State-dependent block of voltage-gated Na+ channels by amitriptyline via the local anesthetic receptor and its implication for neuropathic pain

Pain. 2004 Jul;110(1-2):166-74. doi: 10.1016/j.pain.2004.03.018.

Abstract

Amitriptyline is a tricyclic antidepressant, which also alleviates various pain syndromes at its therapeutic plasma concentration (0.36-0.90 microM). Accumulated evidence suggests that such efficacy may be due to block of voltage-gated Na(+) channels. The Na(+) channel alpha-subunit protein consists of four homologous domains (D1-D4), each with six transmembrane segments (S1-S6). The aims of this study were to locate the amitriptyline receptor in the Na(+) channel alpha-subunit and to compare the amitriptyline affinity in open, inactivated, and resting states of the Na(+) channel. Wild-type and mutant rat skeletal muscle alpha-subunit Na(+) channels were expressed in human embryonic kidney cells and assayed under whole-cell voltage clamp conditions. Our results indicate that the amitriptyline receptor overlaps with the local anesthetic receptor to a great extent in Na(+) channels. Residues N434 (at D1-S6), L1280 (D3-S6), and F1579 (D4-S6) may jointly form parts of the amitriptyline/local anesthetic receptor, with residue L1280 being most critical for amitriptyline binding. Open-channel block by amitriptyline was assessed in inactivation-deficient Na(+) channels and compared with the resting- and inactivated-channel block in wild-type channels. The open-channel block by amitriptyline has the highest affinity, with a 50% inhibitory concentration (IC(50)) of 0.26 microM. The inactivated-channel block by amitriptyline had a weaker affinity (0.51 microM), whereas the resting-channel displayed the weakest affinity (33 microM). We hypothesize that selective block of both persistent late openings and the inactivated state of neuronal Na(+) channel isoforms by amitriptyline also occurs at its therapeutic concentration and likely contributes to its efficacy in pain syndromes.

Publication types

  • Comparative Study

MeSH terms

  • Amitriptyline / pharmacology*
  • Analgesics, Non-Narcotic / pharmacology*
  • Anesthesia, Local*
  • Cell Line
  • Dose-Response Relationship, Drug
  • Electric Stimulation / methods
  • Embryo, Mammalian
  • Humans
  • Ion Channel Gating / drug effects
  • Ion Channel Gating / physiology
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Muscle Proteins / antagonists & inhibitors*
  • Muscle Proteins / chemistry
  • Muscle Proteins / genetics
  • Muscle Proteins / physiology
  • Mutagenesis, Site-Directed
  • NAV1.4 Voltage-Gated Sodium Channel
  • Pain / physiopathology
  • Patch-Clamp Techniques
  • Sodium Channels / chemistry
  • Sodium Channels / genetics
  • Sodium Channels / physiology
  • Time Factors
  • Transfection / methods

Substances

  • Analgesics, Non-Narcotic
  • Muscle Proteins
  • NAV1.4 Voltage-Gated Sodium Channel
  • SCN4A protein, human
  • Sodium Channels
  • Amitriptyline