Pharmacological fractionation of tetrodotoxin-sensitive sodium currents in rat dorsal root ganglion neurons by μ-conotoxins

Br J Pharmacol. 2013 May;169(1):102-14. doi: 10.1111/bph.12119.

Abstract

Background and purpose: Adult rat dorsal root ganglion (DRG) neurons normally express transcripts for five isoforms of the α-subunit of voltage-gated sodium channels: NaV 1.1, 1.6, 1.7, 1.8 and 1.9. Tetrodotoxin (TTX) readily blocks all but NaV 1.8 and 1.9, and pharmacological agents that discriminate among the TTX-sensitive NaV 1-isoforms are scarce. Recently, we used the activity profile of a panel of μ-conotoxins in blocking cloned rodent NaV 1-isoforms expressed in Xenopus laevis oocytes to conclude that action potentials of A- and C-fibres in rat sciatic nerve were, respectively, mediated primarily by NaV 1.6 and NaV 1.7.

Experimental approach: We used three μ-conotoxins, μ-TIIIA, μ-PIIIA and μ-SmIIIA, applied individually and in combinations, to pharmacologically differentiate the TTX-sensitive INa of voltage-clamped neurons acutely dissociated from adult rat DRG. We examined only small and large neurons whose respective INa were >50% and >80% TTX-sensitive.

Key results: In both small and large neurons, the ability of the toxins to block TTX-sensitive INa was μ-TIIIA < μ-PIIIA < μ-SmIIIA, with the latter blocking ≳90%. Comparison of the toxin-susceptibility profiles of the neuronal INa with recently acquired profiles of rat NaV 1-isoforms, co-expressed with various NaV β-subunits in X. laevis oocytes, were consistent: NaV 1.1, 1.6 and 1.7 could account for all of the TTX-sensitive INa , with NaV 1.1 < NaV 1.6 < NaV 1.7 for small neurons and NaV 1.7 < NaV 1.1 < NaV 1.6 for large neurons.

Conclusions and implications: Combinations of μ-conotoxins can be used to determine the probable NaV 1-isoforms underlying the INa in DRG neurons. Preliminary experiments with sympathetic neurons suggest that this approach is extendable to other neurons.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Conotoxins / administration & dosage
  • Conotoxins / pharmacology*
  • Female
  • Ganglia, Spinal / drug effects*
  • Ganglia, Spinal / metabolism
  • Male
  • NAV1.1 Voltage-Gated Sodium Channel / metabolism
  • NAV1.6 Voltage-Gated Sodium Channel / metabolism
  • NAV1.7 Voltage-Gated Sodium Channel / metabolism
  • Neurons / drug effects*
  • Neurons / metabolism
  • Oocytes / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Tetrodotoxin / pharmacology*
  • Xenopus laevis

Substances

  • Conotoxins
  • NAV1.1 Voltage-Gated Sodium Channel
  • NAV1.6 Voltage-Gated Sodium Channel
  • NAV1.7 Voltage-Gated Sodium Channel
  • Tetrodotoxin