Allosteric regulation of the partitioning of glucose-1-phosphate between glycogen and trehalose biosynthesis in Mycobacterium tuberculosis

Biochim Biophys Acta. 2015 Jan;1850(1):13-21. doi: 10.1016/j.bbagen.2014.09.023. Epub 2014 Sep 30.

Abstract

Background: Mycobacterium tuberculosis is a pathogenic prokaryote adapted to survive in hostile environments. In this organism and other Gram-positive actinobacteria, the metabolic pathways of glycogen and trehalose are interconnected.

Results: In this work we show the production, purification and characterization of recombinant enzymes involved in the partitioning of glucose-1-phosphate between glycogen and trehalose in M. tuberculosis H37Rv, namely: ADP-glucose pyrophosphorylase, glycogen synthase, UDP-glucose pyrophosphorylase and trehalose-6-phosphate synthase. The substrate specificity, kinetic parameters and allosteric regulation of each enzyme were determined. ADP-glucose pyrophosphorylase was highly specific for ADP-glucose while trehalose-6-phosphate synthase used not only ADP-glucose but also UDP-glucose, albeit to a lesser extent. ADP-glucose pyrophosphorylase was allosterically activated primarily by phosphoenolpyruvate and glucose-6-phosphate, while the activity of trehalose-6-phosphate synthase was increased up to 2-fold by fructose-6-phosphate. None of the other two enzymes tested exhibited allosteric regulation.

Conclusions: Results give information about how the glucose-1-phosphate/ADP-glucose node is controlled after kinetic and regulatory properties of key enzymes for mycobacteria metabolism.

General significance: This work increases our understanding of oligo and polysaccharides metabolism in M. tuberculosis and reinforces the importance of the interconnection between glycogen and trehalose biosynthesis in this human pathogen.

Keywords: ADP-glucose pyrophosphorylase; Glucose-6-phosphate; Glycogen synthase; Phosphoenolpyruvate; Trehalose-6-phosphate synthase; UDP-glucose pyrophosphorylase.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Allosteric Regulation
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Glucose-1-Phosphate Adenylyltransferase / genetics
  • Glucose-1-Phosphate Adenylyltransferase / metabolism
  • Glucose-6-Phosphate / metabolism
  • Glucosephosphates / metabolism*
  • Glucosyltransferases / genetics
  • Glucosyltransferases / metabolism
  • Glycogen / biosynthesis*
  • Glycogen Synthase / genetics
  • Glycogen Synthase / metabolism
  • Kinetics
  • Metabolic Networks and Pathways*
  • Models, Biological
  • Mycobacterium tuberculosis / enzymology
  • Mycobacterium tuberculosis / metabolism*
  • Recombinant Proteins / metabolism
  • Substrate Specificity
  • Trehalose / biosynthesis*
  • UTP-Glucose-1-Phosphate Uridylyltransferase / genetics
  • UTP-Glucose-1-Phosphate Uridylyltransferase / metabolism

Substances

  • Bacterial Proteins
  • Glucosephosphates
  • Recombinant Proteins
  • Glucose-6-Phosphate
  • Glycogen
  • Trehalose
  • glucose-1-phosphate
  • Glucosyltransferases
  • Glycogen Synthase
  • trehalose-6-phosphate synthase
  • Glucose-1-Phosphate Adenylyltransferase
  • UTP-Glucose-1-Phosphate Uridylyltransferase