Estragole: DNA adduct formation in primary rat hepatocytes and genotoxic potential in HepG2-CYP1A2 cells

Toxicology. 2020 Nov:444:152566. doi: 10.1016/j.tox.2020.152566. Epub 2020 Aug 25.

Abstract

Estragole is a natural constituent in herbs and spices and in products thereof such as essential oils or herbal teas. After cytochrome P450-catalyzed hydroxylation and subsequent sulfation, estragole acts as a genotoxic hepatocarcinogen forming DNA adducts in rodent liver. Because of the genotoxic mode of action and the widespread occurrence in food and phytomedicines a refined risk assessment for estragole is needed. We analyzed the time- and concentration-dependent levels of the DNA adducts N2-(isoestragole-3'-yl)-2'-desoxyguanosine (E3'N2dG) and N6-(isoestragole-3'-yl)-desoxyadenosine (E3'N6dA), reported to be the major adducts formed in rat liver, in rat hepatocytes (pRH) in primary culture after incubation with estragole. DNA adduct levels were measured via UHPLC-ESI-MS/MS using stable isotope dilution analysis. Both adducts were formed in pRH and could already be quantified after an incubation time of 1 h (E3'N6dA at 10 μM, E3'N2dG at 1μM estragole). E3'N2dG, the main adduct at all incubation times and concentrations, could be detected at estragole concentrations < 0.1 μM after 24 h and < 0.5 μM after 48 h. Adduct levels were highest after 6 h and showed a downward trend at later time-points, possibly due to DNA repair and/or apoptosis. While the concentration-response characteristics of adduct formation were apparently linear over the whole concentration range, strong indication for marked hypo-linearity was obtained when the modeling was based on concentrations < 1 μM only. In the micronucleus assay no mutagenic potential of estragole was found in HepG2 cells whereas in HepG2-CYP1A2 cells 1 μM estragole led to a 3.2 fold and 300 μM to a 7.1 fold increase in micronuclei counts. Our findings suggest the existence of a 'practical threshold' dose for DNA adduct formation as an initiating key event of the carcinogenicity of estragole indicating that the default assumption of concentration-response-linearity is questionable, at least for the two major adducts studied here.

Keywords: Carcinogenicity; DNA adducts; Estragole; Genotoxicity; Hepatoma; Liver cells.

MeSH terms

  • Allylbenzene Derivatives
  • Animals
  • Anisoles / toxicity*
  • Carcinogens / toxicity*
  • Cells, Cultured
  • Cytochrome P-450 CYP1A2 / genetics
  • DNA Adducts*
  • Hepatocytes / drug effects*
  • Hepatocytes / metabolism
  • Humans
  • Male
  • Micronucleus Tests
  • Rats, Wistar

Substances

  • Allylbenzene Derivatives
  • Anisoles
  • Carcinogens
  • DNA Adducts
  • estragole
  • CYP1A2 protein, human
  • Cytochrome P-450 CYP1A2