynh, TuAnh Ngoc ^a   Noriega, Chris E ^a   Stewart, Valley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Desk; DHp domain; Histidine kinase

Indexed keywords

PHOSPHATASE; PROTEIN NARX; UNCLASSIFIED DRUG;

ARTICLE; DEPHOSPHORYLATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME MECHANISM; ENZYME REGULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS;

AMINO ACID MOTIFS; BACTERIAL OUTER MEMBRANE PROTEINS; ESCHERICHIA COLI PROTEINS; MULTIENZYME COMPLEXES; MUTAGENESIS, SITE-DIRECTED; NITRATES; PHOSPHORIC MONOESTER HYDROLASES; PHOSPHORYLATION; PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 78650506427     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1013081107     Document Type: Article

References (36)

1. Hoch JA, Silhavy TJ eds (1995) Two-Component Signal Transduction (ASM Press, Washington, DC).
2. Albanesi D, et al. (2009) Structural plasticity and catalysis regulation of a thermosensor histidine kinase. Proc Natl Acad Sci USA 106:16185-16190.
3. McFarland N, McCarter L, Artz S, Kustu S (1981) Nitrogen regulatory locus "glnR" of enteric bacteria is composed of cistrons ntrB and ntrC: Identification of their protein products. Proc Natl Acad Sci USA 78:2135-2139.
4. MacNeil T, Roberts GP, MacNeil D, Tyler B (1982) The products of glnL and glnG are bifunctional regulatory proteins. Mol Gen Genet 188:325-333.
5. Szurmant H, Hoch JA (2010) Interaction fidelity in two-component signaling. Curr Opin Microbiol 13:190-197.
6. Gao R, Stock AM (2009) Biological insights from structures of two-component proteins. Annu Rev Microbiol 63:133-154.
7. Ninfa AJ, 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 USA 83:5909-5913.
8. 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.
9. Wolanin PM, Webre DJ, Stock JB (2003) Mechanism of phosphatase activity in the chemotaxis response regulator CheY. Biochemistry 42:14075-14082.
10. Song Y, Peisach D, Pioszak AA, Xu Z, Ninfa AJ (2004) Crystal structure of the Cterminal domain of the two-component system transmitter protein nitrogen regulator II (NRII; NtrB), regulator of nitrogen assimilation in Escherichia coli. Biochemistry 43:6670-6678.
11. Noriega CE, Lin HY, Chen LL, Williams SB, Stewart V (2010) Asymmetric crossregulation between the nitrate-responsive NarX-NarL and NarQ-NarP twocomponent regulatory systems from Escherichia coli K-12. Mol Microbiol 75:394-412.
12. Zhao R, Collins EJ, Bourret RB, Silversmith RE (2002) Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ. Nat Struct Biol 9:570-575.
13. Li G, Zhang XC (2004) GTP hydrolysis mechanism of Ras-like GTPases. J Mol Biol 340: 921-932.
14. Pazy Y, et al. (2010) Identical phosphatase mechanisms achieved through distinct modes of binding phosphoprotein substrate. Proc Natl Acad Sci USA 107:1924-1929.
15. Finn RD, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38 (Database issue):D211-D222.
16. Trajtenberg F, Graña M, Ruétalo N, Botti H, Buschiazzo A (2010) Structural and enzymatic insights into the ATP binding and autophosphorylation mechanism of a sensor histidine kinase. J Biol Chem 285:24892-24903.
17. Grebe TW, Stock JB (1999) The histidine protein kinase superfamily. Adv Microb Physiol 41:139-227.
18. Roberts DM, Liao RP, Wisedchaisri G, Hol WG, Sherman DR (2004) Two sensor kinases contribute to the hypoxic response of Mycobacterium tuberculosis. J Biol Chem 279: 23082-23087.
19. Jordan S, Hutchings MI, Mascher T (2008) Cell envelope stress response in Grampositive bacteria. FEMS Microbiol Rev 32:107-146.
20. Schneider TD, Stephens RM (1990) Sequence logos: A new way to display consensus sequences. Nucleic Acids Res 18:6097-6100.
21. Lupas AN, Gruber M (2005) The structure of alpha-helical coiled coils. Adv Protein Chem 70:37-78.
22. Hsing W, Russo FD, Bernd KK, Silhavy TJ (1998) Mutations that alter the kinase and phosphatase activities of the two-component sensor EnvZ. J Bacteriol 180:4538-4546.
23. Silversmith RE (2010) Auxiliary phosphatases in two-component signal transduction. Curr Opin Microbiol 13:177-183.
24. Egan SM, Stewart V (1991) Mutational analysis of nitrate regulatory gene narL in Escherichia coli K-12. J Bacteriol 173:4424-4432.
25. Noriega CE, Schmidt R, Gray MJ, Chen LL, Stewart V (2008) Autophosphorylation and dephosphorylation by soluble forms of the nitrate-responsive sensors NarX and NarQ from Escherichia coli K-12. J Bacteriol 190:3869-3876.
26. Atkinson MR, Ninfa AJ (1993) Mutational analysis of the bacterial signal-transducing protein kinase/phosphatase nitrogen regulator II (NRII or NtrB). J Bacteriol 175: 7016-7023.
27. Boesch KC, Silversmith RE, Bourret RB (2000) Isolation and characterization of nonchemotactic CheZ mutants of Escherichia coli. J Bacteriol 182:3544-3552.
28. Blat Y, Eisenbach M (1996) Mutants with defective phosphatase activity show no phosphorylation-dependent oligomerization of CheZ. The phosphatase of bacterial chemotaxis. J Biol Chem 271:1232-1236.
29. Paphavee L, Karen MO (2010) A remote CheZ orthologue retains phosphatase function. Mol Microbiol 77:225-235.
30. Zapf J, Sen U, Madhusudan, Hoch JA, Varughese KI (2000) A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure 8:851-862.
31. Thomas SA, Brewster JA, Bourret RB (2008) Two variable active site residues modulate response regulator phosphoryl group stability. Mol Microbiol 69:453-465.
32. Atkinson MR, Ninfa AJ (1992) Characterization of Escherichia coli glnL mutations affecting nitrogen regulation. J Bacteriol 174:4538-4548.
33. Dutta R, Yoshida T, Inouye M (2000) The critical role of the conserved Thr247 residue in the functioning of the osmosensor EnvZ, a histidine kinase/phosphatase, in Escherichia coli. J Biol Chem 275:38645-38653.
34. Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: A sequence logo generator. Genome Res 14:1188-1190.
35. Sayers EW, et al. (2010) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 38(Database issue):D5-D16.
36. Stewart V, Chen LL (2010) The S helix mediates signal transmission as a HAMP domain coiled-coil extension in the NarX nitrate sensor from Escherichia coli K-12. J Bacteriol 192:734-745.