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First published online July 14, 2008
Journal of Experimental Biology 211, 2460-2466 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.018143
In vivo regulation of rainbow trout lipolysis by catecholamines
Biology Department, University of Ottawa, 30 Marie Curie, Ottawa, Ontario, Canada, K1N 6N5
* Author for correspondence (e-mail: lmagn030{at}uottawa.ca)
Accepted 21 May 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: appearance of glycerol, ectotherms, epinephrine, lipolytic rate, norepinephrine, reesterification
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Raclot and Oudart, 1999;
Hulbert et al., 2007). In the
intact organism, lipolysis is measured as the rate of appearance of glycerol
(Ra glycerol) (Wolfe,
1992), and it has been thoroughly investigated in mammals, mainly
in humans (Klein et al., 1989;
Wolfe et al., 1990;
Klein et al., 1995;
Quisth et al., 2005).
Unfortunately, the information available for other vertebrates is restricted
to two in vivo studies on birds
(Bernard et al., 2002;
Vaillancourt and Weber, 2007)
and one on fish (Bernard et al.,
1999). The lack of data for ectotherms is particularly unfortunate
because an adequate supply of fatty acids is crucial to restructure membrane
phospholipids during homeoviscous adaptation
(Hazel and Williams, 1990) and
to fuel endurance swimming in fish (Moyes
and West, 1995).
The rate of lipolysis is modulated by several hormones, including
catecholamines, insulin and glucagon
(Coppack et al., 1994;
Londos et al., 1999). In
mammals, lipolysis is stimulated by norepinephrine (NE) as well as epinephrine
(Epi) (Fain and Garcia-Sainz,
1983; Nonogaki,
2000), but these hormones have effects that are controversial in
fish. Various species show different responses in vitro, and the
effects of catecholamines on fish lipolysis have not been measured in
vivo using tracer methods. Overall, however, NE appears to inhibit
lipolysis in fish adipose tissue (Farkas,
1967a, Farkas,
1967b; Vianen et al.,
2002), although not in all species
(Farkas, 1967b). NE-induced
inhibition of fish lipolysis also appears to be supported by in vivo
observations that the hormone decreases the level of plasma non-esterified
fatty acids (NEFA) in many species
(Farkas, 1967b;
Minick and Chavin, 1973;
Ince and Thorpe, 1975;
Van Raaij et al., 1995), with
a few exceptions (Leisbon et al.,
1968; Plisetskaya,
1980). However, to assume that the plasma concentration of NEFA
reflects changes in lipolytic rate might lead to erroneous conclusions
(Haman et al., 1997). Even for
Epi, the response can be very different between fish and mammals. Some studies
report in vivo inhibition of lipolysis by Epi for some fish species
(Minick and Chavin, 1973;
Ince and Thorpe, 1975),
whereas others show no local effect on adipose tissue
(Migliorini et al., 1992). The
only information available for rainbow trout shows activation of lipolysis by
both catecholamines in isolated hepatocytes
(Van Heeswijk et al., 2006)
but no effect of Epi on red muscle or on the plasma concentration of NEFA
in vivo (Bilinski and Lau,
1969; Perrier et al.,
1972).
The goal of the present study was to investigate the effects of catecholamines on Ra glycerol in intact fish to obtain an integrated hormonal response rather than tissue- or cell-specific contributions to total fatty acid supply. Our aim was to quantify the effects of NE and Epi on the lipolytic rate of rainbow trout using in vivo tracer kinetics. Based on the balance of evidence presently available, it was hypothesized that trout lipolysis would be inhibited by NE and stimulated by Epi. We also examined the relationship between Ra glycerol and glycerol concentration to determine whether the concentration of glycerol can be used as a reliable index of fish lipolysis.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Surgery
Fish were fasted for 48 h before surgery and did not feed during recovery
or measurements. Double catheterization was performed as described previously
(Haman and Weber, 1996). The
animals were anesthetized in a solution of 0.1 g l–1
ethyl-N-aminobenzoate sulfonic acid (MS-222) buffered with 0.2 g
l–1 sodium bicarbonate, and two PE-50 catheters (Intramedic,
Clay-Adams, Sparks, MD, USA) were implanted in the dorsal aorta. Both
catheters were filled with Cortland saline and sutured to the roof of the
buccal cavity. After surgery, the animals were placed in opaque Plexiglas
chambers (60x16x18 cm) supplied with the same quality water as the
acclimatization tank at a rate of 5–6 l min–1. This low
rate was selected to maintain normoxic conditions without causing swimming.
During recovery from surgery, the catheters were regularly checked for patency
and flushed with Cortland saline containing sodium citrate as an anticoagulant
(13 µmol ml–1). Only animals with a hematocrit (packed
cell volume) >20% after recovery from surgery were used in experiments.
Glycerol kinetics were then measured in the same chambers 24 h after
surgery.
Continuous tracer infusions
The Ra glycerol, also commonly called the lipolytic
rate, was measured by continuous infusion of 2-[3H]glycerol (37
GBqmmol–1; Amersham, Buckinghamshire, UK), as described
previously (Bernard et al.,
1999). The infusate was prepared daily by drying 0.94MBq of the
radioisotope under N2 and resuspending in Cortland saline. This
solution was infused for 3 h at 1 ml h–1 through one of the
catheters using a calibrated syringe pump (Harvard Apparatus, South Natick,
MA, USA). Tracer infusion rates ranged between 375x103 and
148x104 d.p.m. kg–1 min–1.
Because the infusate had a high specific activity, the total amount of
glycerol administered (labeled and unlabeled) was <0.5 nmol
kg–1 min–1. Isotopic steady state was
reached in <1 h. Baseline glycerol kinetics were quantified between 60 and
90 min of infusion before investigating the effects of catecholamines. After
quantifying baseline kinetics, isotope infusion was continued for 30 min while
saline, Epi or NE were administered (see next section) and for an extra 60 min
after catecholamine administration to monitor recovery from hormone
treatment.
Catecholamine administration
A second calibrated syringe pump was activated after 90 min of tracer
infusion to administer saline (control), NE or Epi for 30 min at 1 ml
h–1. To avoid light-induced breakdown of catecholamines,
hormone solutions were prepared under red, low-intensity light, and similar
light conditions were used during administration. The rates of catecholamine
administration were 0.45 nmol kg–1 min–1 for
NE and 1.34 nmol kg–1 min–1 for Epi. These
values were selected to achieve plasma concentrations of 
170 nmol
l–1 (NE) and 500 nmol l–1 (Epi) that
mimic the hormone levels noted after exhaustive swimming
(Butler et al., 1986). A
previous study shows that this rate of epinephrine administration leads to
plasma levels of 500 nmol l–1 in trout
(Weber and Shanghavi,
2000).
Blood sampling and analysis
Eight 0.3 ml blood samples were drawn in each experiment. Plasma was
immediately separated by centrifugation (5000 g for 10 min)
and stored at –80°C until subject to analyses. Each plasma sample
was divided into two aliquots to measure glycerol concentration by
spectrophotometry (Weber et al.,
1993) and glycerol activity by scintillation counting (Beckman
Coulter CS6500, Palo Alto, CA, USA). Infusion of 2-[3H]glycerol
only leads to significant radioactivity in plasma H2O, glucose and
glycerol. The specific activity of glycerol was determined after drying plasma
to eliminate labeled water and, after correction for glucose activity, using
thin layer chromatography, as described previously
(Bernard et al., 1999).
Calculations and statistical analyses
The rate of appearance of glycerol, or lipolytic rate, was calculated using
the steady-state equation of Steele
(Steele, 1959). This equation
was used because it provides more accurate estimates of flux than the
non-steady-state equation when, first, specific activity varies little over
time and, second, when rapid equilibration takes place within the metabolite
pool (caused by a rapid turnover rate relative to pool size)
(Beylot et al., 1987;
Wolfe et al., 1990). The
effects of hormone administration over time were assessed by one-way analyses
of variance with repeated measures (RM ANOVA). When significant changes were
detected, the Holm-Sidak method was used to determine which means were
different from baseline (Figs
1,
2,
3). Differences in mean
glycerol concentrations and Ra glycerol between control
and catecholamine-treated animals were evaluated with unpaired
t-tests (Table 1). The
values given are means ± s.e.m. A level of significance of
P<0.05 was used in all tests.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Effects of NE
Fig. 2 shows the effects of
administration of NE on the concentration of plasma glycerol, specific
activity and Ra glycerol. Baseline values for glycerol
concentration and Ra glycerol averaged 0.20±0.05
µmol ml–1 and 4.4±0.6 µmol kg–1
min–1, respectively. The glycerol concentration and
Ra glycerol were both decreased by norepinephrine
(P<0.05). The concentration reached a minimal value of
0.10±0.03 µmol ml–1 and Ra
glycerol a minimal value of 2.3±0.7 µmol kg–1
min–1 after 30 min of NE administration, and both returned to
baseline during recovery (P>0.05).
Effects of Epi
Fig. 3 shows the effects of
administration of Epi on the concentration of plasma glycerol, specific
activity and Ra glycerol. Baseline values for glycerol
concentration and Ra glycerol averaged 0.22±0.05
µmol ml–1 and 4.4±0.5 µmol kg–1
min–1, respectively. The glycerol concentration and
Ra glycerol were both stimulated by Epi
(P<0.001). The concentration reached a maximal value of
0.55±0.07 µmol ml–1 and Ra
glycerol a maximal value of 8.2±0.8 µmol kg–1
min–1 after 20 min of Epi administration. The concentration
and Ra glycerol stayed elevated until the end of Epi
administration (P<0.001), but they returned to baseline during
recovery (P>0.05). Table
1 summarizes the mean values for plasma glycerol concentration and
Ra glycerol during the final 10 min of administration of
saline, Epi and NE. Both parameters were decreased by NE (P<0.05)
and increased by Epi (P<0.001).
Relationship between glycerol concentration and rate of appearance
Fig. 4 plots the plasma
glycerol concentration versus Ra glycerol (or lipolytic
rate) during the final 10 min of administration of saline (stars), Epi (filled
circles) and NE (unfilled circles). Separate linear regressions were fitted
for the three groups. For Epi, the relationship had a positive slope different
from 0 (r2=0.48, P<0.05). The concentration
and rate of appearance were not significantly related for saline
(r2=0.03, slope not different from 0, P=0.905)
and for NE (r2=0.05, slope not different from 0,
P=0.830).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Assessing lipolytic rate and reesterification in vivo
Ra glycerol is recognized as the best estimate of
lipolysis, and it has been widely used to quantify whole-body lipolytic rates
in vertebrates, including mammals
(Issekutz et al., 1975;
Wolfe, 1992;
Weber et al., 1993;
McClelland et al., 2001;
Henderson et al., 2007;
Houser et al., 2007), birds
(Bernard et al., 2002;
Bernard et al., 2003;
Vaillancourt and Weber, 2007)
and fish (Bernard et al.,
1999). Using Ra glycerol for this purpose is
recommended because the glycerol produced by lipolysis must obligatorily
appear in the circulation, in situ recycling being prevented by the
negligible activities of glycerol kinase in the adipose tissue and muscle of
vertebrates (Newsholme and Taylor,
1969; Brooks et al.,
1982; Reshef et al.,
2003). By contrast, the rate of appearance of NEFA
(Ra NEFA) cannot be used to estimate the lipolytic rate
because a significant fraction of the fatty acids produced by lipolysis is
reesterified in situ. This important difference between glycerol and
NEFA is illustrated by the fact that typical ratios of Ra
NEFA/Ra glycerol measured in vivo or in
vitro are well below 3.0 (Bernard et
al., 1999; Henderson et al.,
2007). The other reason why Ra glycerol
adequately reflects lipolysis is because this pathway is the only significant
source of glycerol (Issekutz et al.,
1975; Wolfe, 1992;
Houser et al., 2007). It could
be argued that this might not be true for fish because some species can use an
alternative pathway to produce glycerol as an antifreeze from glucose and
amino acids (Raymond, 1992;
Raymond and Driedzic, 1997;
Driedzic et al., 2006).
However, this particular adaptation for cold tolerance depends on high
activities of hepatic glycerol-3-phosphatase, an enzyme present only in unique
species such as rainbow smelt (Osmerus mordax) but virtually absent
in species lacking freeze tolerance such as trout and other members of the
smelt family (Treberg et al.,
2002; Lewis et al.,
2004; Walter et al.,
2006). In trout, there is no evidence that glycerol released in
the circulation could be of nonlipolytic origin.
Total reesterification is the sum of primary reesterification (defined as
recycling without fatty acid exit from intracellular sites of lipolysis) and
secondary reesterification (defined as recycling after fatty acid transit
through the circulation). The measurement methods and the equations necessary
to quantify primary, secondary and total reesterification have been detailed
in previous publications (Wolfe et al.,
1990; Wolfe, 1992;
Kalderon et al., 2000;
Reidy and Weber, 2002). In the
present study, we have calculated total reesterification as follows:
 | (1) |
Because the rate of fatty acid oxidation has not been measured in fish, it
was estimated from the metabolic rate, assuming that fatty acids were the only
oxidative fuel used by resting trout. In a previous study
(Bernard et al., 1999), primary
reesterification of rainbow trout was calculated as follows:
 | (2) |
The results from both studies are consistent because primary
reesterification was estimated at 68% of all fatty acids released by lipolysis
(Bernard et al., 1999), and
total reesterification estimated at 87% (present study), suggesting that the
difference (19%) is explained by secondary reesterification.
Opposing effects of NE and Epi on trout lipolysis
At the whole-organism level, the present study shows that NE (inhibition)
and Epi (activation) have opposite effects on the lipolytic rate of rainbow
trout (Figs 2 and
3). Therefore, the regulation
of lipolysis by catecholamines might play a particularly important role during
hypoxia, an environmental stress causing the strong release of NE
(Montpetit and Perry, 1998).
This hormone probably causes the decreases in plasma NEFA concentration
(Van Raaij et al., 1996) and
NEFA turnover rate (Haman et al.,
1997) previously observed when trout are exposed to hypoxic
conditions. The inhibition of lipolysis probably is also responsible for the
decreases in plasma NEFA concentration reported after administration of NE in
bream Abramis brama and pike-perch Sander lucioperca
(Farkas, 1967b), as well as in
goldfish Carassius auratus
(Minick and Chavin, 1973),
pike Esox lucius (Ince and
Thorpe, 1975) and carp Cyprinus carpio
(Van Raaij et al., 1995).
These in vivo effects are consistent with the inhibition of lipolysis
demonstrated in vitro for adipose tissue in carp, pike-perch
(Farkas, 1967b) and tilapia
Oreochromis mossambicus (Vianen
et al., 2002). Administration of Epi causes the stimulation of
lipolysis (Fig. 3), and this
result is consistent with previous studies in fish showing Epi-induced
increases in plasma NEFA concentration [scorpion fish Scorpaena
porcus (Leisbon et al.,
1968), eel Anguilla anguilla
(Larsson, 1973), lamprey
Petromyzon marinus (Plisetskaya,
1980), plaice Pleuronectes platessa
(White and Fletcher, 1989) and
carp (Van Raaij et al.,
1995)], although no such increase could be demonstrated in trout
Oncorhynchus mykiss (Perrier et
al., 1972).
In mammals, NE and Epi increase fatty acid mobilization from adipose tissue
and muscle by activating hormone-sensitive lipase (HSL). The presence of one
or more lipases also activated by hormones, homologous or not to mammalian
HSL, has been reported in the liver and adipose tissue of rainbow trout
(Albalat et al., 2005;
Van Heeswijk et al., 2006). In
trout hepatocytes, both catecholamines activate lipolysis
(Van Heeswijk et al., 2006),
but no Epi-induced stimulation of lipolysis was detected in red muscle slices
from trout (Bilinski and Lau,
1969). Taken together, these in vitro studies suggest
that the increase in lipolytic rate observed in the present study after in
vivo administration of Epi might be caused by the activation of HSL-like
lipases in liver and adipose tissue but not in red muscle. Furthermore, the
potential implication of other lipases such as lipoprotein lipase (LPL) or
other circulating hormones acting indirectly, such as glucagon, insulin or
cortisol, cannot be eliminated (Zechner,
1997; Merkel et al.,
2002; An et al.,
2005). In trout, a homolog of mammalian LPL sensitive to insulin
has also been characterized in several tissues
(Lindberg and Olivecrona,
2002; Albalat et al.,
2006; Magnoni and Weber,
2007). Therefore, further studies will be needed to distinguish
the effects of HSL-like lipases and LPL and to characterize the potential
interactions of catecholamines with other hormones. Even though NE causes the
stimulation of mammalian lipolysis in vivo, it also triggers local
inhibition in adipocytes (Holm,
2003). The same mechanism that causes inhibition in mammalian
adipocytes might also be responsible for the in vivo lipolytic
response reported here in trout (Fig.
2).
Plasma glycerol concentration is not an index of lipolytic rate
The observed changes in Ra glycerol caused by Epi
correlated weakly with changes in plasma glycerol concentration, but no such
correlation was apparent for NE (Fig.
4). Because Epi causes a much stronger stimulation of cardiac
output than NE, the relationship between flux and concentration could be
influenced by differential effects of catecholamines on the cardiovascular
system (Gannon and Brunstock,
1969; Wood and Shelton,
1980; Randall and Perry,
1992). Previous studies have shown that plasma metabolite fluxes
can be increased in two ways: first, by augmenting concentration in plasma
(mass-action effect) or, second, by increasing blood flow (perfusion effect)
(Weber et al., 1987).
Therefore, the stimulating effect of Epi on cardiac output might have
amplified the slope of the relationship between the glycerol concentration and
Ra glycerol. Interestingly, the stimulating effect of NE
on cardiac output appears to have been sufficient to offset the negative
mass-action effect of a decrease in plasma glycerol concentration (thereby
eliminating a potential relationship between flux and concentration in the NE
experiments). A detailed analysis of trout glucose and NEFA metabolism also
showed that the plasma concentration of these metabolites does not reflect
changes in their flux (Haman et al.,
1997). The present study reinforces the idea that changes in
metabolite concentration cannot be used to speculate on possible changes in
metabolite fluxes unless a clear relationship between the two parameters has
been formally established under specified conditions.
High resting lipolytic rates in trout
In previous in vivo studies, the lipolytic rate has been measured
almost exclusively in warm-blooded animals. The rates reported here for trout
[2–8 µmol kg–1 min–1; Figs
1,
2,
3 and Bernard et al.
(Bernard et al., 1999)] fit
within the endotherm range (2–72 µmol kg–1
min–1), but relevant comparisons can only be made if
differences in metabolic rate are taken into account. Therefore, the ratios
between lipolytic rate and metabolic rate were plotted in
Fig. 5 for all vertebrates
measured to date. In endotherms, the ratio varies between 0.01 and 0.03, and
it does not vary much between rest and exercise because lipolytic rate is
stimulated in parallel with metabolic rate. This analysis reveals that
swimming trout fall within the normal vertebrate range (0.03) but that resting
trout have a drastically different ratio of 0.10, more than six times the
average (0.02). What is the physiological significance of this unexpected
observation? We have calculated the theoretical metabolic rate needed to
oxidize all fatty acids supplied by lipolysis at rest (4.6 µmol glycerol
kg–1 min–1 or 14 µmol fatty acid
kg–1 min–1). Assuming that energy metabolism
is only supported by lipids, this theoretical metabolic rate would be 360
µmol O2 kg–1 min–1 (if oleate
is considered as an average fatty acid, requiring 26 molecules of
O2 for oxidation, and if the contribution of glycerol oxidation is
ignored). Because the real metabolic rate of a resting trout is only 46
µmol O2 kg–1 min–1
(Burgetz et al., 1998), we
calculate that 13% of their lipolytic rate can fuel the resting energy
metabolism entirely. Therefore, 87% of the fatty acids released by trout
lipolysis have to undergo reesterification: a much higher proportion than in
endotherms (<70%; see Fig. 5
for references). Such high lipolytic rates (present study) and triacylglycerol
turnover rates (Magnoni et al.,
2008) demonstrate that fatty acid mobilization and
reesterification are particularly active in trout. We propose that this rapid
cycling of fatty acids might be crucial for restructuring membrane
phospholipids and, therefore, might be necessary in all ectotherms for
adequate homeoviscous adaptation.
Conclusion and perspectives
Our results show for the first time that NE inhibits whole-organism
lipolysis in trout, rather than stimulating it as in mammals. Our data support
previous in vitro studies suggesting that fish and mammals regulate
lipid mobilization differently. NE-induced inhibition of fish lipolysis might
play a particularly important role during aquatic hypoxia, when survival often
depends on regulated metabolic depression. In trout, the changes in lipolytic
rate are not well reflected by changes in the concentration of plasma
glycerol. Therefore, glycerol concentration cannot be used as an index of
glycerol flux (Ra glycerol), a recommendation previously
made for other key intermediates of energy metabolism
(Haman et al., 1997). Finally,
the present study demonstrates that resting trout maintain a
disproportionately high lipolytic rate because only 13% of the fatty acids
supplied by lipolysis are sufficient to support total energy expenditure.
Therefore, most mobilized fatty acids must undergo reesterification (87%).
Such cycling implies rapid exchange between fatty acid pools, a metabolic
adaptation improving the capacity for remodeling membrane phospholipids with
fatty acids of different chain length and degree of saturation. Determining
whether such an adaptation is ubiquitous among ectotherms strikes us as a
fascinating avenue for future research.
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Acknowledgments |
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References |
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O2) for vertebrates
measured to date. Values correspond to vertebrates at rest and during exercise
at equivalent intensities (40–70%