DOI: 10.1242/jeb.170.1.93. Analysis of Repolarization of Presynaptic Motor Terminals in <i>Drosophila</i> Larvae Using Potassium-Channel-Blocking Drugs and Mutations

Analysis of Repolarization of Presynaptic Motor Terminals in Drosophila Larvae Using Potassium-Channel-Blocking Drugs and Mutations

10.1242/jeb.170.1.93

Crossref journal-article

The Company of Biologists

Journal of Experimental Biology (237)

Abstract

ABSTRACT In Drosophila melanogaster muscles and neuronal cell bodies at least four different potassium currents have been identified whose activity shapes the electrical properties of these cells. Potassium currents also control repolarization of presynaptic terminals and, therefore, exert a major effect on transmitter release and synaptic plasticity. However, because of the small size of presynaptic terminals in Drosophila, it has not been possible to analyze the potassium currents they express. As a first approach to characterizing the ionic currents present at presynaptic motor terminals of Drosophila larvae, we recorded synaptic currents at the neuromuscular junction. From the alterations in evoked synaptic currents caused by various drugs and by mutations known to affect potassium currents in other tissues, we suggest that the repolarizing mechanism in presynaptic terminals consists of at least four distinct currents. One is affected by aminopyridines or Sh mutations, a second component is affected by the slo mutation, a third is sensitive to quinidine and one or more additional components are blocked by tetraethyl-ammonium. Depolarization depends on a presynaptic calcium current, which displays only slight voltage-dependent inactivation. Because the mechanism of repolarization exerts a major effect on synaptic activity, this analysis provides a framework for further genetic and molecular dissection of the basic processes involved in the regulation of transmitter release.

Bibliography

Gho, M., & Ganetzky, B. (1992). Analysis of Repolarization of Presynaptic Motor Terminals in Drosophila Larvae Using Potassium-Channel-Blocking Drugs and Mutations. Journal of Experimental Biology, 170(1), 93â111.

Authors 2

Michel Gho (first)
Barry Ganetzky (additional)

References 70 Referenced 45

10.1126/science.6093258 / Science / Calcium mediated reduction of ionic currents: A biophysical memory trace by Alkon (1984)
10.1113/jphysiol.1982.sp014345 / J. Physiol., Lond / Calcium inactivation in skeletal muscle fibres of the stick insect, Carausius morosus by Ashcroft (1982)
10.1126/science.1857984 / Science / A component of calcium-activated potassium channels encoded by the Drosophila slo locus by Atkinson (1991)
10.1113/jphysiol.1990.sp018333 / J. Physiol., Lond / Regulation of transmitter release at the squid giant synapse by presynaptic delayed rectifier potassium current by Augustine (1990)
10.1113/jphysiol.1985.sp015819 / J. Physiol., Lond / Calcium entry and transmitter release at voltage-clamped nerve terminals of squids by Augustine (1985)
10.1016/0896-6273(90)90449-P / Neuron / The Drosophila Shaker gene codes for a distinctive K+ current in a subset of neurons by Baker (1990)
10.1007/BF00582267 / Pflügers Arch / Potassium channels in lizard nodes of Ranvier and motor endings by Benoit (1989)
10.1113/jphysiol.1970.sp009235 / J. Physiol., Lond / Modification of transmitter release by ions which prolong the presynaptic action potential by Benoit (1970)
10.1126/science.2493160 / Science / A family of putative potassium channel genes in Drosophila by Butler (1989)
10.1113/jphysiol.1971.sp009365 / J. Physiol., Lond / Voltage clamp studies of a transient outward current in gastropod neural somata by Connors (1971)
10.1113/jphysiol.1980.sp013286 / J. Physiol., Lond / Phasic secretion of acetylcholine at a mammalian neuromuscular junction by Datyner (1980)
10.1016/0896-6273(91)90277-7 / Neuron / The inactivation gate of the Shaker K+ channel behaves like an open-channel blocker by Demo (1991)
10.1113/jphysiol.1967.sp008367 / J. Physiol., Lond / Co-operative action of calcium ions in transmitter release at the neuromuscular junction by Dodge (1967)
10.1523/JNEUROSCI.08-02-00428.1988 / J. Neurosci / The roles of potassium currents in Drosophila muscle by Elkins (1988)
10.1073/pnas.83.21.8415 / Proc. natn. Acad. Sci. U.S.A / A gene affecting a calcium-dependent potassium current in Drosophila by Elkins (1986)
10.1152/jn.1982.47.3.501 / J. Neurophysiol / Drosophila mutants with opposing effects on nerve excitability: genetics and spatial interactions in repetitive firing by Ganetzky (1982)
10.3109/01677068309107069 / J. Neurogenetics / Neurogenetic analysis of potassium currents in Drosophila: Synergistic effects on neuromuscular transmission in double mutants by Ganetzky (1983)
10.1007/BF00657511 / Pflügers Arch / Two distinct calcium-activated potassium currents in larval muscle fibres of Drosophila melanogaster by Gho (1986)
10.1016/0022-1910(76)90230-4 / J. Insect Physiol / Motor innervation of the supercontracting longitudinal ventro-lateral muscles of the blowfly larva by Hardie (1976)
10.1523/JNEUROSCI.11-10-03079.1991 / J. Neurosci / Voltage-sensitive potassium channels in Drosophila photoreceptors by Hardie (1991)
10.1113/jphysiol.1952.sp004717 / J. Physiol., Lond / Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo by Hodgkin (1952)
10.1073/pnas.88.2.380 / Proc. natn. Acad. Sci. U.S.A / Action potential broadening and frequency-dependent facilitation of calcium signals in pituitary nerve terminals by Jackson (1991)
10.1113/jphysiol.1976.sp011592 / J. Physiol., Lond / Properties of the larval neuromuscular junction in Drosophila melanogaster by Jan (1976)
10.1098/rspb.1977.0087 / Proc. R. Soc. Lond. B / Two mutations of synaptic transmission in Drosophila by Jan (1977)
10.1523/JNEUROSCI.09-02-00710.1989 / J. Neurosci / Stereotypic morphology of glutamatergic synapses on identified muscle cells of Drosophila larvae by Johansen (1989)
10.1126/science.6289442 / Science / Molecular biology of learning: modulation of transmitter release by Kandel (1982)
10.1038/2071097a0 / Nature / Release of acetylcholine from a nerve terminal by electrical pulses of variable strength and duration by Katz (1965)
10.1098/rspb.1967.0011 / Proc. R. Soc. Lond. B / The release of acetylcholine from nerve endings by graded electrical pulses by Katz (1967)
10.1113/jphysiol.1967.sp008307 / J. Physiol., Lond / A study of synaptic transmission in the absence of nerve impulses by Katz (1967)
10.1113/jphysiol.1969.sp008875 / J. Physiol., Lond / Tetrodotoxin-resistant electrical activity in presynaptic terminals by Katz (1969)
10.1113/jphysiol.1971.sp009537 / J. Physiol., Lond / The effect of prolonged depolarization on synaptic transfer in the stellate ganglion of the squid by Katz (1971)
10.1113/jphysiol.1973.sp010146 / J. Physiol., Lond / Calcium and potassium systems of a giant barnacle muscle fibre under membrane potential control by Keynes (1973)
10.1016/0896-6273(90)90105-O / Neuron / Mutational and gene dosage analysis of calcium-activated potassium channels in Drosophila: correlation of micro- and macroscopic currents by Komatsu (1990)
10.1523/JNEUROSCI.11-10-03047.1991 / J. Neurosci / Characterization of single calcium channels in Drosophda embryonic nerve and muscle cells by Leung (1991)
10.1113/jphysiol.1989.sp017684 / J. Physiol., Lond / Identification of ionic currents at presynaptic nerve endings of the lizard by Lindgren (1989)
10.1073/pnas.72.1.187 / Proc. natn. Acad. Sci. U.S.A / Calcium role in depolarization-secretion coupling: an aequorin study in squid giant synapse by Llinás (1975)
10.1073/pnas.73.8.2918 / Proc. natn. Acad. Sci. U.S.A / Presynaptic calcium currents and their relation to synaptic transmission: voltage clamp study in squid giant synapse and theoretical model for the calcium gate by Llinás (1976)
10.1016/S0006-3495(81)84898-9 / Biophys. J / Presynaptic calcium currents in squid giant synapse by Llinás (1981)
10.1073/pnas.79.7.2415 / Proc. natn. Acad. Sci. U.S.A / Transmission by presynaptic spike-like depolarization in the squid giant synapse by Llinás (1982)
10.1038/300185a0 / Nature / Action potential repolarization may involve a transient, Ca-sensitive outward current in a vertebrate neurone by MacDermott (1982)
10.1007/BF00670529 / Pflügers Arch / Presynaptic currents in frog motor endings by Mallart (1984)
10.3109/01677069109066212 / J. Neurogenetics / Nerve terminal excitability and neuromuscular transmission in T(X;Y)V7 and Shaker mutants of Drosophila melanogaster by Mallart (1991)
10.1113/jphysiol.1955.sp005397 / J. Physiol., Lond / A further study of the statistical composition of the end-plate potential by Martin (1955)
10.1113/jphysiol.1975.sp011012 / J. Physiol., Lond / Potassium activation in Helix aspersa neurones under voltage clamp: a component mediated by calcium influx by Meech (1975)
10.1523/JNEUROSCI.10-08-02614.1990 / J. Neurosci / Evidence for two calcium-dependent potassium conductances in lizard motor nerve terminals by Morita (1990)
10.1113/jphysiol.1975.sp011111 / J. Physiol., Lond / Evidence for a transient potassium membrane current dependent on calcium influx in crab muscle fibre by Mounier (1975)
10.1085/jgp.58.1.36 / J. gen. Physiol / Two fast transient current components during voltage clamp on snail neurones by Neher (1971)
10.1146/annurev.ph.50.030188.002115 / A. Rev. Physiol / Ionic channels in Drosophila by Papazian (1988)
10.1016/0306-4522(88)90033-4 / Neuroscience / Diversity and ubiquity of K channels by Rudy (1988)
{'key': '2023020216075421900_JEXBIO_170_1_93C50', 'first-page': '1', 'article-title': 'The mutation slo alters membrane excitability and Ca-activated K current in cultures Drosophila ‘giant’ neurons', 'volume': '281', 'author': 'Saito', 'year': '1990', 'journal-title': 'Soc. Neurosci. Abstr'} / Soc. Neurosci. Abstr / The mutation slo alters membrane excitability and Ca-activated K current in cultures Drosophila ‘giant’ neurons by Saito (1990)
10.1523/JNEUROSCI.11-07-02135.1991 / J. Neurosci / Expression of ion channels and mutational effects in giant Drosophila neurons differentiated from cell division-arrested embryonic neuroblasts by Saito (1991)
10.1101/SQB.1983.048.01.025 / Cold Spring Harbor Symp. quant. Biol / Genetic and voltage-clamp analysis of a Drosophila potassium channel by Salkoff (1983)
{'key': '2023020216075421900_JEXBIO_170_1_93C53', 'first-page': '275', 'article-title': 'Development of ion channels in the flight muscles of Drosophila', 'volume-title': 'J. Physiol', 'author': 'Salkoff', 'year': '1985'} / J. Physiol / Development of ion channels in the flight muscles of Drosophila by Salkoff (1985)
10.1038/293228a0 / Nature / Genetic modification of potassium channels in Drosophila Shaker mutants by Salkoff (1981)
10.1016/0896-6273(89)90070-6 / Neuron / Complete separation of four potassium currents in Drosophila by Singh (1989)
10.1242/jeb.152.1.59 / J. exp. Biol / Properties of potassium currents and their role in membrane excitability in Drosophila larval muscles fibers by Singh (1990)
10.1016/0896-6273(91)90278-8 / Neuron / Reopening of Ca2+ channels in mouse cerebellar neurons at resting membrane potentials during recovery from inactivation by Slesinger (1991)
10.1523/JNEUROSCI.08-07-02556.1988 / J. Neurosci / Voltage-gated potassium channels in larval CNS neurons of Drosophila by Solc (1988)
10.1126/science.2437657 / Science / Single-channel and genetic analyses reveal two distinct A-type potassium channels in Drosophda by Solc (1987)
10.3109/01677068909066209 / J. Neurogenetics / Altered synaptic transmission in Drosophila Hyperkinetic mutants by Stern (1989)
10.1007/BF00584489 / Pflügers Arch / Three potassium currents in mouse motor nerve terminals by Tabti (1989)
10.1126/science.2426780 / Science / Occult Drosophila calcium channels and twinning of calcium and voltage-activated potassium channels by Wei (1986)
{'key': '2023020216075421900_JEXBIO_170_1_93C63', 'first-page': '311', 'article-title': 'Genetic and pharmacological analyses of potassium channels in Drosophila', 'volume-title': 'In Neurotox ‘88, Molecular Basis of Drug and Pesticide Action', 'author': 'Wu', 'year': '1988'} / In Neurotox ‘88, Molecular Basis of Drug and Pesticide Action / Genetic and pharmacological analyses of potassium channels in Drosophila by Wu (1988)
10.1126/science.6302847 / Science / Potassium currents in Drosophila: different components affected by mutations of two genes by Wu (1983)
10.1073/pnas.75.8.4047 / Proc. natn. Acad. Sci. U.S.A / A Drosophila mutant with a temperature sensitive block in nerve conduction by Wu (1978)
10.1523/JNEUROSCI.05-10-02626.1985 / J. Neurosci / Voltage clamp analysis of membrane currents in larval muscle fibers of Drosophila: Alteration of potassium currents in Shaker mutants by Wu (1985)
10.1242/jeb.147.1.21 / J. exp. Biol / Actions of dendrotoxin on K+ channels and neuromuscular transmission in Drosophila melanogaster, and its effects in synergy with K+ channel-specific drugs and mutations by Wu (1989)
10.1242/jeb.92.1.13 / J. exp. Biol / Voltage clamp studies on insect skeletal muscle. II. The outward currents by Yamamoto (1981)
10.1126/science.1670967 / Science / Altered synaptic plasticity in Drosophila memory mutants with a defective cAMP cascade by Zhong (1991)
10.1126/science.2047864 / Science / Alteration of four identified K+ currents in Drosophila muscle by mutations in eag by Zhong (1991)

Dates

Type	When
Created	4 years, 4 months ago (April 24, 2021, 11:11 p.m.)
Deposited	2 years, 6 months ago (Feb. 2, 2023, 11:10 a.m.)
Indexed	11 months, 3 weeks ago (Sept. 8, 2024, 8:14 a.m.)
Issued	32 years, 11 months ago (Sept. 1, 1992)
Published	32 years, 11 months ago (Sept. 1, 1992)
Published Online	32 years, 11 months ago (Sept. 1, 1992)
Published Print	32 years, 11 months ago (Sept. 1, 1992)

Funders 0

None

BibTeX

@article{Gho_1992, title={Analysis of Repolarization of Presynaptic Motor Terminals in Drosophila Larvae Using Potassium-Channel-Blocking Drugs and Mutations}, volume={170}, ISSN={1477-9145}, url={http://dx.doi.org/10.1242/jeb.170.1.93}, DOI={10.1242/jeb.170.1.93}, number={1}, journal={Journal of Experimental Biology}, publisher={The Company of Biologists}, author={Gho, Michel and Ganetzky, Barry}, year={1992}, month=sep, pages={93–111} }

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      "first-page": "349",
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      "author": "Ashcroft",
      "year": "1982",
      "journal-title": "J. Physiol., Lond"
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      "key": "2023020216075421900_JEXBIO_170_1_93C3",
      "doi-asserted-by": "publisher",
      "first-page": "551",
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      "article-title": "A component of calcium-activated potassium channels encoded by the Drosophila slo locus",
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      "author": "Atkinson",
      "year": "1991",
      "journal-title": "Science"
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      "first-page": "343",
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      "volume": "431",
      "author": "Augustine",
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      "first-page": "163",
      "DOI": "10.1113/jphysiol.1985.sp015819",
      "article-title": "Calcium entry and transmitter release at voltage-clamped nerve terminals of squids",
      "volume": "367",
      "author": "Augustine",
      "year": "1985",
      "journal-title": "J. Physiol., Lond"
    },
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      "first-page": "129",
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      "article-title": "The Drosophila Shaker gene codes for a distinctive K+ current in a subset of neurons",
      "volume": "2",
      "author": "Baker",
      "year": "1990",
      "journal-title": "Neuron"
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      "author": "Benoit",
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      "author": "Hardie",
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      "author": "Johansen",
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      "author": "Komatsu",
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      "volume": "11",
      "author": "Leung",
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      "year": "1989",
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      "author": "Llin\u00e1s",
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      "volume": "73",
      "author": "Llin\u00e1s",
      "year": "1976",
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      "author": "Llin\u00e1s",
      "year": "1981",
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      "volume": "300",
      "author": "MacDermott",
      "year": "1982",
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      "author": "Mallart",
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      "author": "Martin",
      "year": "1955",
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      "volume": "249",
      "author": "Meech",
      "year": "1975",
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      "first-page": "2614",
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      "article-title": "Evidence for two calcium-dependent potassium conductances in lizard motor nerve terminals",
      "volume": "10",
      "author": "Morita",
      "year": "1990",
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    },
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      "article-title": "Evidence for a transient potassium membrane current dependent on calcium influx in crab muscle fibre",
      "volume": "251",
      "author": "Mounier",
      "year": "1975",
      "journal-title": "J. Physiol., Lond"
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      "article-title": "Two fast transient current components during voltage clamp on snail neurones",
      "volume": "58",
      "author": "Neher",
      "year": "1971",
      "journal-title": "J. gen. Physiol"
    },
    {
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      "first-page": "379",
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      "article-title": "Ionic channels in Drosophila",
      "volume": "50",
      "author": "Papazian",
      "year": "1988",
      "journal-title": "A. Rev. Physiol"
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      "first-page": "729",
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      "article-title": "Diversity and ubiquity of K channels",
      "volume": "25",
      "author": "Rudy",
      "year": "1988",
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      "article-title": "The mutation slo alters membrane excitability and Ca-activated K current in cultures Drosophila \u2018giant\u2019 neurons",
      "volume": "281",
      "author": "Saito",
      "year": "1990",
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      "volume": "11",
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      "author": "Salkoff",
      "year": "1983",
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      "article-title": "Development of ion channels in the flight muscles of Drosophila",
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      "year": "1981",
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      "author": "Singh",
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      "author": "Singh",
      "year": "1990",
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      "author": "Slesinger",
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      "author": "Solc",
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      "author": "Stern",
      "year": "1989",
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      "author": "Tabti",
      "year": "1989",
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      "author": "Wei",
      "year": "1986",
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      "author": "Wu",
      "year": "1978",
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      "volume": "5",
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      "volume": "147",
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      "author": "Yamamoto",
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        9,
        1
      ]
    ]
  },
  "references-count": 70,
  "journal-issue": {
    "issue": "1",
    "published-print": {
      "date-parts": [
        [
          1992,
          9,
          1
        ]
      ]
    }
  },
  "URL": "http://dx.doi.org/10.1242/jeb.170.1.93",
  "relation": {},
  "ISSN": [
    "0022-0949",
    "1477-9145"
  ],
  "subject": [],
  "published": {
    "date-parts": [
      [
        1992,
        9,
        1
      ]
    ]
  }
}