Inhibition of tumor cell proliferation by sigma ligands is associated with K+ Channel inhibition and p27kip1 accumulation

J Pharmacol Exp Ther. 2004 Dec;311(3):1105-14. doi: 10.1124/jpet.104.072413. Epub 2004 Jul 26.

Abstract

Previous studies have shown that sigma receptors are overexpressed in tumor cells. However, the role of sigma receptors remains enigmatic. Recently, we and others have demonstrated that sigma-1 receptor modulates K+ channels in pituitary. In the present report, patch-clamp and Western blot assays were used in small cell lung cancer (SCLC, NCI-H209, and NCI-H146) and leukemic (Jurkat) cell lines to investigate the effects of sigma ligands on voltage-gated K+ channels and cell proliferation. The sigma ligands (+)-pentazocine, igmesine, and 1,3-di(2-tolyl)guanidine (DTG) all reversibly inhibited voltage-activated K+ currents in both cell lines. The potency of sigma ligand-induced inhibition (10 microM) was igmesine = (+)-pentazocine > DTG, pointing to the involvement of sigma-1 receptors. Addition of the K+ channel blockers tetraethylammonium (TEA) and 4-aminopyridin or one of cited sigma ligands in the culture media reversibly inhibited Jurkat cell growth. Interestingly, K+ channel blockers and sigma ligands caused an accumulation of the cyclin-dependent kinase inhibitor p27kip1 and a decrease in cyclin A expression in Jurkat and SCLC cells, whereas no effect could be detected on p21cip1. Moreover, sigma ligands and TEA had no effect on caspase 3 activity. Accordingly, incubation of cells with sigma ligands did not provoke DNA laddering. These data demonstrate that sigma ligands and voltage-dependent channel blockers inhibit cell growth through a cell cycle arrest in the G1 phase but not via an apoptotic mechanism. Altogether, these results indicate that the sigma-1 receptor-induced inhibition of the cell cycle is, at least in part, the consequence of the inhibition of K+ channels.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anilides / pharmacology
  • Apoptosis / physiology
  • Blotting, Western
  • Caspases / metabolism
  • Cell Cycle Proteins / biosynthesis
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects*
  • Cyclin A / biosynthesis
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclin-Dependent Kinase Inhibitor p27
  • DNA Fragmentation / drug effects
  • Down-Regulation / drug effects
  • Electrophysiology
  • G1 Phase / physiology
  • Humans
  • Jurkat Cells
  • Kinetics
  • Membrane Potentials / physiology
  • Oligopeptides / pharmacology
  • Patch-Clamp Techniques
  • Potassium Channel Blockers / pharmacology*
  • Receptors, sigma / drug effects*
  • Tumor Suppressor Proteins / metabolism*

Substances

  • Anilides
  • CDKN1A protein, human
  • Cell Cycle Proteins
  • Cyclin A
  • Cyclin-Dependent Kinase Inhibitor p21
  • Oligopeptides
  • Potassium Channel Blockers
  • Receptors, sigma
  • Tumor Suppressor Proteins
  • aspartyl-glutamyl-valyl-aspartyl-p-nitroanilide
  • Cyclin-Dependent Kinase Inhibitor p27
  • Caspases