Background:
Pain is the leading cause of disability in the developed world but remains a poorly treated condition. Existing analgesics suffer from poor tolerability and a lack of broad efficacy[1]. One promising target for pain treatment is NaV1.7, a voltage-gated sodium channel (NaV) subtype. Genetic studies support a key role of NaV1.7 in pain since gain-of-function and loss-of-function mutations lead to pain syndromes and insensitivity to pain, respectively[2,3]. We recently identified the tarantula venom peptide μ-theraphotoxin-Pn3a (Pn3a) as potent and selective NaV1.7 blocker with effective analgesic properties[4,5]. The aim of this project was to identify the pharmacophore of Pn3a and to develop a more efficacious and safe Pn3a-analogue as lead analgesic compound.
Methods:
We used solid-phase peptide synthesis to produce Pn3a-analogues and confirmed folding via NMR. Fluorescence imaging assays and patch-clamp experiments were performed to pharmacologically characterize potencies at hNaV1.1-hNaV1.8. Surface plasmon resonance was used to examine peptide-lipid bilayer interactions. Improved analogues were tested in mouse models of OD1-induced NaV1.7-mediated pain and in a post-surgical pain model.
Results:
Mutations of R23, K24 and several hydrophobic residues in Pn3a decreased inhibition of NaV1.7. Mutations at four acidic residues decreased IC50 values with two mutants showing improved selectivity and membrane binding. Especially Pn3a[D8N] was more potently analgesic and efficacious than Pn3a in the OD1 and the post-surgical pain models without causing side effects after systemic administration.
Conclusions:
Pn3a is a unique pharmacological tool to define the role of NaV1.7 in pain pathways and has great potential to become a lead substance toward novel treatment approaches for pain. We identified several residues of the pharmacophore of Pn3a as well as promising analogues with improved potency, selectivity and membrane binding properties. We demonstrate that one of these analogues shows improved analgesic efficacy in vivo and is therefore a promising lead molecule for the development of improved safe and effective painkillers.