Identification of the prokaryotic ligand-gated ion channels and their implications for the mechanisms and origins of animal Cys-loop ion channels View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2004-12-20

AUTHORS

Asba Tasneem, Lakshminarayan M Iyer, Eric Jakobsson, L Aravind

ABSTRACT

BACKGROUND: Acetylcholine receptor type ligand-gated ion channels (ART-LGIC; also known as Cys-loop receptors) are a superfamily of proteins that include the receptors for major neurotransmitters such as acetylcholine, serotonin, glycine, GABA, glutamate and histamine, and for Zn2+ ions. They play a central role in fast synaptic signaling in animal nervous systems and so far have not been found outside of the Metazoa. RESULTS: Using sensitive sequence-profile searches we have identified homologs of ART-LGICs in several bacteria and a single archaeal genus, Methanosarcina. The homology between the animal receptors and the prokaryotic homologs spans the entire length of the former, including both the ligand-binding and channel-forming transmembrane domains. A sequence-structure analysis using the structure of Lymnaea stagnalis acetylcholine-binding protein and the newly detected prokaryotic versions indicates the presence of at least one aromatic residue in the ligand-binding boxes of almost all representatives of the superfamily. Investigation of the domain architectures of the bacterial forms shows that they may often show fusions with other small-molecule-binding domains, such as the periplasmic binding protein superfamily I (PBP-I), Cache and MCP-N domains. Some of the bacterial forms also occur in predicted operons with the genes of the PBP-II superfamily and the Cache domains. Analysis of phyletic patterns suggests that the ART-LGICs are currently absent in all other eukaryotic lineages except animals. Moreover, phylogenetic analysis and conserved sequence motifs also suggest that a subset of the bacterial forms is closer to the metazoan forms. CONCLUSIONS: From the information from the bacterial forms we infer that cation-pi or hydrophobic interactions with the ligand are likely to be a pervasive feature of the entire superfamily, even though the individual residues involved in the process may vary. The conservation pattern in the channel-forming transmembrane domains also suggests similar channel-gating mechanisms in the prokaryotic versions. From the distribution of charged residues in the prokaryotic M2 transmembrane segments, we expect that there will be examples of both cation and anion selectivity within the prokaryotic members. Contextual connections suggest that the prokaryotic forms may function as chemotactic receptors for low molecular weight solutes. The phyletic patterns and phylogenetic relationships suggest the possibility that the metazoan receptors emerged through an early lateral transfer from a prokaryotic source, before the divergence of extant metazoan lineages. More... »

PAGES

r4-r4

Identifiers

URI

http://scigraph.springernature.com/pub.10.1186/gb-2004-6-1-r4

DOI

http://dx.doi.org/10.1186/gb-2004-6-1-r4

DIMENSIONS

https://app.dimensions.ai/details/publication/pub.1022537217

PUBMED

https://www.ncbi.nlm.nih.gov/pubmed/15642096


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84 features
85 form
86 fusion
87 genes
88 genus
89 glutamate
90 glycine
91 histamine
92 homolog
93 homology
94 hydrophobic interactions
95 identification
96 implications
97 individual residues
98 information
99 interaction
100 investigation
101 ion channels
102 ions
103 lateral transfer
104 length
105 ligand-binding boxes
106 ligand-gated ion channels
107 ligands
108 lineages
109 low molecular weight solutes
110 major neurotransmitter
111 mechanism
112 members
113 metazoan form
114 metazoan lineages
115 metazoan receptors
116 metazoans
117 molecular weight solutes
118 motif
119 nervous system
120 neurotransmitters
121 operon
122 origin
123 patterns
124 periplasmic binding proteins
125 pervasive feature
126 phyletic patterns
127 phylogenetic analysis
128 phylogenetic relationships
129 possibility
130 presence
131 process
132 prokaryotic M2 transmembrane segments
133 prokaryotic forms
134 prokaryotic homolog
135 prokaryotic ligand-gated ion channels
136 prokaryotic members
137 prokaryotic sources
138 prokaryotic versions
139 protein
140 receptor type ligand-gated ion channels
141 receptors
142 relationship
143 representatives
144 residues
145 role
146 search
147 segments
148 selectivity
149 sensitive sequence profile searches
150 sequence motifs
151 sequence profile searches
152 sequence-structure analysis
153 signaling
154 similar channel-gating mechanisms
155 single archaeal genus
156 solutes
157 source
158 stagnalis acetylcholine-binding protein
159 structure
160 subset
161 superfamily
162 superfamily of proteins
163 synaptic signaling
164 system
165 transfer
166 transmembrane domain
167 transmembrane segments
168 type ligand-gated ion channels
169 version
170 weight solutes
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