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Chapter 10 : Bacterial Na Channels: Progenitors, Progeny, or Parallel Evolution?

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Bacterial Na Channels: Progenitors, Progeny, or Parallel Evolution?, Page 1 of 2

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Abstract:

Eukaryotic voltage-sensitive sodium and calcium channels have a major structural subunit that consists of four linked, homologous domains, which contain six putative transmembrane (TM) segments for an overall total of 24. In the putative pore-lining S5-S6 linker, a glutamate residue appears in the position homologous to that acknowledged as the selectivity filter in eukaryotic sodium and calcium channels. Members of the sodium channel family typically have a selectivity ring consisting of the aspartate, glutamate, lysine, and alanine residues contributed from domains I through IV, respectively. The possibility of bacterial sodium channels being involved in rapid flagellar movement has been raised by Clapham and collaborators. Voltage-gated ion channels (VICs) are a subset of the larger P-loop ion channel family. Most voltage-activated channels exhibit two competing responses to membrane depolarization, which initiates both an activation process that results in channel opening and an inactivation process that ultimately results in channel closing. Analyses of the crystal structures of two 2-TM bacterial potassium channels led to the conclusion that the structure of KcsA represented a closed state and that of the related calcium-gated channel, MthK, crystallized in the presence of bound calcium, represented an open state. The 6-TM channels such as Shaker offer easier genetic manipulation, including the possibility of changing four residues in a functional channel for the price of a single mutation. A strong argument has been made that the bacterial sodium channels represent, or at least are closely related to, progenitors of eukaryotic channels.

Citation: Pavlov E, Bladen C, Diao C, French R. 2005. Bacterial Na Channels: Progenitors, Progeny, or Parallel Evolution?, p 191-207. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch10

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Sodium Channels
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Ion Channels
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Figures

Image of Figure 1.
Figure 1.

Proposed transmembrane topologies of voltage-dependent sodium channels from prokaryotes and eukaryotes. (A) A 6-TM segment structure of NaChBac. (B) Four identical 6-TM domains of the NaChBac protein presumably coassemble to form the functional channel. (C) In contrast to NaChBac, the α subunit of eukaryotic voltage-gated sodium channels is formed from four homologous but nonidentical 6-TM domains linked into a single polypeptide chain. The shaded S4 segments contain several positively charged residues (see Fig. 4 ), which play a primary role in voltage sensing and carry most or all of the measurable gating charge movement. In general, the cytoplasmic loops of eukaryotic Na channels are longer than those of NaChBac, presumably offering more opportunity for modulation of channel activity via various signaling pathways.

Citation: Pavlov E, Bladen C, Diao C, French R. 2005. Bacterial Na Channels: Progenitors, Progeny, or Parallel Evolution?, p 191-207. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch10
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Image of Figure 2.
Figure 2.

Comparison of voltage-dependent activation kinetics of NaV and NaChBac channels. Kinetics of NaChBac activation and inactivation is significantly slower than that of rSkM1 channels; overall voltage dependence of these processes is similar, but here activation in NaChBac appears as a less steep function of voltage than it is for rSkM1 (rNa1.4). (A) Whole-cell patch-clamp recording of current through the NaChBac channel. Currents were induced by membrane depolarization from the holding potential of −140 mV to the range of voltages from −90 to 70mV. The external (bathing) solution contained 140 mM NaCl, 5 mM KCl, 1 mM CaCl, 1mM MgCl, and 10 mM HEPES (pH 7.4); internal (pipette) solution contained 130mM NaF, 10mM EGTA, 10 mM NaCl, and 10 mM HEPES (pH 7.4). Records were collected at room temperature. (B) Current recordings of rSkM1 channel done under experimental conditions identical to those of panel A. (C) Same current trace as on panel B shown on the timescale of panel A. Note the dramatic difference in kinetics between the two channels. (D) G-V relationship of the NaChBac and rSkM1 channels under identical conditions.

Citation: Pavlov E, Bladen C, Diao C, French R. 2005. Bacterial Na Channels: Progenitors, Progeny, or Parallel Evolution?, p 191-207. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch10
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Image of Figure 3.
Figure 3.

Selectivity changes are induced by insertion of an extra negative charge(s) in the pore of NaChBac. Currents conducted by NaChBac and the mutant S195E, recorded when external sodium has been replaced by calcium. (A) Wild-type NaChBac shows no detectable inward current, indicating that it is not permeable for calcium. (B) NaChBac S195E channels, with a point mutation in the pore region substituting neutral serine at position 195 with a negatively charged glutamate (S195E mutant), demonstrate significant inward currents, indicating that this mutated channel is permeable to calcium ions. In both experiments, the external bath solution consisted of 20 mM CaCl, 1mM MgCl, 10mM HEPES, 40 mM tetraethylammonium chloride, 10 mM glucose, and 65 mM CsCl (pH 7.2 with tetraethylammonium hydroxide); the internal pipette solution contained 130mM NaF, 10mM EGTA, 10 mM NaCl, and 10 mM HEPES (pH 7.4). (C) I-V relationship plotted from the current traces shown in panels A and B. Note the difference between reversal potentials for wild-type and mutant channels, consistent with a substantial permeability to Ca ions induced by the mutation. Conversion of NaChBac into a functional calcium channel has been explored in some detail by .

Citation: Pavlov E, Bladen C, Diao C, French R. 2005. Bacterial Na Channels: Progenitors, Progeny, or Parallel Evolution?, p 191-207. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch10
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Image of Figure 4.
Figure 4.

Amino acid sequence alignments for the N-terminal part of S4 voltage sensor segments from 6-TM and 24-TM voltage-gated channels. Note the conserved pattern of basic residues repeated every three amino acids, provided exclusively by arginine in the first three positions for the channels shown, with lysine appearing in the fourth position for some domains in the eukaryotic Na and Ca channels. Other basic residues are seen when some of the sequences are extended in the C-terminal direction, but the residues shown here are thought to account for essentially all of the gating charge movement. National Center for Biotechnology Information (NCBI) GeneBank accession numbers for sequences used in the alignment are Q01668 (Human hCa1.3–α1D, an L-type Ca channel), CAA76659 (rSkM1 or Na1.4), Q9YDF8 (KAP), NP_037102 (Shaker), and AAR21291 (NaChBac). The program used for the alignments was Clustal W version 1.8, which defines “highly conserved” residues as showing =50% identity among the sequence set used for the search.

Citation: Pavlov E, Bladen C, Diao C, French R. 2005. Bacterial Na Channels: Progenitors, Progeny, or Parallel Evolution?, p 191-207. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch10
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Image of Figure 5.
Figure 5.

A putative gate alignment of S6 sequences from NaChBac and other voltage-gated channels shows a highly conserved glycine (shown in white on black), which is thought to provide a flexible link, or gating hinge, near the middle of S6 in most cases. NCBI GeneBank accession numbers for sequences used in the alignment are AAC67239 (Human hCa3.2–α1H, a T-type Ca channel), CAA76659 (rSkM1 or Na1.4), Q9YDF8 (KAP), NP_037102 (Shaker), and BAB05220 (NaChBac). Identical residues are highlighted in bold type. Search software used was as in the legend of Fig. 4 .

Citation: Pavlov E, Bladen C, Diao C, French R. 2005. Bacterial Na Channels: Progenitors, Progeny, or Parallel Evolution?, p 191-207. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch10
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Image of Figure 6.
Figure 6.

Sequence alignment for the pore regions of different voltage-gated channels. Charged groups of the selectivity filter of NaChBac, rSkM1, and Ca channels are shown in white on black; the highly conserved GYG selectivity filter motif of the potassium channels is underlined and italicized. Note that selectivity filter alignment as well as aligned score suggests closer homology between NaChBac and CaV than between NaChBac and rSkM1 channels. The motif xxxxx appears in NaChBac and in eukaryotic Na and Ca channels, but the E is present in all domains only in the Ca channel. The alignments for the K channels are ambiguous due to the low sequence identity and might be better portrayed shifted left three residues so that the TVGYG motif begins under the fully conserved T in the Na and Ca channel sequences. NCBI GeneBank accession numbers for sequences used in the alignment are Q13936 (HumanCa1.2–α1C, an L-type Ca channel), CAA76659 (rSkM1 or Na1.4), Q9YDF8 (KAP), NP_037102 (Shaker), and BAB05220 (NaChBac). Search software used was as in the legend of Fig. 4 .

Citation: Pavlov E, Bladen C, Diao C, French R. 2005. Bacterial Na Channels: Progenitors, Progeny, or Parallel Evolution?, p 191-207. In Kubalski A, Martinac B (ed), Bacterial Ion Channels and Their Eukaryotic Homologs. ASM Press, Washington, DC. doi: 10.1128/9781555816452.ch10
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