Unraveling the Cellular Mechanism of Assembling Cholesterols for Selective Cancer Cell Death

Mol Cancer Res. 2019 Apr;17(4):907-917. doi: 10.1158/1541-7786.MCR-18-0931. Epub 2018 Dec 14.

Abstract

Acquired drug resistance remains a challenge in chemotherapy. Here we show enzymatic, in situ assembling of cholesterol derivatives to act as polypharmaceuticals for selectively inducing death of cancer cells via multiple pathways and without inducing acquired drug resistance. A conjugate of tyrosine and cholesterol (TC), formed by enzyme-catalyzed dephosphorylation of phosphorylate TC, self-assembles selectively on or in cancer cells. Acting as polypharmaceuticals, the assemblies of TC augment lipid rafts, aggregate extrinsic cell death receptors (e.g., DR5, CD95, or TRAILR), modulate the expression of oncoproteins (e.g., Src and Akt), disrupt the dynamics of cytoskeletons (e.g., actin filaments or microtubules), induce endoplasmic reticulum stress, and increase the production of reactive oxygen species, thus resulting in cell death and preventing acquired drug resistance. Moreover, the assemblies inhibit the growth of platinum-resistant ovarian cancer tumor in a murine model. This work illustrates the use of instructed assembly (iA) in cellular environment to form polypharmaceuticals in situ that not only interact with multiple proteins, but also modulate membrane dynamics for developing novel anticancer therapeutics. IMPLICATIONS: As a multifaceted strategy for controlling cancer cell death, iA minimized acquired resistance of cancer cells, which is a new strategy to amplify the genetic difference between cancer and normal cells and provides a promise for overcoming drug resistance in cancer therapy.Visual Overview: http://mcr.aacrjournals.org/content/molcanres/17/4/907/F1.large.jpg.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Animals
  • Antineoplastic Agents / pharmacology
  • Cell Death / physiology
  • Cell Line, Tumor
  • Cholesterol / analogs & derivatives*
  • Cholesterol / pharmacology*
  • Cisplatin / pharmacology
  • Doxorubicin / pharmacology
  • Drug Resistance, Neoplasm
  • Endoplasmic Reticulum Stress
  • HeLa Cells
  • Hep G2 Cells
  • Humans
  • Mice
  • Mice, Inbred BALB C
  • Mitochondrial Dynamics / drug effects
  • Neoplasms / drug therapy*
  • Neoplasms / metabolism
  • Neoplasms / pathology*
  • Proto-Oncogene Proteins c-akt / metabolism
  • Signal Transduction / drug effects
  • src-Family Kinases / metabolism

Substances

  • Actins
  • Antineoplastic Agents
  • Doxorubicin
  • Cholesterol
  • src-Family Kinases
  • Proto-Oncogene Proteins c-akt
  • Cisplatin