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Am J Physiol Cell Physiol 281: C633-C648, 2001;
0363-6143/01 $5.00
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Vol. 281, Issue 2, C633-C648, August 2001

ENaC- and CFTR-dependent ion and fluid transport in mammary epithelia

Sasha Blaug1,2, Kevin Hybiske1, Jonathan Cohn3, Gary L. Firestone1, Terry E. Machen1, and Sheldon S. Miller1,2

1 Department of Molecular and Cell Biology and 2 School of Optometry, University of California, Berkeley, California 94720-3200; and 3 Departments of Medicine and Cell Biology, Duke University Medical Center, Durham, North Carolina 27710-0001

Mammary epithelial 31EG4 cells (MEC) were grown as monolayers on filters to analyze the apical membrane mechanisms that help mediate ion and fluid transport across the epithelium. RT-PCR showed the presence of cystic fibrosis transmembrane conductance regulator (CFTR) and epithelial Na+ channel (ENaC) message, and immunomicroscopy showed apical membrane staining for both proteins. CFTR was also localized to the apical membrane of native human mammary duct epithelium. In control conditions, mean values of transepithelial potential (apical-side negative) and resistance (RT) are -5.9 mV and 829 Omega  · cm2, respectively. The apical membrane potential (VA) is -40.7 mV, and the mean ratio of apical to basolateral membrane resistance (RA/RB) is 2.8. Apical amiloride hyperpolarized VA by 19.7 mV and tripled RA/RB. A cAMP-elevating cocktail depolarized VA by 17.6 mV, decreased RA/RB by 60%, increased short-circuit current by 6 µA/cm2, decreased RT by 155 Omega  · cm2, and largely eliminated responses to amiloride. Whole cell patch-clamp measurements demonstrated amiloride-inhibited Na+ currents [linear current-voltage (I-V) relation] and forskolin-stimulated Cl- currents (linear I-V relation). A capacitance probe method showed that in the control state, MEC monolayers either absorbed or secreted fluid (2-4 µl · cm-2 · h-1). Fluid secretion was stimulated either by activating CFTR (cAMP) or blocking ENaC (amiloride). These data plus equivalent circuit analysis showed that 1) fluid absorption across MEC is mediated by Na+ transport via apical membrane ENaC, and fluid secretion is mediated, in part, by Cl- transport via apical CFTR; 2) in both cases, appropriate counterions move through tight junctions to maintain electroneutrality; and 3) interactions among CFTR, ENaC, and tight junctions allow MEC to either absorb or secrete fluid and, in situ, may help control luminal [Na+] and [Cl-].

amiloride; diphenylamine-2-carboxylate; milk secretion; patch clamp; microelectrodes; electrophysiology; cystic fibrosis; tight junctions; leaky and tight epithelia; epithelial sodium channel; cystic fibrosis transmembrane conductance regulator


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