Aldosterone responsiveness of the epithelial sodium channel (ENaC) in colon is increased in a mouse model for Liddle's syndrome

J Physiol. 2008 Jan 15;586(2):459-75. doi: 10.1113/jphysiol.2007.140459. Epub 2007 Nov 15.

Abstract

Liddle's syndrome is an autosomal dominant form of human hypertension, caused by gain-of-function mutations of the epithelial sodium channel (ENaC) which is expressed in aldosterone target tissues including the distal colon. We used a mouse model for Liddle's syndrome to investigate ENaC-mediated Na+ transport in late distal colon by measuring the amiloride-sensitive transepithelial short circuit current (Delta I SC-Ami) ex vivo. In Liddle mice maintained on a standard salt diet, Delta I SC-Ami was only slightly increased but plasma aldosterone (P Aldo) was severely suppressed. Liddle mice responded to a low or a high salt diet by increasing or decreasing, respectively, their P Aldo and Delta I SC-Ami. However, less aldosterone was required in Liddle animals to achieve similar or even higher Na+ transport rates than wild-type animals. Indeed, the ability of aldosterone to stimulate Delta I SC-Ami was about threefold higher in Liddle animals than in the wild-type controls. Application of aldosterone to colon tissue in vitro confirmed that ENaC stimulation by aldosterone was not only preserved but enhanced in Liddle mice. Aldosterone-induced transcriptional up-regulation of the channel's beta- and gamma-subunit (beta ENaC and gamma ENaC) and of the serum- and glucocorticoid-inducible kinase 1 (SGK1) was similar in colon tissue from Liddle and wild-type animals, while aldosterone had no transcriptional effect on the alpha-subunit (alpha ENaC). Moreover, Na+ feedback regulation was largely preserved in colon tissue of Liddle animals. In conclusion, we have demonstrated that in the colon of Liddle mice, ENaC-mediated Na+ transport is enhanced with an increased responsiveness to aldosterone. This may be pathophysiologically relevant in patients with Liddle's syndrome, in particular on a high salt diet, when suppression of P Aldo is likely to be insufficient to reduce Na+ absorption to an appropriate level.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aldosterone / blood*
  • Aldosterone / physiology
  • Animals
  • Colon / metabolism*
  • Disease Models, Animal
  • Epithelial Sodium Channels / genetics
  • Epithelial Sodium Channels / metabolism*
  • Female
  • Hypertension / genetics
  • Hypertension / metabolism*
  • Hypokalemia / genetics
  • Hypokalemia / metabolism*
  • Immediate-Early Proteins / metabolism
  • Kidney / metabolism
  • Lung / metabolism
  • Male
  • Mice
  • Mice, Mutant Strains
  • Protein Serine-Threonine Kinases / metabolism
  • Renin / blood*
  • Renin / genetics
  • Sodium, Dietary / pharmacology*
  • Syndrome

Substances

  • Epithelial Sodium Channels
  • Immediate-Early Proteins
  • Sodium, Dietary
  • Aldosterone
  • Protein Serine-Threonine Kinases
  • serum-glucocorticoid regulated kinase
  • Renin