Hyperaldosteronism after decreased renal K+ excretion in KCNMB2 knockout mice

Am J Physiol Renal Physiol. 2016 May 15;310(10):F1035-46. doi: 10.1152/ajprenal.00010.2016. Epub 2016 Mar 9.

Abstract

The kidney is the primary organ ensuring K(+) homeostasis. K(+) is secreted into the urine in the distal tubule by two mechanisms: by the renal outer medullary K(+) channel (Kir1.1) and by the Ca(2+)-activated K(+) channel (KCa1.1). Here, we report a novel knockout mouse of the β2-subunit of the KCa1.1 channel (KCNMB2), which displays hyperaldosteronism after decreased renal K(+) excretion. KCNMB2(-/-) mice displayed hyperaldosteronism, normal plasma K(+) concentration, and produced dilute urine with decreased K(+) concentration. The normokalemia indicated that hyperaldosteronism did not result from primary aldosteronism. Activation of the renin-angiotensin-aldosterone system was also ruled out as renal renin mRNA expression was reduced in KCNMB2(-/-) mice. Renal K(+) excretion rates were similar in the two genotypes; however, KCNMB2(-/-) mice required elevated plasma aldosterone to achieve K(+) balance. Blockade of the mineralocorticoid receptor with eplerenone triggered mild hyperkalemia and unmasked reduced renal K(+) excretion in KCNMB2(-/-) mice. Knockout mice for the α-subunit of the KCa1.1 channel (KCNMA1(-/-) mice) have hyperaldosteronism, are hypertensive, and lack flow-induced K(+) secretion. KCNMB2(-/-) mice share the phenotypic traits of normokalemia and hyperaldosteronism with KCNMA1(-/-) mice but were normotensive and displayed intact flow-induced K(+) secretion. Despite elevated plasma aldosterone, KNCMB2(-/-) mice did not display salt-sensitive hypertension and were able to decrease plasma aldosterone on a high-Na(+) diet, although plasma aldosterone remained elevated in KCNMB2(-/-) mice. In summary, KCNMB2(-/-) mice have a reduced ability to excrete K(+) into the urine but achieve K(+) balance through an aldosterone-mediated, β2-independent mechanism. The phenotype of KCNMB2 mice was similar but milder than the phenotype of KCNMA1(-/-) mice.

Keywords: KCa1.1 channel; potassium excretion; α-subunit of the KCa1.1 channel; β2-subunit.

MeSH terms

  • Aldosterone / blood
  • Animals
  • Blood Pressure
  • Epithelial Sodium Channels / metabolism
  • Eplerenone
  • Female
  • Hyperaldosteronism / etiology*
  • Kidney / metabolism*
  • Large-Conductance Calcium-Activated Potassium Channel beta Subunits / deficiency*
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Polyuria / etiology
  • Potassium / urine*
  • Sodium, Dietary / administration & dosage
  • Solute Carrier Family 12, Member 3 / metabolism
  • Spironolactone / analogs & derivatives

Substances

  • Epithelial Sodium Channels
  • Kcnmb2 protein, mouse
  • Large-Conductance Calcium-Activated Potassium Channel beta Subunits
  • Sodium, Dietary
  • Solute Carrier Family 12, Member 3
  • Spironolactone
  • Aldosterone
  • Eplerenone
  • Potassium