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The interaction of ammonia and xenon with the imidazole glycerol phosphate synthase from Thermotoga maritima as detected by NMR spectroscopy

  1. Christoph Liebold1,†,
  2. Felix List1,†,
  3. Hans Robert Kalbitzer1,
  4. Reinhard Sterner1,
  5. Eike Brunner2,*

Article first published online: 27 JUL 2010

DOI: 10.1002/pro.463

Issue

Protein Science

Protein Science

Volume 19, Issue 9, pages 1774–1782, September 2010

Additional Information

How to Cite

Liebold, C., List, F., Kalbitzer, H. R., Sterner, R. and Brunner, E. (2010), The interaction of ammonia and xenon with the imidazole glycerol phosphate synthase from Thermotoga maritima as detected by NMR spectroscopy. Protein Science, 19: 1774–1782. doi: 10.1002/pro.463

Author Information

  1. 1

    Institute of Biophysics and Physical Biochemistry, University of Regensburg, Regensburg 93040, Germany

  2. 2

    Fachrichtung Chemie und Lebensmittelchemie, TU Dresden, Dresden 01062, Germany

  1. †

    Christoph Liebold and Felix List contributed equally to this work.

*TU Dresden, Fachrichtung Chemie und Lebensmittelchemie, Bioanalytische Chemie, Dresden 01062, Germany

Publication History

  1. Issue published online: 23 AUG 2010
  2. Article first published online: 27 JUL 2010
  3. Manuscript Revised: 7 JUL 2010
  4. Manuscript Accepted: 7 JUL 2010
  5. Manuscript Received: 26 MAY 2010

Funded by

  • Deutsche ForschungsgemeinschaftKA 647/19, STE 891/3-4

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References

  • 1
    Zalkin H ( 1993) The amidotransferases. Adv Enzymol Relat Areas Mol Biol 66: 203–309.
  • 2
    Klem TJ, Davisson VJ ( 1993) Imidazole glycerol phosphate synthase: the glutamine amidotransferase in histidine biosynthesis. Biochemistry 32: 5177–5186.
  • 3
    Alifano P, Fani R, Lio P, Lazcano A, Bazzicalupo M, Carlomagno MS, Bruni CB ( 1996) Histidine biosynthetic pathway and genes: structure, regulation, and evolution. Microbiol Rev 60: 44–69.
  • 4
    Beismann-Driemeyer S, Sterner R ( 2001) Imidazole glycerol phosphate synthase from Thermotoga maritima. Quaternary structure, steady-state kinetics, and reaction mechanism of the bienzyme complex. J Biol Chem 276: 20387–20396.
  • 5
    Lang D, Thoma R, Henn-Sax M, Sterner R, Wilmanns M ( 2000) Structural evidence for evolution of the beta/alpha barrel scaffold by gene duplication and fusion. Science 289: 1546–1550.
  • 6
    Douangamath A, Walker M, Beismann-Driemeyer S, Vega-Fernandez MC, Sterner R, Wilmanns M ( 2002) Structural evidence for ammonia tunneling across the (βα)8 barrel of the imidazole glycerol phosphate synthase bienzyme complex. Structure 10: 185–193.
  • 7
    Chaudhuri BN, Lange SC, Myers RS, Chittur SV, Davisson VJ, Smith JL ( 2001) Crystal structure of imidazole glycerol phosphate synthase: a tunnel through (βα)8 barrel joins two active sites. Structure 9: 987–997.
  • 8
    Lipchock JM, Loria JP ( 2008) 1H, 15N and 13C resonance assignment of imidazole glycerol phosphate (IGP) synthase protein HisF from Thermotoga maritima. Biomol NMR Assign 2: 219–221.
  • 9
    Lipchock J, Loria JP ( 2009) Millisecond dynamics in the allosteric enzyme imidazole glycerol phosphate synthase (IGPS) from Thermotoga maritima. J Biomol NMR 45: 73–84.
  • 10
    Huang, X, Holden HM, Raushel FM ( 2001) Channeling of substrates and intermediates in enzyme-catalyzed reactions. Annu Rev Biochem 70: 149–80.
  • 11
    Tilton RF Jr, Kuntz ID Jr, Petsko GA ( 1984) Cavities in proteins: structure of a metmyoglobin-xenon complex solved to 1.9 A. Biochemistry 23: 2849–2857.
  • 12
    Locci E, Dehouck Y, Casu M, Saba G, Lai A, Luhmer M, Reisse J, Bartik K ( 2001) Probing proteins in solution by 129Xe NMR spectroscopy. J Magn Reson 150: 167–174.
  • 13
    Rubin SM, Spence MM, Pines A, Wemmer DE ( 2001) Characterization of the effects of nonspecific xenon-protein interactions on 129Xe chemical shifts in aqueous solution: further development of xenon as a biomolecular probe. J Magn Reson 152: 79–86.
  • 14
    Rubin SM, Lee SY, Ruiz EJ, Pines A, Wemmer DE ( 2002) Detection and characterization of xenon-binding sites in proteins by 129Xe NMR spectroscopy. J Mol Biol 322: 425–440.
  • 15
    Gröger C, Möglich A, Pons M, Koch B, Hengstenberg W, Kalbitzer HR, Brunner E ( 2003) NMR-spectroscopic mapping of an engineered cavity in the I14A mutant of HPr from Staphylococcus carnosus using xenon. J Am Chem Soc 125: 8726–8727.
  • 16
    Dubois L, Da Silva P, Landon C, Huber G, Ponchet M, Vovelle F, Berthault P, Desvaux H ( 2004) Probing the hydrophobic cavity of lipid transfer protein from Nicotiana tabacum through Xenon-Based NMR Spectrsocopy. J Am Chem Soc 126: 15738–15746.
  • 17
    Anedda R, Era B, Casu M, Fais A, Ceccarelli M, Corda M, Ruggerone P ( 2008) Evidences for xenon-induced structural changes in the active site of cyano-metmyoglobins: a 1H NMR study. J Phys Chem B 112: 15856–15866
  • 18
    Möglich A, Koch B, Gronwald W, Hengstenberg W, Brunner E, Kalbitzer HR ( 2004) Solution structure of the active-centre mutant I14A of the histidine-containing phosphocarrier protein from Staphylococcus carnosus. Eur J Biochem 271: 4815–4824.
    Direct Link:
  • 19
    Schumann FH, Riepl H, Maurer T, Gronwald W, Neidig KP, Kalbitzer HR ( 2007) Combined chemical shift changes and amino acid specific chemical shift mapping of protein-protein interactions. J Biomol NMR 39: 275–289.
  • 20
    Xu Y, Tang P ( 1997) Amphiphilic sites for general anesthetic action? Evidence from 129Xe -[1H] intermolecular nuclear Overhauser effects. Biochim Biophys Acta 1323: 154–162.
  • 21
    Jaenicke R ( 1999) Stability and folding of domain proteins. Prog Biophys Mol Biol 71: 155–241.
  • 22
    Amaro R, Tajkhorshid E, Luthey-Schulten Z ( 2003) Developing an energy landscape for the novel function of a (βα)8 barrel: ammonia conduction through HisF. Proc Natl Acad Sci USA 100: 7599–7604.
  • 23
    Amaro RE, Myers RS, Davisson VJ, Luthey-Schulten ZA ( 2005) Structural elements in IGP synthase exclude water to optimize ammonia transfer. Biophys J 89: 475–487.
  • 24
    Brunori M, Gibson QH ( 2001) Cavities and packing defects in the structural dynamics of myoglobin. EMBO Rep 2: 674–679.
  • 25
    Breitbach K, Köhler J, Steinmetz I ( 2008) Induction of protective immunity against Burkholderia pseudomallei using attenuated mutants with defects in the intracellular life cycle. Trans R Soc Trop Med Hyg 102 ( Suppl 1): S89–S94.
  • 26
    Gomez MJ, Neyfakh AA ( 2006) Genes involved in intrinsic antibiotic resistance of Acinetobacter baylyi. Antimicrob Agents Chemother 50: 3562–3567.
  • 27
    Gronwald W, Moussa S, Elsner R, Jung A, Ganslmeier B, Trenner J, Kremer W, Neidig KP, Kalbitzer HR ( 2002) Automated assignment of NOESY NMR spectra using a knowledge based method (KNOWNOE). J Biomol NMR 23: 271–287.
  • 28
    Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, Oldfield E, Markley JL, Sykes BD ( 1995) 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 6: 135–140.
  • 29
    Markley JL, Bax A, Arata Y, Hilbers CW, Kaptein R, Sykes BD, Wright PE, Wüthrich K ( 1998) Recommendations for the presentation of NMR structures of proteins and nucleic acids--IUPAC-IUBMB-IUPAB Inter-Union Task Group on the standardization of databases of protein and nucleic acid structures determined by NMR spectroscopy. Eur J Biochem 256: 1–15.
    Direct Link:
  • 30
    Roe DC ( 1985) Sapphire NMR tube for high-resolution studies at elevated pressure. J Magn Reson 63: 388–391.
  • 31
    Haake M, Goodson BM, Laws DD, Brunner E, Cyrier MC, Havlin RH, Pines A ( 1998) NMR of supercritical laser-polarized xenon. Chem Phys Lett 292: 686–690.
  • 32
    Baumer D, Fink A, Brunner E ( 2003) Measurement of the 129Xe NMR chemical shift of supercritical xenon. Z Phys Chem 217: 289–293.
  • 33
    Gill SC, von Hippel PH ( 1989) Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 182: 319–326.
  • 34
    Pace CN, Vajdos F, Fee L, Grimsley G, Gray T ( 1995) How to measure and predict the molar absorption coefficient of a protein. Protein Sci 4: 2411–2423.
    Direct Link:
  • 35
    Ho BK, Gruswitz F ( 2008) Hollow: Generating accurate representations of channel and interior surfaces in molecular structures. BMC Struct Biol 8:1–6.
  • 36
    Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J ( 2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 34 ( Web Server issue): W116–W118.
  • 37
    Delano WL ( 2002) The PyMOL Molecular Graphics System, Version v.099rc6, Schrödinger, LLC.
  • 38
    Thoma R, Obmolova G, Lang DA, Schwander M, Jenö P, Sterner R, Wilmanns M ( 1999) Efficient expression, purification and crystallisation of two hyperthermostable enzymes of histidine biosynthesis. FEBS Lett 454: 1–6.
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