Beta-adrenergic control of plasma glucose and free fatty acid levels in the air-breathing African catfish Clarias gariepinus Burchell 1822
1 Institute of Biology Leiden, Leiden University, PO Box 9516, 2300 RA,
Leiden, the Netherlands
2 Department of Molecular Pharmacology, University Centre for Pharmacy,
University of Groningen, 9713 AV, Groningen, the Netherlands
* Author for correspondence (e-mail: heeswijk{at}rulsfb.leidenuniv.nl)
Accepted 29 March 2005
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Summary |
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Key words: ß-adrenergic stimulation, FFA, noradrenaline, isoprenaline, air-breathing, African catfish, Clarias gariepinus
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Introduction |
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Some fish species on the other hand can frequently encounter hypoxia at the
organismal level, as water is a relative poor source of oxygen and, by nature,
often has strongly fluctuating oxygen levels. As in mammals, catecholamine
levels in fish are elevated during hypoxia but FFA levels fall rapidly,
particularly in hypoxia-tolerant fish species like carp Cyprinus
carpio (Van Raaij et al.,
1996; Van Ginneken et al.,
1998
) and tilapia Oreochromis mossambicus
(Vianen et al., 2002
). In
tilapia, noradrenaline appeared to be solely responsible for mediating this
decrease by a reduction of adipose lipolysis
(Vianen et al., 2002
). The
suppression of plasma FFA levels by noradrenaline is possibly a protective
mechanism against fatty acid poisoning in fish under hypoxia
(Van den Thillart et al.,
2002
).
In mammals, 2-adrenoceptors are known for their
anti-lipolytic action (Fain and
Garcia-Sainz, 1983
; Smith,
1983
) and, therefore, they were the most likely receptors to
mediate a decrease in FFA levels in fish. However, both at the organismal
level (Van den Thillart et al.,
2001
) and at the cellular level in adipose tissue
(Vianen et al., 2002
),
2-adrenoceptors were not directly involved in mediating
decreased FFA concentrations by noradrenaline. Activation of
ß-adrenoceptors, on the other hand, completely mimicked the effect of
noradrenaline in lowering plasma FFA levels
(Van den Thillart et al.,
2001
) and decreasing adipose tissue lipolysis
(Vianen et al., 2002
). This
was a novel finding as ß-adrenoceptor activation in mammals strongly
enhances lipolysis.
Van den Thillart et al.
(2001) hypothesised that this
change in the role of noradrenaline from fish to mammals may be connected to
the transition from water- to air-breathing. Therefore, in the present study
the effect of ß-adrenoceptor stimulation on plasma FFA levels was
investigated in the air-breathing African catfish Clarias gariepinus.
Clarias species are among the best-known air-breathing fish species
(Graham, 1997
) and are mostly
classified as facultative air-breathers
(Magid, 1971
;
Jordan, 1976
;
Bevan and Kramer, 1987
),
meaning that they can live indefinitely on aquatic oxygen and breathe air only
when necessary. When African catfish are subjected to low aquatic oxygen
tensions, the air-breathing frequency increased, resulting in a constant total
oxygen consumption (Magid,
1971
; Jordan,
1976
). In this way, African catfish can sustain a complete aerobic
metabolism at low aquatic oxygen tensions and it is thus unlikely that it
experiences functional hypoxia in its natural surroundings. Therefore, we
hypothesised that the decreasing effect of ß-adrenergic stimulation on
plasma FFA levels would not be present in this species. Plasma glucose levels
were measured because ß-adrenergic stimulation has a known hyperglycemic
effect.
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Materials and methods |
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Pre-experimental protocol
The experiments were conducted in flow chambers supplied with well-aerated
water of 25°C as part of a 3 m3 recirculation system. The flow
rate through the flow chambers was approximately 1 l min1.
The fish could move back and forth freely without being able to turn. The flow
chambers were closed with a darkened lid to prevent startling of the fish by
outside movements. The flow chambers contained about 2 cm of air to allow
air-breathing.
Before the start of an experiment, the fish were placed individually in the flow chambers and deprived of food from that moment on. After 3 days of acclimatisation, a fish was anaesthetised in a MS222 solution (300 mg ml l1, tricaine methanesulphonate, Argent Chem. Lab., Redmond, WA, USA). After cessation of gill movements, the fish was placed on an operation table with the ventral side up. Both gills were opened with operation clamps and continuously irrigated with well-aerated water containing MS222 (150 mg ml l1).
Fish were cannulated in the dorsal aorta after Soivio et al.
(1975). After cannulation the
fish were placed back into the flow chambers and allowed to recover for 2 days
during which the cannulae were filled with a PVP (poly-vinyl-pyrrolidon,
Merck, Amsterdam, The Netherlands) solution with 4% sodium citrate as
anticoagulant. During the experiment the cannulae were filled with a 1% sodium
citratesaline solution. This 5 day pre-experimental protocol has been
shown to minimise the effects of handling, anaesthesia and surgery
(Van Raaij et al., 1996
).
Experimental protocol
Five different infusion protocols were used. A control infusion was carried
out with Ringer's saline (Wolf,
1963). Two different agonists were infused: noradrenaline
(
- and ß-agonist, 154 µg kg1) and
isoprenaline (nonselective ß-agonist, 27 µg kg1).
Based on a half-life of 10 and 100 min, respectively (G. J. Vianen,
unpublished results) and an extracellular volume of 8% of the body mass, these
amounts would result in a 106 mol l1
concentration in the blood of the fish at the end of infusion. Similar
concentrations of noradrenaline and isoprenaline evoked a significant effect
in carp (Van den Thillart et al.,
2001
). In some experiments isoprenaline infusion was preceded by a
bolus injection of an antagonist: either atenolol (selective
ß1-antagonist, 213 µg kg1 resulting in
105 mol l1) or ICI 118,551 (selective
ß2-antagonist, 250 µg kg1 resulting in
105 mol l1). In carp, atenolol and ICI
118,551 were applied at the same concentration and evoked clear and opposing
effects on plasma FFA levels (Van den
Thillart et al., 2001
). These antagonists at this concentration
were therefore considered to be selective and appropriate.
The experiments started between 08.30 h and 09.30 h by taking two initial blood samples at time t=0.75 and 0.25 h before start of infusion. Together with the second blood sampling, the fish received a bolus of Ringer's saline or a bolus of Ringer's saline containing the antagonist. At t=0 h, a 1.5 h infusion period started using Ringer's saline or Ringer's saline containing the agonist plus 1 mg ml l1 ascorbic acid as antioxidant. To this purpose a microinfusion pump (Fine Mechanical Dept., Leiden University, The Netherlands) was used at an infusion rate of 7.4 µl min1. During infusion, blood was sampled at t=0.5 and 1 h. To allow sampling the infusion pump was stopped for 300 s, after which infusion was resumed using a 10x higher speed for 33 s, followed by infusion at normal speed. Immediately after infusion a blood sample was taken at t=1.5 h and subsequently at t=2.5, 3.5, 5.5, 9.5 and 24 h.
Analytical procedures
Blood sampling (270 µl) was done using gas-tight microliter syringes
containing 30 µl of 4% sodium citrate as anticoagulant. On whole blood
samples the hematocrit (2x9 µl) and hemoglobin content (2x10
µl) were determined. The hematocrit was measured by filling heparinized
capillaries followed by centrifugation in a mini-centrifuge (Compur M1100,
Bayer, München, Germany). The hemoglobin concentration was measured using
a hemoglobin test kit from Roche (Almere, The Netherlands). The remaining
blood was centrifuged for 5 min at 15 000 g and plasma was
separated immediately. 50 µl samples of untreated plasma were stored at
80°C for FFA determination. For glucose and lactate measurements, a
plasma sample was added to 6% trichloric acetic acid in a 1:4 volume ratio,
mixed and put on ice for at least 20 min to precipitate plasma proteins. After
centrifugation, two samples of the supernatant were stored at 20°C
and analysed within a week.
After neutralisation with 1 mol l1
K3PO4, plasma concentrations of lactate were measured
according to the method of Hohorst
(Bergmeyer, 1970) and glucose
by an enzymatic test kit (Instruchemie, Delfzijl, The Netherlands). Plasma FFA
concentrations were measured using an enzymatic test kit (Waco Chemicals,
Instruchemie).
Chemicals
Noradrenaline-bitartrate, isoprenaline-hydrochloride and ICI
118,551-hydrochloride were obtained from Sigma (Zwijndrecht, The Netherlands).
Atenolol-hydrochloride was a kind gift from AstraZeneca (Macclesfield,
Cheshire, UK). All other chemicals were of analytical grade.
Data analyses and statistics
Data are presented as means ± S.E.M. All values were
normalised relative to the initial values to compensate for the effect of
individual variation. The mean cellular hemoglobin content (MCHC) was
calculated as hemoglobin concentration divided by the hematocrit. The area
under the curve (AUC) during infusion (01.5 h) was calculated for the
relative glucose data in % h.
Statistical differences (P<0.05) were tested using Sigmastat 2.03. Differences between sampling points and initial values within each group were tested with a repeated-measures analysis of variance (ANOVA) on ranks according to Dunnett's method, while differences between groups were tested with a MannWhitney rank sum test or an ANOVA on ranks.
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Results |
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The initial lactate concentration was 0.63±0.06 mmol l1. No significant changes occurred in any infusion groups except for the isoprenaline + atenolol group, in which the lactate concentration came slightly above 1.0 mmol l1 from t=1 to 5.5 h. This increase was significantly different from the initial values, but was not different from the saline and isoprenaline infusion.
The initial plasma glucose concentration was 2.82±0.13 mmol l1. The glucose concentration in the saline infused group showed a marked decrease after the infusion, resulting in significantly different values at t=3.5 and 5.5 h of 56.8±13.7% and 51.0±14.9% of the initial value, respectively. Subsequently, the plasma glucose concentration returned to the initial value (Fig. 2).
|
When infusion of isoprenaline was preceded by either of the two antagonists, plasma glucose levels significantly increased (Fig. 3). When the selective ß2-antagonist ICI 118,551 was used, the maximal glucose level at the end of infusion was 221.3±32.5%, which was not significantly higher than in the absence of ICI 118,551. With the selective ß1-antagonist atenolol present, even higher maximum levels of 271.4±33.4% were noticed, but again no significant difference from the infusion with isoprenaline alone was found. After infusion the glucose levels, as compared to the saline infusion, stayed significantly elevated with both antagonists up to t=3.5 h for ICI 118,551 and up to 5.5 h for atenolol. No significant differences were found compared to the isoprenaline infusion, except for atenolol after 9.5 h.
|
The mean initial FFA concentration amounted to 0.29±0.02 mmol l1. The FFA concentration in the saline group showed a marked decrease immediately after the beginning of the experiment from 106.8±11.4% at t=0.75 h to 61.6±5.1% at t=0.5 h. The FFA concentration was maintained at this low level up to t=2.5 h, after which a clear overshoot occurred to a significantly different value of 201.3±23.1% at t=9.5 h. After 24 h, the FFA levels had returned close to the initial value (Fig. 4).
|
As the FFA levels had already dropped during the infusion of saline, it was difficult to visually distinguish the effect of the antagonists. Therefore, the data of all three isoprenaline infusions were corrected for the saline infusion data (Fig. 5). With the selective ß1-antagonist atenolol present, the FFA concentration followed the same course as when only isoprenaline was administered; at t=0.5 h the FFA levels were significantly different from the initial values only and at t=1 and 1.5 h they also differed significantly from the saline infusion. The FFA level at the end of infusion was decreased by 38.8±6.8% as compared to saline infusion. With the selective ß2-antagonist ICI 118,551 present, the decrease of FFA levels was delayed by 0.5 h, resulting in a rightward shift of the timeresponse curve during the isoprenaline infusion. After 0.5 h, the FFA concentration was significantly different as compared to the infusion with only isoprenaline, but not significantly different as compared to the initial value and the saline infusion. At the end of the infusion the FFA levels were no longer significantly different from the isoprenaline infusion and the maximal reduction was similar, namely 31.1±2.4%, being 33.5% of the initial value.
|
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Discussion |
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The infusion of saline induced a significant decrease in plasma glucose and
FFA levels in African catfish, which reflects a circadian fluctuation in both
metabolites (Van Heeswijk et al.,
2005). Comparable circadian fluctuations in blood metabolites have
been reported for numerous other fish species (see review by
Boujard and Leatherland, 1992
).
Such a decrease in metabolites is most likely linked to the moment of feeding
and the concomitant release of hormones. Although the fish in our study were
fasted for 3 days, a feeding-entrained hormonal release could still have been
present (Gutierrez et al.,
1984
).
In contrast to isoprenaline, noradrenaline induced a rise in both
hematocrit and, to a lesser extent, hemoglobin with a non-significant decline
in MCHC. This means that the increase in hematocrit is mainly due to extra
erythrocytes brought into circulation from the spleen, which releases
erythrocytes upon stimulation of -adrenoceptors
(Nilsson and Grove, 1974
). An
increase in hematocrit due to erythrocyte swelling upon ß-adrenergic
stimulation was not evident (Soivio and
Nikinmaa, 1981
; Nikinmaa et
al., 1987
). A catecholamine-induced cell swelling is not present
in all fish species (Perry and Reid,
1992
). When present, as in carp, it is almost absent in normoxic
conditions as compared to hypoxic conditions
(Salama and Nikinmaa, 1990
),
which explains why ß-adrenergic stimulation by isoprenaline in normoxic
carp (Van den Thillart et al.,
2001
), as in African catfish in this study, did not have a
significant effect on hematocrit and MCHC.
Glucose
Both catecholamines (noradrenaline and isoprenaline) induced hyperglycemia
in African catfish, as reported for numerous fish species (see review by
Fabbri et al., 1998). This is
generally accepted to be mainly mediated by ß-adrenoceptor stimulated
glycogenolysis and ß-adrenoceptor inhibited glycolysis in the liver
(Birnbaum et al., 1976
;
Janssens and Lowrey, 1987
;
Mommsen et al., 1988
;
Wright et al., 1989
;
Reid et al., 1992
). However,
the presence of stimulatory
-adrenoceptors has been demonstrated in
vitro (Brighenti et al.,
1987
; Moon et al.,
1993
; Fabbri et al.,
1995
,
1999
). Although the fact that
isoprenaline completely mimicked the effect of noradrenaline also suggests
that in African catfish hyperglycemia was mainly mediated by
ß-adrenoceptors, our data do not allow differentiation between ß-
and
-adrenoceptor effects.
Blockage of either of the ß1- or
ß2-adrenoceptors did not inhibit the increase in plasma
glucose levels to any extent, suggesting that these receptors are not the main
receptors mediating this increase. Blockage of either or both
ß-adrenoceptors actually led to further enhanced glucose levels when
compared to infusion with isoprenaline only, although the difference was only
significant for the ß1-adrenoceptor. This finding could imply
the presence of a stimulatory ß-adrenoceptor type on the liver of African
catfish other than ß1 and ß2. The only other
ß-adrenoceptor reported to be present in fish is the
ß3-adrenoceptor. The first report of a functional
ß3-adrenoceptor was on adipose tissue of tilapia by Vianen et
al. (2002). Nickerson et al.
(2003
) using molecular tools
identified two types of the ß3-adrenoceptor in trout, where it
was expressed mainly in blood, gill and heart. In contrast to these two
studies, the hepatic ß-adrenoceptor from African catfish was not
identified directly but indirectly using antagonists. The results from this
study (see Fig. 5) and from Van
den Thillart et al. (2001
)
suggest functional selectivity of these antagonists. These data should be
treated cautiously, however, as several studies indicate a possible
discrepancy in the characteristics of adrenergic ligands between mammals and
teleost (Brighenti et al.,
1987
; Moon and Mommsen,
1990
; Fabbri et al.,
1992
). Additional experiments with African catfish hepatocytes
using both pharmacological and molecular tools will identify the subtype of
the hepatic ß-adrenoceptor in this species.
Only one ß-adrenoceptor (not ß1 and
ß2) mediated the hepatic glucose release in African catfish.
Also in eel Anguilla anguilla
(Fabbri et al., 2001) and
trout there was only one ß-adrenoceptor type present in the liver
(Fabbri et al., 1995
;
Dugan and Moon, 1998
); in trout
it was identified as a ß2-adrenoceptor
(Reid et al., 1992
;
McKinley and Hazel, 1993
). In
rockfish Sebastes caurinus hepatocytes, glucose release was mediated
by the ß1-adrenoceptor although the presence of another
adrenoceptor could not be excluded (Danulat
and Mommsen, 1990
). Both ß1- and
ß2-adrenoceptors were responsible in carp for an increase in
plasma glucose levels (Van den Thillart et
al., 2001
), although only one binding site appeared to be present
in carp liver (Janssens and Lowrey,
1987
). Two different binding sites were present on hepatic
membranes of the Australian lungfish Neoceratodus forsteri
(Janssens and Grigg, 1988
) and
of bullhead catfish Ictalurus melas
(Fabbri et al., 1992
).
A straightforward explanation for the increasing effect of a
ß1- and ß2-blockage on plasma glucose levels
is that both adrenoceptor types had a suppressing effect on the glucose
release. The presence of inhibitory ß1- and
ß2-adrenoreceptors on the liver has not been reported in
literature as only stimulatory hepatic ß-adrenoceptors have been found
(see review by Fabbri et al.,
1998). However, an additional target organ involved in the
potentiation by ß1- and ß2-adrenoceptor
blockage is the pancreas. In vivo catecholamine administration both
reduced and enhanced plasma insulin levels
(Ince and Thorpe, 1977
;
Zelnik et al., 1977
;
Mommsen and Plisetskaya,
1991
). In vitro, however, ß-adrenergic stimulation
of the pancreatic islet cells by isoprenaline consistently enhanced the basal
release of insulin (Tilzey et al.,
1985a
,b
;
Milgram et al., 1991
). The
effects of adrenaline and noradrenaline in vitro were biphasic:
inhibition at low adrenaline concentrations (1010 mol
l1) and stimulation at high concentrations
(106 mol l1) in trout Oncorhynchus
mykiss (Tilzey et al.,
1985a
), while in anglerfish Lophius americanus,
increasing noradrenaline concentrations induced a switch from stimulation to
inhibition (Milgram et al.,
1991
). These differential effects were most likely caused by
differences in the ratio of inhibitory
- and stimulatory
ß-adrenoceptors (Milgram et al.,
1991
; Mommsen and Plisetskaya,
1991
). Based on these literature data, the injection of
ß-adrenoceptor antagonists in our study possibly blocked an
isoprenaline-induced insulin release in African catfish. As insulin is a known
hypoglycemic hormone in fish (Mommsen and
Plisetskaya, 1991
), ß-adrenoceptor blockage could thus
indirectly have resulted in a larger increase in plasma glucose than without
this blockage. In future experiments, the infusion of cannulated African
catfish with the same agonists/antagonist in combination with insulin
measurements will demonstrate if this hypothesis is correct.
Free fatty acids
In carp, ß-adrenergic stimulation was specifically responsible for
reduced plasma FFA levels; -adrenergic stimulation appeared to have
only indirect effects (Van den Thillart et
al., 2001
). Vianen et al.
(2002
) showed that the
decrease in plasma FFA in tilapia was due to a ß-adrenoceptor mediated
decrease in adipocyte lipolysis;
-adrenoceptor blockage had no effect
on a noradrenaline-mediated decrease in adipocyte lipolysis, suggesting no
involvement of
-adrenoceptors. In African catfish, the ß-agonist
isoprenaline and the
- and ß-agonist noradrenaline had comparable
suppressive effects on the plasma FFA levels, suggesting that in this species
it is also a mainly ß-adrenoceptor mediated process. No specific
ß-adrenoceptor agonists have been studied in other fish species.
Noradrenaline, however, has been used frequently and reduced plasma FFA levels
in all studies (carp and bream Abramis brama, Farkas,
1967a
,b
;
goldfish Carassius auratus,
Minick and Chavin, 1973
; pike
Esox lucius, Ince and Thorpe,
1975
, carp, Van Raaij et al.,
1995
).
When the isoprenaline infusion was preceded by the
ß1-antagonist, the decrease in plasma FFA levels was identical
to that measured when only isoprenaline was infused. Injection of the
ß2-antagonist, on the other hand, delayed the decrease in
plasma FFA levels significantly. This rightward shift in the
timeresponse curve indicates that ß2-adrenoceptors
mediated the decrease in plasma FFA levels in African catfish. The reduction
in adipocyte lipolytic rate in tilapia was mediated by ß1
and/or ß2-adrenoceptors, in combination with the
ß3-adrenoceptor (Vianen et
al., 2002). In carp, however, ß1-adrenoceptors
mediated a decrease in FFA levels, while ß2-adrenoceptors
mediated an increase. These opposite effects were believed to result from a
decreased adipose lipolysis and an increased hepatic lipolysis, respectively
(Van den Thillart et al.,
2001
). The fact that no stimulatory effect was found in African
catfish like in carp implies that lipolysis in African catfish liver cannot or
only barely be stimulated by ß-adrenoceptors.
The data presented here indicate that ß-adrenergic stimulation
mediated the same physiological reaction in air-breathing African catfish as
in other waterbreathing fish species, namely suppression of plasma FFA levels.
For Clarias, aquatic oxygen is still the primary source of oxygen as
they are normally classified as a facultative airbreathers
(Magid, 1971;
Jordan, 1976
;
Bevan and Kramer, 1987
).
Apparently, air-breathing in this species did not lead to an evolutionary
change in the control of lipolysis as we hypothesised. Recent experiments
showed that environmental hypoxia is potentially a stress condition for
African catfish, i.e. submersion without access to aerial oxygen (J.C.F.v.H.,
J. van Pelt and G.E.E.J.M.v.d.T., unpublished observations). African catfish
is caught at a depth of over 50 m in Lake Victoria
(Goudswaard and Witte, 1997
),
which makes it highly unlikely that it will surface to breathe air. Hence, in
its natural habitat African catfish is also likely to become hypoxic. Obligate
air-breathers like adult lungfish (Protopterus sp.), on the other
hand, are vitally dependent on aerial oxygen and can only live when allowed to
air-breathe (Graham, 1997
).
The respiratory behaviour of adult African lungfish Protopterus
aethiopicus was indeed not affected by decreasing aquatic oxygen tensions
when allowed to air-breathe (Johansen and
Lenfant, 1968
) as opposed to African catfish
(Johnston et al., 1983
). Hence
environmental hypoxia, even when it only means submersion as in African
catfish, is by definition not a physiologically relevant situation for African
lungfish, rendering this species an interesting model fish for our
hypothesis.
Air-breathing in fishes has evolved independently in several fish lineages.
The evolution of air-breathing was originally thought of as a way to survive
environmental hypoxia (Graham,
1997). Some authors have suggested, however, that the function of
air-breathing is to maintain activity levels when aquatic oxygen levels are
low (Grigg, 1965
;
Burleson et al., 1998
;
Farmer and Jackson, 1998
).
Therefore, the main driving force for the evolution of air-breathing may not
necessarily be survival of hypoxia, but rather coping with hypoxia by
sustaining high activity levels. The suppressive role of noradrenaline on
plasma FFA levels is hypothesised to be a survival mechanism during hypoxia
(Van den Thillart et al.,
2002
). Therefore, an alternative drive for the evolution of
air-breathing is supported by our finding, that noradrenaline has a similar
suppressive effect on plasma FFA levels in air-breathing African catfish, as
in other waterbreathing fishes. Hence, air-breathing in African catfish most
likely did not evolve as a survival mechanism for hypoxia.
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