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INTRODUCTION
In teleost fish, osmotic balance is safeguarded by coordinated ion
and water transport by the gill, intestinal tract and kidney (see
Evans, 2008). Freshwater (FW) fish that are challenged by the
continuous osmotic gain of water and loss of salt to the dilute
surroundings counteract this by producing large volumes of dilute
urine, retaining ions in the kidney along with compensatory uptake
of ions from the food and by the gills. Seawater (SW) fish, by
contrast, counter the osmotic loss of water to the concentrated
environment by drinking and intestinal processing of SW in
conjunction with greatly reduced glomerular filtration and urine
production. To compensate for the overall salt gain, active secretion
of NaCl by the gill is crucial. Euryhaline fish species can move
between FW and SW habitats and accordingly are able to complete
the major functional changes in their osmoregulatory tissues, as
outlined above. Several studies have characterized how salinity
changes may induce adjustment in ion-transporter expression in
both gill (see Evans et al., 2005) and intestine (Aoki et al., 2003;
Seidelin et al., 2000; Sundell et al., 2003; Veillette et al., 2005)
whereas expressional changes in ion transporters in renal tissue are
equivocal and may differ among species (e.g. McCormick et al.,
1989; Tipsmark et al., 2008b).
Aquaporins (AQPs) play an integral role in cellular and
transcellular water movement in mammals (Hill et al., 2004a). Up
until now, 13 isoforms have been reported in mammals, whereas
17 isoforms have been identified in the pufferfish (Fugu rubripes)
and zebrafish (Danio rerio) genomes. Yet in fish only five of these
have received research attention (duplicate forms of AQP-1, AQP-
4, AQP-3 and AQPe – the latter two belonging to the
aquaglyceroporin subfamily). The current consensus is that duplicate
isoforms of AQP-1 (a and b) are involved in intestinal uptake of
water in marine fish since increased expression of both forms is
found in SW compared with the levels in FW in several species
[Japanese eel (A. japonica) (Aoki et al., 2003); European eel
(Martinez et al., 2005a); European sea bass (Dicentrarchus labrax)
(Giffard-Mena et al., 2007); gilthead sea bream (Sparus aurata)
(Raldua et al., 2008)]. In the kidney, available data are less
consistent, since studies in European sea bass (Giffard-Mena et al.,
2007) and black porgy [Acanthopagrus schlegel (An et al., 2008)]
report elevated renal AQP-1 expression in SW whereas the opposite
results have been reported for both AQP-1 isoforms in juvenile
European eel (Martinez et al., 2005b). In intestine and kidney,
available evidence suggests that AQP-1 is localized exclusively in
apical membranes. In the gill, data on AQP-1 expression is scarce.
Expression levels were found to be low in European eel (Martinez
et al., 2005b) and European sea bass (Giffard-Mena et al., 2007)
and did not change with salinity. In black porgy, gill expression of
AQP-1 was higher in FW than in SW but the function and
localization remain unclear (An et al., 2008).
AQP-3 expression has been found at low levels in different
intestinal regions, where a role in mucus secretion has been
suggested (Cutler et al., 2007). In the kidney, low levels of AQP-
3 have been reported in the apical membrane of tubule cells (Cutler
and Cramb, 2002). In the gill, data consistently suggests that AQP-
3 expression is elevated in response to hypo-osmotic challenge
[European eel (Cutler and Cramb, 2002); silver sea bream (Deane
and Woo, 2006); Japanese eel (Tse et al., 2006); European sea bass
(Giffard-Mena et al., 2007)]. AQP-3 has been located in pavement
The Journal of Experimental Biology 213, 368-379
© 2010. Published by The Company of Biologists Ltd
doi:10.1242/jeb.034785
Aquaporin expression dynamics in osmoregulatory tissues of Atlantic salmon during
smoltification and seawater acclimation
C. K. Tipsmark*, K. J. Sørensen and S. S. Madsen
Institute of Biology, University of Southern Denmark, Campusvej 55, DK-5230 Odense M, Denmark
*Author for correspondence (ckt@biology.sdu.dk)
Accepted 27 October 2009
SUMMARY
Osmotic balance in fish is maintained through the coordinated regulation of water and ion transport performed by epithelia in
intestine, kidney and gill. In the current study, six aquaporin (AQP) isoforms found in Atlantic salmon (Salmo salar) were classified
and their tissue specificity and mRNA expression in response to a hyperosmotic challenge and during smoltification were
examined. While AQP-1a was generic, AQP-1b had highest expression in kidney and AQP-3 was predominantly found in
oesophagus, gill and muscle. Two novel teleost isoforms, AQP-8a and -8b, were expressed specifically in liver and intestinal
segments, respectively. AQP-10 was predominantly expressed in intestinal segments, albeit at very low levels. Transfer from
freshwater (FW) to seawater (SW) induced elevated levels of intestinal AQP-1a, -1b and -8b mRNA, whereas only AQP-8b was
stimulated during smoltification. In kidney, AQP-1a, -3 and -10 were elevated in SW whereas AQP-1b was reduced compared with
FW levels. Correspondingly, renal AQP-1a and -10 peaked during smoltification in April and March, respectively, as AQP-1b and
AQP-3 declined. In the gill, AQP-1a and AQP-3 declined in SW whereas AQP-1b increased. Gill AQP-1a and -b peaked in April,
whereas AQP-3 declined through smoltification. These reciprocal isoform shifts in renal and gill tissues may be functionally linked
with the changed role of these organs in FW compared with SW. The presence and observed dynamics of the AQP-8b isoform
specifically in intestinal sections suggest that this is a key water channel responsible for water uptake in the intestinal tract of
seawater salmonids.
Key words: AQP-1, AQP-3, AQP-8, AQP-10, gill, kidney, intestine.
THEJOURNALOFEXPERIMENTALBIOLOGY