Selective blockade of voltage-gated potassium channels reduces inflammatory bone resorption in experimental periodontal disease

J Bone Miner Res. 2004 Jan;19(1):155-64. doi: 10.1359/JBMR.0301213.

Abstract

The effects of the potassium channel (Kv1.3) blocker kaliotoxin on T-cell-mediated periodontal bone resorption were examined in rats. Systemic administration of kaliotoxin abrogated the bone resorption in conjunction with decreased RANKL mRNA expression by T-cells in gingival tissue. This study suggests a plausible therapeutic approach for inflammatory bone resorption by targeting Kv1.3.

Introduction: Kv1.3 is a critical potassium channel to counterbalance calcium influx at T-cell receptor activation. It is not known if Kv1.3 also regulates RANKL expression by antigen-activated T-cells, and consequently affects in vivo bone resorption mediated by activated T-cells.

Materials and methods: Actinobacillus actinomycetemcomitans 29-kDa outer membrane protein-specific Th1-clone cells were used to evaluate the expression of Kv1.3 (using reverse transcriptase-polymerase chain reaction [RT-PCR] and Western blot analyses) and the effects of the potassium channel blocker kaliotoxin (0-100 nM) on T-cell activation parameters ([3H]thymidine incorporation assays and ELISA) and expression of RANKL and osteoprotegerin (OPG; flow cytometry, Western blot, and RT-PCR analyses). A rat periodontal disease model based on the adoptive transfer of activated 29-kDa outer membrane protein-specific Th1 clone cells was used to analyze the effects of kaliotoxin in T-cell-mediated alveolar bone resorption and RANKL and OPG mRNA expression by gingival T-cells. Stimulated 29-kDa outer membrane protein-specific Th1 clone cells were transferred intravenously on day 0 to all animals used in the study (n = 7 animals per group). Ten micrograms of kaliotoxin were injected subcutaneously twice per day on days 0, 1, 2, and 3, after adoptive transfer of the T-cells. The control group of rats was injected with saline as placebo on the same days as injections for the kaliotoxin-treated group. The MOCP-5 osteoclast precursor cell line was used in co-culture studies with fixed 29-kDa outer membrane protein-specific Th1-clone cells to measure T-cell-derived RANKL-mediated effects on osteoclastogenesis and resorption pit formation assays in vitro. Statistical significance was evaluated by Student's t-test.

Results: Kaliotoxin decreased T-cell activation parameters of 29-kDa outer membrane protein-specific Th1 clone cells in vitro and in vivo. Most importantly, kaliotoxin administration resulted in an 84% decrease of the bone resorption induced in the saline-treated control group. T-cells recovered from the gingival tissue of kaliotoxin-treated rats displayed lower ratios of RANKL and OPG mRNA expression than those recovered from the control group. The ratio of RANKL and osteoprotegerin protein expression and induction of RANKL-dependent osteoclastogenesis by the activated T-cells were also markedly decreased after kaliotoxin treatments in vitro.

Conclusion: The use of kaliotoxin or other means to block Kv1.3 may constitute a potential intervention therapy to prevent alveolar bone loss in periodontal disease.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Acid Phosphatase / analysis
  • Adoptive Transfer
  • Aggregatibacter actinomycetemcomitans / chemistry
  • Alveolar Bone Loss / drug therapy*
  • Alveolar Bone Loss / immunology
  • Alveolar Bone Loss / physiopathology
  • Animals
  • Antigen Presentation / drug effects
  • Antigen Presentation / immunology
  • Bacterial Outer Membrane Proteins / immunology
  • Bacterial Outer Membrane Proteins / pharmacology
  • Blotting, Western
  • CD3 Complex / immunology
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Differentiation / drug effects
  • Cell Differentiation / immunology
  • Coculture Techniques
  • Down-Regulation / immunology
  • Down-Regulation / physiology
  • Female
  • Gene Expression
  • Glycoproteins / genetics
  • Glycoproteins / metabolism
  • Immunoglobulin G / blood
  • Interferon-gamma / metabolism
  • Isoenzymes / analysis
  • Kv1.3 Potassium Channel
  • Lipopolysaccharides / pharmacology
  • Lymphocyte Activation / drug effects
  • Maxilla / pathology
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Osteoclasts / immunology
  • Osteoclasts / physiology
  • Osteoprotegerin
  • Periodontitis / drug therapy*
  • Periodontitis / immunology
  • Periodontitis / physiopathology
  • Potassium Channels / drug effects
  • Potassium Channels / genetics
  • Potassium Channels / physiology*
  • Potassium Channels, Voltage-Gated / antagonists & inhibitors
  • RANK Ligand
  • Rats
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Receptors, Tumor Necrosis Factor
  • Scorpion Venoms / pharmacology*
  • Spleen / cytology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / transplantation
  • Tartrate-Resistant Acid Phosphatase

Substances

  • Bacterial Outer Membrane Proteins
  • CD3 Complex
  • Carrier Proteins
  • Glycoproteins
  • Immunoglobulin G
  • Isoenzymes
  • Kcna3 protein, rat
  • Kv1.3 Potassium Channel
  • Lipopolysaccharides
  • Membrane Glycoproteins
  • Omp29 protein, Actinobacillus actinomycetemcomitans
  • Osteoprotegerin
  • Potassium Channels
  • Potassium Channels, Voltage-Gated
  • RANK Ligand
  • Receptors, Cytoplasmic and Nuclear
  • Receptors, Tumor Necrosis Factor
  • Scorpion Venoms
  • Tnfrsf11b protein, rat
  • kaliotoxin
  • Interferon-gamma
  • Acid Phosphatase
  • Tartrate-Resistant Acid Phosphatase