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Crystal structures of beryllium fluoride-free and beryllium fluoride-bound CheY in complex with the conserved C-terminal peptide of CheZ reveal dual binding modes specific to CheY conformation.

Guhaniyogi J, Robinson VL, Stock AM
J Mol Biol 359 624-45 (2006)
Related entries: 2fka, 2flk, 2flw, 2fmf, 2fmh, 2fmi

Cited: 36 times
EuropePMC logo PMID: 16674976

Abstract

Chemotaxis, the environment-specific swimming behavior of a bacterial cell is controlled by flagellar rotation. The steady-state level of the phosphorylated or activated form of the response regulator CheY dictates the direction of flagellar rotation. CheY phosphorylation is regulated by a fine equilibrium of three phosphotransfer activities: phosphorylation by the kinase CheA, its auto-dephosphorylation and dephosphorylation by its phosphatase CheZ. Efficient dephosphorylation of CheY by CheZ requires two spatially distinct protein-protein contacts: tethering of the two proteins to each other and formation of an active site for dephosphorylation. The former involves interaction of phosphorylated CheY with the small highly conserved C-terminal helix of CheZ (CheZ(C)), an indispensable structural component of the functional CheZ protein. To understand how the CheZ(C) helix, representing less than 10% of the full-length protein, ascertains molecular specificity of binding to CheY, we have determined crystal structures of CheY in complex with a synthetic peptide corresponding to 15 C-terminal residues of CheZ (CheZ(200-214)) at resolutions ranging from 2.0 A to 2.3A. These structures provide a detailed view of the CheZ(C) peptide interaction both in the presence and absence of the phosphoryl analog, BeF3-. Our studies reveal that two different modes of binding the CheZ(200-214) peptide are dictated by the conformational state of CheY in the complex. Our structures suggest that the CheZ(C) helix binds to a "meta-active" conformation of inactive CheY and it does so in an orientation that is distinct from the one in which it binds activated CheY. Our dual binding mode hypothesis provides implications for reverse information flow in CheY and extends previous observations on inherent resilience in CheY-like signaling domains.

Articles - 2fmk mentioned but not cited (4)

  1. Crystal structures of beryllium fluoride-free and beryllium fluoride-bound CheY in complex with the conserved C-terminal peptide of CheZ reveal dual binding modes specific to CheY conformation. Guhaniyogi J, Robinson VL, Stock AM. J Mol Biol 359 624-645 (2006)
  2. Interaction of CheY with the C-terminal peptide of CheZ. Guhaniyogi J, Wu T, Patel SS, Stock AM. J Bacteriol 190 1419-1428 (2008)
  3. Protein-protein interaction network prediction by using rigid-body docking tools: application to bacterial chemotaxis. Matsuzaki Y, Ohue M, Uchikoga N, Akiyama Y. Protein Pept Lett 21 790-798 (2014)
  4. Structural characterization of the ANTAR antiterminator domain bound to RNA. Walshe JL, Siddiquee R, Patel K, Ataide SF. Nucleic Acids Res 50 2889-2904 (2022)


Reviews citing this publication (2)

  1. Bacterial response regulators: versatile regulatory strategies from common domains. Gao R, Mack TR, Stock AM. Trends Biochem Sci 32 225-234 (2007)
  2. Auxiliary phosphatases in two-component signal transduction. Silversmith RE. Curr Opin Microbiol 13 177-183 (2010)

Articles citing this publication (30)

  1. Rosetta FlexPepDock ab-initio: simultaneous folding, docking and refinement of peptides onto their receptors. Raveh B, London N, Zimmerman L, Schueler-Furman O. PLoS One 6 e18934 (2011)
  2. Switched or not?: the structure of unphosphorylated CheY bound to the N terminus of FliM. Dyer CM, Dahlquist FW. J Bacteriol 188 7354-7363 (2006)
  3. High-resolution global peptide-protein docking using fragments-based PIPER-FlexPepDock. Alam N, Goldstein O, Xia B, Porter KA, Kozakov D, Schueler-Furman O. PLoS Comput Biol 13 e1005905 (2017)
  4. Regulation of response regulator autophosphorylation through interdomain contacts. Barbieri CM, Mack TR, Robinson VL, Miller MT, Stock AM. J Biol Chem 285 32325-32335 (2010)
  5. A new perspective on response regulator activation. Stock AM, Guhaniyogi J. J Bacteriol 188 7328-7330 (2006)
  6. Acetylation represses the binding of CheY to its target proteins. Liarzi O, Barak R, Bronner V, Dines M, Sagi Y, Shainskaya A, Eisenbach M. Mol Microbiol 76 932-943 (2010)
  7. Selective photoaffinity labeling identifies the signal peptide binding domain on SecA. Musial-Siwek M, Rusch SL, Kendall DA. J Mol Biol 365 637-648 (2007)
  8. Structure and binding specificity of the receiver domain of sensor histidine kinase CKI1 from Arabidopsis thaliana. Pekárová B, Klumpler T, Třísková O, Horák J, Jansen S, Dopitová R, Borkovcová P, Papoušková V, Nejedlá E, Sklenář V, Marek J, Zídek L, Hejátko J, Janda L. Plant J 67 827-839 (2011)
  9. AnchorDock: Blind and Flexible Anchor-Driven Peptide Docking. Ben-Shimon A, Niv MY. Structure 23 929-940 (2015)
  10. Probing the roles of the two different dimers mediated by the receiver domain of the response regulator PhoB. Mack TR, Gao R, Stock AM. J Mol Biol 389 349-364 (2009)
  11. An atypical receiver domain controls the dynamic polar localization of the Myxococcus xanthus social motility protein FrzS. Fraser JS, Merlie JP, Echols N, Weisfield SR, Mignot T, Wemmer DE, Zusman DR, Alber T. Mol Microbiol 65 319-332 (2007)
  12. Segmental motions, not a two-state concerted switch, underlie allostery in CheY. McDonald LR, Boyer JA, Lee AL. Structure 20 1363-1373 (2012)
  13. Structure-function analysis of Arabidopsis thaliana histidine kinase AHK5 bound to its cognate phosphotransfer protein AHP1. Bauer J, Reiss K, Veerabagu M, Heunemann M, Harter K, Stehle T. Mol Plant 6 959-970 (2013)
  14. Structure and activity of the flagellar rotor protein FliY: a member of the CheC phosphatase family. Sircar R, Greenswag AR, Bilwes AM, Gonzalez-Bonet G, Crane BR. J Biol Chem 288 13493-13502 (2013)
  15. Sinorhizobium meliloti CheA complexed with CheS exhibits enhanced binding to CheY1, resulting in accelerated CheY1 dephosphorylation. Dogra G, Purschke FG, Wagner V, Haslbeck M, Kriehuber T, Hughes JG, Van Tassell ML, Gilbert C, Niemeyer M, Ray WK, Helm RF, Scharf BE. J Bacteriol 194 1075-1087 (2012)
  16. Structural dynamics of the two-component response regulator RstA in recognition of promoter DNA element. Li YC, Chang CK, Chang CF, Cheng YH, Fang PJ, Yu T, Chen SC, Li YC, Hsiao CD, Huang TH. Nucleic Acids Res 42 8777-8788 (2014)
  17. Snapshots of Conformational Changes Shed Light into the NtrX Receiver Domain Signal Transduction Mechanism. Fernández I, Otero LH, Klinke S, Carrica MDC, Goldbaum FA. J Mol Biol 427 3258-3272 (2015)
  18. Action at a distance: amino acid substitutions that affect binding of the phosphorylated CheY response regulator and catalysis of dephosphorylation can be far from the CheZ phosphatase active site. Freeman AM, Mole BM, Silversmith RE, Bourret RB. J Bacteriol 193 4709-4718 (2011)
  19. Chemosensory regulation of a HEAT-repeat protein couples aggregation and sporulation in Myxococcus xanthus. Darnell CL, Wilson JM, Tiwari N, Fuentes EJ, Kirby JR. J Bacteriol 196 3160-3168 (2014)
  20. Nuclear magnetic resonance structure and dynamics of the response regulator Sma0114 from Sinorhizobium meliloti. Sheftic SR, Garcia PP, White E, Robinson VL, Gage DJ, Alexandrescu AT. Biochemistry 51 6932-6941 (2012)
  21. Conformational dynamics are a key factor in signaling mediated by the receiver domain of a sensor histidine kinase from Arabidopsis thaliana. Otrusinová O, Demo G, Padrta P, Jaseňáková Z, Pekárová B, Gelová Z, Szmitkowska A, Kadeřávek P, Jansen S, Zachrdla M, Klumpler T, Marek J, Hritz J, Janda L, Iwaï H, Wimmerová M, Hejátko J, Žídek L. J Biol Chem 292 17525-17540 (2017)
  22. Evidence for Pentapeptide-Dependent and Independent CheB Methylesterases. Velando F, Gavira JA, Rico-Jiménez M, Matilla MA, Krell T. Int J Mol Sci 21 E8459 (2020)
  23. Use of restrained molecular dynamics to predict the conformations of phosphorylated receiver domains in two-component signaling systems. Foster CA, West AH. Proteins 85 155-176 (2017)
  24. Role of Position K+4 in the Phosphorylation and Dephosphorylation Reaction Kinetics of the CheY Response Regulator. Foster CA, Silversmith RE, Immormino RM, Vass LR, Kennedy EN, Pazy Y, Collins EJ, Bourret RB. Biochemistry 60 2130-2151 (2021)
  25. The structures of T87I phosphono-CheY and T87I/Y106W phosphono-CheY help to explain their binding affinities to the FliM and CheZ peptides. McAdams K, Casper ES, Matthew Haas R, Santarsiero BD, Eggler AL, Mesecar A, Halkides CJ. Arch Biochem Biophys 479 105-113 (2008)
  26. A fragment-based docking simulation for investigating peptide-protein bindings. Liao JM, Wang YT, Wang YT, Lin CS. Phys Chem Chem Phys 19 10436-10442 (2017)
  27. Fission yeast Duf89 and Duf8901 are cobalt/nickel-dependent phosphatase-pyrophosphatases that act via a covalent aspartyl-phosphate intermediate. Sanchez AM, Jacewicz A, Shuman S. J Biol Chem 298 101851 (2022)
  28. The W-Acidic Motif of Histidine Kinase WalK Is Required for Signaling and Transcriptional Regulation in Streptococcus mutans. Kong L, Su M, Sang J, Huang S, Wang M, Cai Y, Xie M, Wu J, Wang S, Foster SJ, Zhang J, Han A. Front Microbiol 13 820089 (2022)
  29. Structural basis of the bacterial flagellar motor rotational switching. Tan J, Zhang L, Zhou X, Han S, Zhou Y, Zhu Y. Cell Res (2024)
  30. The Solvation of the E. coli CheY Phosphorylation Site Mapped by XFMS. Hamid M, Khalid MF, Chaudhary SU, Khan S. Int J Mol Sci 23 12771 (2022)


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