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First published online March 14, 2008
Journal of Experimental Biology 211, 1114-1119 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016758
Aquaporins play a role in desiccation and freeze tolerance in larvae of the goldenrod gall fly, Eurosta solidaginis
Department of Zoology, Miami University, Oxford, OH 45056, USA
* Author for correspondence (e-mail: philipbn{at}muohio.edu)
Accepted 27 January 2008
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Summary |
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Key words: aquaporins, osmotic stress, water balance, freeze-tolerant insects
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) and kidney cells
(Nielsen et al., 1993),
aquaporins are found in other mammals, anurans, arthropods, plants and yeast
(Borgnia et al., 1999). These
small pore proteins are highly selective, allowing only water and small
uncharged solutes, such as glycerol and urea, to passively diffuse through the
membrane (Ishibashi et al.,
1994). Aquaporins are implicated in various responses to osmotic
challenge, including urine concentration in mammals
(Nielsen et al., 1995), water
shunting in sap-sucking insects (Beuron et
al., 1995) and the tolerance of sea water consumption in birds
(Müller et al.,
2006).
Although most insects are freeze intolerant and must rely on supercooling
for winter survival, some are freeze tolerant and can withstand ice formation
within their extracellular fluids (Salt,
1961). During freezing, only water molecules join the growing ice
lattice, thus concentrating solutes in the remaining unfrozen fraction of
water, termed freeze concentration. The resulting osmotic gradient draws water
out of the cells, thereby preventing lethal intracellular freezing
(Lee, 1989).
The inability of most cells to survive freezing is due to an inadequate
amount of intracellular water being replaced with cryoprotectant molecules,
such as glycerol (Hagedorn et al.,
2002). Consequently, efforts to improve cell survival during
cryopreservation have turned to the artificial expression of aquaporins. RNA
insertion and protein overexpression of aquaporins successfully increases the
survival of mouse oocytes during cryopreservation
(Edashige, 2003) and the
viability of baker's yeast in bread dough after freezing
(Tanghe et al., 2002). In
addition, a recent report by Izumi et al.
(Izumi et al., 2006) provides
evidence that aquaporins promote freeze tolerance in a rice stem boring
insect. By blocking the functionality of the protein with mercuric chloride, a
known inhibitor of some aquaporins
(Preston et al., 1993), they
reported a reduction in cell survival during freezing.
Similar to freezing, desiccation places an organism under osmotic stress.
In desiccated plants, Smith-Espinoza et al.
(Smith-Espinoza et al., 2003)
and Barrieu et al. (Barrieu et al.,
1999) found an increase in aquaporin transcription and protein
concentration. Likewise, mammals increase aquaporin expression in response to
dehydration (Ishibashi et al.,
1997). The upregulated expression of aquaporins suggests they play
a role in desiccation tolerance.
Overwintering larvae of the goldenrod gall fly, Eurosta
solidaginis (Fitch), are both freeze tolerant and desiccation resistant.
Larvae acquire freeze tolerance during the autumn, in part through the
accumulation of glycerol and sorbitol
(Morrissey and Baust, 1976),
and can survive extended periods of subzero exposure to temperatures below
–50°C (Storey and Storey,
1988; Lee, 1991).
Also, larvae are subjected to desiccating conditions as the surrounding gall
tissues of the goldenrod plant (Solidago sp.) senesce and dry in the
autumn (Rojas et al., 1986)
and during cold, dry winters; Ramløv and Lee
(Ramløv and Lee, 2000)
reported that the rate of water loss for these overwintering larvae is among
the lowest reported for any insect.
We hypothesized that aquaporins play an important role in the ability of E. solidaginis to survive freezing and desiccation. To first determine whether aquaporins are present in E. solidaginis, we immunoblotted soluble proteins of control and desiccated larvae against mammalian anti-AQP2, -AQP3 and -AQP4 antibodies. To test the role of aquaporins in freeze tolerance, we froze isolated fat body, midgut and salivary glands in the presence or absence of the aquaporin inhibitor mercuric chloride and assessed cell viability after freezing.
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MATERIALS AND METHODS |
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4 months).
Desiccation treatment
Three replicates of 10 larvae from each acclimation group were placed in a
Petri dish and dehydrated in a desiccator over fresh Drierite (0% relative
humidity) for 4 days at 4°C. The larvae lost 3–7% of their fresh
body mass during this desiccation treatment.
Protein extraction and SDS-PAGE
Groups of 10 larvae were homogenized in a 2 ml glass homogenizer with a
buffer containing 150 mmol l–1 NaCl, 10 mmol
l–1 Tris-HCl (pH 7.2), 0.1% sodium deoxycholate and protease
inhibitors [5 µg ml–1 aprotinin, 5 µg
ml–1 antipain, 5 µg ml–1 leupeptin and 1
mmol l–1 PMSF (phenylmethanesulfonylfluoride)]
(Goel et al., 2006;
Yi et al., 2007). After the
homogenate was sonicated with an ultrasonic processor (Cole Parmer, Vernon
Hills, IL, USA) and incubated on ice for 30 min, it was centrifuged twice at
16 000 g for 20 min at 4°C to remove any insoluble
fragments. The resulting supernatant contained soluble proteins, whose
concentration was determined using the Bio-Rad protein assay (Bio-Rad,
Hercules, CA, USA) with BSA (bovine serum albumin) as a standard. Protein
samples (50 µg) were mixed with Laemmli sample buffer containing 5%
β-mercaptoethanol and incubated at either 95°C for 3 min or 60°C
for 10 min, and then analysed by SDS-PAGE on a 4–15% gradient gel
(Bio-Rad). Precision Plus protein standard kit (Bio-Rad) was used as a
reference.
Protein staining and immunoblotting
Following electrophoresis, proteins were transferred to a nitrocellulose
membrane (Bio-Rad). The membrane was stained with 0.1% Ponceau S staining
solution (Sigma Chemical Company, Saint Louis, MO, USA) for 10 min and rinsed
with ultrapure water to verify that proteins were transferred. After digitally
scanning the membranes, they were destained for 30 s in an aqueous solution of
0.1 mol l–1 NaOH and were used for immunoblotting as
described by Yi et al. (Yi et al.,
2007). Non-specific protein antigens were blocked at 4°C
overnight in 10% non-fat milk Western wash buffer (10 mmol
l–1 Tris, 100 mmol l–1 NaCl and 0.1% Tween
20 at pH 7.5). The membranes were incubated with corresponding primary
antibodies in a 5% non-fat milk solution at 21°C for 2 h. Rabbit
anti-actin (1:400), anti-AQP2 (1:500), anti-AQP3 (1:200) and anti-AQP4
(1:1000), and goat anti-rabbit IgG-HRP (horseradish peroxidase) conjugates
were purchased from Sigma Chemical Company. After three 15 min washes in
Western wash buffer, the membranes were incubated for 2 h with secondary
antibody (goat anti-rabbit IgG-HRP conjugates) diluted 1:1000 in Western wash
buffer. Membranes were then washed in Western wash buffer, incubated for 2 min
in ECL (enhanced chemiluminescence) detection reagents (Amersham Biosciences,
Piscataway, NJ, USA) and exposed to autoradiography film. Although all
immunoblots were replicated to verify findings, only representative Western
blots are included in the results presented here. Bands were normalized to
4°C samples and semi-quantified using ImageQuant 5.2 (Molecular Dynamics,
Sunnyvale, CA, USA).
Role of aquaporins in freeze tolerance
Larvae acclimated to 4°C were dissected in Coast's solution
(Coast, 1988) on a silicone
elastomer-filled Petri dish (Yi and Lee,
2003). Fat bodies (3.5 mg wet mass) and midguts (0.15 mg
wet mass) were dissected while larvae were pinned with their ventral side
uppermost, whereas salivary glands (0.12 mg wet mass) were dissected
while larvae were pinned with their dorsal side uppermost. Dissected tissues
were transferred to 1 ml of fresh Coast's solution for 1 h at 21°C.
Tissues were then transferred to 1 ml of Coast's solution + 0.25 mol
l–1 glycerol and incubated at 4°C for 1 h. Following the
incubation, they were placed into 100 µl of Coast's solution, Coast's
solution + 0.25 mol l–1 glycerol, or Coast's solution + 0.25
mol l–1 glycerol + 0.2 mmol l–1 mercuric
chloride (HgCl2), based on a modified protocol from Izumi et al.
(Izumi et al., 2006).
To determine whether the effects of mercuric chloride were permanent,
tissues were exposed to β-mercaptoethanol, a reducing agent, which
reverses the inhibitory effect of mercuric chloride
(Preston et al., 1992). The
dissection and incubation procedure remained the same except for an additional
step in which tissues were incubated in Coast's solution + 0.25 mol
l–1 glycerol + 0.2 mmol l–1 HgCl2
for 15 min at 21°C before being frozen in 100 µl of Coast's solution +
0.25 mol l–1 glycerol + 0.2 mmol l–1
HgCl2 + 2 mmol l–1 β-mercaptoethanol.
The microcentrifuge tubes containing the tissues were cooled at a rate of 0.2°C min–1 (4°C to –20°C) over 2 h and kept at –20°C for 2 h. When the temperature of the ethanol bath reached –4°C, the microcentrifuge tubes were sprayed with Super Friendly Freeze'It (Fisher Scientific Company, Hanover Park, IL, USA) to seed ice nucleation and freezing of the treatment solutions. All control tissues were kept at 4°C for 4 h.
Cell viability assay
All tissues were thawed at 21°C for 1 h prior to the assessment of cell
survival using the Live/Dead sperm viability kit [Molecular Probes, Inc.,
Eugene, OR, USA (Yi and Lee,
2003)] containing SYBR 14 dye (1 mmol l–1 in
DMSO) and propidium iodide (2.4 mmol l–1 in water). Working
solutions of SYBR (2 µl per 100 µl Coast's solution) and propidium
iodide (4 µl per 100 µl Coast's solution) were prepared for all samples.
The tissues were incubated in 25 µl SYBR stain for 15 min on glass
microscope slides. The addition of 25 µl propidium iodide to the slides was
followed by a second 15 min incubation. The SYBR stain is membrane permeable
and can penetrate the nuclei of all cells, whereas propidium iodide can only
enter damaged cells that have lost plasma membrane integrity. The slides were
covered with a coverslip and examined on a fluorescence microscope (Olympus
BX60) (Davis and Lee, 2001;
Yi and Lee, 2003). Cell
viability was assessed using the following criteria: live cells fluoresced
green and dead cells fluoresced orange to bright red. The percentage survival
of the midgut and salivary gland from each individual was based on the mean of
three counts of 100 cells. There are fewer fat body cells per larvae,
therefore the viability of the fat body was based solely on the total count of
cells (130–200) dissected from each individual. The individual
(N=4) average for each tissue was used to calculate the mean ±
s.e.m. for each treatment.
Statistics
Data were compared using an analysis of variance and Bonferroni–Dunn
post-hoc tests (Statview 4.5, Cary, NC, USA). Statistical
significance was set at P<0.05. Values are presented as means
± s.e.m.
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RESULTS |
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). Anti-AQP3
identified two pronounced protein bands with apparent molecular masses of 25
and 75 kDa, and two faint bands of 40 and 50 kDa
(Fig. 2B). Previous reports
suggest that AQP3 is 26 kDa (Rai et
al., 2006) and that any larger immunoidentified bands are either
glycosylated or oligomers (Lu et al.,
1996). Therefore, we propose that the 25 kDa band is a monomer and
the 75 kDa band corresponds to a trimer of AQP3. Although the expected AQP4
size is 31 kDa (Rash et al.,
1998), we observed a single band at 60 kDa
(Fig. 2C), which is probably
dimeric AQP4 (Neely et al.,
1999). As suggested by semi-quantitative densitometry, the concentration of all three aquaporin homologues varied depending on temperature acclimation and/or desiccation treatment when compared with 4°C acclimated larvae. For AQP2 immunoblots (N=2), the density of the 26 kDa band for each of the three treatments (4°C desiccated, –20°C frozen and –20°C frozen + desiccated) was 27–77 % lower than that of the 4°C acclimated larvae (Fig. 2A). In contrast, the AQP3 immunoblots (N=3) of treated samples suggest an almost 50% increase in concentration at 25 kDa compared with the 4°C acclimated larvae (Fig. 2B). Lastly, the 4°C acclimated larvae expressed a slightly higher concentration of AQP4 (N=2) compared with the other treatment groups (Fig. 2C).
Effect of aquaporins on freeze tolerance
A high proportion of the control tissues fluoresced green following vital
dye staining, which indicates survival of the cells
(Fig. 3A,G,M). The high
survival rate of the fat body (95.7±0.6%), midgut (98.3±0.8%)
and salivary gland (97.9±0.7%) control tissues at 4°C indicates
minimal mechanical damage to the tissues during dissection (Figs
4 and
5).
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Mercuric chloride was used to assess whether aquaporin function is necessary for larval survival during freezing. We held mercuric chloride controls (Coast's solution + 0.25 mol l–1 glycerol + 0.2 mmol l–1 HgCl2) at 4°C for 4 h and did not see a difference in survival compared with tissues frozen in Coast's solution and glycerol, suggesting that mercuric chloride was not toxic to unfrozen tissues (Fig. 3E,K). However, when these tissues were frozen in the presence of mercuric chloride, there was a significant reduction in cell survival. As seen in Fig. 3B,D, survival of fat body was significantly lower compared with tissues frozen in Coast's solution and glycerol alone (Fig. 4A, P<0.0001). Similarly, Fig. 3H,J indicates that survival of the midgut was significantly lower when frozen in the presence of mercuric chloride (Fig. 4B, P<0.0001).
Tissues were frozen with β-mercaptoethanol to determine whether the effects of mercuric chloride were reversible. Neither fat body (Fig. 3F) nor midgut (Fig. 3L) differed in cell survival compared with tissues frozen in Coast's solution and glycerol (Fig. 4A,B). This suggests that aquaporin blocking by mercuric chloride is reversible.
Unlike the fat body and midgut, the salivary gland did not exhibit a significant reduction in cell survival when frozen with mercuric chloride (Fig. 5). Because there was no difference between salivary glands frozen in Coast's solution + 0.25 mol l–1 glycerol (Fig. 3N) or Coast's solution + 0.25 mol l–1 glycerol + 0.2 mmol l–1 HgCl2 (Fig. 3P), neither mercuric chloride controls nor β-mercaptoethanol treatments were run.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)
reported that an aquaporin protein isolated from Drosophila
melanogaster (DRIP) is 44% identical to human AQP4. Aquaporins within the
order Diptera are even more closely related, as shown by AeaAQP (from
the mosquito Aedes aegypti), which has an amino acid sequence that is
65% identical to DRIP (Kaufmann et al.,
2005). Thus, even between phylogenetically distant species,
aquaporin proteins retain conserved elements, which allowed us to use
mammalian antisera to confirm the presence of aquaporin-like proteins in
E. solidaginis.
Desiccation regulates aquaporins
Many organisms adapt to desiccation and osmotic stress by regulating
various proteins, such as LEAs in plants [e.g. dehydrins
(Close, 1996)] and heat shock
proteins in insects (Hayward et al.,
2004). Similarly, the aquaporins in our study were either
upregulated (AQP3) or downregulated (AQP2 and AQP4) following desiccation of
the larvae. Among the three aquaporins characterized, AQP3 is especially
intriguing because it is permeable to water and glycerol
(Ishibashi et al., 1994), both
of which are important during osmotic stress caused by desiccation and
freezing. In our study, soluble AQP3 levels from 4°C acclimated larvae
increased by 50% with desiccation (Fig.
2B), which is similar to the upregulation previously reported in
kidneys of dehydrated rats (Ecelbarger et
al., 1995). This upregulation of AQP3 may be part of a coordinated
set of physiological changes that increase the permeability of water and
glycerol across the cell membrane as larvae prepare for the osmotic stress
associated with host plant senescence and extracellular ice formation. To our
knowledge, this is the first report of insect aquaporins being regulated in
response to desiccation.
Aquaporins promote freeze tolerance
The normally high level of freeze tolerance in E. solidaginis
tissues was significantly reduced when aquaporin channels were blocked with
mercuric chloride. This high mortality in the fat body and midgut occurred
despite tissues being frozen in a solution that also contained glycerol, a
cryoprotectant that promotes freeze tolerance
(Fig. 4). Izumi et al.
(Izumi et al., 2006) suggested
that cell survival of freezing depends on a portion of intracellular water
being replaced by glycerol and demonstrated that mercuric chloride blocks both
water and glycerol movement in the fat body. Similarly, the inability to
regulate cell volume was suggested as the cause of reduced freeze tolerance in
an earthworm that was exposed to copper
(Bindesbøl et al.,
2005). Because copper has been reported as an aquaporin inhibitor
(Zelenina et al., 2004), the
loss of freeze tolerance in the earthworm may be a result of blocked aquaporin
channels. We propose that the decrease in cell survival of the mercury-exposed
fat body and midgut tissues in our study are a result of obstructed water
and/or glycerol flux through aquaporins, which is essential for freeze
tolerance.
Just as there is a diversity of aquaporins among different mammalian
tissues (Borgnia et al., 1999),
aquaporin isoforms expressed in E. solidaginis may also vary among
tissues. Unlike fat body and midgut tissues, salivary glands frozen in the
presence of mercuric chloride exhibited high levels of cell survival. This
result was unexpected because other arthropods, such as the tick, Ixodes
ricinus, have mercury-sensitive aquaporins in their salivary glands
(Bowman and Sauer, 2004).
Although we did not directly test the cause of cell survival in this study,
our findings may be the result of an abundance of mercury-insensitive
aquaporins in the salivary gland.
Ring and Danks (Ring and Danks,
1994) hypothesized that cold tolerance is linked to (and probably
derived from) an organism's response to desiccation stress. Because both
stresses require the control of solutes and body water, organisms often employ
similar mechanisms to cope with desiccation and freezing. The results from
this study suggest that aquaporins play a role in both desiccation and freeze
tolerance in E. solidaginis.
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Acknowledgments |
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