Metabolomics and proteomics identify the toxic form and the associated cellular binding targets of the anti-proliferative drug AICAR

J Biol Chem. 2019 Jan 18;294(3):805-815. doi: 10.1074/jbc.RA118.004964. Epub 2018 Nov 26.

Abstract

5-Aminoimidazole-4-carboxamide 1-β-d-ribofuranoside (AICAR, or acadesine) is a precursor of the monophosphate derivative 5-amino-4-imidazole carboxamide ribonucleoside 5'-phosphate (ZMP), an intermediate in de novo purine biosynthesis. AICAR proved to have promising anti-proliferative properties, although the molecular basis of its toxicity is poorly understood. To exert cytotoxicity, AICAR needs to be metabolized, but the AICAR-derived toxic metabolite was not identified. Here, we show that ZMP is the major toxic derivative of AICAR in yeast and establish that its metabolization to succinyl-ZMP, ZDP, or ZTP (di- and triphosphate derivatives of AICAR) strongly reduced its toxicity. Affinity chromatography identified 74 ZMP-binding proteins, including 41 that were found neither as AMP nor as AICAR or succinyl-ZMP binders. Overexpression of karyopherin-β Kap123, one of the ZMP-specific binders, partially rescued AICAR toxicity. Quantitative proteomic analyses revealed 57 proteins significantly less abundant on nuclei-enriched fractions from AICAR-fed cells, this effect being compensated by overexpression of KAP123 for 15 of them. These results reveal nuclear protein trafficking as a function affected by AICAR.

Keywords: drug metabolism; nucleoside/nucleotide analogue; proteomics; purine; small molecule; yeast genetics; yeast metabolism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus / drug effects
  • Aminoimidazole Carboxamide / analogs & derivatives*
  • Aminoimidazole Carboxamide / pharmacokinetics
  • Aminoimidazole Carboxamide / pharmacology
  • Cell Nucleus / chemistry
  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism*
  • Cell Proliferation / drug effects*
  • Chromatography, Affinity
  • Proteomics*
  • Ribonucleotides* / pharmacokinetics
  • Ribonucleotides* / pharmacology
  • Saccharomyces cerevisiae / chemistry
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / metabolism*
  • Saccharomyces cerevisiae Proteins / chemistry
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism*

Substances

  • Ribonucleotides
  • Saccharomyces cerevisiae Proteins
  • Aminoimidazole Carboxamide
  • AICA ribonucleotide