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BMC Evol Biol
2019 Feb 26;19Suppl 1:46. doi: 10.1186/s12862-019-1369-4.
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Are there gap junctions without connexins or pannexins?
Slivko-Koltchik GA
,
Kuznetsov VP
,
Panchin YV
.
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BACKGROUND: Gap junctions (GJ) are one of the most common forms of intercellular communication. GJs are assembled from proteins that form channels connecting the cytoplasm of adjacent cells. They are considered to be the main or the only type of intercellular channels and the universal feature of all multicellular animals. Two unrelated protein families are currently considered to be involved in this function, namely, connexins and pannexins (pannexins/innexins). Pannexins were hypothesized to be the universal GJ proteins of multicellular animals, distinct from connexins that are characteristic of chordates only. Here we have revised this supposition by applying growing high throughput sequencing data from diverse metazoan species.
RESULTS: Pannexins were found in Chordates, Ctenophores, Cnidarians, and in the most major groups of bilateral protostomes. Yet some metazoans appear to have neither connexins nor pannexins in their genomes. We detected no connexins or pannexins/innexins homologues in representatives of all five classes of echinoderms and their closest relatives hemichordates with available genomic sequences. Despite this, our intracellular recordings demonstrate direct electrical coupling between blastomeres at the 2-cell embryo of the echinoderm (starfish Asterias rubens). In these experiments, carboxyfluorescein fluorescent dye did not diffuse between electrically coupled cells. This excludes the possibility that the observed electrical coupling is mediated by incomplete cytoplasm separation during cleavage.
CONCLUSION: Functional GJs are present in representatives of the clade that lack currently recognized GJ protein families. New undiscovered protein families utilized for intercellular channels are predicted. It is possible that the new type(s) of intercellular channels are present in parallel to pannexin and connexin gap junctions in animal groups, other than Echinodermata.
Fig. 1. Gap junctions versus syncytium or incomplete cleavage. a Cells connected by GJs are electrically coupled via intercellular channels. Electrical current pulse applied through intracellular microelectrode I2 results in a small ion molecule flow through GJs and leads to membrane potential changes in the adjacent cell recorded by electrode V1. If tracer dye ejected from V1 electrode (green) is bigger than the GJ channel pore size, it is restricted to the cytoplasm of one cell. b Incompletely divided or fused cells show a voltage drop on shared plasma membranes in response to the electrical current pulse applied via I2 (Ric < < Rgj) and at the same time big molecules freely diffuse through the shared cytoplasm
Fig. 2. GJ proteins evolution. Connexin (blue) and pannexin (red) presence (+) or absence (−) in the multicellular animal main taxonomic groups is indicated in simplified phylogenetic tree. The blue arrowhead points out a hypothetical connexin acquisition event in Chordate evolution. The red arrowhead shows a hypothetical event of pannexin loss at the base of Echinodermata/Hemichordata’s sister group branch
Fig. 3. Electrical coupling in A. rubens early embryos. a-c Microelectrode V1 placed in one blastomere registers the membrane potential changes, whereas I2 electrode inside the adjacent blastomere is used to inject current pulses. a, b Fluorescent dye applied via V1 electrode stain only injected cell . Plain light background a and fluorescence image b of 2-cell embryo. c Negative current impulses (red) are applied to test electrical coupling. Electrical potential changes (blue) are recorded via V1 electrode. (a, b and c are from the same experiment). d. V1/I2 values in two different situations from 51 current impulse experiments. The difference between IC and GJ is significant (p-value< 0.05). On the left (A) V1/I2 value was measured in incompletely cleaved zygote and corresponds to cell input resistance R, on the right (B) V1/I2 was measured in separated blastomeres
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