The role of passive transbilayer drug movement in multidrug resistance and its modulation

J Biol Chem. 1996 May 31;271(22):12897-902. doi: 10.1074/jbc.271.22.12897.

Abstract

The successful lowering of the intracellular concentration of multidrug resistance (MDR)-type drugs by P-glycoprotein (Pgp) relies on its ability to overcome the passive influx rate of each MDR-type drug. Thus, the aim of the present work was to study the effect of passive transbilayer drug movement on the multidrug resistance and its modulation. Fluorescence quenching studies indicated that whereas the Pgp substrate rhodamine 123 traverses an artificial lipid membrane with a lifetime of 3 min, the transbilayer movement rate of the MDR modulators, quinidine and quinine, was too fast to be detected with present methods. Transbilayer movement rates of drugs and modulators were estimated from their equilibration rate throughout artificial multilamellar vesicles. The equilibration rate of five selected modulators was faster than the equilibration rate of five representative MDR-type drugs tested, which was comparable with the rate of rhodamine 123 equilibration. Moreover, the carrier-type peptide ionophore, valinomycin, which is freely mobile in the membrane, inhibited Pgp-mediated efflux of rhodamine 123 from MDR cells. In contrast, the channel-forming ionophore gramicidin D, a Pgp substrate that flip-flops slowly across the membrane, did not modulate cellular Pgp activity. Pgp, with a turnover number of about 900 min-1 can keep pace with the influx of an MDR-drug like rhodamine 123 exhibiting a transbilayer movement with a lifetime of minutes. On the other hand, Pgp would fail to protect MDR cells against cytotoxic drugs that are freely mobile through biological membranes and that re-enter cells faster than their Pgp-mediated active efflux rate. The relatively fast transbilayer movement exhibited by MDR modulators suggest that in contrast to MDR-type drugs, MDR modulators traverse the plasma membrane faster than the maximal expulsion rate of Pgp.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily B, Member 1 / metabolism
  • Antineoplastic Agents / metabolism
  • Antineoplastic Agents / pharmacokinetics
  • Biological Transport
  • Drug Resistance, Multiple*
  • Drug Synergism
  • Fluorescent Dyes / metabolism
  • Lipid Bilayers*
  • Liposomes
  • Rhodamine 123
  • Rhodamines / metabolism
  • Substrate Specificity
  • Verapamil / metabolism

Substances

  • ATP Binding Cassette Transporter, Subfamily B, Member 1
  • Antineoplastic Agents
  • Fluorescent Dyes
  • Lipid Bilayers
  • Liposomes
  • Rhodamines
  • Rhodamine 123
  • Verapamil