Role of biogenic amines and cHH in the crustacean hyperglycemic stress response
BRAIN Center, Department of Biology, University of Trieste, via Giorgieri 7, I-34127 Trieste, Italy
* Author for correspondence (e-mail: ferrero{at}units.it)
Accepted 23 June 2005
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Summary |
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5-HT induced in P. elegans a rapid and massive release of cHH from the eyestalk into the hemolymph followed by hyperglycemia. On the contrary, DA did not significantly affect cHH release and hyperglycemia. In addition, we measured the level and variation of 5-HT in the eyestalk and hemolymph of P. elegans following copper contamination. The release of 5-HT from the eyestalk is very rapid and dose dependent. In the hemolymph, a peak of 5-HT occurs after 30 min, and again the circulating concentration of 5-HT is dose dependent on copper exposure. After 1 h, the level of 5-HT slowly decreases to basal level.
The release of 5-HT from the eyestalk into the hemolymph after copper exposure precedes the release of cHH, confirming its role as a neurotransmitter acting on cHH neuroendocrine cells. The fact that copper induced a rapid and massive release of 5-HT from the eyestalk can explain its demonstrated role in inducing the release of cHH and the consequent hyperglycemia in intact but not eyestalkless animals.
Key words: Palaemon elegans, copper, glucose, serotonin, dopamine, ELISA
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Introduction |
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Our recent study (Lorenzon et al.,
2004b) demonstrated that, in the shrimp P. elegans,
exposure to copper induced a dose-related rapid and massive release of cHH
from the eyestalk into the hemolymph at the highest, lethal concentration,
while a gradual and reduced discharge was revealed at the lowest
concentration. The relationship between exposure to toxicant and release of
cHH was confirmed by variation of blood glucose with a dose-related
hyperglycemia that peaked 2 h after exposure to copper.
In order to understand the effect of stressors on hemolymph glucose, it is
important to study the underlying hormonal mechanism. Biogenic amines and
enkephalin have been found to mediate the release of several neurohormones
from crustacean neuroendocrine tissues. Serotonin (5-HT; 5-hydroxytryptamine)
is well known as a neurotransmitter in crustaceans on several grounds, and its
levels have been measured in the nervous system and hemolymph of various
crustacean species (Elofsson et al.,
1982; Laxmyr,
1984
; Kulkarni and Fingerman,
1992
), thus suggesting a possible role as a neurohormone
(Rodrigues-Soza et al., 1997). Serotonin has long been known to have a potent
hyperglycemic effect in several crustacean species
(Bauchau and Mengeot, 1966
;
Keller and Beyer, 1968
;
Lee et al., 2000
; Lorenzon et
al., 1999
,
2004a
;
Santos et al., 2001
). Lee et
al. (2001
) confirmed the role
of 5-HT in mediating the release of cHH. In the crayfish Orconectes
limosus, injection of 5-HT caused a significant increase in the
circulating level of cHH (Santos et al.,
2001
). In P. clarkii, cHH release increased as a
dose-related function of 5-HT concentration
(Escamilla-Chimal et al.,
2002
).
For dopamine (DA), studies on different species have reported contrasting
results. In P. clarkii (Sarojini
et al., 1995), P. elegans, the crayfish Astacus
leptodactylus and the mantis shrimp Squilla mantis (Lorenzon et
al., 1999
,
2004a
), DA inhibits the
release of cHH from the SG, causing a decrease in hemolymph glucose level.
Injection into eyestalkless animals is ineffective. By contrast, in the crab
Cancer maenas (Lüschen et
al., 1993
) and in the tiger shrimp, Penaeus monodon
(Kuo et al., 1995
), DA was
shown to elevate hemolymph glucose. More recently, Zou et al.
(2003
) demonstrated a
dose-dependent effect of DA on the increase of cHH and glucose in the
hemolymph of P. clarkii.
5-HT apparently plays a regulatory role in eyestalk hormone release, as has
been previously demonstrated for MIH (molt inhibiting hormone), a neuropeptide
belonging to the same family as cHH
(Mattson and Spaziani, 1986),
in the crab Cancer antennarius and by the recently described
widespread occurrence of 5-HT1r (type 1 serotonin receptor) in
eyestalk ganglia (Spitzer et al.,
2005
).
In our previous work, we demonstrated in P. elegans that 5-HT has
a marked dose-related effect in elevating glucose level but that it is
ineffective in eyestalkless animals; DA injection in intact and eyestalkless
animals produced a reduction below initial levels of hemolymph glucose
(Lorenzon et al., 1999). The
release of cHH and the consequent hyperglycemia is stress related, in
particular after copper exposure (Lorenzon
et al., 2004b
). However, to our knowledge, there is a lack of
information on the variation of 5-HT following stress and little connecting it
with the hyperglycemic response.
As a consequence, the aim of this paper was to monitor the variation of cHH in the eyestalks and hemolymph of Palaemon elegans (Decapoda, Caridea) after injection of 5-HT and DA and relate it to the variation in amount and time course of blood glucose. Moreover, we intended to assess the level and variation of 5-HT in the eyestalk and hemolymph of P. elegans following copper contamination.
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Materials and methods |
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They were stocked in 120 liter glass tanks with closed-circuit-filtered and
thoroughly aerated 36 salinity artificial sea water
(Prodac®, Padova, Italy) at 1618°C and a natural L:D
photoperiod at 300 lux intensity (type 49 fluorescent tube by Philips, Monza,
Italy) during the light phase. They were fed ad libitum with bits of
shrimp, cuttlefish or fish every second day; dead animals were removed
daily.
Apparently healthy animals of both sexes and intermolt, having a body mass of 11.5 g, were used. Forty-eight hours before use, animals were housed individually in 500 ml plastic net cages immersed in larger tanks, for individual recognition. Animals were not fed during the experiment.
Hemolymph sampling and determination of glycemia
The animals were blotted dry and hemolymph (50 µl) was withdrawn, from
the pericardial sinus, into sterile 1 ml syringes fitted with 25 g needles.
Animals (N=10 for each treatment) were bled at 0 h, usually between
09.00 and 10.00 h to reduce possible interference due to circadian changes in
blood glucose level (Kallen et al.,
1990).
Hemolymph glucose content was quantified using a One Touch® II Meter (Lifescan, Miltipas, CA, USA) and commercial kit test strips (precision of strips ±3% coefficient of variation in the tested range). Due to the short time of processing, no anticoagulant was needed. In the results, variations of glycemia defined as increments are given as the mean of: {[(experimental value)/(value displayed by the same animal at 0 h)]1}x100.
Effect of 5-HT and DA on blood glucose level
Variation of glycemia following injection with 5-HT and DA at the
concentration of 108 mol g1 live mass
(concentration in the range previously tested by
Lorenzon et al., 1999) was
tested on groups of intact P. elegans (N=10 for each
treatment). At 0 h, 0.5 h, 1 h, 2 h, 3 h and 24 h after injection, animals
were bled as described above. A control group injected with saline was tested
at the same time. Sterile saline for marine crustaceans was prepared with
pyrogen-free distilled water and analytical-grade chemicals, according to
Smith and Ratcliffe (1978
),
and autoclaved fro 25 min. All reagents were supplied by Sigma-Aldrich (St
Louis, MO, USA).
Eyestalk homogenate and hemolymph treatment for ELISA of cHH and 5-HT variation
Groups of 10 P. elegans were injected with 5-HT or DA
(108 mol g1 live mass) or exposed to
CuCl2 (0.1 and 5 mg l1 of Cu2+);
untreated and saline-injected animals were used as controls. Eyestalks were
removed at time 0 h and then at 0.5 h, 1 h and 2 h (and 3 h only for
Cu2+) from the 10 animals of each different experimental group.
Animals were anesthetized for 1 min on ice before ablation. The eyestalk was
quickly frozen and the eyecup was cut off to remove visual and screening
pigment. Eyestalk homogenate was prepared from 20 eyestalks homogenized in 2
ml of cold phosphate-buffered saline (PBS; Sigma), pH 8.0, and then
centrifuged for 1 h at 930 g and 4°C. The clear homogenate
was quickly deep frozen at 20°C and stored until required for
study.
Hemolymph was withdrawn from the different groups of 10 P. elegans for each treatment, as described above, at time 0 h and then at 0.5 h, 1 h and 2 h (and 3 h only for Cu2+) and immediately centrifuged for 1 min at 10 300 g and 4°C to prevent coagulation. The supernatant plasma fraction was then stored at 20°C.
Direct ELISA of cHH
The ELISA was performed as described by Lorenzon et al.
(2004b).
6xHis-NencHHwt (Mr=11 kDa;
Mettulio et al., 2004
)
recombinant protein was used as standard
(y=1.495140.37828x; correlation coefficients of the
fitted curves are >0.99 for all the data; r=0.9937,
S.D.=0.44, P<0.001;
Lorenzon et al., 2004b
).
Briefly, 100 µl of the eyestalk homogenate (ES = eyestalk) or hemolymph
from the different treatments, as well as standards, were loaded onto a
96-microwell plate (Costar, Bethesda, MD, USA) and incubated in duplicate
overnight at 4°C. Then, 100 µl of the biotinylated anti-NencHH
(anti N. norvegicus cHH; interspecific cross-reactivity tested by
Giulianini et al., 2002)
antibody (1 µg µl1), diluted 1:1000, was added to each
well and the plate was incubated for 3 h at 36°C. After removal of the
biotinylated antibody, plates were washed extensively, followed by the
addition of 100 µl of streptavidin-peroxidase (Sigma) solution (diluted
1:5000), and incubated for 1 h at room temperature. The plates were once again
washed and developed with 2,2'-azino-bis
3-ethylbenz-thiazoline-6-sulphonic acid solution (Sigma; liquid substrate
ready for use) in darkness for 1 h at room temperature (100 µl per
well).
The absorbance was measured in a multiwell plate reader (Anthos 2020, version 1.1; Anthos, Krefeld, Germany) at 405 nm.
Quantification of 5-HT in the hemolymph and eyestalk of P. elegans
A commercially available competitive serotonin ELISA kit (ICN Biochemicals,
Costa Mesa, CA, USA) was used to determine the concentration of 5-HT in the
hemolymph or eyestalk homogenate. The absolute value of 5-HT was obtained from
the linear curve-fit of the standards. Sample values were then inserted into
the equation and the amount of unknown 5-HT thereby determined
(Fig. 1).
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Results |
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Injection of 5-HT (108 mol g1 live mass) induced a strong release of cHH from the eyestalk of P. elegans (Fig. 2). From 30 min after injection, the cHH content decreased drastically to 0.25±0.11 pmol ES1 equiv. (ES equivalent), a value significantly different (P=0.001) from the initial value (5.60±2.6 pmol ES1 equiv.) of untreated animals and from the saline-injected controls at the same time (5.41±1.86 ES1 equiv.; P=0.001); values remained significantly (P<0.05) below the resting and control level throughout the experimental period. By contrast, DA (108 mol g1 live mass; Fig. 2) produced no significant effect on cHH eyestalk content.
|
|
Injection of 108 mol g1 live mass of 5-HT (Fig. 4) induced a marked hyperglycemia, and blood glucose gradually rose from the first 30 min after injection to a peak at 2 h of628±191% (63.90±1.91 mg dl1), which was significantly different from the initial value (9.20±1.93 mg dl1; P=0.001) and from the control at the same time, which showed an increase of 37±22% (12.90±2.56 mg dl1; P=0.001). Afterwards, the blood glucose value started to decrease and returned to the initial value after 24 h (data not shown). No significant (P>0.05 compared with the saline control) increase in blood glucose level (Fig. 4) was recorded in P. elegans after injection of DA (108 mol g1 live weight).
|
Variation of 5-HT level in the hemolymph and eyestalk of P. elegans following copper exposure
Fig. 5 shows the time course
of 5-HT in the hemolymph of P. elegans after exposure to
Cu2+ (5 and 0.1 mg l1). In control animals,
maintained in uncontaminated water, the level of circulating 5-HT was
4.85±0.98 ng ml1. The highest, lethal concentration
(LC50=3.27 mg l1 at 96 h;
Lorenzon et al., 2000) of 5 mg
l1 induced a marked and significant (P=0.001
vs initial value and control) increase of circulating 5-HT from the
initial value of 4.41±0.51 ng ml1 to
31.85±5.71 ng ml1 in the first 30 min after
exposure.
|
The value remained significantly elevated at 1 h (28.15 ng ml1), compared with the initial value and control (P=0.001), and decreased thereafter. At 2 h, the level of circulating 5-HT was 8.34 ng ml1, which was not significantly different from the initial value of 4.41 ng ml1 and from the control (P>0.05). All further values were also not significantly different from the initial value and control (Fig. 5).
At the lower concentration of copper (0.1 mg l1; Fig. 5), the maximum increment in circulating 5-HT of 11.08±2.83 ng ml1 was detected after 30 min of exposure and was significantly different from the initial value of 5.22±1.24 ng ml1 (P=0.009) and from the control (P=0.019). The value obtained after 1 h (10.31±2.94 ng ml1) was still significantly different from the initial value (P=0.016) and from the control (P=0.012). Thereafter, the level of circulating 5-HT started to decrease and was not significantly different (P>0.05) from the initial value and from the control for the rest of the experiment.
|
At the lowest concentration of copper (Fig. 6), the level of 5-HT in the eyestalk decreased from 8.69±1.91 ng ml1 to 4.63±0.89 ng ml1 (P=0.02 vs initial value) in the first 30 min of exposure, which was also significantly different from the control (P=0.001). This value remained at the same level throughout the experimental period.
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Discussion |
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Our data accord with previous studies by Lee et al.
(2001) that confirm the role
of 5-HT in enhancing the release of cHH, which in turn elicits a hyperglycemic
response in P. clarkii. Moreover, cHH release increases as a function
of 5-HT concentration in vivo, and a similar trend was reported in an
in vitro system by Escamilla-Chimal et al.
(2002
). In O. limosus,
injection of 5-HT caused a significant increase of the circulating level of
cHH (Santos et al., 2001
).
Our present and previous data on the effects of DA demonstrate that, in
P. elegans, A. leptodactylus and S. mantis (Lorenzon et al.,
1999,
2004a
), DA has no significant
effect on the release of cHH and on the increase of hemolymph glucose level.
Likewise, 5-HT and its receptor inhibitors, but not DA, affect serum
ecdysteroid titer in intact C. antennarius. The lack of effect in
eyestalk-ablated animals suggests a control on MIH release
(Mattson and Spaziani,
1986
).
Our findings confirm those by Sarojini et al.
(1995) in P. clarkii
but are in contrast with those by Lüschen et al.
(1993
) for C. maenas,
Kuo et al. (1995
) for P.
monodon and Komali et al.
(2005
) in the freshwater prawn
Macrobrachium malcolmsonii, where DA induced hyperglycemia. The
present data on release of cHH are also at variance with those of Zou et al.
(2003
), who demonstrated in
P. clarkii that DA induced the release of cHH and an increase in
blood glucose level.
In the present paper, we also present the time course of 5-HT level in the
eyestalk and hemolymph of P. elegans following exposure to different
concentrations of copper. The circulating basal level of 5-HT in P.
elegans was 4.81±0.98 ng ml1, which is higher
than that found by Sneddon et al.
(2000) in C. maenas,
where the basal level of 5-HT in the hemolymph was
1 ng
ml1, and different from those found in the crayfish
Pacifastacus leniusculus (Elofsson
et al., 1982
).
The release of 5-HT from the eyestalk is very rapid (within 30 min) and dose dependent. In the hemolymph, a peak of increment is revealed after 30 min, and again the circulating concentration of 5-HT is dose dependent on copper exposure. After 1 h, the level of 5-HT slowly declines to the initial basal level.
In a previous work (Lorenzon et al.,
2004b), we demonstrated the role of copper in inducing release of
cHH from the eyestalk into the hemolymph, with a consequent increase in blood
glucose level in a dose-related manner. The release of cHH from the eyestalk
reached the maximum after 2 h of exposure, and in the hemolymph the maximum
peak of circulating cHH was reached after 2 h of exposure. The release of 5-HT
from the eyestalk (Elofsson et al.,
1982
; Kulkarni and Fingerman,
1992
) into the hemolymph after stress precedes the release of cHH,
confirming its role as a neurotransmitter acting on cHH neuroendocrine cells
(Saenz et al., 1997
;
Garcia and Aréchiga,
1998
; Escamilla-Chimal et al.,
2002
). The fact that copper induces the rapid and massive release
of 5-HT from the eyestalk explains its demonstrated role in inducing the
release of cHH (Lorenzon et al.,
2004b
) and the consequent hyperglycemia in intact but not in
eyestalkless animals (Lorenzon et al.,
2000
). The basal level of cHH in the hemolymph of P.
elegans is higher than in other species
(Webster, 1996
;
Chang et al., 1998
;
Stentiford et al., 2001
;
Zou et al., 2003
) and that
could be related to the species or, in the presence of similar eyestalk cHH
content (Lorenzon et al.,
2004b
) and rate of synthesis and release, to a smaller relative
volume of the body fluid compartment and/or possibly to a slower turnover of
the circulating hormone.
Therefore, further information is needed about the time course and detailed mechanisms that regulate the release of 5-HT and cHH and their binding to receptors, as well as about their half-life and catabolism in the hemolymph.
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Acknowledgments |
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