A Mathematical Model of the Pancreatic Ductal Epithelium
Y. Sohma
1,
*, M.A. Gray
1
, Y. Imai
2
, B.E. Argent
1
1
Department of Physiological Sciences, University Medical School, Framlington Place, Newcastle upon Tyne NE2 4HH, UK
2
Department of Physiology, Osaka Medical College, Takatsuki Osaka 569, Japan
Received: 18 October 1995/Revised: 5 July 1996
Abstract. A mathematical model of the HCO
3
-
-secreting
pancreatic ductal epithelium was developed using net-
work thermodynamics. With a minimal set of assump-
tions, the model accurately reproduced the experimen-
tally measured membrane potentials, voltage divider ra-
tio, transepithelial resistance and short-circuit current of
nonstimulated ducts that were microperfused and bathed
with a CO
2
/HCO
3
-
-free, HEPES-buffered solution, and
also the intracellular pH of duct cells bathed in a CO
2
/
HCO
3
-
-buffered solution. The model also accurately
simulated: (i) the effect of step changes in basolateral K
+
concentration, and the effect of K
+
channel blockers on
basolateral membrane potential; (ii) the intracellular
acidification caused by a Na
+
-free extracellular solution
and the effect of amiloride on this acidification; and (iii)
the intracellular alkalinization caused by a Cl
-
-free ex-
tracellular solution and the effect of DIDS on this alka-
linization. In addition, the model predicted that the lu-
minal Cl
-
conductance plays a key role in controlling
both the HCO
3
-
secretory rate and intracellular pH during
HCO
3
-
secretion. We believe that the model will be help-
ful in the analysis of experimental data and improve our
understanding of HCO
3
-
-transporting mechanisms in pan-
creatic duct cells.
Key words: Pancreatic duct — Mathematical model —
HCO
3
-
secretion — Intracellular pH regulation — Cystic
fibrosis transmembrane conductance regulator
Introduction
The ductal epithelial cells of the pancreas form a network
of branching tubules whose function is to convey diges-
tive enzymes (secreted by the acinar cells) into the in-
testine [3, 5]. However, the ducts are not merely passive
conduits but also secrete an alkaline fluid, rich in
NaHCO
3
, which washes the digestive enzymes down the
ductal tree and also partially neutralizes acid chyme en-
tering the duodenum from the stomach. The maximum
concentration of HCO
3
-
found in pancreatic juice depends
on the species, and varies between about 70 mM in the rat
and 145 mM in cat, dog and humans [3, 5].
The ductal tree forms only a small proportion of the
pancreatic mass (2 to 14% depending on species, [3]),
and this virtually precludes the direct study of duct cell
function in situ. However, in the 1980s a number of
groups developed techniques for the isolation of small
interlobular and intralobular pancreatic ducts (which are
probably the main site of HCO
3
-
secretion [3]), and have
used electrophysiological and spectrofluorometric tech-
niques to study the cellular mechanism of HCO
3
-
secre-
tion [9, 23, 24, 38]. As a result of these studies, most of
which have been performed on ducts isolated from the
rat pancreas, the HCO
3
-
secretory model shown in Fig. 1
has been proposed [9, 23, 24]. In brief, the initial step in
HCO
3
-
transport is thought to be diffusion of CO
2
into the
duct cell and its hydration to carbonic acid by carbonic
anhydrase. The carbonic acid then dissociates into H
+
and HCO
3
-
ions and the proton is translocated back across
the basolateral membrane on a Na
+
/H
+
exchanger. Ef-
fectively, this is the active transport step for HCO
3
-
, with
the energy being provided by the Na
+
gradient estab-
lished by the Na
+
/K
+
ATPase. Once accumulated inside
the duct cell, the HCO
3
-
ion is then secreted across the
apical membrane on a Cl
-
/HCO
3
-
exchanger. The rate at
which these exchangers cycle is thought to be controlled
by the opening of Cl
-
channels on the apical plasma
membrane. To date, cyclic AMP-activated, cystic fibro-
sis transmembrane conductance regulator (CFTR) Cl
-
channels, and Ca
2+
-activated Cl
-
channels have been
identified on the apical plasma membrane of the duct
Correspondence to: B.E. Argent
* Present address: Department of Physiology, Osaka Medical College,
Takatsuki Osaka 569, Japan
J. Membrane Biol. 154, 53–67 (1996) The Journal of
Membrane
Biology
© Springer-Verlag New York Inc. 1996