Potassium conservation is impaired in mice with reduced renal expression of Kir4.1

Am J Physiol Renal Physiol. 2018 Nov 1;315(5):F1271-F1282. doi: 10.1152/ajprenal.00022.2018. Epub 2018 Aug 15.

Abstract

To better understand the role of the inward-rectifying K channel Kir4.1 (KCNJ10) in the distal nephron, we initially studied a global Kir4.1 knockout mouse (gKO), which demonstrated the hypokalemia and hypomagnesemia seen in SeSAME/EAST syndrome and was associated with reduced Na/Cl cotransporter (NCC) expression. Lethality by ~3 wk, however, limits the usefulness of this model, so we developed a kidney-specific Kir4.1 "knockdown" mouse (ksKD) using a cadherin 16 promoter and Cre-loxP methodology. These mice appeared normal and survived to adulthood. Kir4.1 protein expression was decreased ~50% vs. wild-type (WT) mice by immunoblotting, and immunofluorescence showed moderately reduced Kir4.1 staining in distal convoluted tubule that was minimal or absent in connecting tubule and cortical collecting duct. Under control conditions, the ksKD mice showed metabolic alkalosis and relative hypercalcemia but were normokalemic and mildly hypermagnesemic despite decreased NCC expression. In addition, the mice had a severe urinary concentrating defect associated with hypernatremia, enlarged kidneys with tubulocystic dilations, and reduced aquaporin-3 expression. On a K/Mg-free diet for 1 wk, however, ksKD mice showed marked hypokalemia (serum K: 1.5 ± 0.1 vs. 3.0 ± 0.1 mEq/l for WT), which was associated with renal K wasting (transtubular K gradient: 11.4 ± 0.8 vs. 1.6 ± 0.4 in WT). Phosphorylated-NCC expression increased in WT but not ksKD mice on the K/Mg-free diet, suggesting that loss of NCC adaptation underlies the hypokalemia. In conclusion, even modest reduction in Kir4.1 expression results in impaired K conservation, which appears to be mediated by reduced expression of activated NCC.

Keywords: basolateral renal transport; low-potassium diet; potassium adaptation; potassium channelopathy; renal potassium channels.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Alkalosis / blood
  • Alkalosis / genetics
  • Alkalosis / physiopathology
  • Animals
  • Aquaporin 3 / metabolism
  • Gene Knockdown Techniques
  • Genotype
  • Hypercalcemia / blood
  • Hypercalcemia / genetics
  • Hypercalcemia / physiopathology
  • Hyperkalemia / blood
  • Hyperkalemia / genetics
  • Hyperkalemia / physiopathology
  • Hypernatremia / blood
  • Hypernatremia / genetics
  • Hypernatremia / physiopathology
  • Kidney Concentrating Ability
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Nephrons / metabolism*
  • Nephrons / physiopathology
  • Phenotype
  • Phosphorylation
  • Potassium Channels, Inwardly Rectifying / deficiency*
  • Potassium Channels, Inwardly Rectifying / genetics
  • Potassium, Dietary / blood*
  • Renal Reabsorption*
  • Solute Carrier Family 12, Member 3 / metabolism

Substances

  • Aqp3 protein, mouse
  • Kcnj10 (channel)
  • Potassium Channels, Inwardly Rectifying
  • Potassium, Dietary
  • Slc12a3 protein, mouse
  • Solute Carrier Family 12, Member 3
  • Aquaporin 3