Genetic, electrophysiological, and pathological studies on patients with SCN9A-related pain disorders

J Peripher Nerv Syst. 2023 Dec;28(4):597-607. doi: 10.1111/jns.12590. Epub 2023 Aug 18.

Abstract

Background and aims: Voltage-gated sodium channel Nav1.7, encoded by the SCN9A gene, has been linked to diverse painful peripheral neuropathies, represented by the inherited erythromelalgia (EM) and paroxysmal extreme pain disorder (PEPD). The aim of this study was to determine the genetic etiology of patients experiencing neuropathic pain, and shed light on the underlying pathogenesis.

Methods: We enrolled eight patients presenting with early-onset painful peripheral neuropathies, consisting of six cases exhibiting EM/EM-like disorders and two cases clinically diagnosed with PEPD. We conducted a gene-panel sequencing targeting 18 genes associated with hereditary sensory and/or autonomic neuropathy. We introduced novel SCN9A mutation (F1624S) into a GFP-2A-Nav1.7rNS plasmid, and the constructs were then transiently transfected into HEK293 cells. We characterized both wild-type and F1624S Nav1.7 channels using an automated high-throughput patch-clamp system.

Results: From two patients displaying EM-like/EM phenotypes, we identified two SCN9A mutations, I136V and P1308L. Among two patients diagnosed with PEPD, we found two additional mutations in SCN9A, F1624S (novel) and A1632E. Patch-clamp analysis of Nav1.7-F1624S revealed depolarizing shifts in both steady-state fast inactivation (17.4 mV, p < .001) and slow inactivation (5.5 mV, p < .001), but no effect on channel activation was observed.

Interpretation: Clinical features observed in our patients broaden the phenotypic spectrum of SCN9A-related pain disorders, and the electrophysiological analysis enriches the understanding of genotype-phenotype association caused by Nav1.7 gain-of-function mutations.

Keywords: Nav1.7; SCN9A; erythromelalgia; paroxysmal extreme pain disorder; patch-clamp analysis.

Publication types

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

MeSH terms

  • Erythromelalgia* / genetics
  • Erythromelalgia* / pathology
  • HEK293 Cells
  • Humans
  • Mutation / genetics
  • NAV1.7 Voltage-Gated Sodium Channel / genetics
  • Pain
  • Peripheral Nervous System Diseases*

Substances

  • NAV1.7 Voltage-Gated Sodium Channel
  • SCN9A protein, human

Supplementary concepts

  • Paroxysmal Extreme Pain Disorder