Intermolecular Interactions between Coencapsulated Drugs Inhibit Drug Crystallization and Enhance Colloidal Stability of Polymeric Micelles

Mol Pharm. 2017 Oct 2;14(10):3568-3576. doi: 10.1021/acs.molpharmaceut.7b00591. Epub 2017 Sep 1.

Abstract

Novel "pairs" of drugs possessing pharmacological synergies could be encapsulated into polymeric micelles and exert superb therapeutic effects in vivo upon intravenous administration, with the prerequisite that the micelles remain stable. NADP(H) quinone oxidoreductase 1 (NQO1) inhibitors, such as β-lapachone (LPC) and tanshinone IIA (THA), are structurally and pharmacologically similar molecules that are poorly water-soluble, crystallize extremely fast, and demonstrate synergistic anticancer effect when used together with paclitaxel (PTX). However, when coencapsulated with PTX in poly(ethylene glycol)-b-poly(d,l-lactic acid) (PEG-PLA) micelles, only PTX/LPC but not the PTX/THA pair yields satisfactory colloidal stability. To reveal the molecular mechanism contributing to the colloidal stability of the coencapsulated micelles, we investigated the molecular interactions of PTX/LPC and PTX/THA, through both experimental methods (crystallization kinetics, 13C NMR) and molecular dynamic simulation. We observed that PTX was capable of inhibiting LPC but not THA crystallization both in an aqueous environment and in the solid state, which could be attributed to the strong hetero-intermolecular interactions (π-π, H-bonding) between LPC and PTX, which disrupted the homo-intermolecular interactions between LPC molecules and thus formed a favorable miscible binary system. In comparison, the lack of a strong PTX/THA interaction left the strong THA/THA stacking interaction undisturbed and the fast THA crystallization tendency unrestrained. We conclude that the intermolecular interactions, i.e., the "pharmaceutical synergy", between the coencapsulated drugs critically control the colloidal stability of polymeric micelles and, therefore, should be evaluated when coencapsulated drug delivery systems are designed for optimal therapeutic benefits.

Keywords: crystallization; molecular dynamic simulation; paclitaxel; polymer micelles; synergistic anticancer therapy; tanshinone IIA; β-lapachone.

MeSH terms

  • Abietanes / pharmacology
  • Antineoplastic Agents / pharmacology*
  • Chemistry, Pharmaceutical
  • Colloids
  • Crystallization
  • Drug Carriers / chemistry*
  • Drug Compounding / methods*
  • Drug Synergism
  • Enzyme Inhibitors
  • Humans
  • Micelles
  • Molecular Dynamics Simulation
  • NAD(P)H Dehydrogenase (Quinone) / antagonists & inhibitors*
  • Nanoparticles / chemistry
  • Naphthoquinones / pharmacology
  • Paclitaxel / pharmacology
  • Polyethylene Glycols / chemistry

Substances

  • Abietanes
  • Antineoplastic Agents
  • Colloids
  • Drug Carriers
  • Enzyme Inhibitors
  • Micelles
  • Naphthoquinones
  • monomethoxypolyethyleneglycol-polylactide block copolymer
  • tanshinone
  • Polyethylene Glycols
  • beta-lapachone
  • NAD(P)H Dehydrogenase (Quinone)
  • NQO1 protein, human
  • Paclitaxel