AE2 Cl-/HCO3- exchanger is required for normal cAMP-stimulated anion secretion in murine proximal colon

Am J Physiol Gastrointest Liver Physiol. 2010 Apr;298(4):G493-503. doi: 10.1152/ajpgi.00178.2009. Epub 2010 Jan 28.

Abstract

Anion secretion by colonic epithelium is dependent on apical CFTR-mediated anion conductance and basolateral ion transport. In many tissues, the NKCC1 Na(+)-K(+)-2Cl(-) cotransporter mediates basolateral Cl(-) uptake. However, additional evidence suggests that the AE2 Cl(-)/HCO(3)(-) exchanger, when coupled with the NHE1 Na(+)/H(+) exchanger or a Na(+)-HCO(3)(-) cotransporter (NBC), contributes to HCO(3)(-) and/or Cl(-) uptake. To analyze the secretory functions of AE2 in proximal colon, short-circuit current (I(sc)) responses to cAMP and inhibitors of basolateral anion transporters were measured in muscle-stripped wild-type (WT) and AE2-null (AE2(-/-)) proximal colon. In physiological Ringer, the magnitude of cAMP-stimulated I(sc) was the same in WT and AE2(-/-) colon. However, the I(sc) response in AE2(-/-) colon exhibited increased sensitivity to the NKCC1 inhibitor bumetanide and decreased sensitivity to the distilbene derivative SITS (which inhibits AE2 and some NBCs), indicating that loss of AE2 results in a switch to increased NKCC1-supported anion secretion. Removal of HCO(3)(-) resulted in robust cAMP-stimulated I(sc) in both AE2(-/-) and WT colon that was largely mediated by NKCC1, whereas removal of Cl(-) resulted in sharply decreased cAMP-stimulated I(sc) in AE2(-/-) colon relative to WT controls. Inhibition of NHE1 had no effect on cAMP-stimulated I(sc) in AE2(-/-) colon but caused a switch to NKCC1-supported secretion in WT colon. Thus, in AE2(-/-) colon, Cl(-) secretion supported by basolateral NKCC1 is enhanced, whereas HCO(3)(-) secretion is diminished. These results show that AE2 is a component of the basolateral ion transport mechanisms that support anion secretion in the proximal colon.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • 1-Methyl-3-isobutylxanthine / pharmacology
  • 4-Acetamido-4'-isothiocyanatostilbene-2,2'-disulfonic Acid / pharmacology
  • Acetazolamide / pharmacology
  • Amiloride / analogs & derivatives
  • Amiloride / pharmacology
  • Animals
  • Animals, Newborn
  • Anion Transport Proteins / antagonists & inhibitors
  • Anion Transport Proteins / genetics
  • Anion Transport Proteins / metabolism*
  • Anions / metabolism*
  • Antiporters / antagonists & inhibitors
  • Antiporters / genetics
  • Antiporters / metabolism*
  • Bicarbonates / metabolism
  • Bumetanide / pharmacology
  • Carbonic Anhydrase II / genetics
  • Carbonic Anhydrase II / metabolism
  • Carbonic Anhydrase III / genetics
  • Carbonic Anhydrase III / metabolism
  • Carbonic Anhydrase Inhibitors / pharmacology
  • Carbonic Anhydrases / genetics
  • Carbonic Anhydrases / metabolism
  • Cation Transport Proteins / antagonists & inhibitors
  • Cation Transport Proteins / metabolism
  • Cecum / pathology
  • Chlorides / metabolism
  • Colforsin / pharmacology
  • Colon / drug effects
  • Colon / metabolism*
  • Colon / pathology
  • Cyclic AMP / physiology*
  • Electrophysiological Phenomena
  • Gene Expression / genetics
  • Ion Channels / genetics
  • Ion Pumps / genetics
  • Mice
  • Mice, Inbred Strains
  • Mice, Knockout
  • SLC4A Proteins
  • Sodium-Hydrogen Exchanger 1
  • Sodium-Hydrogen Exchangers / antagonists & inhibitors
  • Sodium-Hydrogen Exchangers / metabolism
  • Sodium-Potassium-Chloride Symporters / drug effects
  • Sodium-Potassium-Chloride Symporters / metabolism
  • Solute Carrier Family 12, Member 2

Substances

  • Anion Transport Proteins
  • Anions
  • Antiporters
  • Bicarbonates
  • Carbonic Anhydrase Inhibitors
  • Cation Transport Proteins
  • Chlorides
  • Ion Channels
  • Ion Pumps
  • SLC4A Proteins
  • Slc12a2 protein, mouse
  • Slc4a3 protein, mouse
  • Slc9a1 protein, mouse
  • Sodium-Hydrogen Exchanger 1
  • Sodium-Hydrogen Exchangers
  • Sodium-Potassium-Chloride Symporters
  • Solute Carrier Family 12, Member 2
  • Bumetanide
  • Colforsin
  • 4-Acetamido-4'-isothiocyanatostilbene-2,2'-disulfonic Acid
  • Amiloride
  • Cyclic AMP
  • Carbonic Anhydrase II
  • Carbonic Anhydrase III
  • Carbonic Anhydrases
  • Acetazolamide
  • 1-Methyl-3-isobutylxanthine
  • ethylisopropylamiloride