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First published online May 15, 2009
Journal of Experimental Biology 212, 1731-1744 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.029306
Review Article |
Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut
Tata Institute of Fundamental Research, Colaba, Mumbai 400 005, India
* Author for correspondence (e-mail: tripathi{at}tifr.res.in)
Accepted 16 March 2009
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Summary |
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 TOP Summary IntroductionStructure of midgut regionsBidirectional transport in...References |
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.cm2)
that correlates with little or no lateral intercellular volume. The primary
transport system driving base secretion into the lumen appears to be a
bafilomycin-A1-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.
Key words: stereology, microperfusion, H+ V-ATPase, carbonic anhydrase, ion-selective microelectrodes, SIET, H+ gradients, surface pH
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Introduction |
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TOPSummaryIntroductionStructure of midgut regionsBidirectional transport in...References |
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;
Dow et al., 1997;
Dow and Davies, 2001;
Maddrell and O'Donnell, 1992;
O'Donnell and Spring, 2000),
the midgut and hindgut of most species have not been as amenable to study,
possibly on account of their musculature.
Insect organs such as the midgut are appealing as the epithelium is
single-layered and the number and type of cells are limited. This permits
in vitro physiological studies with excellent control of key
variables: (1) solution composition at the apical or basal surfaces with
minimum diffusion barriers, (2) hydrostatic pressure, particularly across the
intercellular septa or tight-junctions, and (3) electrical potential
(Tripathi and Boulpaep, 1989).
Furthermore, the cells should be accessible with conventional and
ion-selective microelectrodes, which permit evaluation of the cellular
handling of ingested primary electrolytes such as K+,
Na+, H+, Cl–,
HCO3–, and possible organic substrates
co-transported with these ions, and also patch-clamp and fluorescence studies
of the cytosol. Combined with other studies such as imaging of transparent gut
structures with pH-indicator dyes, localization of membrane transport proteins
with fluorescent-labelled antibodies, and scanning of extracellular fluid
adjacent to individual cells for ion gradients (the SIET technique), it is
possible to get valuable information on the functional organization of the
gut, its developmental changes and its ultrastructural design
(Boudko et al., 2001a;
Onken et al., 2006).
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; Cioffi,
1979; Clements,
1992; Dow, 1984;
Dow, 1986;
Dow and Peacock, 1989;
Lehane and Billingsley, 1996;
Moffett and Cummings, 1994;
Okech et al., 2008;
Onken et al., 2008;
Patrick et al., 2006;
Smith et al., 2007;
Smith et al., 2008;
Volkmann and Peters, 1989a;
Volkmann and Peters, 1989b;
Zhuang et al., 1999). These
studies have revealed large longitudinal gradients of pH along the length of
the gut. However, the cellular basis of generation of these gradients and
their biological significance is not completely understood, with several
competing models proposed. It is therefore of interest to know if the midgut
of Drosophila, given its potential in genomics, provides an
opportunity for testing these hypotheses.
Despite the wealth of data that has made Drosophila an invaluable
model system for studying development of structure and function of organ
systems, there have been few studies on the structure
(Dimitriadis, 1991;
Dimitriadis and Kastritsis,
1984; Filshie et al.,
1971; Gartner,
1985) and function (Romero et
al., 2000; Sciortino et al.,
2001) of the gut. The recent resurgence of interest in the
structure and function of Drosophila midgut has coincidentally
occurred on two fronts. Microperfusion of the midgut and stereological
analysis of ultrastructure under controlled conditions
(Shanbhag and Tripathi, 2005)
has enabled description of the transport properties of the epithelium and
analysis of the cellular basis of generation of axial H+ gradients
in different segments. The identification of stem cells in adult midgut and
hindgut segments (Lin et al.,
2008; Micchelli and Perrimon,
2006; Ohlstein and Spradling,
2006; Takashima et al.,
2008) has shown that Drosophila midgut epithelial
development and maintenance is analogous to mammalian intestinal crypt
development. In this review, we focus on the structural specialization of the
epithelium of various regions of the midgut and the mechanisms of
acid–base transport by this epithelium in larval and adult stages.
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Structure of midgut regions |
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TOPSummaryIntroductionStructure of midgut regionsBidirectional transport in...References |
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).
Gartner (Gartner, 1985)
attempted the first stereological analysis of the anterior part of the adult
epithelium and observed the presence of regenerative cells and the primary
epithelial cells of the anterior midgut only, concluding that these were the
only two cell types lining the epithelium. Dimitriadis and Kastritsis
(Dimitriadis and Kastritsis,
1984; Dimitriadis,
1991), however, analysed the entire midgut in detail and
identified at least three specialized regions of the midgut and made the first
attempts to correlate the structure of the individual segments and cell types
with function. The identification of the middle segment as an acid-secreting
part has been verified and has invited immediate comparison with mammalian
epithelia, particularly the gastric epithelium containing parietal cells
(Baumann, 2001;
Dubreuil, 2004;
Dubreuil et al., 1998;
Dubreuil et al., 2001;
Yao and Forte, 2003).
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),
allowing stereological analysis of epithelial geometry simultaneously with
physiological studies. Fig. 1
shows the basic organization of the midgut into at least three separate parts:
an anterior near-neutral part, a strongly acidic middle segment and a third
zone of increasing alkalinity. The posterior midgut epithelium has been best
studied, but in principle all segments are amenable to perfusion studies. The
epithelium is tight because of long septa between cells
(Fig. 2A). Notable among its
properties is the amplification of the apical and basal membranes
(Fig. 3A,B,C,
Table 1). The value of
ultrastructure is further shown in its sensitivity in detecting changes
produced by physiological manoeuvres such as Na+ replacement, which
can produce massive and irreversible loss of plasma membrane
(Fig. 3D–I), particularly
when done on the basal side. The apical and basal membranes have
portasome-like particles (Fig.
2D,E, inset) indicative of H+ V-ATPase location on both
membranes.
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Adult midgut
The adult midgut is segmented into anterior, middle and posterior regions
(Fig. 4). The basic membrane
areas and volumes of the anterior and posterior midgut of the adult epithelium
(Table 2) reveal that their
transport role is modest and correlate with smaller pH gradients. The anterior
segment is probably absorptive and confirms the basic observations of Gartner
(Gartner, 1985) pertaining to
the anterior midgut only but also reveals that there is a degree of variation
of the anterior gut along its length (Fig.
4B,C, Fig. 5,
Fig. 6). Posterior segment
cells (Fig. 4E,
Fig. 7) 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 (Tripathi and Boulpaep,
1989). Much less is known of the role of this epithelium in
adults, which requires further study in both ultrastructure and
physiology.
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The middle adult acidic segment (Fig.
4D; Figs 8,
9,
10) has attracted a good deal
of attention for its striking architecture, with alternate cells `facing'
opposite directions. It would be appropriate to refer to them as secretory and
absorptive cells on account of the great asymmetry of their apical and basal
membranes (Fig. 8D–H).
Cells of the middle segment are alternately absorptive (apically amplified
9-fold, basally >90-fold) and secretory (apically amplified by
>90-fold and basally 10-fold). The terminology suggested is based on
the direction of net transport predicted on areal considerations alone.
Table 3 shows that the apical
and basal membranes of these two cell types are amplified more than 100-fold
in either direction; their back-to-back geometry predicts significant
recycling of solutes and water and provides a structural basis for
bidirectional transport. The function of the secretory cells, composition of
the secreted contents, regulation of secretion, and membrane turnover are
still not clear, despite many studies
(Lehane and Billingsley, 1996;
Yao and Forte, 2003). The
apical membranes form a cavity that can be seen spontaneously in either `open'
or `closed' configuration (Figs
9 and
10) discharging membrane-bound
granular material.
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Bidirectional transport in individual regions |
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TOPSummaryIntroductionStructure of midgut regionsBidirectional transport in...References |
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;
Shanbhag and Tripathi, 2008)
(Figs 11,
12). Similar gradients have
been seen in a wide variety of insect midgut epithelia
(Dadd, 1975;
Boudko et al., 2001b;
Corena et al., 2002;
Dow, 1986;
Moffett and Cummings, 1994;
Onken et al., 2008;
Zhuang et al., 1999).
Regardless of the direction of secretion of acid or base, the energetics of
transport in insect epithelia is believed to be primarily driven by vacuolar
or H+ V-ATPases in the Malpighian tubule and also the midgut
(Beyenbach, 2001;
Dow and Davies, 2001). The
fluxes of other electrolytes have been proposed to be driven as secondary
transport processes. Furthermore, it is also possible that many of the
membrane transporters in insects could be isoforms of mammalian transporters
that do not bind inhibitors or agonists as they do in mammals. In the
posterior larval midgut of Drosophila, a variety of inhibitors had no
effect on transport that was still sensitive to bafilomycin-A1
(Shanbhag and Tripathi,
2005).
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;
Corena et al., 2005;
Ridgway and Moffett, 1986;
Seron et al., 2004). The
location of this pool is a subject of active study as many enzymes are
glycosylphosphatidylinositol-anchored and it is possible to localize these
pools to either intracellular or extracellular or both compartments. Strong CA
activity was localized at the apical membranes of goblet cells in the anterior
and middle midgut region of Manduca sexta that is associated with the
lumen alkalinization, but no CA activity was found in the posterior midgut
goblet cells. Lepidopteran midgut is also divided into regions that show a
substantial degree of structural and functional differentiation
(Ridgway and Moffett,
1986).
The localization of CA in the Drosophila midgut has not yet been
achieved, but there are several interesting approaches that can be tried.
Corena et al. have localized CA in the mosquito midgut
(Corena et al., 2004), and a
similar approach with membrane permeant and impermeant inhibitor would be a
valuable approach. The removal of the peritrophic membrane by microperfusion
improves access of the luminal perfusate to the apical membrane. It is
possible that the in vivo conditions of the peritrophic space may be
altered in terms of enzymes like CA that are located there
(Smith et al., 2007), but
there is good reason to assume that the intracellular enzyme-catalysed
H+ pool is intact in perfused midguts, as shown below. As the
ectoperitrophic space is a likely candidate for such a location, it would be
important to verify this localization with antibodies to CA9 in both perfused
and unperfused preparations where the peritrophic membrane is intact
(Fig. 2C). The dissipation of
the acid gradient by inhibition of CA with acetazolamide
(Shanbhag and Tripathi, 2008)
is easily detected on pH paper (Fig.
11D,E). However, the effects of inhibition of CA involved in base
secretion in the posterior midgut are not easily detected by this simple
method. One then has to rely on a more sensitive method (e.g. ion-selective
microelectrodes) to detect acid or base fluxes. Such an approach is shown in
Fig. 13.
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;
O'Donnell et al., 1996;
Wieczorek et al., 1999;
Wieczorek et al., 2003). One
line of evidence for a basal location of the ATPase in the Drosophila
posterior midgut (Shanbhag and Tripathi,
2005), where the lumen is strongly alkaline, is the presence of
portasome-like structures in the BEL (Fig.
2E, inset). The intracellular pH being more alkaline than the BEL
or unstirred layer of the bath (Fig.
13A) provides even stronger evidence for the predominantly basal
location of the H+ V-ATPase. Thirdly, sensitivity to bafilomycin is
also greater in this preparation from the bath side, with hardly any effect
detected from the lumen. Thus, one can measure acid extrusion rates from the
basal side (Fig. 13B), and see
its reversible inhibition by acetazolamide, even without the peritrophic
membrane (from the lumen or bath) and bafilomycin (from the bath only).
Adult midgut
Perfusion of each midgut region is important to know the overall driving
forces for ions in each segment. Representative traces for three adult
segments are shown in Fig. 14
along with basic membrane potential data under free-flow conditions in control
Ringer and taking into account the fact that the ends of the segments are
damaged but electrically isolating the lumen from the bath. The anterior
region has a low transepithelial potential; the middle and posterior segments
have a transepithelial potential whose polarity favours net H+
flux, which can occur passively for the observed gradients. Therefore, primary
and secondary active transport processes have to be independently tested in
these segments along with a complete characterization of all electrochemical
driving forces and passive properties of individual cell membranes and the
paracellular pathway. Whereas the larval gut has a predominant H+
V-ATPase as primary transporter, the situation in the adult is far from
clear.
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Microperfusion and electrophysiological approaches have given us new tools
to investigate membrane transport processes in an important genomic organism
with many characterized mutations, e.g. labial
(Dubreuil et al., 1998), where
individual cuprophilic cells may be absent. For a complete understanding of
the role of pH gradients in the Drosophila gut, experiments need to
be designed to supplement the approach shown here with newer techniques. For
instance, it is still not clear how base is secreted across the apical
membranes in the posterior midgut in either larva or adult. It would be of
interest to examine whether transporters like NDAE1
(Romero et al., 2000;
Sciortino et al., 2001) are
involved in the exit of base in the posterior midgut. Likewise, the transport
of other electrolytes and osmolytes needs clarification, as it is very likely
to be linked to the transport of acid and base in this epithelium. The
approach shown here can contribute to this end.
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Footnotes |
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References |
|---|
|
TOPSummaryIntroductionStructure of midgut regionsBidirectional transport in...References |
|---|
Anderson, E. and Harvey, W. R. (1966). Active
transport by the Cecropia midgut. II. Fine structure of the midgut
epithelium. J. Cell Biol.
31,107
-134.
Baumann, O. (2001). Posterior midgut epithelial cells differ in their organization of the membrane skeleton from other Drosophila epithelia. Exp. Cell Res. 270,176 -187.[CrossRef][Medline]
Beyenbach, K. W. (2001). Energizing epithelial
transport with the vacuolar H+-ATPase. News Physiol.
Sci. 16,145
-151.
Beyenbach, K. W., Pannabecker, T. L. and Nagel, W. (2000). Central role of the apical membrane H+-ATPase in electrogenesis and epithelial transport in Malpighian tubules. J. Exp. Biol. 203,1459 -1468.[Abstract]
Boudko, D. Y., Moroz, L. L., Linser, P. J., Trimarchi, J. R., Smith, P. J. S. and Harvey, W. R. (2001a). In situ analysis of pH gradients in mosquito larvae using non-invasive, self-referencing, pH-sensitive microelectrodes. J. Exp. Biol. 204,691 -699.[Abstract]
Boudko, D. Y., Moroz, L. L., Harvey, W. R. and Linser, P. J.
(2001b). Alkalinization by chloride/bicarbonate pathway in larval
mosquito midgut. Proc. Natl. Acad. Sci. USA
98,15354
-15359.
Cioffi, M. (1979). The morphology and fine structure of the larval midgut of a moth (Manduca sexta) in relation to active ion transport. Tissue Cell 11,467 -479.[CrossRef][Medline]
Clements, A. N. (1992). The Biology of Mosquitoes. London: Chapman and Hall.
Corena, M. P., Seron, T. J., Lehman, H. K., Ochrietor, J. D.,
Kohn, A., Tu, C. and Linser, P. J. (2002). Carbonic anhydrase
in the midgut of larval Aedes aegypti: cloning, localization and
inhibition. J. Exp. Biol.
205,591
-602.
Corena, M. P., Fiedler, M. M., VanEkeris, L., Tu, C., Silverman, D. N. and Linser, P. J. (2004). Alkalization of larval mosquito midgut and the role of carbonic anhydrase in different species of mosquitoes. Comp. Biochem. Physiol. 137C,207 -225.
Corena, M. P., VanEkeris, L., Salazar, M. I., Bowers, D.,
Fiedler, M. M., Silverman, D., Tu, C. and Linser, P. J.
(2005). Carbonic anhydrase in the adult mosquito midgut.
J. Exp. Biol. 208,3263
-3273.
Dadd, R. H. (1975). Alkalinity within the midgut of mosquito larvae with alkaline-active digestive enzymes. J. Insect Physiol. 21,1847 -1853.[CrossRef][Medline]
Dimitriadis, V. K. (1991). Fine structure of the midgut of adult Drosophila auraria and its relationship to the sites of acidophilic secretion. J. Insect Physiol. 37,167 -177.[CrossRef]
Dimitriadis, V. K. and Kastritsis, C. D. (1984). Ultrastructural analysis of the midgut of Drosophila auraria larvae: morphological observations and their physiological implications. Can. J. Zool. 62,659 -669.
Dow, J. A. T. (1984). Extremely high pH in biological systems: a model for carbonate transport. Am. J. Physiol. 246,R633 -R636.[Medline]
Dow, J. A. T. (1986). Insect midgut function. Adv. Insect Physiol. 19,187 -328.
Dow, J. A. T. and Peacock, J. M. (1989).
Microelectrode evidence for the electrical isolation of goblet cell cavities
in Manduca sexta middle midgut. J. Exp. Biol.
143,101
-114.
Dow, J. A. T. and Davies, S. A. (2001). The Drosophila melanogaster Malpighian tubules. Adv. Insect Physiol. 28,1 -83.[CrossRef]
Dow, J. A. T., Davies, S. A., Guo, Y., Graham, S., Finbow, M. E. and Kaiser, K. (1997). Molecular genetic analysis of V-ATPase function in Drosophila melanogaster. J. Exp. Biol. 200,237 -245.[Abstract]
Dubreuil, R. R. (2004). Copper cells and stomach acid secretion in the Drosophila midgut. Int. J. Biochem. Cell Biol. 36,745 -752.[Medline]
Dubreuil, R. R., Frankel, J., Wang, P., Howrylak, J., Kappil, M.
and Grushko, T. A. (1998). Mutations of 
spectrin and
labial block cuprophilic cell differentiation and acid secretion in
the middle midgut of Drosophila larvae. Dev.
Biol. 194,1
-11.[CrossRef][Medline]
Dubreuil, R. R., Grushko, T. and Baumann, O. (2001). Differential effects of a labial mutation on the development, structure, and function of stomach acid-secreting cells in Drosophila melanogaster larvae and adults. Cell Tissue Res. 306,167 -178.[CrossRef][Medline]
Filshie, B. K., Poulson, D. F. and Waterhouse, D. F. (1971). Ultrastructure of the copper-accumulating region of the Drosophila larval midgut. Tissue Cell 3, 77-102.[CrossRef][Medline]
Gartner, L. P. (1985). The fine structural morphology of the midgut of adult Drosophila: a morphometric analysis. Tissue Cell 17,883 -888.[CrossRef][Medline]
Lehane, M. J. and Billingsley, P. F. (1996). Biology of the Insect Midgut. London: Chapman and Hall.
Lin, G., Xu, N. and Xi, R. (2008). Paracrine Wingless signalling controls self-renewal of Drosophila intestinal stem cells. Nature 455,1119 -1122.[CrossRef][Medline]
Maddrell, S. H. P. and O'Donnell, M. J. (1992).
Insect Malpighian tubules: V-ATPase action in ion and fluid transport.
J. Exp. Biol. 172,417
-429.
Micchelli, C. A. and Perrimon, N. (2006). Evidence that stem cells reside in the adult Drosophila midgut epithelium. Nature 439,475 -479.[CrossRef][Medline]
Moffett, D. F. and Cummings, S. A. (1994). Transepithelial potential and alkalization in an in situ preparation of tobacco hornworm (Manduca sexta) midgut. J. Exp. Biol. 194,341 -345.[Abstract]
O'Donnell, M. J. and Spring, J. H. (2000). Modes of control of insect Malpighian tubules: synergism, antagonism, cooperation and autonomous regulation. J. Insect Physiol. 46,107 -117.[CrossRef][Medline]
O'Donnell, M. J., Dow, J. A. T., Huesmann, G. R., Tublitz, N. J. and Maddrell, S. H. P. (1996). Separate control of anion and cation transport in Malpighian tubules of Drosophila melanogaster.J. Exp. Biol. 199,1163 -1175.[Abstract]
Ohlstein, B. and Spradling, A. (2006). The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439,470 -474.[CrossRef][Medline]
Okech, B. A., Boudko, D. Y., Linser, P. J. and Harvey, W. R.
(2008). Cationic pathway of pH regulation in larvae of
Anopheles gambiae. J. Exp. Biol.
211,957
-968.
Onken, H., Moffett, S. B. and Moffett, D. F. (2006). The isolated anterior stomach of larval mosquitoes (Aedes aegypti): voltage-clamp measurements with a tubular epithelium. Comp. Biochem. Physiol. 143A,24 -34.
Onken, H., Moffett, S. B. and Moffett, D. F. (2008). Alkalinization in the isolated and perfused anterior midgut of the larval mosquito, Aedes aegypti. J. Insect Sci. 8,1 -20.
Patrick, M. L., Aimanova, K., Sanders, H. R. and Gill, S. S.
(2006). P-type Na+/K+-ATPase and V-type
H+-ATPase expression patterns in the osmoregulatory organs of
larval and adult mosquito Aedes aegypti. J. Exp. Biol.
209,4638
-4651.
Ridgway, R. L. and Moffett, D. F. (1986). Regional differences in the histochemical localization of carbonic anhydrase in the midgut of tobacco hornworm (Manduca sexta). J. Exp. Zool. 237,407 -412.[CrossRef]
Romero, M. F., Henry, D., Nelson, S., Harte, P. J., Dillon, A.
K. and Sciortino, C. M. (2000). Cloning and characterization
of a Na+-driven anion exchanger (NDAE1). J. Biol.
Chem. 275,24552
-24559.
Sciortino, C. M., Shrode, L. D., Fletcher, B. R., Harte, P. J. and Romero, M. F. (2001). Localization of endogenous and recombinant Na+-driven anion exchanger protein NDAE1 from Drosophila melanogaster. Am. J. Physiol. 281,C449 -C463.
Seron, T. J., Hill, J. and Linser, P. J.
(2004). A GPI-Linked carbonic anhydrase expressed in the larval
mosquito midgut. J. Exp. Biol.
207,4559
-4572.
Shanbhag, S. and Tripathi, S. (2005). Electrogenic H+ transport and pH gradients generated by a V-H+-ATPase in the isolated perfused larval Drosophila midgut. J. Membrane Biol. 206, 61-72.[CrossRef][Medline]
Shanbhag, S. and Tripathi, S. (2008). Segmental bidirectional transport of H+ in the adult Drosophila midgut. Comp. Biochem. Physiol. 150A, A11.29, S138.
Smith, K. E., VanEkeris, L. A. and Linser, P. J.
(2007). Cloning and characterization of AgCA9, a novel
-carbonic anhydrase from Anopheles gambiae Giles sensu
stricto (Diptera: Culicidae) larvae. J. Exp.
Biol. 210,3919
-3930.
Smith, K. E., VanEkeris, L. A., Okech, B. A., Harvey, W. R. and
Linser, P. J. (2008). Larval anopheline mosquito recta
exhibit a dramatic change in localization patterns of ion transport proteins
in response to shifting salinity: a comparison between anopheline and culine
larvae. J. Exp. Biol.
211,3067
-3076.
Takashima, S., Mkrtchyan, M., Hartenstein, A. Y., Merriam, J. R. and Hartenstein, V. (2008). The behaviour of Drosophila adult hindgut stem cells is controlled by Wnt and Hh signalling. Nature 454,651 -655.[CrossRef][Medline]
Tripathi, S. and Boulpaep, E. L. (1989).
Mechanisms of water transport by epithelial cells. Q. J. Exp.
Physiol. 74,385
-417.
Volkmann, A. and Peters, W. (1989a). Investigations on the midgut caeca of mosquito larvae. I. Fine-structure. Tissue Cell 21,243 -251.[CrossRef][Medline]
Volkmann, A. and Peters, W. (1989b). Investigations on the midgut caeca of mosquito larvae. II. Functional-aspects. Tissue Cell 21,253 -261.[CrossRef][Medline]
Wieczorek, H., Brown, D., Grinstein, S., Ehrenfeld, J. and Harvey, W. R. (1999). Animal plasma membrane energization by proton-motive V-ATPases. BioEssays 21,637 -648.[CrossRef][Medline]
Wieczorek, H., Huss, M., Merzendorfer, H., Reineke, S., Vitavska, O. and Zeiske, W. (2003). The insect plasma membrane H+ V-ATPase: intra-, inter-, and supramolecular aspects. J. Bioenerg. Biomembr. 35,359 -366.[CrossRef][Medline]
Yao, X. and Forte, J. G. (2003). Cell biology of acid secretion by the parietal cell. Annu. Rev. Physiol. 65,103 -131.[CrossRef][Medline]
Zhuang, Z., Linser, P. J. and Harvey, W. R. (1999). Antibody to H+ V-ATPase subunit E colocalizes with portasomes in alkaline larval midgut of freshwater mosquito (Aedes aegypti). J. Exp. Biol. 202,2449 -2460.[Abstract]
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