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Crystal structure of the response regulator 02 receiver domain, the essential YycF two-component system of Streptococcus pneumoniae in both complexed and native states.

Bent CJ, Isaacs NW, Mitchell TJ, Riboldi-Tunnicliffe A
J Bacteriol 186 2872-9 (2004)
Related entries: 1nxo, 1nxp, 1nxw

Cited: 38 times
EuropePMC logo PMID: 15090529

Abstract

A variety of bacterial cellular responses to environmental signals are mediated by two-component signal transduction systems comprising a membrane-associated histidine protein kinase and a cytoplasmic response regulator (RR), which interpret specific stimuli and produce a measured physiological response. In RR activation, transient phosphorylation of a highly conserved aspartic acid residue drives the conformation changes needed for full activation of the protein. Sequence homology reveals that RR02 from Streptococcus pneumoniae belongs to the OmpR subfamily of RRs. The structures of the receiver domains from four members of this family, DrrB and DrrD from Thermotoga maritima, PhoB from Escherichia coli, and PhoP from Bacillus subtilis, have been elucidated. These domains are globally very similar in that they are composed of a doubly wound alpha(5)beta(5); however, they differ remarkably in the fine detail of the beta4-alpha4 and alpha4 regions. The structures presented here reveal a further difference of the geometry in this region. RR02 is has been shown to be the essential RR in the gram-positive bacterium S. pneumoniae R. Lange, C. Wagner, A. de Saizieu, N. Flint, J. Molnos, M. Stieger, P. Caspers, M. Kamber, W. Keck, and K. E. Amrein, Gene 237:223-234, 1999; J. P. Throup, K. K. Koretke, A. P. Bryant, K. A. Ingraham, A. F. Chalker, Y. Ge, A. Marra, N. G. Wallis, J. R. Brown, D. J. Holmes, M. Rosenberg, and M. K. Burnham, Mol. Microbiol. 35:566-576, 2000). RR02 functions as part of a phosphotransfer system that ultimately controls the levels of competence within the bacteria. Here we report the native structure of the receiver domain of RR02 from serotype 4 S. pneumoniae (as well as acetate- and phosphate-bound forms) at different pH levels. Two native structures at 2.3 A, phased by single-wavelength anomalous diffraction (xenon SAD), and 1.85 A and a third structure at pH 5.9 revealed the presence of a phosphate ion outside the active site. The fourth structure revealed the presence of an acetate molecule in the active site.

Articles - 1nxt mentioned but not cited (2)

  1. Crystal structure of the response regulator 02 receiver domain, the essential YycF two-component system of Streptococcus pneumoniae in both complexed and native states. Bent CJ, Isaacs NW, Mitchell TJ, Riboldi-Tunnicliffe A. J Bacteriol 186 2872-2879 (2004)
  2. A Variable Active Site Residue Influences the Kinetics of Response Regulator Phosphorylation and Dephosphorylation. Immormino RM, Silversmith RE, Bourret RB. Biochemistry 55 5595-5609 (2016)


Reviews citing this publication (4)

  1. A matter of life and death: cell wall homeostasis and the WalKR (YycGF) essential signal transduction pathway. Dubrac S, Bisicchia P, Devine KM, Msadek T. Mol. Microbiol. 70 1307-1322 (2008)
  2. Molecular strategies for phosphorylation-mediated regulation of response regulator activity. Gao R, Stock AM. Curr. Opin. Microbiol. 13 160-167 (2010)
  3. Microbial biochemistry, physiology, and biotechnology of hyperthermophilic Thermotoga species. Conners SB, Mongodin EF, Johnson MR, Montero CI, Nelson KE, Kelly RM. FEMS Microbiol. Rev. 30 872-905 (2006)
  4. Crystallizing new approaches for antimicrobial drug discovery. Schmid MB. Biochem. Pharmacol. 71 1048-1056 (2006)

Articles citing this publication (32)

  1. Identification of direct residue contacts in protein-protein interaction by message passing. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T. Proc. Natl. Acad. Sci. U.S.A. 106 67-72 (2009)
  2. Mechanism of activation for transcription factor PhoB suggested by different modes of dimerization in the inactive and active states. Bachhawat P, Swapna GV, Montelione GT, Stock AM. Structure 13 1353-1363 (2005)
  3. Structural analysis and solution studies of the activated regulatory domain of the response regulator ArcA: a symmetric dimer mediated by the alpha4-beta5-alpha5 face. Toro-Roman A, Mack TR, Stock AM. J. Mol. Biol. 349 11-26 (2005)
  4. YycH and YycI interact to regulate the essential YycFG two-component system in Bacillus subtilis. Szurmant H, Mohan MA, Imus PM, Hoch JA. J. Bacteriol. 189 3280-3289 (2007)
  5. Domain orientation in the inactive response regulator Mycobacterium tuberculosis MtrA provides a barrier to activation. Friedland N, Mack TR, Yu M, Hung LW, Terwilliger TC, Waldo GS, Stock AM. Biochemistry 46 6733-6743 (2007)
  6. A common dimerization interface in bacterial response regulators KdpE and TorR. Toro-Roman A, Wu T, Stock AM. Protein Sci. 14 3077-3088 (2005)
  7. Crystal structures of the receiver domain of the response regulator PhoP from Escherichia coli in the absence and presence of the phosphoryl analog beryllofluoride. Bachhawat P, Stock AM. J. Bacteriol. 189 5987-5995 (2007)
  8. From principal component to direct coupling analysis of coevolution in proteins: low-eigenvalue modes are needed for structure prediction. Cocco S, Monasson R, Weigt M. PLoS Comput. Biol. 9 e1003176 (2013)
  9. 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)
  10. Involvement of WalK (VicK) phosphatase activity in setting WalR (VicR) response regulator phosphorylation level and limiting cross-talk in Streptococcus pneumoniae D39 cells. Wayne KJ, Li S, Kazmierczak KM, Tsui HC, Winkler ME. Mol. Microbiol. 86 645-660 (2012)
  11. 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)
  12. A transcriptional study of acidogenic chemostat cells of Clostridium acetobutylicum--cellular behavior in adaptation to n-butanol. Schwarz KM, Kuit W, Grimmler C, Ehrenreich A, Kengen SW. J. Biotechnol. 161 366-377 (2012)
  13. The crystal structure of Bacillus subtilis YycI reveals a common fold for two members of an unusual class of sensor histidine kinase regulatory proteins. Santelli E, Liddington RC, Mohan MA, Hoch JA, Szurmant H. J. Bacteriol. 189 3290-3295 (2007)
  14. The X-ray crystal structures of two constitutively active mutants of the Escherichia coli PhoB receiver domain give insights into activation. Arribas-Bosacoma R, Kim SK, Ferrer-Orta C, Blanco AG, Pereira PJ, Gomis-Rüth FX, Wanner BL, Coll M, Solà M. J. Mol. Biol. 366 626-641 (2007)
  15. The Response Regulator BfmR Is a Potential Drug Target for Acinetobacter baumannii. Russo TA, Manohar A, Beanan JM, Olson R, MacDonald U, Graham J, Umland TC. mSphere 1 (2016)
  16. Discovery of novel inhibitors of Streptococcus pneumoniae based on the virtual screening with the homology-modeled structure of histidine kinase (VicK). Li N, Wang F, Niu S, Cao J, Wu K, Li Y, Yin N, Zhang X, Zhu W, Yin Y. BMC Microbiol. 9 129 (2009)
  17. Response regulator YycF essential for bacterial growth: X-ray crystal structure of the DNA-binding domain and its PhoB-like DNA recognition motif. Okajima T, Doi A, Okada A, Gotoh Y, Tanizawa K, Utsumi R. FEBS Lett. 582 3434-3438 (2008)
  18. Conformational changes of Spo0F along the phosphotransfer pathway. Varughese KI. J. Bacteriol. 187 8221-8227 (2005)
  19. Structural basis of a physical blockage mechanism for the interaction of response regulator PmrA with connector protein PmrD from Klebsiella pneumoniae. Luo SC, Lou YC, Rajasekaran M, Chang YW, Hsiao CD, Chen C. J. Biol. Chem. 288 25551-25561 (2013)
  20. Crystal structure of nonphosphorylated receiver domain of the stress response regulator RcsB from Escherichia coli. Filippova EV, Wawrzak Z, Ruan J, Pshenychnyi S, Schultz RM, Wolfe AJ, Anderson WF. Protein Sci. 25 2216-2224 (2016)
  21. ATP forms a stable complex with the essential histidine kinase WalK (YycG) domain. Celikel R, Veldore VH, Mathews I, Devine KM, Varughese KI. Acta Crystallogr. D Biol. Crystallogr. 68 839-845 (2012)
  22. Quorum-sensing based bacteriocin production is down-regulated by N-terminally truncated species of gene activators. Straume D, Kjos M, Nes IF, Diep DB. Mol. Genet. Genomics 278 283-293 (2007)
  23. The Response Regulator YycF Inhibits Expression of the Fatty Acid Biosynthesis Repressor FabT in Streptococcus pneumoniae. Mohedano ML, Amblar M, de la Fuente A, Wells JM, López P. Front Microbiol 7 1326 (2016)
  24. Preliminary crystallographic studies of the regulatory domain of response regulator YycF from an essential two-component signal transduction system. Zhao H, Heroux A, Sequeira RD, Tang L. Acta Crystallogr Sect F Struct Biol Cryst Commun 65 719-722 (2009)
  25. Putative osmosensor--OsHK3b--a histidine kinase protein from rice shows high structural conservation with its ortholog AtHK1 from Arabidopsis. Kushwaha HR, Singla-Pareek SL, Pareek A. J. Biomol. Struct. Dyn. 32 1318-1332 (2014)
  26. The Structure of the Biofilm-controlling Response Regulator BfmR from Acinetobacter baumannii Reveals Details of Its DNA-binding Mechanism. Draughn GL, Milton ME, Feldmann EA, Bobay BG, Roth BM, Olson AL, Thompson RJ, Actis LA, Davies C, Cavanagh J. J. Mol. Biol. 430 806-821 (2018)
  27. Conformational Dynamics of Response Regulator RegX3 from Mycobacterium tuberculosis. Ahmad A, Cai Y, Chen X, Shuai J, Han A. PLoS ONE 10 e0133389 (2015)
  28. Two-component system response regulators involved in virulence of Streptococcus pneumoniae TIGR4 in infective endocarditis. Trihn M, Ge X, Dobson A, Kitten T, Munro CL, Xu P. PLoS ONE 8 e54320 (2013)
  29. A sporulation signature protease is required for assembly of the spore surface layers, germination and host colonization in Clostridioides difficile. Marini E, Olivença C, Ramalhete S, Aguirre AM, Ingle P, Melo MN, Antunes W, Minton NP, Hernandez G, Cordeiro TN, Sorg JA, Serrano M, Henriques AO. PLoS Pathog 19 e1011741 (2023)
  30. Crystal structure of the inactive state of the receiver domain of Spo0A from Paenisporosarcina sp. TG-14, a psychrophilic bacterium isolated from an Antarctic glacier. Lee CW, Park SH, Lee SG, Shin SC, Han SJ, Kim HW, Park HH, Kim S, Kim HJ, Park H, Park H, Lee JH. J. Microbiol. 55 464-474 (2017)
  31. REC domain stabilizes the active heptamer of σ54-dependent transcription factor, FleR from Pseudomonas aeruginosa. Sahoo PK, Sheenu, Jain D. iScience 26 108397 (2023)
  32. 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)


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