Bioflavonoids as poisons of human topoisomerase II alpha and II beta

Biochemistry. 2007 May 22;46(20):6097-108. doi: 10.1021/bi7000664. Epub 2007 Apr 26.

Abstract

Bioflavonoids are human dietary components that have been linked to the prevention of cancer in adults and the generation of specific types of leukemia in infants. While these compounds have a broad range of cellular activities, many of their genotoxic effects have been attributed to their actions as topoisomerase II poisons. However, the activities of bioflavonoids against the individual isoforms of human topoisomerase II have not been analyzed. Therefore, we characterized the activity and mechanism of action of three major classes of bioflavonoids, flavones, flavonols, and isoflavones, against human topoisomerase IIalpha and IIbeta. Genistein was the most active bioflavonoid tested and stimulated enzyme-mediated DNA cleavage approximately 10-fold. Generally, compounds were more active against topoisomerase IIbeta. DNA cleavage with both enzyme isoforms required a 5-OH and a 4'-OH and was enhanced by the presence of additional hydroxyl groups on the pendant ring. Competition DNA cleavage and topoisomerase II binding studies indicate that the 5-OH group plays an important role in mediating genistein binding, while the 4'-OH moiety contributes primarily to bioflavonoid function. Bioflavonoids do not require redox cycling for activity and function primarily by inhibiting enzyme-mediated DNA ligation. Mutagenesis studies suggest that the TOPRIM region of topoisomerase II plays a role in genistein binding. Finally, flavones, flavonols, and isoflavones with activity against purified topoisomerase IIalpha and IIbeta enhanced DNA cleavage by both isoforms in human CEM leukemia cells. These data support the hypothesis that bioflavonoids function as topoisomerase II poisons in humans and provide a framework for further analysis of these important dietary components.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Alanine / genetics
  • Amino Acid Substitution / genetics
  • Antigens, Neoplasm / chemistry
  • Antigens, Neoplasm / genetics
  • Antineoplastic Agents, Phytogenic / toxicity
  • Cell Line, Tumor
  • DNA Damage / drug effects
  • DNA Topoisomerases, Type II / chemistry
  • DNA Topoisomerases, Type II / genetics
  • DNA-Binding Proteins / antagonists & inhibitors*
  • DNA-Binding Proteins / chemistry
  • DNA-Binding Proteins / genetics
  • Drug Resistance, Neoplasm
  • Flavones / chemistry
  • Flavones / toxicity
  • Flavonoids / chemistry
  • Flavonoids / classification
  • Flavonoids / toxicity*
  • Flavonols / chemistry
  • Flavonols / toxicity
  • Genistein / toxicity
  • Glycine / genetics
  • Humans
  • Isoenzymes / antagonists & inhibitors
  • Isoenzymes / chemistry
  • Isoenzymes / genetics
  • Isoflavones / chemistry
  • Isoflavones / toxicity
  • Structure-Activity Relationship
  • Topoisomerase II Inhibitors*

Substances

  • Antigens, Neoplasm
  • Antineoplastic Agents, Phytogenic
  • DNA-Binding Proteins
  • Flavones
  • Flavonoids
  • Flavonols
  • Isoenzymes
  • Isoflavones
  • Topoisomerase II Inhibitors
  • Genistein
  • DNA Topoisomerases, Type II
  • Alanine
  • Glycine