High inorganic triphosphatase activities in bacteria and mammalian cells: identification of the enzymes involved

PLoS One. 2012;7(9):e43879. doi: 10.1371/journal.pone.0043879. Epub 2012 Sep 12.

Abstract

Background: We recently characterized a specific inorganic triphosphatase (PPPase) from Nitrosomonas europaea. This enzyme belongs to the CYTH superfamily of proteins. Many bacterial members of this family are annotated as predicted adenylate cyclases, because one of the founding members is CyaB adenylate cyclase from A. hydrophila. The aim of the present study is to determine whether other members of the CYTH protein family also have a PPPase activity, if there are PPPase activities in animal tissues and what enzymes are responsible for these activities.

Methodology/principal findings: Recombinant enzymes were expressed and purified as GST- or His-tagged fusion proteins and the enzyme activities were determined by measuring the release of inorganic phosphate. We show that the hitherto uncharacterized E. coli CYTH protein ygiF is a specific PPPase, but it contributes only marginally to the total PPPase activity in this organism, where the main enzyme responsible for hydrolysis of inorganic triphosphate (PPP(i)) is inorganic pyrophosphatase. We further show that CyaB hydrolyzes PPP(i) but this activity is low compared to its adenylate cyclase activity. Finally we demonstrate a high PPPase activity in mammalian and quail tissue, particularly in the brain. We show that this activity is mainly due to Prune, an exopolyphosphatase overexpressed in metastatic tumors where it promotes cell motility.

Conclusions and general significance: We show for the first time that PPPase activities are widespread in bacteria and animals. We identified the enzymes responsible for these activities but we were unable to detect significant amounts of PPP(i) in E. coli or brain extracts using ion chromatography and capillary electrophoresis. The role of these enzymes may be to hydrolyze PPP(i), which could be cytotoxic because of its high affinity for Ca(2+), thereby interfering with Ca(2+) signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Adenylyl Cyclases / metabolism
  • Amino Acid Sequence
  • Animals
  • Bacteria / enzymology*
  • Biocatalysis
  • Cell Survival
  • Electrophoresis, Capillary
  • Escherichia coli / enzymology
  • Escherichia coli Proteins / chemistry
  • Escherichia coli Proteins / metabolism
  • Hydrolysis
  • Inorganic Chemicals / metabolism*
  • Inorganic Pyrophosphatase / metabolism
  • Mammals / metabolism*
  • Molecular Sequence Data
  • Nitrosomonas europaea / enzymology
  • Phosphoprotein Phosphatases / chemistry
  • Phosphoprotein Phosphatases / metabolism*
  • Polyphosphates / isolation & purification
  • Polyphosphates / metabolism
  • Rats
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Subcellular Fractions / enzymology
  • Substrate Specificity

Substances

  • Escherichia coli Proteins
  • Inorganic Chemicals
  • Polyphosphates
  • Recombinant Proteins
  • Adenosine Triphosphate
  • Phosphoprotein Phosphatases
  • Inorganic Pyrophosphatase
  • Adenylyl Cyclases
  • triphosphoric acid

Grants and funding

LB is a Research Director and BL is a Research Associate at the Funds for Scientific Research – FNRS (Belgium). DD is a Research Fellows of the Fonds pour la Formation à la Recherche dans l'Industrie et dans l'Agriculture (F.R.I.A.). This work was supported by grants of the “Fonds de la Recherche Fondamendale collective” (Grants and 2.4558.04 and 2.4508.10). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.