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Mechanistic signs of double-barreled structure in a fluoride ion channel
Abstract
The Fluc family of F− ion channels protects prokaryotes and lower eukaryotes from the toxicity of environmental F−. In bacteria, these channels are built as dual-topology dimers whereby the two subunits assemble in antiparallel transmembrane orientation. Recent crystal structures suggested that Fluc channels contain two separate ion-conduction pathways, each with two F− binding sites, but no functional correlates of this unusual architecture have been reported. Experiments here fill this gap by examining the consequences of mutating two conserved F−-coordinating phenylalanine residues. Substitution of each phenylalanine specifically extinguishes its associated F− binding site in crystal structures and concomitantly inhibits F− permeation. Functional analysis of concatemeric channels, which permit mutagenic manipulation of individual pores, show that each pore can be separately inactivated without blocking F− conduction through its symmetry-related twin. The results strongly support dual-pathway architecture of Fluc channels.
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The 'Fluc' family of small membrane proteins comprises the CrcB F− channel of Escherichia coli.
“a group of small membrane proteins generically known as the ‘Fluc’ family, which comprises the CrcB F− channel of Escherichia coli (Last et al., 2016; Stockbridge et al., 2013)”
From Role of the CrcB transporter of Pseudomonas putida in the multi‐level stress response elicited by mineral fluoride (2022) · cites this paper as Last et al., 2016
Mutation of either F82 or F85 to a non-polarizable hydrophobic residue like isoleucine greatly reduces or abolishes F− transport, depending on the homologue.
“Mutation of either F82 or F85 to a non-polarizable hydrophobic residue like isoleucine greatly reduces or abolishes F− transport, depending on the homologue(73, 76).”
From Membrane exporters of fluoride ion (2021) · cites this paper as [76]
Of dozens of mutations, none have allowed detectable throughput of any other anion.
“Of dozens of mutations, none have allowed detectable throughput of any other anion, and increasing the bore of the channel by paring back sidechains has not yet been shown to decrease selectivity(73, 75, 76, 85).”
From Membrane exporters of fluoride ion (2021) · cites this paper as [76]
Increasing the bore of the channel by paring back sidechains has not yet been shown to decrease selectivity.
“Of dozens of mutations, none have allowed detectable throughput of any other anion, and increasing the bore of the channel by paring back sidechains has not yet been shown to decrease selectivity(73, 75, 76, 85).”
From Membrane exporters of fluoride ion (2021) · cites this paper as [76]
Electrophysiological experiments showed that fluoride uses both conduits to flow down its electrochemical gradient.
“electrophysiological experiments showed that fluoride uses both conduits to flow down its electrochemical gradient (76).”
From Membrane exporters of fluoride ion (2021) · cites this paper as [76]
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Citations
Cites
Crystal structures of a double-barrelled fluoride ion channel
Stockbridge, R. B., Kolmakova-Partensky, L., Shane, T., Koide, A., Koide, S., Miller, C., & Newstead, S. (2015) · Nature · doi:10.1038/nature14981 · Cited by 119
Self-citationBacterial fluoride resistance, Fluc channels, and the weak acid accumulation effect
Ji, C., Stockbridge, R. B., & Miller, C. (2014) · Journal of General Physiology · doi:10.1085/jgp.201411243 · Cited by 97
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Cited by
Sorted by citations
Membrane exporters of fluoride ion
McIlwain, B. C., Ruprecht, M. T., & Stockbridge, R. B. (2021) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-071520-112507 · Cited by 69
Calero, P., Gurdo, N., & Nikel, P. I. (2022) · Environmental Microbiology · doi:10.1111/1462-2920.16110 · Cited by 56
Metadata
- Authors
- Last, N. B., Kolmakova-Partensky, L., Shane, T., & Miller, C.
- Affiliations
- Department of Biochemistry, Howard Hughes Medical Institute, Brandeis University, Waltham, United States
- ORCID
- Miller, Christopher
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2016-07-23
- Volume
- 5
- ISSN
- 2050-084X
- PMC
- PMC4969038
- Cited by
- 34
- References
- 2
- Language
- en
- Licence
- Funders
- Howard Hughes Medical Institute
- National Institute of General Medical Sciences (RO1-GM107023)
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