Low Conductance Gap Junctions Mediate Specific Electrical Coupling in Body-wall Muscle Cells of Caenorhabditis elegans

Abstract

Invertebrate innexins and their mammalian homologues, the pannexins, are gap junction proteins. Although a large number of such proteins have been identified, few of the gap junctions that they form have been characterized to provide combined information of biophysical properties, coupling pattern, and molecular compositions. We adapted the dual whole cell voltage clamp technique to in situ analysis of electrical coupling in Caenorhabditis elegans body-wall muscle. We found that body-wall muscle cells were electrically coupled in a highly organized and specific pattern. The coupling was characterized by small (350 pS or less) junctional conductance (G j ), which showed a bell-shaped relationship with junctional potential (V j ) but was independent of membrane potential (V m ). Injection of currents comparable to the junctional current (I j ) into body-wall muscle cells caused significant depolarization, suggesting important functional relevance. The innexin UNC-9 appeared to be a key component of the gap junctions. Both Myc-and green fluorescent protein-tagged UNC-9 was localized to muscle intercellular junctions. G j was greatly inhibited in unc-9(fc16), a putative null mutant. Specific inhibition of UNC-9 function in muscle cells reduced locomotion velocity. Despite UNC-9 expression in both motor neurons and body-wall muscle cells, analyses of miniature and evoked postsynaptic currents in the unc-9 mutant showed normal neuromuscular transmission. These analyses provide a relatively detailed description of innexin-based gap junctions in a native tissue and suggest that innexin-based small conductance gap junctions can play an important role in processes such as locomotion.

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“…We have, however, found a marker, the UNC-9 innexin gap junction protein (31), that localized to the anterior PLM neurite in both wild-type animals and lin-44 and lin-17 mutants. In wildtype animals, UNC-9::GFP was found in patches in the anterior neurite near the cell body.…”

Gap Junctions Synchronize Action Potentials and Ca2+ Transients in Caenorhabditis elegans Body Wall Muscle

“…Neural control could be important because each motoneuron forms synapses with several muscle cells that are located at the same longitudinal level (5,6). In addition, gap junctions could play a role because muscle cells in parallel are electrically coupled, whereas those in series are not (7). However, precise roles of neural inputs and muscle gap junctions in synchronizing muscle activities are poorly defined.…”

Dissection of neuronal gap junction circuits that regulate social behavior in Caenorhabditis elegans

“…Both unc-9 and unc-7 are expressed broadly in the nervous system, and null mutants in these genes have strong locomotion defects; unc-9 is also expressed in body wall muscles (35)(36)(37). To bypass indirect effects of locomotion on aggregation and narrow down sites of unc-9 action, we targeted unc-9 using a cell-specific Cre-Lox strategy (Fig.…”