Allosteric regulation and substrate activation in cytosolic nucleotidase II from Legionella pneumophila

FEBS J. 2014 Mar;281(6):1613-1628. doi: 10.1111/febs.12727. Epub 2014 Feb 17.

Abstract

Cytosolic nucleotidase II (cN-II) from Legionella pneumophila (Lp) catalyzes the hydrolysis of GMP and dGMP displaying sigmoidal curves, whereas catalysis of IMP hydrolysis displayed a biphasic curve in the initial rate versus substrate concentration plots. Allosteric modulators of mammalian cN-II did not activate LpcN-II although GTP, GDP and the substrate GMP were specific activators. Crystal structures of the tetrameric LpcN-II revealed an activator-binding site at the dimer interface. A double mutation in this allosteric-binding site abolished activation, confirming the structural observations. The substrate GMP acting as an activator, partitioning between the allosteric and active site, is the basis for the sigmoidicity of the initial velocity versus GMP concentration plot. The LpcN-II tetramer showed differences in subunit organization upon activator binding that are absent in the activator-bound human cN-II structure. This is the first observation of a structural change induced by activator binding in cN-II that may be the molecular mechanism for enzyme activation.

Database: The coordinates and structure factors reported in this paper have been submitted to the Protein Data Bank under the accession numbers 2BDE and 4G63. The accession number of GMP complexed LpcN-II is 4OHF.

Structured digital abstract: LpcN-II and LpcN-II bind by molecular sieving (View interaction) LpcN-II and LpcN-II bind by x-ray crystallography (View interaction) [Structured digital abstract was added on 5 March 2014 after original online publication].

Keywords: 5′-nucleotidase; GMP-complexed LpcN-II structure; allostery; heterotropic activation; substrate activation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 5'-Nucleotidase / chemistry*
  • 5'-Nucleotidase / genetics
  • 5'-Nucleotidase / metabolism*
  • Allosteric Regulation
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism*
  • Catalytic Domain
  • Crystallography, X-Ray
  • Deoxyguanine Nucleotides / metabolism
  • Enzyme Activation
  • Guanosine Diphosphate / metabolism
  • Guanosine Triphosphate / metabolism
  • Humans
  • Kinetics
  • Legionella pneumophila / enzymology*
  • Legionella pneumophila / genetics
  • Models, Molecular
  • Mutagenesis, Site-Directed
  • Nitrophenols / metabolism
  • Organophosphorus Compounds / metabolism
  • Protein Conformation
  • Protein Structure, Quaternary
  • Protein Structure, Tertiary
  • Species Specificity
  • Substrate Specificity

Substances

  • Bacterial Proteins
  • Deoxyguanine Nucleotides
  • Nitrophenols
  • Organophosphorus Compounds
  • Guanosine Diphosphate
  • nitrophenylphosphate
  • Guanosine Triphosphate
  • deoxyguanosine triphosphate
  • 5'-Nucleotidase