Opening of single gap junction channels during formation of electrical coupling between embryonic muscle cells

Chow, Ida; Young, Steven H.

doi:10.1016/0012-1606(87)90298-3

Cited by 32 publications

(14 citation statements)

References 24 publications

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“…After the junctional conductance of well-coupled cell pairs had been reduced by OAG or PKC, stepwise changes of the junctional current could be examined. The discrete conductances can be compared to those observed previously during spontaneously occurring uncoupling (Somogyi & Kolb, 1988a) and to conductances found in lacrimal gland (120 pS; Neyton & Trautman, 1985), in embryonic heart (135-165 pS; Veenstra & De Haan, 1986, in neonatal heart (53 pS; Burt & Spray, 1988) and in Xenopus myolomal muscle cells (114 pS; Chow & Young, 1987). It will be discussed whether the examined conductances reflect subconductance states of one channel or altogether different channel types.…”

Section: Introductionmentioning

confidence: 98%

Inhibition of electrical coupling in pairs of murine pancreatic acinar cells by OAG and isolated protein kinase C

1989

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Gap junctional coupling was studied in pairs of murine pancreatic acinar cells using the double whole-cell patch-clamp technique. During stable electrical coupling, addition of OAG (1-oleoyl-2-acetyl-sn-glycerol) induced a progressive reduction of the junctional conductance to the detectable limit (approximately 3 pS). Prior to complete electrical uncoupling, various discrete single channel conductances between 20 and 100 pS could be observed. Polymyxin B, a potent inhibitor of the protein kinase C (PKC) system, completely suppressed OAG-stimulated electrical uncoupling. Dialysis of cell pairs with solutions containing PKC, isolated from rat brain, also caused electrical uncoupling. The presence of 0.1 mM dibutyryl cyclic AMP and 5 mM ATP in the pipette solution, which serves to stabilize the junctional conductance, did not suppress the effects of OAG or isolated PKC. We conclude that an increase of protein kinase C activity leads to the closure of gap junction channels, presumably via a PKC-dependent phosphorylation of the junctional peptide, and that this mechanism is dominant over cAMP-dependent upregulatory effects in the experimental time range (less than or equal to 1 hr). A correlation of the observed single channel conductances with the appearance of channel subconductance states or various channel populations is discussed.

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Section: Introductionmentioning

confidence: 98%

Inhibition of electrical coupling in pairs of murine pancreatic acinar cells by OAG and isolated protein kinase C

1989

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“…Highresolution ultrastructural evaluation of pore size is consistent with a channel at least as large as required for this unitary conductance (6,7). Several investigators have found average unitary conductance values ranging from 120 to 200 pS in a variety of tissues [200 pS in reconstituted lens junctions (8); 140-150 pS in reconstituted or incorporated liver gap junctions (9,10); 120 pS in lacrimal gland (11); 135-165 pS in embryonic heart (12,13); 114 pS in Xenopus myotomal muscle cells (14)]. However, in each of these studies smaller events were also identified, and the possibility was considered that these smaller events might reflect either the true unitary conductance of the channel or subconductance states ofchannels due to partial closure.…”

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confidence: 99%

Single-channel events and gating behavior of the cardiac gap junction channel.

Burt

Spray

1988

Proc. Natl. Acad. Sci. U.S.A.

185

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The activity of gap junction channels between pairs of neonatal rat heart cells in culture was studied under control conditions and during uncoupling procedures by using dual whole-cell voltage clamp techniques. Under control conditions gap junctional conductance ranged from 0.05 to 35 nS. In cell pairs exhibiting low gap junctional conductance (<500 pS), single-channel events with a unitary conductance of 53 ± 2 pS (5 experiments; 186 events) were apparent. Event duration and open-time probability were estimated to be 0.95 sec and 0.17, respectively. When the junctional conductance in wellcoupled cell pairs (with initial junctional conductance, >5 nS) was reduced by cytoplasmic acidification or application of heptanol, single-channel events could be visualized. Compared to low-conductance controls, unitary channel conductance was unaltered (for acidification the conductance was 58 ± 3 pS in 11 experiments with 253 events; for heptanol the conductance was 61 ± 1 pS in 2 experiments with 171 events), while the probability of channels being open was decreased. The constancy of unitary channel conductance under control conditions and during uncoupling procedures suggests that opening and closing of the gap junction channel are all-or-none processes during which no stable subconductance states are formed. (8); 140-150 pS in reconstituted or incorporated liver gap junctions (9, 10); 120 pS in lacrimal gland (11); 135-165 pS in embryonic heart (12, 13); 114 pS in Xenopus myotomal muscle cells (14)]. However, in each of these studies smaller events were also identified, and the possibility was considered that these smaller events might reflect either the true unitary conductance of the channel or subconductance states ofchannels due to partial closure. While graded closure ofthe gapjunction channel has been proposed to account for graded changes in the selective permeability to molecules of specific sizes (15), other quantitative studies have failed to demonstrate graded changes in selectivity and have indicated that channel closure is an all-or-none process (5, 16).In the present study the unitary conductance of gap junctions between poorly coupled neonatal rat myocardial cells was examined and compared to unitary conductances recorded from well-coupled cell pairs after junctional conductance had been reduced by cytoplasmic acidification or exposure to heptanol. We found an average single-channel conductance of 53 pS under control conditions that was unaltered as channel open time was reduced by these uncoupling treatments. No evidence for stable subconductance states of a larger channel was discerned during uncoupling. MATERIALS AND METHODSCells were isolated from neonatal rat hearts as described (17) and were generally used between 9 and 30 hr after plating, during which time they progressed from spherical to slightly spread morphology (Fig. 1A). Single-electrode voltage clamps with patch electrodes were used. For measurement of gapjunctional conductance, cells were clamped to a common holding potential, us...

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“…However, it may be inappropriate to relate the conductance of the single channels formed between two cardiac, liver, muscle or lacrimal cells to those formed between leech neurones, since I have observed conductances for the earliest connections which are much smaller than the 100 pS single-channel conductances calculated by and the 100-300 pS levels measured by Neyton & Trautmann (1985), Veenstra & DeHaan (1986), Spray et al (1986), Chow & Young (1987) and Young et al (1987) for non-rectifying junctions and by Zampighi, Hall & Kreman (1985) for a voltage-dependent junction. There have been recent reports of single-channel conductances within the range of 50-60pS in neonatal rat and embryonic chicken heart cells (Burt & Spray, 1988;Veenstra & DeHaan, 1988).…”

Section: Discussionmentioning

confidence: 95%

“…It is unclear whether this is due to the properties of the same channels, present in greater numbers, if the properties of the existing channels change, or if the channels present early in the process of synapse formation are subsequently replaced by channels with non-rectifying properties. Of these possibilities, substantial evidence from both physiological (Loewenstein, Kanno & Socolar, 1978;Chow & Young, 1987) and morphological studies (Johnson, Hammer, Sheridan & Revel, 1974;Azarnia, Dahl & Loewenstein, 1981;DeMaziere & Scheuermann, 1985;Walensky, Patterson & Willard, 1985) has consistently shown that increasing numbers of channels, rather than changing channel conductance, accompanies greater electrical connectivity. The distinction of whether the channels that compose the connections during this later stage of synapse formation are those with properties that are rectifying, non-rectifying, or a combination of the two is open to speculation.…”

Section: Discussionmentioning

confidence: 99%

Voltage‐dependent properties of electrical synapses formed between identified leech neurones in vitro.

Davis

1989

The Journal of Physiology

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SUMMARY1. The voltage-dependent properties of rectifying and non-rectifying electrical synapses formed between identified leech neurones were quantified during their regeneration in vitro.2. Junctional conductance increased with time in culture. This was evaluated by making comparisons between cell pairs maintained in vitro for differing amounts of time, as well as by taking repeated measurements from a single cell pair at different time intervals.3. Non-rectifying electrical synapses were formed between certain identified neurones of the same type. Thus, Leydig cells cultured with Leydig cells established non-rectifying electrical connections, as did Retzius cells, longitudinal motoneurones (L cells) and anterior pagoda (AP) cells, each paired with its own cell type.4. Rectifying synapses developed when sensory neurones (P cells or N cells) were paired with the other neurones mentioned above that form non-rectifying connections between themselves. The cell combinations examined were L cell-P cell, Leydig cell-N cell, and AP cell-P cell. The direction of current flow across these rectifying synapses was consistently from the sensory neurone to the other cell in the pair.5. Non-rectifying connections early in the process of synapse regeneration (1-3 days) showed non-linearities greater than those observed in established nonrectifying synapses. There was a subtle, but clear, voltage dependence even at the later stages of synapse formation (4-18 days).6. In contrast to non-rectifying connections, rectifying synapses formed between cells at early times in culture showed less voltage dependence than those observed at later times.7. The marked non-linearities of the non-rectifying connections at early stages in synapse formation along with the reduced voltage dependence of the rectifying connections within the same time period revealed unexpected similarities between the two. At the early stages of synapse formation, the two types of electrical synapse were essentially indistinguishable for one direction of junctional current.

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Opening of single gap junction channels during formation of electrical coupling between embryonic muscle cells

Cited by 32 publications

References 24 publications

Inhibition of electrical coupling in pairs of murine pancreatic acinar cells by OAG and isolated protein kinase C

Inhibition of electrical coupling in pairs of murine pancreatic acinar cells by OAG and isolated protein kinase C

Single-channel events and gating behavior of the cardiac gap junction channel.

Voltage‐dependent properties of electrical synapses formed between identified leech neurones in vitro.

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