Luteolin, an emerging anti-cancer flavonoid, poisons eukaryotic DNA topoisomerase I

Biochem J. 2002 Sep 1;366(Pt 2):653-61. doi: 10.1042/BJ20020098.

Abstract

Luteolin, a naturally occurring flavonoid, is abundant in our daily dietary intake. It exhibits a wide spectrum of pharmacological properties, but little is known about its biochemical targets other than the fact that it induces topoisomerase II-mediated apoptosis. In the present study, we show that luteolin completely inhibits the catalytic activity of eukaryotic DNA topoisomerase I at a concentration of 40 microM, with an IC50 of 5 microM. Preincubation of enzyme with luteolin before adding a DNA substrate increases the inhibition of the catalytic activity (IC50=0.66 microM). Treatment of DNA with luteolin before addition of topoisomerase I reduces this inhibitory effect. Subsequent fluorescence tests show that luteolin not only interacts directly with the enzyme but also with the substrate DNA, and intercalates at a very high concentration (>250 microM) without binding to the minor groove. Direct interaction between luteolin and DNA does not affect the assembly of the enzyme-DNA complex, as evident from the electrophoretic mobility-shift assays. Here we show that the inhibition of topoisomerase I by luteolin is due to the stabilization of topoisomerase-I DNA-cleavable complexes. Hence, luteolin is similar to camptothecin, a class I inhibitor, with respect to its ability to form the topoisomerase I-mediated 'cleavable complex'. But, unlike camptothecin, luteolin interacts with both free enzyme and substrate DNA. The inhibitory effect of luteolin is translated into concanavalin A-stimulated mouse splenocytes, with the compound inducing SDS-K+-precipitable DNA-topoisomerase complexes. This is the first report on luteolin as an inhibitor of the catalytic activity of topoisomerase I, and our results further support its therapeutic potential as a lead anti-cancer compound that poisons topoisomerases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amsacrine / pharmacology
  • Animals
  • Antineoplastic Agents / isolation & purification
  • Antineoplastic Agents / pharmacology*
  • Base Sequence
  • Betulinic Acid
  • Catalysis
  • Cell Nucleus / enzymology
  • DNA, Superhelical / chemistry*
  • DNA, Superhelical / metabolism*
  • Enzyme Inhibitors / isolation & purification
  • Enzyme Inhibitors / pharmacology
  • Etoposide / pharmacology
  • Flavonoids / isolation & purification
  • Flavonoids / pharmacology*
  • Kinetics
  • Liver / enzymology
  • Luteolin
  • Nucleic Acid Denaturation
  • Oligodeoxyribonucleotides
  • Pentacyclic Triterpenes
  • Plant Leaves / chemistry
  • Quercetin / pharmacology
  • Rats
  • Spectrometry, Fluorescence
  • Topoisomerase I Inhibitors*
  • Triterpenes / pharmacology

Substances

  • Antineoplastic Agents
  • DNA, Superhelical
  • Enzyme Inhibitors
  • Flavonoids
  • Oligodeoxyribonucleotides
  • Pentacyclic Triterpenes
  • Topoisomerase I Inhibitors
  • Triterpenes
  • Amsacrine
  • Etoposide
  • Quercetin
  • Luteolin
  • Betulinic Acid