The isolated voltage sensing domain of the Shaker potassium channel forms a voltage-gated cation channel

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Abstract

Domains in macromolecular complexes are often considered structurally and functionally conserved while energetically coupled to each other. In the modular voltage-gated ion channels the central ion-conducting pore is surrounded by four voltage sensing domains (VSDs). Here, the energetic coupling is mediated by interactions between the S4-S5 linker, covalently linking the domains, and the proximal C-terminus. In order to characterize the intrinsic gating of the voltage sensing domain in the absence of the pore domain, the Shaker Kv channel was truncated after the 4^th transmembrane helix S4 (Shaker-iVSD). Shaker-iVSD showed significantly altered gating kinetics and formed a cation-selective ion channel with a strong preference for protons. Ion conduction in Shaker-iVSD developed despite identical primary sequence, indicating an allosteric influence of the pore domain. Shaker-iVSD also displays pronounced 'relaxation'. Closing of the pore correlates with entry into relaxation suggesting that the two processes are energetically related.

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Juan Zhao

Departments of Physics and of Physiology, Université de Montréal, Montréal, Canada

Competing interests
The authors declare that no competing interests exist.
Rikard Blunck

Departments of Physics and of Physiology, Université de Montréal, Montréal, Canada

For correspondence
rikard.blunck@umontreal.ca

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0003-4484-2907

Funding

Canadian Institutes of Health Research (MOP-136894)

Rikard Blunck

Natural Sciences and Engineering Research Council of Canada (DG- 327201-2012)

Rikard Blunck

Canadian Institutes of Health Research (MOP-102689)

Rikard Blunck

Natural Sciences and Engineering Research Council of Canada (CDMC-CREATE postdoctoral fellowship)

Juan Zhao

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the guidelines of the CDEA of Université de Montréal (licence No. 16-033).

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.