Ae4 (Slc4a9) Anion Exchanger Drives Cl- Uptake-dependent Fluid Secretion by Mouse Submandibular Gland Acinar Cells

J Biol Chem. 2015 Apr 24;290(17):10677-88. doi: 10.1074/jbc.M114.612895. Epub 2015 Mar 5.

Abstract

Transcellular Cl(-) movement across acinar cells is the rate-limiting step for salivary gland fluid secretion. Basolateral Nkcc1 Na(+)-K(+)-2Cl(-) cotransporters play a critical role in fluid secretion by promoting the intracellular accumulation of Cl(-) above its equilibrium potential. However, salivation is only partially abolished in the absence of Nkcc1 cotransporter activity, suggesting that another Cl(-) uptake pathway concentrates Cl(-) ions in acinar cells. To identify alternative molecular mechanisms, we studied mice lacking Ae2 and Ae4 Cl(-)/HCO3 (-) exchangers. We found that salivation stimulated by muscarinic and β-adrenergic receptor agonists was normal in the submandibular glands of Ae2(-/-) mice. In contrast, saliva secretion was reduced by 35% in Ae4(-/-) mice. The decrease in salivation was not related to loss of Na(+)-K(+)-2Cl(-) cotransporter or Na(+)/H(+) exchanger activity in Ae4(-/-) mice but correlated with reduced Cl(-) uptake during β-adrenergic receptor activation of cAMP signaling. Direct measurements of Cl(-)/HCO3 (-) exchanger activity revealed that HCO3 (-)-dependent Cl(-) uptake was reduced in the acinar cells of Ae2(-/-) and Ae4(-/-) mice. Moreover, Cl(-)/HCO3 (-) exchanger activity was nearly abolished in double Ae4/Ae2 knock-out mice, suggesting that most of the Cl(-)/HCO3 (-) exchanger activity in submandibular acinar cells depends on Ae2 and Ae4 expression. In conclusion, both Ae2 and Ae4 anion exchangers are functionally expressed in submandibular acinar cells; however, only Ae4 expression appears to be important for cAMP-dependent regulation of fluid secretion.

Keywords: Bicarbonate; Chloride Transport; Epithelium; Exchanger; Salivary Gland; Secretion.

Publication types

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

MeSH terms

  • Acinar Cells / metabolism*
  • Animals
  • Bicarbonates / metabolism
  • Chloride-Bicarbonate Antiporters / deficiency
  • Chloride-Bicarbonate Antiporters / genetics
  • Chloride-Bicarbonate Antiporters / metabolism*
  • Chlorides / metabolism*
  • Cyclic AMP / metabolism
  • Female
  • Ion Transport
  • Male
  • Mice
  • Mice, 129 Strain
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Saliva / metabolism
  • Submandibular Gland / cytology
  • Submandibular Gland / metabolism*

Substances

  • Bicarbonates
  • Chloride-Bicarbonate Antiporters
  • Chlorides
  • Slc4a2 protein, mouse
  • Slc4a9 protein, mouse
  • Cyclic AMP