A voltage-dependent gap junction in Drosophila melanogaster

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Abstract

Steady-state and kinetic analyses of gap junctional conductance, g(j), in salivary glands of Drosophila melanogaster third instar larvae reveal a strong and complex voltage dependence that can be elicited by two types of voltages. Voltages applied between the cells, i.e., transjunctional voltages, V(j), and those applied between the cytoplasm and the extracellular space, inside-outside voltages, V(i,o), markedly alter g(j). Alteration of V(i-o) while holding V(j) = 0, i.e., by equal displacement of the voltages in the cells, causes g(j) to increase to a maximum on hyperpolarization and to decrease to near zero on depolarization. These conductance changes associated with v(i-o) are fit by a model in which there are two independent gates in series, one in each membrane, where each gate is equally sensitive to V(i-o) and exhibits first order kinetics. V(j)'s generated by applying voltage steps of either polarity to either cell, substantially reduce g(j). These conductance changes exhibit complex kinetics that depend on V(i-o) as well as V(j). At more positive V(i-o)'s, the changes in g(j) have two phases, an early phase consisting of a decrease in g(j) for either polarity of V(j) and a later phase consisting of an increase in g(j) on hyperpolarizing either cell and a decrease on depolarizing either cell. At negative V(i-o)'s in the plateau region of the g(j)-V(i-o) relation, the later slow increase in g(j) is absent on hyperpolarizing either cell. Also, the early decrease in g(j) for either polarity of V(j) is faster the more positive the V(i-o). The complex time course elicited by applying voltage steps to one cell can be explained as combined actions of V(i-o) and V(j), with the early phase ascribable to V(j), but influenced by V(i-o), and the later phase to the changes in V(i-o) associated with the generation of V(j). The substantially different kinetics and sensitivity of changes in g(j) by V(i-o) and V(j) suggests that the mechanisms of gating by these two voltages are different. Evidently, these gap-junction channels are capable of two distinct, but interactive forms of voltage dependence.

Original languageEnglish (US)
Pages (from-to)114-126
Number of pages13
JournalBiophysical Journal
Volume59
Issue number1
StatePublished - 1991

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Gap Junctions
Drosophila melanogaster
Extracellular Space
Salivary Glands
Larva
Cytoplasm
Membranes

ASJC Scopus subject areas

  • Biophysics

Cite this

A voltage-dependent gap junction in Drosophila melanogaster. / Verselis, Vytautas; Bennett, Michael V. L.; Bargiello, T. A.

In: Biophysical Journal, Vol. 59, No. 1, 1991, p. 114-126.

Research output: Contribution to journalArticle

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abstract = "Steady-state and kinetic analyses of gap junctional conductance, g(j), in salivary glands of Drosophila melanogaster third instar larvae reveal a strong and complex voltage dependence that can be elicited by two types of voltages. Voltages applied between the cells, i.e., transjunctional voltages, V(j), and those applied between the cytoplasm and the extracellular space, inside-outside voltages, V(i,o), markedly alter g(j). Alteration of V(i-o) while holding V(j) = 0, i.e., by equal displacement of the voltages in the cells, causes g(j) to increase to a maximum on hyperpolarization and to decrease to near zero on depolarization. These conductance changes associated with v(i-o) are fit by a model in which there are two independent gates in series, one in each membrane, where each gate is equally sensitive to V(i-o) and exhibits first order kinetics. V(j)'s generated by applying voltage steps of either polarity to either cell, substantially reduce g(j). These conductance changes exhibit complex kinetics that depend on V(i-o) as well as V(j). At more positive V(i-o)'s, the changes in g(j) have two phases, an early phase consisting of a decrease in g(j) for either polarity of V(j) and a later phase consisting of an increase in g(j) on hyperpolarizing either cell and a decrease on depolarizing either cell. At negative V(i-o)'s in the plateau region of the g(j)-V(i-o) relation, the later slow increase in g(j) is absent on hyperpolarizing either cell. Also, the early decrease in g(j) for either polarity of V(j) is faster the more positive the V(i-o). The complex time course elicited by applying voltage steps to one cell can be explained as combined actions of V(i-o) and V(j), with the early phase ascribable to V(j), but influenced by V(i-o), and the later phase to the changes in V(i-o) associated with the generation of V(j). The substantially different kinetics and sensitivity of changes in g(j) by V(i-o) and V(j) suggests that the mechanisms of gating by these two voltages are different. Evidently, these gap-junction channels are capable of two distinct, but interactive forms of voltage dependence.",
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N2 - Steady-state and kinetic analyses of gap junctional conductance, g(j), in salivary glands of Drosophila melanogaster third instar larvae reveal a strong and complex voltage dependence that can be elicited by two types of voltages. Voltages applied between the cells, i.e., transjunctional voltages, V(j), and those applied between the cytoplasm and the extracellular space, inside-outside voltages, V(i,o), markedly alter g(j). Alteration of V(i-o) while holding V(j) = 0, i.e., by equal displacement of the voltages in the cells, causes g(j) to increase to a maximum on hyperpolarization and to decrease to near zero on depolarization. These conductance changes associated with v(i-o) are fit by a model in which there are two independent gates in series, one in each membrane, where each gate is equally sensitive to V(i-o) and exhibits first order kinetics. V(j)'s generated by applying voltage steps of either polarity to either cell, substantially reduce g(j). These conductance changes exhibit complex kinetics that depend on V(i-o) as well as V(j). At more positive V(i-o)'s, the changes in g(j) have two phases, an early phase consisting of a decrease in g(j) for either polarity of V(j) and a later phase consisting of an increase in g(j) on hyperpolarizing either cell and a decrease on depolarizing either cell. At negative V(i-o)'s in the plateau region of the g(j)-V(i-o) relation, the later slow increase in g(j) is absent on hyperpolarizing either cell. Also, the early decrease in g(j) for either polarity of V(j) is faster the more positive the V(i-o). The complex time course elicited by applying voltage steps to one cell can be explained as combined actions of V(i-o) and V(j), with the early phase ascribable to V(j), but influenced by V(i-o), and the later phase to the changes in V(i-o) associated with the generation of V(j). The substantially different kinetics and sensitivity of changes in g(j) by V(i-o) and V(j) suggests that the mechanisms of gating by these two voltages are different. Evidently, these gap-junction channels are capable of two distinct, but interactive forms of voltage dependence.

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