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NikR-operator complex structure and the mechanism of repressor activation by metal ions.

Schreiter ER, Wang SC, Zamble DB, Drennan CL
Proc Natl Acad Sci U S A 103 13676-81 (2006)
Cited: 70 times
EuropePMC logo PMID: 16945905

Abstract

Metal ion homeostasis is critical to the survival of all cells. Regulation of nickel concentrations in Escherichia coli is mediated by the NikR repressor via nickel-induced transcriptional repression of the nickel ABC-type transporter, NikABCDE. Here, we report two crystal structures of nickel-activated E. coli NikR, the isolated repressor at 2.1 A resolution and in a complex with its operator DNA sequence from the nik promoter at 3.1 A resolution. Along with the previously published structure of apo-NikR, these structures allow us to evaluate functional proposals for how metal ions activate NikR, delineate the drastic conformational changes required for operator recognition, and describe the formation of a second metal-binding site in the presence of DNA. They also provide a rare set of structural views of a ligand-responsive transcription factor in the unbound, ligand-induced, and DNA-bound states, establishing a model system for the study of ligand-mediated effects on transcription factor function.

Reviews - 2hzv mentioned but not cited (7)

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Articles - 2hzv mentioned but not cited (10)

  1. NikR-operator complex structure and the mechanism of repressor activation by metal ions. Schreiter ER, Wang SC, Zamble DB, Drennan CL. Proc Natl Acad Sci U S A 103 13676-13681 (2006)
  2. Molecular dynamics simulation of the Escherichia coli NikR protein: equilibrium conformational fluctuations reveal interdomain allosteric communication pathways. Bradley MJ, Chivers PT, Baker NA. J Mol Biol 378 1155-1173 (2008)
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  5. Structural basis of low-affinity nickel binding to the nickel-responsive transcription factor NikR from Escherichia coli. Phillips CM, Schreiter ER, Stultz CM, Drennan CL. Biochemistry 49 7830-7838 (2010)
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  8. Nickel Metalloregulators and Chaperones. Higgins K. Inorganics (Basel) 7 (2019)
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Reviews citing this publication (12)

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Articles citing this publication (41)

  1. Nickel Sequestration by the Host-Defense Protein Human Calprotectin. Nakashige TG, Zygiel EM, Drennan CL, Nolan EM. J Am Chem Soc 139 8828-8836 (2017)
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  3. Structural basis for the specialization of Nur, a nickel-specific Fur homolog, in metal sensing and DNA recognition. An YJ, Ahn BE, Han AR, Kim HM, Chung KM, Shin JH, Cho YB, Roe JH, Cha SS. Nucleic Acids Res 37 3442-3451 (2009)
  4. High-affinity Ni2+ binding selectively promotes binding of Helicobacter pylori NikR to its target urease promoter. Zambelli B, Danielli A, Romagnoli S, Neyroz P, Ciurli S, Scarlato V. J Mol Biol 383 1129-1143 (2008)
  5. The N-terminal arm of the Helicobacter pylori Ni2+-dependent transcription factor NikR is required for specific DNA binding. Benanti EL, Chivers PT. J Biol Chem 282 20365-20375 (2007)
  6. The transcription factor AmrZ utilizes multiple DNA binding modes to recognize activator and repressor sequences of Pseudomonas aeruginosa virulence genes. Pryor EE, Waligora EA, Xu B, Dellos-Nolan S, Wozniak DJ, Hollis T. PLoS Pathog 8 e1002648 (2012)
  7. Structure, function, and targets of the transcriptional regulator SvtR from the hyperthermophilic archaeal virus SIRV1. Guillière F, Peixeiro N, Kessler A, Raynal B, Desnoues N, Keller J, Delepierre M, Prangishvili D, Sezonov G, Guijarro JI. J Biol Chem 284 22222-22237 (2009)
  8. Engineering a uranyl-specific binding protein from NikR. Wegner SV, Boyaci H, Chen H, Jensen MP, He C. Angew Chem Int Ed Engl 48 2339-2341 (2009)
  9. Modeling of the structure and interactions of the B. anthracis antitoxin, MoxX: deletion mutant studies highlight its modular structure and repressor function. Chopra N, Agarwal S, Verma S, Bhatnagar S, Bhatnagar R. J Comput Aided Mol Des 25 275-291 (2011)
  10. Ni(II) coordination to mixed sites modulates DNA binding of HpNikR via a long-range effect. West AL, Evans SE, González JM, Carter LG, Tsuruta H, Pozharski E, Michel SL. Proc Natl Acad Sci U S A 109 5633-5638 (2012)
  11. Role of the N-terminus in determining metal-specific responses in the E. coli Ni- and Co-responsive metalloregulator, RcnR. Higgins KA, Chivers PT, Maroney MJ. J Am Chem Soc 134 7081-7093 (2012)
  12. Comprehensive mapping of the Helicobacter pylori NikR regulon provides new insights in bacterial nickel responses. Vannini A, Pinatel E, Costantini PE, Pelliciari S, Roncarati D, Puccio S, De Bellis G, Peano C, Danielli A. Sci Rep 7 45458 (2017)
  13. Holo-Ni(II)HpNikR is an asymmetric tetramer containing two different nickel-binding sites. West AL, St John F, Lopes PE, MacKerell AD, Pozharski E, Michel SL. J Am Chem Soc 132 14447-14456 (2010)
  14. Mycobacterium tuberculosis NmtR harbors a nickel sensing site with parallels to Escherichia coli RcnR. Reyes-Caballero H, Lee CW, Giedroc DP. Biochemistry 50 7941-7952 (2011)
  15. The Ni2+ binding properties of Helicobacter pylori NikR. Zambelli B, Bellucci M, Danielli A, Scarlato V, Ciurli S. Chem Commun (Camb) 3649-3651 (2007)
  16. Crystal structure and centromere binding of the plasmid segregation protein ParB from pCXC100. Huang L, Yin P, Zhu X, Zhang Y, Ye K. Nucleic Acids Res 39 2954-2968 (2011)
  17. Conformational and thermodynamic hallmarks of DNA operator site specificity in the copper sensitive operon repressor from Streptomyces lividans. Tan BG, Vijgenboom E, Worrall JA. Nucleic Acids Res 42 1326-1340 (2014)
  18. Holo-Ni2+ Helicobacter pylori NikR contains four square-planar nickel-binding sites at physiological pH. Benini S, Cianci M, Ciurli S. Dalton Trans 40 7831-7833 (2011)
  19. Structural studies of E73 from a hyperthermophilic archaeal virus identify the "RH3" domain, an elaborated ribbon-helix-helix motif involved in DNA recognition. Schlenker C, Goel A, Tripet BP, Menon S, Willi T, Dlakić M, Young MJ, Lawrence CM, Copié V. Biochemistry 51 2899-2910 (2012)
  20. Structure and function of AvtR, a novel transcriptional regulator from a hyperthermophilic archaeal lipothrixvirus. Peixeiro N, Keller J, Collinet B, Leulliot N, Campanacci V, Cortez D, Cambillau C, Nitta KR, Vincentelli R, Forterre P, Prangishvili D, Sezonov G, van Tilbeurgh H. J Virol 87 124-136 (2013)
  21. Linkage, mobility, and selfishness in the MazF family of bacterial toxins: a snapshot of bacterial evolution. Chopra N, Saumitra, Pathak A, Bhatnagar R, Bhatnagar S. Genome Biol Evol 5 2268-2284 (2013)
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  25. In vivo recognition of the fecA3 target promoter by Helicobacter pylori NikR. Romagnoli S, Agriesti F, Scarlato V. J Bacteriol 193 1131-1141 (2011)
  26. On the interaction of Helicobacter pylori NikR, a Ni(II)-responsive transcription factor, with the urease operator: in solution and in silico studies. Mazzei L, Dobrovolska O, Musiani F, Zambelli B, Ciurli S. J Biol Inorg Chem 20 1021-1037 (2015)
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  28. The structure and function of Mycobacterium tuberculosis MazF-mt6 toxin provide insights into conserved features of MazF endonucleases. Hoffer ED, Miles SJ, Dunham CM. J Biol Chem 292 7718-7726 (2017)
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  31. CdbA is a DNA-binding protein and c-di-GMP receptor important for nucleoid organization and segregation in Myxococcus xanthus. Skotnicka D, Steinchen W, Szadkowski D, Cadby IT, Lovering AL, Bange G, Søgaard-Andersen L. Nat Commun 11 1791 (2020)
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  34. Enhanced adsorption and recovery of uranyl ions by NikR mutant-displaying yeast. Kuroda K, Ebisutani K, Iida K, Nishitani T, Ueda M. Biomolecules 4 390-401 (2014)
  35. Geobacter uraniireducens NikR displays a DNA binding mode distinct from other members of the NikR family. Benanti EL, Chivers PT. J Bacteriol 192 4327-4336 (2010)
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  37. Surface plasmon resonance and isothermal titration calorimetry to monitor the Ni(II)-dependent binding of Helicobacter pylori NikR to DNA. Fabini E, Zambelli B, Mazzei L, Ciurli S, Bertucci C. Anal Bioanal Chem 408 7971-7980 (2016)
  38. Allosteric regulation of the nickel-responsive NikR transcription factor from Helicobacter pylori. Baksh KA, Pichugin D, Prosser RS, Zamble DB. J Biol Chem 296 100069 (2021)
  39. Integrative computational protocol for the discovery of inhibitors of the Helicobacter pylori nickel response regulator (NikR). Segura-Cabrera A, Guo X, Rojo-Domínguez A, Rodríguez-Pérez MA. J Mol Model 17 3075-3084 (2011)
  40. Searching for the Nik operon: how a ligand-responsive transcription factor hunts for its DNA binding site. Phillips CM, Stultz CM, Drennan CL. Biochemistry 49 7757-7763 (2010)
  41. Functional annotation of a novel toxin-antitoxin system Xn-RelT of Xenorhabdus nematophila; a combined in silico and in vitro approach. Gautam LK, Yadav M, Rathore JS. J Mol Model 23 189 (2017)


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