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Area of Science:

  • Molecular Biology
  • Biophysics
  • Structural Biology

Background:

  • Archetypal voltage-gated ion channels (VGICs) open upon depolarization.
  • Hyperpolarization- and cAMP-activated ion (HCN) channels exhibit unique hyperpolarization-dependent opening.
  • The conserved architecture suggests inverse coupling between voltage sensor and pore gates in HCN channels.

Purpose of the Study:

  • To investigate the structural determinants of hyperpolarization activation in HCN channels.
  • To understand the inverse coupling between voltage sensor and pore gates.
  • To elucidate the common principles of voltage gating across the VGIC superfamily.

Main Methods:

  • Structure-guided protein engineering of mosaic channels.
  • Systematic assembly of channels with varying gating phenotypes.
  • Analysis of voltage-activation properties.

Main Results:

  • HCN channel voltage sensor intrinsically drives pore opening in both directions.
  • The S4 segment length is not the primary determinant for hyperpolarization activation.
  • Tight voltage sensor-pore interface interactions promote an hERG-like inactivated state, preventing depolarization-induced opening.
  • Synergy between the cyclic nucleotide-binding domain and pore gate interactions dictates hyperpolarization-dependent gating.

Conclusions:

  • Identified essential structural elements determining HCN channel gating polarity.
  • Revealed an unexpected common principle underlying voltage gating in VGICs.
  • Demonstrated that specific interactions, not just S4 length, dictate gating direction.