Understanding Miltefosine-Membrane Interactions Using Molecular Dynamics Simulations

Langmuir. 2015 Apr 21;31(15):4503-12. doi: 10.1021/acs.langmuir.5b00178. Epub 2015 Apr 7.

Abstract

Coarse-grained molecular dynamics simulations are used to calculate the free energies of transfer of miltefosine, an alkylphosphocholine anticancer agent, from water to lipid bilayers to study its mechanism of interaction with biological membranes. We consider bilayers containing lipids with different degrees of unsaturation: dipalmitoylphosphatidylcholine (DPPC, saturated, containing 0%, 10%, and 30% cholesterol), dioleoylphosphatidylcholine (DOPC, diunsaturated), palmitoyloleoylphosphatidylcholine (POPC, monounsaturated), diarachidonoylphosphatidylcholine (DAPC, polyunsaturated), and dilinoleylphosphatidylcholine (DUPC, polyunsaturated). These free energies, calculated using umbrella sampling, were used to compute the partition coefficients (K) of miltefosine between water and the lipid bilayers. The K values for the bilayers relative to that of pure DPPC were found to be 5.3 (DOPC), 7.0 (POPC), 1.0 (DAPC), 2.2 (DUPC), 14.9 (10% cholesterol), and 76.2 (30% cholesterol). Additionally, we calculated the free energy of formation of miltefosine-cholesterol complexes by pulling the surfactant laterally in the DPPC + 30% cholesterol system. The free energy profile that we obtained provides further evidence that miltefosine tends to associate with cholesterol and has a propensity to partition into lipid rafts. We also quantified the kinetics of the transport of miltefosine through the various bilayers by computing permeance values. The highest permeance was observed in DUPC bilayers (2.28 × 10(-2) m/s) and the lowest permeance in the DPPC bilayer with 30% cholesterol (1.10 × 10(-7) m/s). Our simulation results show that miltefosine does indeed interact with lipid rafts, has a higher permeability in polyunsaturated, loosely organized bilayers, and has higher flip-flop rates in specific regions of cellular membranes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 1,2-Dipalmitoylphosphatidylcholine / chemistry
  • Antineoplastic Agents / chemistry*
  • Cholesterol / chemistry
  • Kinetics
  • Lipid Bilayers / chemistry*
  • Membrane Microdomains / chemistry*
  • Molecular Dynamics Simulation*
  • Phosphatidylcholines / chemistry
  • Phosphorylcholine / analogs & derivatives*
  • Phosphorylcholine / chemistry
  • Thermodynamics
  • Water / chemistry

Substances

  • Antineoplastic Agents
  • Lipid Bilayers
  • Phosphatidylcholines
  • Water
  • Phosphorylcholine
  • 1,2-diarachidonoyl-glycero-3-phosphocholine
  • 1,2-Dipalmitoylphosphatidylcholine
  • miltefosine
  • Cholesterol
  • 1,2-oleoylphosphatidylcholine
  • 1-palmitoyl-2-oleoylphosphatidylcholine