Hydrolysis of 2'3'-cGAMP by ENPP1 and design of nonhydrolyzable analogs

Nat Chem Biol. 2014 Dec;10(12):1043-8. doi: 10.1038/nchembio.1661. Epub 2014 Oct 26.

Abstract

Agonists of mouse STING (TMEM173) shrink and even cure solid tumors by activating innate immunity; human STING (hSTING) agonists are needed to test this therapeutic hypothesis in humans. The endogenous STING agonist is 2'3'-cGAMP, a second messenger that signals the presence of cytosolic double-stranded DNA. We report activity-guided partial purification and identification of ecto-nucleotide pyrophosphatase/phosphodiesterase (ENPP1) to be the dominant 2'3'-cGAMP hydrolyzing activity in cultured cells. The hydrolysis activity of ENPP1 was confirmed using recombinant protein and was depleted in tissue extracts and plasma from Enpp1(-/-) mice. We synthesized a hydrolysis-resistant bisphosphothioate analog of 2'3'-cGAMP (2'3'-cG(s)A(s)MP) that has similar affinity for hSTING in vitro and is ten times more potent at inducing IFN-β secretion from human THP1 monocytes. Studies in mouse Enpp1(-/-) lung fibroblasts indicate that resistance to hydrolysis contributes substantially to its higher potency. 2'3'-cG(s)A(s)MP is therefore improved over natural 2'3'-cGAMP as a model agonist and has potential as a vaccine adjuvant and cancer therapeutic.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / chemical synthesis
  • Antineoplastic Agents / pharmacology*
  • Cell Line, Tumor
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Hydrolysis
  • Interferon-beta
  • Membrane Proteins / agonists*
  • Membrane Proteins / deficiency
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Monocytes / drug effects
  • Monocytes / metabolism
  • Monocytes / pathology
  • Nucleotides, Cyclic / chemistry
  • Nucleotides, Cyclic / metabolism*
  • Nucleotides, Cyclic / pharmacology
  • Organothiophosphorus Compounds / chemical synthesis
  • Organothiophosphorus Compounds / pharmacology*
  • Phosphoric Diester Hydrolases / genetics
  • Phosphoric Diester Hydrolases / metabolism
  • Pyrophosphatases / antagonists & inhibitors*
  • Pyrophosphatases / genetics
  • Pyrophosphatases / metabolism
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Second Messenger Systems / genetics
  • Signal Transduction

Substances

  • Antineoplastic Agents
  • Membrane Proteins
  • Nucleotides, Cyclic
  • Organothiophosphorus Compounds
  • Recombinant Proteins
  • STING1 protein, human
  • Sting1 protein, mouse
  • cyclic guanosine monophosphate-adenosine monophosphate
  • Interferon-beta
  • Phosphoric Diester Hydrolases
  • ectonucleotide pyrophosphatase phosphodiesterase 1
  • Pyrophosphatases