The glial sodium-potassium-2-chloride cotransporter is required for synaptic transmission in the Drosophila visual system

Drew Stenesen, Andrew T. Moehlman, Jeffrey N. Schellinger, Aylin R Rodan, Helmut Kramer

Research output: Contribution to journalArticle

Abstract

The Drosophila Ncc69 gene encodes a Na + -K + -2Cl -cotransporter (NKCC) that is critical for regulating intra- and extracellular ionic conditions in different tissues. Here, we show that the Ncc69 transporter is necessary for fly vision and that its expression is required non-autonomously in glia to maintain visual synaptic transmission. Flies mutant for Ncc69 exhibit normal photoreceptor depolarization in response to a light pulse but lack the ON and OFF-transients characteristic of postsynaptic responses of lamina neurons, indicating a failure in synaptic transmission. We also find that synaptic transmission requires the Ncc69 regulatory kinases WNK and Fray in glia. The ERG phenotype is associated with a defect in the recycling of the histamine neurotransmitter. Ncc69 mutants exhibit higher levels of the transport metabolite carcinine in lamina cartridges, with its accumulation most intense in the extracellular space. Our work reveals a novel role of glial NKCC transporters in synaptic transmission, possibly through regulating extracellular ionic conditions.

Original languageEnglish (US)
Article number2475
JournalScientific Reports
Volume9
Issue number1
DOIs
StatePublished - Dec 1 2019

Fingerprint

Sodium-Potassium-Chloride Symporters
Synaptic Transmission
Neuroglia
Drosophila
Diptera
Extracellular Space
Recycling
Histamine
Neurotransmitter Agents
Phosphotransferases
Phenotype
Neurons
Light
Genes

ASJC Scopus subject areas

  • General

Cite this

The glial sodium-potassium-2-chloride cotransporter is required for synaptic transmission in the Drosophila visual system. / Stenesen, Drew; Moehlman, Andrew T.; Schellinger, Jeffrey N.; Rodan, Aylin R; Kramer, Helmut.

In: Scientific Reports, Vol. 9, No. 1, 2475, 01.12.2019.

Research output: Contribution to journalArticle

@article{aee70e60c5b34353bb1620b50988e548,
title = "The glial sodium-potassium-2-chloride cotransporter is required for synaptic transmission in the Drosophila visual system",
abstract = "The Drosophila Ncc69 gene encodes a Na + -K + -2Cl − -cotransporter (NKCC) that is critical for regulating intra- and extracellular ionic conditions in different tissues. Here, we show that the Ncc69 transporter is necessary for fly vision and that its expression is required non-autonomously in glia to maintain visual synaptic transmission. Flies mutant for Ncc69 exhibit normal photoreceptor depolarization in response to a light pulse but lack the ON and OFF-transients characteristic of postsynaptic responses of lamina neurons, indicating a failure in synaptic transmission. We also find that synaptic transmission requires the Ncc69 regulatory kinases WNK and Fray in glia. The ERG phenotype is associated with a defect in the recycling of the histamine neurotransmitter. Ncc69 mutants exhibit higher levels of the transport metabolite carcinine in lamina cartridges, with its accumulation most intense in the extracellular space. Our work reveals a novel role of glial NKCC transporters in synaptic transmission, possibly through regulating extracellular ionic conditions.",
author = "Drew Stenesen and Moehlman, {Andrew T.} and Schellinger, {Jeffrey N.} and Rodan, {Aylin R} and Helmut Kramer",
year = "2019",
month = "12",
day = "1",
doi = "10.1038/s41598-019-38850-x",
language = "English (US)",
volume = "9",
journal = "Scientific Reports",
issn = "2045-2322",
publisher = "Nature Publishing Group",
number = "1",

}

TY - JOUR

T1 - The glial sodium-potassium-2-chloride cotransporter is required for synaptic transmission in the Drosophila visual system

AU - Stenesen, Drew

AU - Moehlman, Andrew T.

AU - Schellinger, Jeffrey N.

AU - Rodan, Aylin R

AU - Kramer, Helmut

PY - 2019/12/1

Y1 - 2019/12/1

N2 - The Drosophila Ncc69 gene encodes a Na + -K + -2Cl − -cotransporter (NKCC) that is critical for regulating intra- and extracellular ionic conditions in different tissues. Here, we show that the Ncc69 transporter is necessary for fly vision and that its expression is required non-autonomously in glia to maintain visual synaptic transmission. Flies mutant for Ncc69 exhibit normal photoreceptor depolarization in response to a light pulse but lack the ON and OFF-transients characteristic of postsynaptic responses of lamina neurons, indicating a failure in synaptic transmission. We also find that synaptic transmission requires the Ncc69 regulatory kinases WNK and Fray in glia. The ERG phenotype is associated with a defect in the recycling of the histamine neurotransmitter. Ncc69 mutants exhibit higher levels of the transport metabolite carcinine in lamina cartridges, with its accumulation most intense in the extracellular space. Our work reveals a novel role of glial NKCC transporters in synaptic transmission, possibly through regulating extracellular ionic conditions.

AB - The Drosophila Ncc69 gene encodes a Na + -K + -2Cl − -cotransporter (NKCC) that is critical for regulating intra- and extracellular ionic conditions in different tissues. Here, we show that the Ncc69 transporter is necessary for fly vision and that its expression is required non-autonomously in glia to maintain visual synaptic transmission. Flies mutant for Ncc69 exhibit normal photoreceptor depolarization in response to a light pulse but lack the ON and OFF-transients characteristic of postsynaptic responses of lamina neurons, indicating a failure in synaptic transmission. We also find that synaptic transmission requires the Ncc69 regulatory kinases WNK and Fray in glia. The ERG phenotype is associated with a defect in the recycling of the histamine neurotransmitter. Ncc69 mutants exhibit higher levels of the transport metabolite carcinine in lamina cartridges, with its accumulation most intense in the extracellular space. Our work reveals a novel role of glial NKCC transporters in synaptic transmission, possibly through regulating extracellular ionic conditions.

UR - http://www.scopus.com/inward/record.url?scp=85061966390&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85061966390&partnerID=8YFLogxK

U2 - 10.1038/s41598-019-38850-x

DO - 10.1038/s41598-019-38850-x

M3 - Article

C2 - 30792494

AN - SCOPUS:85061966390

VL - 9

JO - Scientific Reports

JF - Scientific Reports

SN - 2045-2322

IS - 1

M1 - 2475

ER -