effect of tachycardia on lipid metabolism and expression of fatty acid

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JOURNAL OF PHYSIOLOGY AND PHARMACOLOGY 2015, 66, 5, 691-699
www.jpp.krakow.pl
B. WOJCIK1,2, E. HARASIM1, P. ZABIELSKI1, A. CHABOWSKI1, J. GORSKI1,2
EFFECT OF TACHYCARDIA ON LIPID METABOLISM AND EXPRESSION
OF FATTY ACID TRANSPORTERS IN HEART VENTRICLES OF THE RAT
1
Department of Physiology, Medical University of Bialystok, Bialystok, Poland;
Medical Institute, Lomza State University for Applied Sciences, Lomza, Poland
2
Tachycardia increases oxidation of the plasma-borne long chain fatty acids in the heart. The aim of the present study
was to examine effect of tachycardia on: 1) the total level of free fatty acids, diacylglycerols, triacylglycerols and
phospholipids in both heart ventricles; 2) 14C-palmitate incorporation in the lipid fractions; 3) expression of fatty acid
and glucose transporters in the ventricles. Tachycardia was induced in anesthetized rats by electrical atrial pacing at the
rate of 600/min. Samples of the left (LV) and right (RV) ventricle were taken after 30 and 60 min pacing. The level free
fatty acids, diacylglycerols, triacylglycerols and phospholipids was determined by means of gas-liquid chromatography
and 14C-palmitate incorporation by liquid scintillation counting, respectively. Expression of fatty acid- and glucosetransporters was determined using Western blot technique. In LV, 30min pacing increased the content of diacylglycerols
whereas the content of other lipids remained stable. After 60 min of pacing the levels of the examined lipid fractions did
not differ from the respective control values. In RV, the content of diacylglycerols and triacylglycerols was reduced both
after 30 and 60 min pacing. Tachycardia also affected incorporation of 14C-palmitate in lipid fractions of goth ventricles.
30 min pacing up-regulated plasmalemmal expression of FAT/CD36 (fatty acid translocase) in both ventricles and
reduced its microsomal expression in LV. After 60 min pacing they did not differ from the respective control values.
Plasmalemmal expression of FATP-1 (fatty acid transport protein 1) increased and its microsomal expression decreased
in RV after 30 min pacing. After 60 min pacing the plasmalemmal FATP-1 expression remained elevated whereas the
microsomal expression did not differ from the control value. Pacing did not affect or expression of FABPpm (plasma
membrane associated fatty acid binding protein) in either plasma membranes and microsomal compartments. Thirty min
pacing increased plasmalemmal and reduced microsomal expression of GLUT-4 (glucotransporter 4) in both ventricles.
It increased plasmalemmal expression of GLUT-1 (glucotransporter 1) in RV. It returned to normal after 60 min pacing.
It is concluded that tachycardia induces numerous changes in metabolism of myocardial lipids as well as expression of
fatty acid and glucose transporters in both heart ventricles.
K e y w o r d s : lipid metabolism, 14C-palmitate incorporation, fatty acid transporters, glucose transporters, tachycardia, heart
ventricles, pacing, triacylglycerols
INTRODUCTION
Blood-borne long chain fatty acids cover an essential part of
energy sources used by the heart (1). Their utilization increases
during increased contractile activity of the heart in vivo (2) and in
isolated cardiomyocytes (3). There are only very few data available
on effect of tachycardia on endogenous heart lipid metabolism. The
level of triacylglycerol in the left ventricle was found to be stable
during 15 and 30 min atrial pacing in the rat (4). Luiken at al. (3)
reported that 3 min electrostimulation of cardiomyocytes increased
incorporation of 14C-palmitate in the fraction of triacylglycerols. It
returned to normal values after 30 min stimulation. In the same
settings, incorporation of the label in the fraction of phospholipids
remained unchanged during stimulation (3). Recent data indicate
that tachycardia produces changes in metabolism of bioactive
sphingolipids in both ventricles of the rat (5). Such changes could
have an important impact on the heart resistance to
ischemia/reperfusion injury (6). We are not aware of other data
regarding the effects of tachycardia on the level of lipid fractions in
the myocardium. Also, it remains an open question whether
tachycardia affects distribution of the plasma-borne long chain
fatty acids in particular lipid fractions in the myocardium.
Long chain free fatty acids are transported across the plasma
membrane mostly with the assistance of fatty acid translocase
(FAT/CD36), plasma membrane associated fatty acid binding
protein (FABPpm) and fatty acid transport proteins (FATP1 and
FATP6) (7, 8). Studies on isolated cardiomyocytes showed that
contractile activity induced by electrical stimulation increases
plasmalemmal content of FAT/CD36 (9, 10). As far, no data are
available regarding an effect of in vivo tachycardia on behavior
of the fatty acid transporters in myocardium.
The aim of the present study was to examine effect of
tachycardia on: 1) the total level of free fatty acids,
diacylglycerols, triacylglycerols and phospholipids in the left
and right heart ventricles; 2) incorporation of 14C-palmitate in
the lipid fractions; 3) expression of fatty acid and glucose
692
transporters in the plasmalemmal and microsomal fractions of
the both ventricles of the rat.
Subcellular fractionation of cardiac myocytes
The experimental protocol was approved by the Ethical
Committee on the Animal Research at the Medical University of
Bialystok.
The experiments were carried out on male Wistar rats, 230 –
250 grams of body weight. The rats were housed in standard
conditions: temperature 21°C, 12 h light/12 h dark cycle, had free
access to tap water and commercially available rat pellet diet. The
rats were anaesthetized with thiopental (80 mg/100 g of body
weight). After anesthesia, the right jugular vein was exposed and
two electrodes were inserted in it. The electrodes were located at
the aperture of the vein. The location of the tips of the electrodes
was checked after the experiment, to confirm proper positioning.
The electrodes were connected to SC-04 stimulator. The heart
rate was continuously monitored by ECG through electrodes
administered into skeletal muscles of the four limbs. The resting
heart rate after anesthesia was 366 ± 29/min. The rats were
divided into four groups (n = 10 rats in each group): two control
groups, with 30 and 60 min of anesthesia but no pacing, and two
paced groups, subjected to heart stimulation for 30 and 60 min,
respectively. The parameters of the stimuli were: frequency
600/min, 4V, duration 100 ms. To follow incorporation of the
blood-borne free fatty acids in myocardial lipid fractions,
albumin bound 14C-palmitate (Perkin Elmer, S.A. 561 µCi/mmol)
was administered in the tail vein at a dose of 5 µCi/100 g of body
weight at zero time. Blood from the abdominal aorta and samples
of the right and left ventricle were taken.
Isolation of plasma membranes (PM) and low density
microsomes (LDM) from the left and right ventricle was
performed by subcellular fractionation. Differential
centrifugation was carried out as it was described previously
with minor modifications (15-17). After thawing, ventricles
were minced and incubated for 30 min in ice-cold high-salt
solution (2 mol/l NaCl, 20 mmol/l HEPES pH 7.4, 5 mmol/l
NaN3 and protease inhibitors). Thereafter, the suspension was
centrifuged (5 min, 1000 g) and the pellet was homogenized in
6.0 ml TES-buffer (20 mmol/l Tris pH 7.4, 1 mmol/l EDTA,
250 mmol/l sucrose and protease inhibitors) using a tightly
fitting 10-ml Potter-Elvehjem glass homogenizer with 10
strokes. Afterwards, the homogenate was spun (5 min, 1000 g)
and the pellet was re-homogenized in 4.0 ml TES-buffer. The
resulting homogenate was combined with the previous
supernatant and centrifuged (10 min, 100 g). Obtained pellet
(P1) was resuspended in 300 µl TES-buffer and saved.
Subsequently, the supernatant was spun (10 min, 5000 g) and
the pellet (P2) was resuspended in 300 µl TES-buffer and
saved. The supernatant was centrifuged again (20 min, 20 000
g) and the pellet (P3) was resuspended in 300 µl TES-buffer
and saved. Next, the supernatant was centrifuged (30 min,
48,000 g) and the pellet (P4) was resuspended in 150 µl TESbuffer and saved. After the last centrifugation of supernatant
(65 min, 250,000 g), received pellet (P5) was resuspended in
150 µl TES-buffer and saved. It has been established upon
analysis of P1-P5 pellets with ATPase sodium/potassium pump
(Na+/K+) and glucose transporter 4 (GLUT-4) immunoblotting,
that fractions P2 refers as PM- fraction and P5 as LDM fraction
according to Fuller et al. (15).
Measurement of the level of lipids
Immunoblotting
Samples of each ventricle were blotted dry and frozen in
liquid nitrogen. Next, they were pulverized in an aluminum
mortar precooled in liquid nitrogen. The powder was transferred
into a glass tube containing methanol at a temperature of –20°C
(11). Lipids were extracted according to Bligh and Dyer (12).
They were separated into different fractions by means of thinlayer chromatography. Silica plates, 220 µm (Merck) and
developing mixture composed of heptane, diisopropyl ether and
acetic acid (60 : 40 : 3 v/v/v) was employed (13). The plates
were dried, sprayed with 0.5% solution of 3’7’dichlorofloresceine in methanol, exposed briefly to ammonia
vapors and visualized under an ultraviolet lamp. The procedure
enabled localization of different lipid bands. Bands containing
the fractions of free fatty acids (FFA), diacylglycerols (DG),
triacylglycerols (TG) and phospholipids (PH) were scraped off
and methylated (14). For plasma FFA, 100 µl of plasma was
extracted and methylated using the same approach. The
individual fatty acids of each fraction were identified and
quantified by means of gas-liquid chromatography (HewlettPackard 5890 Series II gas chromatograph with Varian CPSIL88, capillary column (50 mm × 0.25 mm internal diameter)
and flame-ionization detector (FID) (Agilent Technologies, CA,
USA). Methylpentadecanoic acid (Aldrich) was used as an
internal standard. Total FFA, DG, TG and PH content was
estimated as a sum of the particular fatty acid species. For
labeled palmitate lipid incorporation measurement the procedure
of separation of the lipids was repeated using another muscle and
plasma samples. The bands containing the above lipid fractions
and plasma FFA were scraped off the plates into the scintillation
vials, a scintillation cocktail (Ultima Gold, Packard) was added
and the radioactivity was counted using Packard Tri-Carb 1900
LSC counter.
Routine Western blotting procedure was used to assess the
expression of fatty acids and glucose transporters in isolated
PM and LDM fractions, as it was described in details
previously (18). Protein concentration in each sample was
determined by using the bicinchonic acid method (BCA) with
bovine serum albumin (BSA) as a standard. Briefly, after SDSPAGE separation, transfer, and blocking the membranes were
incubated overnight at 4°C with corresponding primary
antibodies in appropriate dilutions i.e. FAT/CD36 (1:500;
Abcam, UK), FABPpm (1:30000; a gift from Dr. CallesEscandon), FATP-1, Glut-1, Glut-4 (1:200; Santa Cruz
Biotechnology, USA) and β-actin (1:1000; Sigma-Aldrich,
USA). Thereafter, appropriate HRP-conjugated secondary
antibody (1:3000; Santa Cruz Biotechnology, USA) was used
to visualize blotted proteins. Signals obtained by
immunoblotting were quantified densitometrically using a
ChemiDoc XRS + visualization system and ImageLab software
(Bio Rad, Hercules, CA, USA). Equal protein concentrations
were loaded in each lane (25 µg) what was also confirmed by
Ponceau S staining. Protein expression was standardized to βactin expression and the control group was set as 100%.
Additionally, purity of isolated PM and LDM from the left and
right ventricle was confirmed by measuring the expression of
ATP-ase Na+/K+ (1:200; Santa Cruz Biotechnology, USA) and
Glut-4 (1:200; Santa Cruz Biotechnology, USA) according to
Fuller et al. (15).
MATERIALS AND METHODS
Statistical analysis
Statistical significance for both the within ventricle and
between ventricles comparisons was estimated by ANOVA with
Tukey HSD post-hoc test, using Statistica 10 software package.
693
RESULTS
min pacing increased incorporation of the label in each ventricle
comparing to the respective 60 min controls (Fig. 2F).
Free fatty acids
Phospholipids
Plasma FFA concentration was stable during pacing (Fig.
1A). The incorporation of 14C-palmitate in this fraction during
pacing did not differ from the respective control value (Fig. 1B).
The level of FFA fraction in the left ventricle was not affected by
stimulation (Fig. 2A). In the right ventricle, it was stable after 30
min stimulation. Sixty min control level of the fraction in the
right ventricle was higher than 30 min control level and it was
reduced after 60 min stimulation (Fig. 2A).
Incorporation of the label increased in both ventricles after
30 min pacing as compared to the respective controls. After 60
min stimulation the incorporation decreased as compared to the
appropriate value after 30 min pacing. However, it was higher in
each ventricle than the respective 60 min control (Fig. 2B).
Diacylglycerols
Thirty min pacing increased the content of diacylglycerols in
the left ventricle and reduced it in the right one comparing to the
appropriate control value. After 60 min pacing, the level of
diacylglycerols in the left ventricle was lower than after 30 min
but it remained on the same level in the right one. The control
levels of diacylglycerols in the right ventricle were higher than
in the left one. The level after 30 min pacing in the right ventricle
was lower and after 60 min was higher from the corresponding
value in the left ventricle (Fig. 2C). Pacing did not affect
incorporation of the label in the left ventricle comparing to the
respective controls. In the right ventricle, both 30 and 60 min
pacing increased the label incorporation comparing to the
respective values without pacing (Fig. 2D).
Triacylglycerols
Pacing did not affect the level of triacylglycerols in the left
ventricle. In the right ventricle, it was reduced after 30 min
pacing and remained further stable. The control levels in the
right ventricle were higher than in the left one (Fig. 2E).
Thirty min pacing did not affect the incorporation of the
label in the left ventricle and elevated it in the right one. Sixty
The level of phospholipids in each ventricle remained stable
during pacing. There were no differences in the level of
phospholipids between the ventricles (Fig. 2G).
Thirty min pacing increased incorporation of the label in
both ventricles. It did not differ from the respective control in
either ventricle after 60 min pacing (Fig. 2H).
Expression of fatty acid transporters
Fatty acid translocase (FAT/CD36)
Thirty min pacing increased expression of the plasmalemmal
fraction of FAT/CD36 in both ventricles. It returned to basal
levels after 60 min pacing. Expression of the microsomal
fraction of the protein decreased after 30 min pacing in the left
ventricle and normalized after 60 min pacing.
Plasma membrane associated fatty acid binding protein
(FABPpm)
Sixty min pacing increased expression of the plasmalemmal
fraction of the protein in the left ventricle as compared to 60 min
control.
Fatty acid transport protein 1 (FATP-1)
fraction and reduced expression of the microsomal fraction of
the protein in the right ventricle. After 60 min pacing, expression
of the plasmalemmal fraction of the protein remained elevated in
the ventricle.
Expression of glucose transporters
Glucotransporter 4 (GLUT-4)
Thirty min pacing elevated expression of the plasmalemmal
fraction of protein and reduced expression of its microsomal
Fig. 1. Impact of atrial pacing on plasma fatty acids content (panel A) and 14C-palmitate incorporation (panel B) after 30 minutes and
60 minutes of stimulation. To measure plasma FFA content and 14C-palmitate incorporation we used 100 ml of the plasma sample and
the same approach as for the tissue lipid fractions. Values are mean ± S.E.M., n = 8 per group, cP < 0.05 60min vs. 30 min of
stimulation.
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Fig. 2. Impact of atrial pacing on left and right ventricle content and 14C-palmitate incorporation of free fatty acids (FFA; panel A, B),
diacylglycerols (DG; panel C, D), triacylglycerols (TG; panel E, F) and phospholipids (PH; panel G, H) after 30 minutes and 60
minutes of stimulation. Values are mean ± S.E.M., n = 8 per group. aP < 0.05 pacing vs. control (within ventricle type); bP < 0.05 right
vs. left ventricle (within stimulation duration); cP < 0.05 60min vs. 30 min of stimulation (within ventricle type).
695
Fig. 3. Effect of atrial pacing on plasmalemmal (A)
and microsomal (B) expression of FAT/CD36 in the
left and right ventricle. The data are expressed as the
mean ± S.E.M. and are based on six independent
determinations (n = 6). aP < 0.05 control vs. pacing
(within ventricle type) and cP < 0.05 pacing 60 min vs.
pacing 30 min of stimulation duration (within
ventricle type).
and microsomal (B) expression of FABPpm in the left
and right ventricle. The data are expressed as the mean
± S.E.M. and are based on six independent
ventricle type).
696
and microsomal (B) expression of FATP1 in the left
ventricle type).
and microsomal (B) expression of GLUT-4 in the left
ventricle type).
697
and microsomal (B) expression of GLUT-1 in the left
ventricle type).
fraction in both ventricles. The expression was normalized after
60 min pacing.
Glucotransporter 1 (GLUT-1)
fraction of the protein in the right ventricle. It normalized after
60 min pacing.
DISCUSSION
The control levels of phospholipids, di- and triacylglycerols in
the left ventricle are similar to the levels previously reported
whereas the level of free fatty acids is higher than the previous one
(19). However, in the present study, the control rats underwent
surgery and it could result in mobilization of the latter compound.
The results obtained herein, show that the effect of pacing on the
heart lipid metabolism depends on time of pacing, ventricle and
examined lipid fraction. Regarding the left ventricle, pacing
elevated only transiently the level of diacylglycerols and the levels
of other fractions remained stable during stimulation. The data
concerning triacylglycerols in the left ventricle are in agreement
with previously reported results (4). Interestingly, 30 min pacing
reduced the level of diacylglycerols and triacylglycerols in the
right ventricle. It took place in spite of increased incorporation of
the label in the two fractions. It would indicate that both di- and
triacylglycerols are utilized during pacing and that the rate of their
utilization exceeds the rate of re-synthesis. A mechanism
responsible for mobilization of triacylglycerols only in the right
ventricle remains uncertain. It is likely that tachycardia puts
relatively greater burden on the right ventricle than on the left one.
As a result, more endogenous energy sources had to be used in the
right than the left ventricle.
Contractile activity affects incorporation of the blood-borne
free fatty acids in different lipid fractions in skeletal muscles (20).
As mentioned in the introduction, electrical stimulation of isolated
cardiomyocytes increased transiently incorporation of the label in
triacylglycerol but not in phospholipid fraction. The present data
show that increased work output during tachycardia induces
incorporation of 14C-palmitate in each examined lipid fraction in
the right ventricle and depending on time, in each fraction, with the
exception for diacylglycerols, in the left ventricle. It indicates that
tachycardia increases turnover of fatty acids in different lipid
fractions in both ventricles. Muscular exercise was shown to
induce a number of changes in the content and composition of fatty
acids in different lipid fractions in the left heart ventricle of the rat
(21). The present results would suggest that exercise induced
tachycardia could be responsible for the above changes.
As indicated in the Introduction, long chain free fatty acids
enter cardiomyocytes mostly via protein-mediated transport
facilitated by fatty acid transporters (7, 8). The transporters
translocate to the plasma membrane upon stimulation of the
isolated cardiomyocytes. As a result, expression of the
transporters in the plasma membrane increases at the expense of
the expression in the microsomal fraction (9, 10). Therefore, we
studied the expression of the transporters in both cellular
compartments (plasma membrane as well as low density
microsomes) in both ventricles during tachycardia in vivo. The
results obtained clearly indicate that tachycardia induces the
698
process of translocation of FAT/CD36 to the plasma membrane
in either ventricle. FAT/CD36 is the major transporter of long
chain fatty acids across the plasma membrane. Elevation in its
plasmalemmal expression in the ventricles during pacing would
correspond with the data indicating increased utilization of the
fatty acids by myocardium during tachycardia (22). In the right
ventricle, the transport of fatty acids was additionally, supported
by increased plasmalemmal expression of FATP-1 during the
first 30 min of tachycardia, which also corresponds to increased
utilization of long chain fatty acids, as indicated by increased
incorporation of 14C-palmitate in each examined lipid fraction.
Increased contractile activity induces translocation both
FAT/CD36 and GLUT-4 in isolated cardiomyocytes (23, 24). We
investigated whether in vivo tachycardia also induces changes in
the expression of glucotransporters. And, we showed that in case
of GLUT-4, the principal glucose transporter in myocardium,
tachycardia induces elevation in its expression in the plasma
membrane and reduces expression in microsomes in both
ventricles. These data are also in line with the reports indicating
increased utilization of glucose by myocardium during
tachycardia (22, 25).
Reports on metabolic differences between the left and right
heart ventricle are very scarce. The level of glycogen and
triacylglycerols was previously shown to be similar in both
ventricles. Additionally, the degree of exercise-induced
reduction in the level of glycogen was similar (4). El Alwani et
al. reported lower level of ceramide in the right ventricle than in
the left one (26). Other differences in metabolism of selected
sphingolipids between the ventricles were also reported (5).
According to Broderick and King, the control level of GLUT4 in
the both ventricles was similar (27) and we confirmed it
presently. We also showed elevation in the plasmalemmal
expression of GLUT-1, but only in the right ventricle after 30
min pacing. Our contribution provides data indicating the
existence of several differences in metabolism of lipids and
expression of FATP-1 and FAT/CD36 between the two ventricles
during tachycardia. So far, the physiological meaning of the
differences in metabolism between the two ventricles remains
obscure.
It is concluded that tachycardia induces numerous changes
in metabolism of endogenous lipids as well expression of fatty
acid and glucose transporters in both heart ventricles. Observed
changes depended on either lipid fraction, type of transporter,
time of pacing and location (left and right ventricle).
Abbreviations: DG, diacylglycerols; FABPpm, plasma
membrane associated fatty acid binding protein; FAT/CD36,
fatty acid translocase; FATP1 and FATP6, fatty acid transport
proteins 1 and 6; FFA, free fatty acids; GLUT1 and GLUT4,
glucotransporter 1 and 4; LV, left ventricle; PH, phospholipids;
RV, right ventricle; TG, triacylglycerols;
Acknowledgements: This work was supported by the
Medical
University
of
Bialystok,
grants
nr
N/ST/ZB/15/006/1118 and N/ST/ZB/15/003/1118.
Conflict of interest. None declared.
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R e c e i v e d : March 19, 2015
A c c e p t e d : July 22, 2015
Author’s address: Prof. Jan Gorski, Department of
Physiology, Medical University of Bialystok, 1 Kilinskiego
Street, 15-089 Bialystok, Poland.
E-mail: [email protected]

effect of tachycardia on lipid metabolism and expression of fatty acid

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