Extracellular K(+) and opening of voltage-gated potassium channels activate T cell integrin function: physical and functional association between Kv1.3 channels and beta1 integrins

J Exp Med. 2000 Apr 3;191(7):1167-76. doi: 10.1084/jem.191.7.1167.

Abstract

Elevated extracellular K(+) ([K(+)](o)), in the absence of "classical" immunological stimulatory signals, was found to itself be a sufficient stimulus to activate T cell beta1 integrin moieties, and to induce integrin-mediated adhesion and migration. Gating of T cell voltage-gated K(+) channels (Kv1.3) appears to be the crucial "decision-making" step, through which various physiological factors, including elevated [K(+)](o) levels, affect the T cell beta1 integrin function: opening of the channel leads to function, whereas its blockage prevents it. In support of this notion, we found that the proadhesive effects of the chemokine macrophage-inflammatory protein 1beta, the neuropeptide calcitonin gene-related peptide (CGRP), as well as elevated [K(+)](o) levels, are blocked by specific Kv1.3 channel blockers, and that the unique physiological ability of substance P to inhibit T cell adhesion correlates with Kv1.3 inhibition. Interestingly, the Kv1.3 channels and the beta1 integrins coimmunoprecipitate, suggesting that their physical association underlies their functional cooperation on the T cell surface. This study shows that T cells can be activated and driven to integrin function by a pathway that does not involve any of its specific receptors (i.e., by elevated [K(+)](o)). In addition, our results suggest that undesired T cell integrin function in a series of pathological conditions can be arrested by molecules that block the Kv1.3 channels.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Adhesion / physiology
  • Cell Movement / physiology
  • Cell Polarity
  • Chemokine CCL4
  • Electric Conductivity
  • Humans
  • Integrin beta1 / immunology*
  • Ion Channel Gating / physiology*
  • Kv1.3 Potassium Channel
  • Lymphocyte Activation / immunology*
  • Macrophage Inflammatory Proteins / immunology
  • Potassium / immunology*
  • Potassium Channel Blockers
  • Potassium Channels / immunology*
  • Potassium Channels, Voltage-Gated*
  • Substance P / immunology
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / physiology

Substances

  • Chemokine CCL4
  • Integrin beta1
  • KCNA3 protein, human
  • Kv1.3 Potassium Channel
  • Macrophage Inflammatory Proteins
  • Potassium Channel Blockers
  • Potassium Channels
  • Potassium Channels, Voltage-Gated
  • Substance P
  • Potassium