Alkylphenol inverse agonists of HCN1 gating: H-bond propensity, ring saturation and adduct geometry differentially determine efficacy and potency

Biochem Pharmacol. 2019 May:163:493-508. doi: 10.1016/j.bcp.2019.02.013. Epub 2019 Feb 13.

Abstract

Background and purpose: In models of neuropathic pain, inhibition of HCN1 is anti-hyperalgesic. 2,6-di-iso-propyl phenol (propofol) and its non-anesthetic congener, 2,6-di-tert-butyl phenol, inhibit HCN1 channels by stabilizing closed state(s).

Experimental approach: Using in vitro electrophysiology and kinetic modeling, we systematically explore the contribution of ligand architecture to alkylphenol-channel coupling.

Key results: When corrected for changes in hydrophobicity (and propensity for intra-membrane partitioning), the decrease in potency upon 1-position substitution (NCO∼OH >> SH >>> F) mirrors the ligands' H-bond acceptor (NCO > OH > SH >>> F) but not donor profile (OH > SH >>> NCO∼F). H-bond elimination (OH to F) corresponds to a ΔΔG of ∼4.5 kCal mol-1 loss of potency with little or no disruption of efficacy. Substitution of compact alkyl groups (iso-propyl, tert-butyl) with shorter (ethyl, methyl) or more extended (sec-butyl) adducts disrupts both potency and efficacy. Ring saturation (with the obligate loss of both planarity and π electrons) primarily disrupts efficacy.

Conclusions and implications: A hydrophobicity-independent decrement in potency at higher volumes suggests the alkylbenzene site has a volume of ≥800 Å3. Within this, a relatively static (with respect to ligand) H-bond donor contributes to initial binding with little involvement in generation of coupling energy. The influence of π electrons/ring planarity and alkyl adducts on efficacy reveals these aspects of the ligand present towards a face of the channel that undergoes structural changes during opening. The site's characteristics suggest it is "druggable"; introduction of other adducts on the ring may generate higher potency inverse agonists.

Keywords: 2-Fluoro-13-di-iso-propylbenzene; Alkylphenol; Anti-hyperalgesia; Cyclohexanol; HCN channels; Inverse agonists; Kinetic modeling; Neuropathic pain; Phenyl-fluorine; Phenyl-isocyanate; Phenyl-thiol; Propofol.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Cryoelectron Microscopy
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / chemistry
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / genetics
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels / metabolism*
  • Ion Channel Gating / drug effects*
  • Mice
  • Models, Molecular
  • Oocytes / drug effects
  • Oocytes / metabolism*
  • Phenols / chemistry
  • Phenols / pharmacology*
  • Potassium Channels / chemistry
  • Potassium Channels / genetics
  • Potassium Channels / metabolism*
  • Protein Conformation
  • Protein Isoforms
  • Structure-Activity Relationship
  • Xenopus laevis

Substances

  • Hcn1 protein, mouse
  • Hyperpolarization-Activated Cyclic Nucleotide-Gated Channels
  • Phenols
  • Potassium Channels
  • Protein Isoforms