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Non-Native R1 Substitution in the S4 Domain Uniquely Alters Kv4.3 Channel Gating

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  • Matthew R Skerritt
  • Donald L Campbell

Abstract

The S4 transmembrane domain in Shaker (Kv1) voltage-sensitive potassium channels has four basic residues (R1–R4) that are responsible for carrying the majority of gating charge. In Kv4 channels, however, R1 is replaced by a neutral valine at position 287. Among other differences, Kv4 channels display prominent closed state inactivation, a mechanism which is minimal in Shaker. To determine if the absence of R1 is responsible for important variation in gating characteristics between the two channel types, we introduced the V287R mutant into Kv4.3 and analyzed its effects on several voltage sensitive gating transitions. We found that the mutant increased the voltage sensitivity of steady-state activation and altered the kinetics of activation and deactivation processes. Although the kinetics of macroscopic inactivation were minimally affected, the characteristics of closed-state inactivation and recovery from open and closed inactivated states were significantly altered. The absence of R1 can only partially account for differences in the effective voltage sensitivity of gating between Shaker and Kv4.3. These results suggest that the S4 domain serves an important functional role in Kv4 channel activation and deactivation processes, and also those of closed-state inactivation and recovery.

Suggested Citation

  • Matthew R Skerritt & Donald L Campbell, 2008. "Non-Native R1 Substitution in the S4 Domain Uniquely Alters Kv4.3 Channel Gating," PLOS ONE, Public Library of Science, vol. 3(11), pages 1-7, November.
  • Handle: RePEc:plo:pone00:0003773
    DOI: 10.1371/journal.pone.0003773
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    References listed on IDEAS

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    1. Stephen B. Long & Xiao Tao & Ernest B. Campbell & Roderick MacKinnon, 2007. "Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment," Nature, Nature, vol. 450(7168), pages 376-382, November.
    2. Ming Zhou & João H. Morais-Cabral & Sabine Mann & Roderick MacKinnon, 2001. "Potassium channel receptor site for the inactivation gate and quaternary amine inhibitors," Nature, Nature, vol. 411(6838), pages 657-661, June.
    3. Richard W. Aldrich, 2001. "Fifty years of inactivation," Nature, Nature, vol. 411(6838), pages 643-644, June.
    4. Dorine M. Starace & Francisco Bezanilla, 2004. "A proton pore in a potassium channel voltage sensor reveals a focused electric field," Nature, Nature, vol. 427(6974), pages 548-553, February.
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