Potent cytotoxicity of the phosphatase inhibitor microcystin LR and microcystin analogues in OATP1B1- and OATP1B3-expressing HeLa cells

Mol Cancer Ther. 2007 Feb;6(2):587-98. doi: 10.1158/1535-7163.MCT-06-0500.

Abstract

Microcystins are a family of cyclic peptides that are potent inhibitors of the protein phosphatase families PP1 and PP2A. Only three human proteins are thought to be able to mediate the hepatic uptake of microcystins (the organic anion-transporting polypeptides OATP1B1, OATP1B3, and OATP1A2), and the predominant hepatic expression of these transporters accounts for the liver-specific toxicity of microcystins. A significant obstacle in the study of microcystins as anticancer drugs is the requirement of specific transport proteins for cellular uptake. We report that OATP1B3 mRNA is up-regulated in non-small cell lung cancer tumors in comparison with normal control tissues. This finding led to the exploration of microcystins as potential anticancer agents. We have developed a HeLa cell model with functional OATP1B1 and OATP1B3 activity. Transiently transfected HeLa cells are over 1,000-fold more sensitive to microcystin LR than the vector-transfected control cells, showing that transporter expression imparts marked selectivity for microcystin cytotoxicity. In addition, microcystin analogues showed variable cytotoxicities in the OATP1B1- and OATP1B3-transfected cells, including two analogues with IC(50) values <1 nmol/L. Cytotoxicity of microcystin analogues seems to correlate to the inhibition of PP2A in these cells and induces rapid cell death as seen by chromatin condensation and cell fragmentation. These studies show that microcystin-induced phosphatase inhibition results in potent cytotoxicity when microcystin compounds can gain intracellular access and are a potent novel class of therapeutic agents for tumors expressing these uptake proteins.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Proliferation / drug effects*
  • Enzyme Inhibitors / pharmacology*
  • Growth Inhibitors
  • HeLa Cells
  • Humans
  • Liver / metabolism
  • Liver-Specific Organic Anion Transporter 1
  • Lung / metabolism
  • Lung Neoplasms / metabolism*
  • Lung Neoplasms / pathology
  • Marine Toxins
  • Microcystins / chemistry
  • Microcystins / pharmacology*
  • Organic Anion Transporters / genetics
  • Organic Anion Transporters / metabolism*
  • Organic Anion Transporters, Sodium-Independent / genetics
  • Organic Anion Transporters, Sodium-Independent / metabolism*
  • Peptides, Cyclic / pharmacology
  • Phosphoprotein Phosphatases / antagonists & inhibitors
  • Solute Carrier Organic Anion Transporter Family Member 1B3
  • Tumor Stem Cell Assay

Substances

  • Enzyme Inhibitors
  • Growth Inhibitors
  • Liver-Specific Organic Anion Transporter 1
  • Marine Toxins
  • Microcystins
  • Organic Anion Transporters
  • Organic Anion Transporters, Sodium-Independent
  • Peptides, Cyclic
  • SLCO1B1 protein, human
  • SLCO1B3 protein, human
  • Solute Carrier Organic Anion Transporter Family Member 1B3
  • Phosphoprotein Phosphatases
  • cyanoginosin LR