A Luminescence-Based Coupled Enzyme Assay Enables High-Throughput Quantification of the Bacterial Second Messenger 3'3'-Cyclic-Di-AMP

Chembiochem. 2021 Mar 16;22(6):1030-1041. doi: 10.1002/cbic.202000667. Epub 2020 Dec 4.

Abstract

Cyclic dinucleotide signaling systems, which are found ubiquitously throughout nature, allow organisms to rapidly and dynamically sense and respond to alterations in their environments. In recent years, the second messenger, cyclic di-(3',5')-adenosine monophosphate (c-di-AMP), has been identified as an essential signaling molecule in a diverse array of bacterial genera. We and others have shown that defects in c-di-AMP homeostasis result in severe physiological defects and virulence attenuation in many bacterial species. Despite significant advancements in the field, there is still a major gap in the understanding of the environmental and cellular factors that influence c-di-AMP dynamics due to a lack of tools to sensitively and rapidly monitor changes in c-di-AMP levels. To address this limitation, we describe here the development of a luciferase-based coupled enzyme assay that leverages the cyclic nucleotide phosphodiesterase, CnpB, for the sensitive and high-throughput quantification of 3'3'-c-di-AMP. We also demonstrate the utility of this approach for the quantification of the cyclic oligonucleotide-based anti-phage signaling system (CBASS) effector, 3'3'-cGAMP. These findings establish CDA-Luc as a more affordable and sensitive alternative to conventional c-di-AMP detection tools with broad utility for the study of bacterial cyclic dinucleotide physiology.

Keywords: RECON; bacteria; cyclic dinucleotides; luciferase-based coupled enzyme assay; quantification; signaling molecules.

Publication types

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

MeSH terms

  • 3',5'-Cyclic-GMP Phosphodiesterases / metabolism*
  • Adenosine Monophosphate / metabolism
  • Bacteria / metabolism
  • Bacterial Proteins / metabolism*
  • Dinucleoside Phosphates / analysis*
  • Dinucleoside Phosphates / chemistry
  • Dinucleoside Phosphates / metabolism
  • Enzyme Assays / methods*
  • High-Throughput Screening Assays
  • Hydrolysis
  • Luciferases / metabolism
  • Luminescent Measurements / methods
  • Mycobacterium tuberculosis / enzymology

Substances

  • Bacterial Proteins
  • Dinucleoside Phosphates
  • cyclic diadenosine phosphate
  • Adenosine Monophosphate
  • Luciferases
  • 3',5'-Cyclic-GMP Phosphodiesterases