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Direct and indirect roles of His-418 in metal binding and in the activity of β-galactosidase (E. coli)

  1. Douglas H. Juers1,†,
  2. Beatrice Rob2,
  3. Megan L. Dugdale2,
  4. Nastaron Rahimzadeh2,
  5. Clarence Giang2,
  6. Michelle Lee2,
  7. Brian W. Matthews1,
  8. Reuben E. Huber2,*

Article first published online: 16 APR 2009

DOI: 10.1002/pro.140

Issue

Protein Science

Protein Science

Volume 18, Issue 6, pages 1281–1292, June 2009

Additional Information

How to Cite

Juers, D. H., Rob, B., Dugdale, M. L., Rahimzadeh, N., Giang, C., Lee, M., Matthews, B. W. and Huber, R. E. (2009), Direct and indirect roles of His-418 in metal binding and in the activity of β-galactosidase (E. coli). Protein Science, 18: 1281–1292. doi: 10.1002/pro.140

Author Information

  1. 1

    Instititute of Molecular Biology, Howard Hughes Medical Institute and Department of Physics, University of Oregon, Eugene, Oregon 97403-1229

  2. 2

    Division of Biochemistry, Faculty of Science, University of Calgary, Calgary Alberta, Canada, T2N 1N4

  1. †

    Department of Physics, Whitman College, Walla Walla WA 99362, USA

*Division of Biochemistry, Faculty of Science, University of Calgary, Calgary Alberta, Canada T2N 1N4

Publication History

  1. Issue published online: 26 MAY 2009
  2. Article first published online: 16 APR 2009
  3. Accepted manuscript online: 16 APR 2009 12:00AM EST
  4. Manuscript Accepted: 9 APR 2009
  5. Manuscript Revised: 2 APR 2009
  6. Manuscript Received: 2 JAN 2009

Funded by

  • NIH. Grant Number: GM20066
  • National Science and Engineering Research Council (Canada). Grant Number: 4691

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References

  • 1
    Huber RE, Kurz G, Wallenfels K ( 1976) A quantitation of the factors which affect the hyrolase and trangalactosylase activities of ß-galactosidase (E. coli) on lactose. Biochemistry 15: 1994–2001.
  • 2
    Huber RE, Gaunt MT ( 1983) Importance of hydroxyls at positions 3, 4, and 6 for binding to the galactose site of ß-galactosidase (Escherichia coli). Arch Biochem Biophys 220: 263–271.
  • 3
    Juers DH, Heightman TD, Vasella A, McCarter JD, Mackenzie L, Withers SG, Matthews BW ( 2001) A structural view of the action of Escherichia coli (lacZ) ß-galactosidase. Biochemistry 40: 14781–14794.
  • 4
    Huber RE, Hakda S, Cheng C, Cupples CG, Edwards RA ( 2003) Trp-999 of ß-galactosidase (Escherichia coli) is a key residue for binding, catalysis, and synthesis of allolactose, the natural Lac operon inducer. Biochemistry 42: 1796–1803.
  • 5
    Tenu JP, Viratelle OM, Yon J ( 1972) Kinetic study of the activation process of ß-galactosidase from Escherichia coli by Mg2+. Eur J Biochem 26: 112–118.
    Direct Link:
  • 6
    Huber RE, Parfett C, Woulfe-Flanagan H, Thompson DJ ( 1979) Interaction of divalent cations with ß-galactosidase (Escherichia coli). Biochemistry 18: 4090–4095.
  • 7
    Sutendra G, Wong S, Fraser ME, Huber RE ( 2007) ß-Galactosidase (Escherichia coli) has a second catalytically important Mg2+ site. Biochem Biophys Res Comm 352: 566–570.
  • 8
    Sinnott ML, Withers SG, Viratelle OM ( 1978) The necessity of magnesium cation for acid assistance of aglycone departure in catalysis by Escherichia coli (lacZ) ß-galactosidase. Biochem J 175: 539–536.
  • 9
    Richard JP, Huber RE, Lin S, Heo C, Amyes TL ( 1996) Structure-reactivity relationships for ß-galactosidase (Escherichia coli. lac Z). III. Evidence that Glu-461 participates in Bronsted acid-base catalysis of ß-D-galactopyranosyl group transfer. Biochem 35: 12377–12386.
  • 10
    Richard JP, McCall DA, Heo CK, Toteva MM ( 2005) Ground state, transition state, and metal-cation effects of the 2-hydroxyl group on ß-D-galactopyranosyl transfer catalyzed by ß-galactosidase (Escherichia coli, lacZ). Biochemistry 44: 11872–11881.
  • 11
    Xu J, McRae MA, Harron S, Rob B, Huber RE ( 2004) A study of the relationship of interactions between Asp-201, Na+ or K+, and galactosyl C6-hydroxyl and their effects on binding and reactivity of ß-galactosidase. Biochem Cell Biol 82: 275–284.
  • 12
    Edwards RA, Cupples CG, Huber RE ( 1990) Site directed mutants of ß-galactosidase show that Tyr-503 is unimportant in Mg2+ binding but that Glu-461 is very important and may be a ligand of Mg2+. Biochem Biophys Res Commun 171: 33–37.
  • 13
    Jacobson RH, Zhang X-J, DuBose RF, Matthews BW ( 1994) Three-dimensional structure of ß-galactosidase from E. coli. Nature 369: 761–766.
  • 14
    Roth NJ, Huber RE ( 1994) Site directed substitutions suggest that His-418 of ß-galactosidase (E. coli) is a ligand to Mg2+. Biochem Biophys Res Comm 201: 866–870.
  • 15
    Roth NJ, Huber RE ( 1996) Glu-416 of ß-galactosidase (Escherichia coli) is a Mg2+ ligand and ß-galactosidases with substitutions for Glu-416 are inactivated rather than activated by Mg2+. Biochem Biophys Res Commun 219: 111–115.
  • 16
    Potterton L, McNicholas S, Krissinel E, Gruber J, Cowtan K, Emsley P, Murshudov GN, Cohen S, Perrakis A, Noble M ( 2004) Developments in the CCP4 molecular-graphics project. Acta Crystallogr D 60: 2288–2294.
    Direct Link:
  • 17
    Glusker JP ( 1991) Structural aspects of metal binding to functional groups in proteins. Adv Prot Chem 42: 1–76.
  • 18
    Gong L, Guo W, Xionga J, Lia R, Wu X, Li W ( 2006) Structures and stability of ionic liquid model with imidazole and hydrogen fluorides chains: density functional theory study. Chem Phys Lett 425: 167–178.
  • 19
    Kraulis JP ( 1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J Appl Crystallogr 24: 946–950.
    Direct Link:
  • 20
    Juers DH, Wigley RH, Zhang X, Huber RE, Tronrud DE, Matthews BW ( 2000) High resolution refinement of ß-galactosidase in a new crystal form reveals multiple metal binding sites and provides a structural basis for 〈-complementation. Protein Sci 9: 1685–1699.
    Direct Link:
  • 21
    Huber RE, Brockbank RL ( 1987) Strong inhibitory effect of furanoses and sugar lactones on ß-galactosidase of Escherichia coli. Biochemistry 26: 1526–1531.
  • 22
    Petterson EF, Goddard TD, Huang CC, Couch GS, Greenblat DM, Meng EC, Ferrin TE ( 2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Comput Chem 25: 1605–1612.
    Direct Link:
  • 23
    Huber RE, Gaunt MT, Hurlburt KL ( 1984) Binding and reactivity at the “glucose” site of galactosyl-beta galactosidase (Escherichia coli). Arch Biochem Biophys 234: 151.
  • 24
    Tenu JP, Viratelle OM, Garnier J, Yon J ( 1971) pH dependence of the activity of ß-galactosidase from Escherichia coli. Eur J Biochem 20: 363–370.
    Direct Link:
  • 25
    Hill JA, Huber RE ( 1971) Effects of various concentrations of Na+ and Mg2+ on the activity of ß-galactosidase. Biochim Biophys Acta 250: 530–537.
  • 26
    Hill JA, Huber RE ( 1974) The mechanism of Na+ activation of E.coli ß-galactosidase and the inhibitory effect of high concentrations of Mg2+ on this activation. Int J Biochem 5: 773–779.
  • 27
    Case GS, Sinnott ML ( 1973) The role of magnesium ions in ß-galactosidase-catalysed hydrolyses. Biochem J 133: 99–104.
  • 28
    Viratelle OM, Yon JM ( 1973) Nucleophilic competition in some ß-galactosidase-catalyzed reactions. Eur J Biochem 33: 110–116.
    Direct Link:
  • 29
    Huber RE, Gupta MN, Khare SK ( 1994) The active site and mechanism of the ß-galactosidase from Escherichia coli. Int J Biochem 26: 309–318.
  • 30
    Richard JP ( 1998) The enhancement of enzyme rate accelerations by bronsted acid–base catalysis. Biochemistry 37: 4305–4309.
  • 31
    Wickson VM, Huber RE ( 1970) The non-simultaineous dissociation and loss of activity of ß-galactosidase in urea. Biochim Biophys Acta 207: 150–155.
  • 32
    Gallagher CN, Huber RE ( 1997) Monomer-dimer equilibrium of uncomplemented M15 ß-galactosidase from Escherichia coli. Biochemistry 36: 1281–1286.
  • 33
    Jobe A, Bourgeois S ( 1972) Lac repressor-operator interaction VI. The natural inducer of the lac operon. J Mol Biol 69: 397–408.
  • 34
    Kunkel TA ( 1987) Approaches to efficient site directed mutagenesis. Mol Biol Rep 1: 1–2.
  • 35
    Kunkel TA, Roberts JD, Zakour RA ( 1987) Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol 154: 367–382.
  • 36
    Cupples CG, Miller JH, Huber RE ( 1990) Determination of the roles of Glu-461 in ß-galactosidase (E. coli) using site-specific mutagenesis. J Biol Chem 265: 5512–5518.
  • 37
    Kabsch W ( 1988) Evaluation of single-crystal X-ray diffraction data from a position-sensitive detector. J Appl Cryst 21: 916–924.
    Direct Link:
  • 38
    Leslie AGW, From chemistry to biology. In: MorasD, PodjarnyAD, ThierryJ-C, Eds. ( 1991), Crystallographic computing 5, Oxford: Oxford University Press, pp 50–61.
  • 39
    Evans PR ( 1993) In: proceedings of a CCP4 study weekendon data collection and processing, Daresbury: SERC Daresbury Laboratory, pp 114–122.
  • 40
    Tronrud DE ( 1997) TNT refinement package. Methods Enzymol 277: 306–319.
  • 41
    Lamzin VS, Wilson KS ( 1993) Automated refinement of protein models. Acta Crystallogr D Biol Crystallogr 49: 129–147.
    Direct Link:
  • 42
    McRee D ( 1999) XtalView/Xfit–a versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125: 156–165.
  • 43
    Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL ( 1998) Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905–921.
    Direct Link:
  • 44
    Edelsbrunner H, Koehl P ( 2005) The geometry of biomolecular solvation. Discrete and Computational Geometry. (MSRI Publications) 52: 243–275.
  • 45
    Zhang XJ, Matthews BW ( 1995) EDPDB: a multifunctional tool for protein structure analysis. J Appl Cryst 28: 624–630.
    Direct Link:
  • 46
    Deschavanne PJ, Viratelle OM, Yon JM ( 1978) Conformational adaptability of the active site of ß-galactosidase. J Biol Chem 253:833–837.
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