Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut.
2009
SUMMARY There is a resurgence of interest in the Drosophila midgut on
account of its potential value in understanding the structure, development and
function of digestive organs and related epithelia. The recent identification
of regenerative or stem cells in the adult gut of Drosophila has
opened up new avenues for understanding development and turnover of cells in
insect and mammalian gastrointestinal tracts. Conversely, the physiology of
the Drosophila gut is less well understood as it is a difficult
epithelial preparation to study under controlled conditions. Recent progress
in microperfusion of individual segments of the Drosophila midgut, in
both larval and adult forms, has enabled ultrastructural and
electrophysiological study and preliminary characterization of cellular
transport processes in the epithelium. As larvae are more active feeders, the
transport rates are higher than in adults. The larval midgut has at least
three segments: an anterior neutral zone, a short and narrow acid-secreting
middle segment and a long and wider posterior segment (which is the best
studied) that secretes base (probably HCO 3 – ) into
the lumen. The posterior midgut has a lumen-negative transepithelial potential
(35–45 mV) and a high resistance (800–1400 Ω.cm 2 )
that correlates with little or no lateral intercellular volume. The primary
transport system driving base secretion into the lumen appears to be a
bafilomycin-A 1 -sensitive, electrogenic H + V-ATPase
located on the basal membrane, which extrudes acid into the haemolymph, as
inferred from the extracellular pH gradients detected adjacent to the basal
membrane. The adult midgut is also segmented (as inferred from longitudinal
gradients of pH dye-indicators in the lumen) into anterior, middle and
posterior regions. The anterior segment is probably absorptive. The middle
midgut secretes acid (pH<4.0), a process dependent on a
carbonic-anhydrase-catalysed H + pool. Cells of the middle segment
are alternately absorptive (apically amplified by ≈9-fold, basally
amplified by >90-fold) and secretory (apically amplified by >90-fold and
basally by ≈10-fold). Posterior segment cells have an extensively dilated
basal extracellular labyrinth, with a volume larger than that of anterior
segment cells, indicating more fluid reabsorption in the posterior segment.
The luminal pH of anterior and posterior adult midgut is 7–9. These
findings in the larval and adult midgut open up the possibility of determining
the role of plasma membrane transporters and channels involved in driving not
only H + fluxes but also secondary fluxes of other solutes and water
in Drosophila .
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