Pivotal role of the lipid Raft SK3-Orai1 complex in human cancer cell migration and bone metastases

Cancer Res. 2013 Aug 1;73(15):4852-61. doi: 10.1158/0008-5472.CAN-12-4572. Epub 2013 Jun 17.

Abstract

The SK3 channel, a potassium channel, was recently shown to control cancer cell migration, a critical step in metastasis outgrowth. Here, we report that expression of the SK3 channel was markedly associated with bone metastasis. The SK3 channel was shown to control constitutive Ca(2+) entry and cancer cell migration through an interaction with the Ca(2+) channel Orai1. We found that the SK3 channel triggers an association with the Orai1 channel within lipid rafts. This localization of an SK3-Orai1 complex seemed essential to control cancer cell migration. This suggests that the formation of this complex in lipid rafts is a gain-of-function, because we showed that none of the individual proteins were able to promote the complete phenotype. We identified the alkyl-lipid Ohmline as a disrupting agent for SK3-Orai1 lipid raft localization. Upon Ohmline treatment, the SK3-Orai1 complex moved away from lipid rafts, and SK3-dependent Ca(2+) entry, migration, and bone metastases were subsequently impaired. The colocalization of SK3 and Orai1 in primary human tumors and bone metastases further emphasized the clinical relevance of our observations. Targeting SK3-Orai1 in lipid rafts may inaugurate innovative approaches to inhibit bone metastases.

MeSH terms

  • Animals
  • Blotting, Western
  • Bone Neoplasms / metabolism*
  • Bone Neoplasms / secondary
  • Calcium Channels / metabolism*
  • Cell Line, Tumor
  • Cell Movement
  • Disease Models, Animal
  • Female
  • Humans
  • Immunohistochemistry
  • Membrane Microdomains / metabolism*
  • Mice
  • Mice, Nude
  • Neoplasm Invasiveness / pathology
  • Neoplasms, Experimental / metabolism*
  • Neoplasms, Experimental / secondary*
  • ORAI1 Protein
  • Patch-Clamp Techniques
  • Small-Conductance Calcium-Activated Potassium Channels / metabolism*

Substances

  • Calcium Channels
  • KCNN3 protein, human
  • ORAI1 Protein
  • ORAI1 protein, human
  • Small-Conductance Calcium-Activated Potassium Channels