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Chapter 6 : Voltage-Gated K Channels

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Abstract:

This chapter gives an overview on voltage-gated K channels. The introduction of molecular biology into the channel field, coupled with the ability to use patch-clamping techniques to precisely analyze properties of channels from many different types of cells, revitalized ion channel biophysics. The structure of the pore-forming domain formed by segments S5-P-S6 of the crystal structure of the full-length voltage-gated K channel (KvAP) protein was similar to that of the MthK crystal, suggesting that it was in an open conformation. The chapter discusses experiments performed on Shaker that are most informative about the structure and voltage-sensing domain. Three types of crevasse models can be envisioned. The first model implies that the transmembrane movement of S4 is relatively large and that the rest of the protein remains relatively static. The second model depicts the opposite extreme in which there is little transmembrane movement of S4, but the location of the barrier and the structures of the crevasses change. The third model is a hybrid of the other two; S4 charges move outward during activation, but this movement is accompanied by an inward movement of the transition barrier and a change in the structures of the crevasses. The first and largest category of 6-TM KK channel sequences has the same length of S2-S3 linkers as most eukaryotic Kv channels; this category is the most similar to eukaryotic Kv channels. According to the authors, the most closely related sequence to that of KvAP is the KvCA sequence from .

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6

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Figures

Image of Figure 1.
Figure 1.

Side view of ribbon representation of two subunits of crystal structures of the transmembrane regions of KcsA ( ) and MthK ( ). The spheres in the P segment represent backbone oxygen atoms that bind K ions.

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6
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Image of Figure 2.
Figure 2.

Crystal structures of the KvAP channel. (a) One subunit of the full-length structure. (b) Structure of the isolated voltage-sensing domain in orientation relative to the bilayer used in developing models. The lines represent the boundries of a lipid bilayer: S1-S3 in medium gray, S4 in dark gray, S5-P-S6 in light gray.

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6
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Image of Figure 3.
Figure 3.

Schematic representations of three crevasse models. Circles with + inside represent positively charged side chains of S4. (A) Model in which S4 moves outwardly relative to a single transition barrier during activation ( ). (B) Transport model in which S4 does not move much, but the location of the transition barrier changes during activation ( ). (C) Hybrid model in which S4 moves outwardly and the transition barrier moves inwardly during activation.

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6
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Image of Figure 4.
Figure 4.

(A) Model of the KvAP channel developed to fit EM data and be consistent with models of . (B) Model of the open KvAP channel based on the crystal structures of the isolated voltage-sensing domain for S1-S4 and the full-length protein for the pore-forming domain (S5-P-S6). S1, S2, L45, and pore-forming domains are about the same in both models. The voltage-sensing domains are dark and the pore-forming domain is light. The S3-S4 paddles are encircled.

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6
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Image of Figure 5.
Figure 5.

Alignment of transmembrane segments from the Shaker, a category 1 bacterial Kv protein (KvVP) from , and KvAP. The Shaker sequence is shaded according to the mutability of residues calculated from a multisequence alignment of eukaryotic Kv channel sequences; the KvVP sequence is shaded according to the mutability of residues within a prokaryotic family of putative 6-TM channels with sequences intermediate between those of eukaryotic Kv and KvAP, and the KvAP sequence is shaded according to the mutability of residues among numerous distantly related families of 6-TM channels. Color code: black background, highly conserved; gray background, moderately conserved; white background, poorly conserved. Simplified numbers of charge residues in the voltage-sensing domain that interact during the helical screw transitions are indicated in italics below the KvAP sequence. The parentheses indicate insertions of the indicated number of residues in the Shaker S1-S2 and S3-S4 loops.

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6
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Image of Figure 6.
Figure 6.

Models of S4 and S5 segments of adjacent subunits of Shaker channels in resting (A) and open (B) conformations illustrating residue pairs that have been shown to be proximal by formation of Cd-binding sites and/or disulfide bridges when replaced by cysteines. Distances between β-carbons of specific pairs are indicated in each figure. (Reprinted from with permission.)

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6
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Image of Figure 7.
Figure 7.

Models of the extracellular loops of the Shaker channel in the open conformation. Residues where LRET probes have been attached are indicated in the subunit on the right, residues where TEA tethers have been attached are indicated in the subunit on the bottom, and charged residues of the loops are indicated in the subunits on the left and top. (Reprinted from with permission.)

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6
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Image of Figure 8.
Figure 8.

Helical wheel representation of a Kv channel as viewed from outside the cell illustrating residues that are well conserved (black), moderately conserved (gray), or poorly conserved (white) ( ). S1-S4 residues of eukaryotic channels that are classified as tolerant from results of experimental mutagenesis ( ) are indicated by dashed lines around the residues.

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6
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Image of Figure 9.
Figure 9.

Alignments of the voltage-sensing domain of category 3 prokaryotic Kv channels with varying lengths of S3-S4 and S4-S5 linkers. Most charged residues are highlighted in black.

Citation: Guy H, Shrivastava I. 2005. Voltage-Gated K Channels, p 97-121. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch6
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