Two inwardly rectifying potassium channels, Irk1 and Irk2, play redundant roles in Drosophila renal tubule function

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Abstract

Inwardly rectifying potassium channels play essential roles in renal physiology across phyla. Barium-sensitive K+conductances are found on the basolateral membrane of a variety of insect Malpighian (renal) tubules, includingDrosophila melanogaster. We found that barium decreases the lumen-positive transepithelial potential difference in isolated perfused Drosophila tubules and decreases fluid secretion and transepithelial K+ flux. In those insect species in which it has been studied, transcripts from multiple genes encoding inwardly rectifying K+ channels are expressed in the renal (Malpighian) tubule. In Drosophila melanogaster, this includes transcripts of the Irk1, Irk2, and Irk3genes. The role of each of these gene products in renal tubule function is unknown. We found that simultaneous knockdown of Irk1 and Irk2 in the principal cell of the fly tubule decreases transepithelial K+ flux, with no additive effect of Irk3 knockdown, and decreases barium sensitivity of transepithelial K+ flux by ∼50%. Knockdown of any of the three inwardly rectifying K+ channels individually has no effect, nor does knocking down Irk3 simultaneously withIrk1 or Irk2. Irk1/Irk2 principal cell double-knockdown tubules remain sensitive to the kaliuretic effect of cAMP. Inhibition of the Na+/K+-ATPase with ouabain and Irk1/Irk2 double knockdown have additive effects on K+ flux, and 75% of transepithelial K+ transport is due to Irk1/Irk2 or ouabain-sensitive pathways. In conclusion, Irk1 and Irk2play redundant roles in transepithelial ion transport in the Drosophila melanogaster renal tubule and are additive to Na+/K+-ATPase-dependent pathways.

Original languageEnglish (US)
Pages (from-to)R747-R756
JournalAmerican Journal of Physiology - Regulatory Integrative and Comparative Physiology
Volume309
Issue number7
DOIs
StatePublished - Sep 1 2015

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Inwardly Rectifying Potassium Channel
Drosophila
Kidney
Barium
Malpighian Tubules
Ouabain
Drosophila melanogaster
Insects
Fluids and Secretions
Ion Transport
Diptera
Genes
Membranes

Keywords

  • Barium
  • Dir
  • DKirIII
  • Epithelial ion transport
  • Ion-specific electrode
  • Ir
  • Kir
  • Malpighian tubule
  • Ramsay assay

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)

Cite this

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title = "Two inwardly rectifying potassium channels, Irk1 and Irk2, play redundant roles in Drosophila renal tubule function",
abstract = "Inwardly rectifying potassium channels play essential roles in renal physiology across phyla. Barium-sensitive K+conductances are found on the basolateral membrane of a variety of insect Malpighian (renal) tubules, includingDrosophila melanogaster. We found that barium decreases the lumen-positive transepithelial potential difference in isolated perfused Drosophila tubules and decreases fluid secretion and transepithelial K+ flux. In those insect species in which it has been studied, transcripts from multiple genes encoding inwardly rectifying K+ channels are expressed in the renal (Malpighian) tubule. In Drosophila melanogaster, this includes transcripts of the Irk1, Irk2, and Irk3genes. The role of each of these gene products in renal tubule function is unknown. We found that simultaneous knockdown of Irk1 and Irk2 in the principal cell of the fly tubule decreases transepithelial K+ flux, with no additive effect of Irk3 knockdown, and decreases barium sensitivity of transepithelial K+ flux by ∼50{\%}. Knockdown of any of the three inwardly rectifying K+ channels individually has no effect, nor does knocking down Irk3 simultaneously withIrk1 or Irk2. Irk1/Irk2 principal cell double-knockdown tubules remain sensitive to the kaliuretic effect of cAMP. Inhibition of the Na+/K+-ATPase with ouabain and Irk1/Irk2 double knockdown have additive effects on K+ flux, and 75{\%} of transepithelial K+ transport is due to Irk1/Irk2 or ouabain-sensitive pathways. In conclusion, Irk1 and Irk2play redundant roles in transepithelial ion transport in the Drosophila melanogaster renal tubule and are additive to Na+/K+-ATPase-dependent pathways.",
keywords = "Barium, Dir, DKirIII, Epithelial ion transport, Ion-specific electrode, Ir, Kir, Malpighian tubule, Ramsay assay",
author = "Yipin Wu and Michel Baum and Huang, {Chou Long} and Rodan, {Aylin R.}",
year = "2015",
month = "9",
day = "1",
doi = "10.1152/ajpregu.00148.2015",
language = "English (US)",
volume = "309",
pages = "R747--R756",
journal = "American Journal of Physiology - Heart and Circulatory Physiology",
issn = "0363-6135",
publisher = "American Physiological Society",
number = "7",

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T1 - Two inwardly rectifying potassium channels, Irk1 and Irk2, play redundant roles in Drosophila renal tubule function

AU - Wu, Yipin

AU - Baum, Michel

AU - Huang, Chou Long

AU - Rodan, Aylin R.

PY - 2015/9/1

Y1 - 2015/9/1

N2 - Inwardly rectifying potassium channels play essential roles in renal physiology across phyla. Barium-sensitive K+conductances are found on the basolateral membrane of a variety of insect Malpighian (renal) tubules, includingDrosophila melanogaster. We found that barium decreases the lumen-positive transepithelial potential difference in isolated perfused Drosophila tubules and decreases fluid secretion and transepithelial K+ flux. In those insect species in which it has been studied, transcripts from multiple genes encoding inwardly rectifying K+ channels are expressed in the renal (Malpighian) tubule. In Drosophila melanogaster, this includes transcripts of the Irk1, Irk2, and Irk3genes. The role of each of these gene products in renal tubule function is unknown. We found that simultaneous knockdown of Irk1 and Irk2 in the principal cell of the fly tubule decreases transepithelial K+ flux, with no additive effect of Irk3 knockdown, and decreases barium sensitivity of transepithelial K+ flux by ∼50%. Knockdown of any of the three inwardly rectifying K+ channels individually has no effect, nor does knocking down Irk3 simultaneously withIrk1 or Irk2. Irk1/Irk2 principal cell double-knockdown tubules remain sensitive to the kaliuretic effect of cAMP. Inhibition of the Na+/K+-ATPase with ouabain and Irk1/Irk2 double knockdown have additive effects on K+ flux, and 75% of transepithelial K+ transport is due to Irk1/Irk2 or ouabain-sensitive pathways. In conclusion, Irk1 and Irk2play redundant roles in transepithelial ion transport in the Drosophila melanogaster renal tubule and are additive to Na+/K+-ATPase-dependent pathways.

AB - Inwardly rectifying potassium channels play essential roles in renal physiology across phyla. Barium-sensitive K+conductances are found on the basolateral membrane of a variety of insect Malpighian (renal) tubules, includingDrosophila melanogaster. We found that barium decreases the lumen-positive transepithelial potential difference in isolated perfused Drosophila tubules and decreases fluid secretion and transepithelial K+ flux. In those insect species in which it has been studied, transcripts from multiple genes encoding inwardly rectifying K+ channels are expressed in the renal (Malpighian) tubule. In Drosophila melanogaster, this includes transcripts of the Irk1, Irk2, and Irk3genes. The role of each of these gene products in renal tubule function is unknown. We found that simultaneous knockdown of Irk1 and Irk2 in the principal cell of the fly tubule decreases transepithelial K+ flux, with no additive effect of Irk3 knockdown, and decreases barium sensitivity of transepithelial K+ flux by ∼50%. Knockdown of any of the three inwardly rectifying K+ channels individually has no effect, nor does knocking down Irk3 simultaneously withIrk1 or Irk2. Irk1/Irk2 principal cell double-knockdown tubules remain sensitive to the kaliuretic effect of cAMP. Inhibition of the Na+/K+-ATPase with ouabain and Irk1/Irk2 double knockdown have additive effects on K+ flux, and 75% of transepithelial K+ transport is due to Irk1/Irk2 or ouabain-sensitive pathways. In conclusion, Irk1 and Irk2play redundant roles in transepithelial ion transport in the Drosophila melanogaster renal tubule and are additive to Na+/K+-ATPase-dependent pathways.

KW - Barium

KW - Dir

KW - DKirIII

KW - Epithelial ion transport

KW - Ion-specific electrode

KW - Ir

KW - Kir

KW - Malpighian tubule

KW - Ramsay assay

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U2 - 10.1152/ajpregu.00148.2015

DO - 10.1152/ajpregu.00148.2015

M3 - Article

VL - 309

SP - R747-R756

JO - American Journal of Physiology - Heart and Circulatory Physiology

JF - American Journal of Physiology - Heart and Circulatory Physiology

SN - 0363-6135

IS - 7

ER -