1 Laboratoire des Adaptations de l'Organisme à l'Exercice Musculaire, Hôpital Purpan, 31059 Toulouse Cedex, France; 2 Institut National de la Santé et de la Recherche Médicale Unité 317, Université Paul Sabatier, 31062 Toulouse Cedex 4, France; and 3 Department of Sport Medicine, Third Faculty of Medicine, Charles University, 10 000 Prague 10, Czech Republic
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The aim of this study was to investigate the
effect of aerobic exercise training on the lipolytic response of
adipose tissue in obese subjects. Thirteen men (body mass index = 36.9 ± 1.3 kg/m2) were submitted
to aerobic physical training on a cycloergometer (30-45 min, 4 days a wk) for 3 mo. Adipocyte sensitivity to the action of
catecholamines and insulin was studied in vitro before and after
training. Training induced a decrease in the percentage of fat mass
(P < 0.05) without changing the body
weight. Basal lipolysis and hormone-sensitive lipase activity were
significantly decreased after training
(P < 0.05). The lipolytic effects of epinephrine, isoprenaline (-adrenoceptor agonist), and dobutamine (
1-adrenoceptor agonist) were
significantly increased (P < 0.05) but not those of procaterol
(
2-adrenoceptor agonist). The
antilipolytic effects of
2-adrenoceptor and insulin were
significantly decreased (P < 0.05).
Lipolysis stimulation by agents acting at the postreceptor level was
unchanged after training. In conclusion, aerobic physical training in
obese male subjects modifies adipose tissue lipolysis through an
enhancement of
-adrenergic response and a concomitant blunting of
adipocyte antilipolytic activity.
adipose tissue biopsy; catecholamines; insulin; hormone-sensitive lipase
![]() |
INTRODUCTION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
OBESITY is associated with increased morbidity and especially coronary heart disease risk. Weight loss through dietary energy restriction is the most common form of treatment for the obese patient. However, hypocaloric diet alone leads to a decrease in fat mass, with a parallel decrease in fat-free mass. The decrease in muscle mass can be prevented by adding exercise training to the diet (3).
During aerobic exercise, nonesterified fatty acids (NEFA) constitute an
important fuel oxidized by working muscle. The NEFA are released into
the circulation as a product of triacylglycerol hydrolysis in the
adipose tissue. This lipolysis is a key step in the metabolic process
leading to the decrease of fat mass. Lipolysis is mainly regulated by
catecholamines, which are lipolytic through -adrenoceptors (AR) and
antilipolytic through
2-AR and insulin, which is an antilipolytic hormone (17). Increasing the
sensitivity of adipose tissue to the lipolytic action of catecholamines can facilitate lipid mobilization from fat stores. In healthy nonobese
subjects, many studies have shown that aerobic exercise training
induces an increase in catecholamine-stimulated lipolysis in isolated
adipocytes in both cross-sectional (8, 9, 20) and longitudinal (10) designs.
A recent study examined the effect of training combined with diet restriction on in vitro lipolysis in obese subjects and found that training blunted the dietary-induced decline of lipolysis (21). To our knowledge, no study has shown the effect of aerobic training on lipolysis in obese subjects without a concurrent nutritional intervention. Moreover, alterations of catecholamine-stimulated lipolysis have been reported in obesity (19, 22); therefore, it is of particular interest to determine whether the disturbed lipolytic sensitivity can be influenced by training.
The present study was undertaken to explore the effect of endurance training without modification of diet on adipose tissue metabolism in obese subjects to assess the mechanisms underlying the effects of training in overweight therapy. Adipose tissue sensitivity to catecholamines and insulin was studied in vitro before and after 12 wk of aerobic training in 13 obese male subjects.
![]() |
MATERIALS AND METHODS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Subjects
Thirteen obese nondiabetic males [age 41.2 ± 1.5 yr (range 27-49 yr) and body mass index 36.9 ± 1.3 kg/m2 (range 29.4-47.1 kg/m2)] were recruited for the study. The characteristics of the subjects are presented in Table 1. Two patients were treated for mild hypertension with calcium channel antagonists, and one patient was treated with small doses of L-thyroxine (75 µg/day) for hypothyroidism. All the subjects were sedentary before the study. Their weight had been stable for 6 mo before the study. Their nutrition had not changed during that period. The subjects were instructed not to change their nutritional habits during the course of the study. The stable nutritional pattern was verified with a 4-day dietary record obtained at the beginning, at the 6th wk, and at the end of the study period. The experiment was approved by the Ethics Committee of the 3rd Medical Faculty of Charles University, Prague. All subjects gave their informed consent to participate in the study.
|
Design of the Study
Subjects took part in a 12-wk aerobic training program, which is described in Exercise training protocol. Before and after the training program, the following measurements and tests were carried out: body composition measurements, maximal oxygen output (Maximum aerobic capacity.
O2 max was assessed
with a graded test conducted on an electromagnetically
braked bicycle ergometer (ergometrics 800s Ergoline). The initial
workload was 50 W, and it was increased by 0.2 W/kg of lean body mass
every minute until exhaustion.
O2 was measured with a
Vmax apparatus (Sensor Medics) during the test, and the highest
O2 value was
considered as
O2 max.
Exercise training protocol. The training program consisted of exercise on a bicycle ergometer 4 days a wk; each session lasted between 30 and 45 min, after individual prescription. The subjects cycled at a target heart rate calculated from the Karvonen equation (14); the heart rate corresponded to 50% of the heart rate reserve (maximal heart rate minus resting heart rate) during the first 2 wk and progressed to 60-65% of the heart rate reserve during the subsequent weeks.
Anthropometric assessment. During the study, body weight was measured regularly. The percentage of body fat was determined before and after training by hydrostatic weighing with the method of Siri (27).
Methods
Fat cell isolation and measurement of lipolysis. Fat cells were isolated, and lipolysis was measured as described previously (8). Briefly, a subcutaneous abdominal fat biopsy (200-300 mg) was performed under local anesthesia 10-15 cm from the umbilicus, and adipocytes were isolated with collagenase.Digestion was performed for 60 min at 37°C in a Krebs-Ringer bicarbonate buffer, pH 7.4, containing 90 mg glucose/100 ml and 4% bovine serum albumin with 0.5 mg/ml collagenase (KRBA) (25). At the end of digestion, the fat cell suspension was filtered and washed three times. Fat cell volume was determined from ~200 adipocytes for each subject before and after the training period.
As an indicator of adipocyte lipolysis, the quantity of glycerol released into the medium was measured. Aliquots (100 µl) of the continuously stirred cell suspension were placed in 1.5-ml conical tubes. The cell concentrations were 14.86 ± 1.77 cell/µl before and 17.18 ± 1.68 cell/µl after training, P = 0.393. Four of these aliquots contained only 20 µl KRBA for determination of spontaneous lipolysis, and the others contained 20 µl of drugs at various concentrations. Another four tubes with 20 µl KRBA were immediately placed on ice to provide an evaluation of the initial quantity of glycerol contained in the medium. The remaining tubes were incubated in a shaking water bath for 4 h.
The quantity of glycerol released into the medium was measured with an ultrasensitive bioluminescence technique to estimate adipocyte lipolysis (15). The bioluminometer was an LKB 1251 (LKB Wallac, Stockholm, Sweden), coupled with a distributor (LKB 1291) for adding luciferase. All measurements were performed in triplicate.
Glycerol release after addition of various agents was expressed as an
increase of glycerol concentration above the level of basal lipolytic
rate in micromoles of glycerol released per 100 mg of lipids per 4 h.
The results were not modified when expressed in micromoles of glycerol
released per 106 cells, adipocyte
volume being unchanged by training. The lipolytic responsiveness was
assessed with epinephrine, isoproterenol (nonselective -AR agonist),
dobutamine (
1-AR agonist), and
procaterol (
2-AR agonist). The
antilipolytic
2-AR
responsiveness of adipocytes was assessed by the mean of the inhibitory
concentration-dependent action of epinephrine in the presence of a
-AR antagonist (propranolol). For a better evaluation of the
inhibitory action of the
2-AR and of insulin, the basal levels of glycerol were increased by addition
of 2 µg/ml of adenosine deaminase to remove adenosine released into
the incubation medium by isolated fat cells.
The effects of agents acting at the postreceptor level were evaluated with forskolin (direct activator of adenylate cyclase), cAMP (stimulator of the protein kinase hormone-sensitive lipase complex), 3-isobutyl-1-methylxanthine (IBMX), and theophylline (inhibitor of phosphodiesterase).
Determination of hormone-sensitive lipase activity. The assay was performed as described by Frayn et al. (13). Packed fat cells (300 µl) that had been stored in liquid nitrogen were homogenized at 4°C in 2.0 ml of a buffer containing 0.25 mol/l sucrose, 1 mmol/l EDTA, 1 mmol/l dithiothreitol, and 20 µg/l each of the protease inhibitors antipain and leupeptin. The homogenate was then centrifuged at 100,000 g at 4°C for 45 min. The fat cake was removed, and the fat-free infranatant was recovered for analysis of hormone-sensitive lipase (HSL) activity with 1(3)-[3H]oleoyl-2-O-oleylglycerol as substrate. A diacylglycerol analog was used as substrate assay activity, because HSL has 10-fold higher activity toward diacylglycerol than triacylglycerol. The diacylglycerol lipase activity is not dependent on the phosphorylation state of the enzyme. Moreover, because this substrate has only one hydrolyzable ester bond at the 1(3)-position, neither the diacylglycerol analog nor its hydrolysis products are substrates for monoacylglycerol lipase, which is abundant in adipose tissue. One unit of enzyme activity equals 1 µmol of fatty acid produced per minute at 37°C. The protein concentration was determined with Lowry's method (18).
Biochemical determination. Glycerol in plasma (20 µl) was analyzed with an ultrasensitive radiometric method (5); the intra-assay and interassay variabilities were 5.0% and 9.2%, respectively. Blood glucose and plasma NEFA were determined with a glucose-oxidase technique (Biotrol, Paris, France) and an enzymatic procedure (Wako, Unipath, Dardilly, France), respectively. Plasma insulin concentrations were measured with RIA kits (Sanofi Diagnostics Pasteur, Marnes la Coquette, France). Plasma triglyceride and cholesterol concentrations were assayed with commercial kits.
Reagents. The following reagents were used during fat cell isolation and measurement of lipolysis: bovine serum albumin; fraction V, fatty acid free; collagenase from Clostridium histolyticum; adenosine deaminase; dibutyryl-cAMP; incubation enzymes; luciferase from Photobacterium fischeri (Boehringer-Mannheim, Meylan, France); epinephrine bitartrate; dobutamine hydrochloride; isoproterenol hydrochloride; procaterol hydrochloride; DL-propranolol hydrochloride; IBMX; forskolin (Sigma, Saint Quentin Fallavier, France); 40 IU/ml orgasuline rapide (Organon, Saint-Denis, France); theophylline Bruneau (Delalande, Quétigny, France).
Statistical analysis
All the values are means ± SE. Student's paired t-test and analysis of variance (two-way on dose and training effect ANOVA with repeated measures on dose) with Bonferroni's test for post hoc analysis were used for statistical comparisons as appropriate. P < 0.05 was the threshold of significance. All calculations were performed with software statistical packages (SuperAnova and Statview, Abacus Concepts, Berkeley, CA). ![]() |
RESULTS |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The aerobic training program increased
O2max by 5.7%, the
increase being significant for the total
O2max
(P < 0.05) and not significant when
related to either body weight or fat-free mass (Table 1). No
significant change of body weight (decrease by 1.3%) or fat-free mass
was observed, whereas the decrease of fat mass by 3.6% was significant
(P < 0.05; Table 1).
Plasma results. No significant change was observed in plasma glycerol and NEFA concentrations (Table 2). Fasting blood glucose and plasma insulin levels were unchanged by training. The blood lipids changed partially during training: total cholesterol decreased significantly (P < 0.01), whereas the decrease of triglycerides was not significant. High-density lipoprotein (HDL) concentrations did not change after training (Table 2).
|
In vitro lipolytic response. The mean adipocyte volume did not change after training (0.876 ± 0.063 nl after vs. 0.878 ± 0.045 nl before), whereas basal lipolysis decreased significantly (Table 3). HSL activity showed a significant decrease from 225.1 ± 8.0 mU/mg protein before to 100.5 ± 2.3 mU/mg protein after training (P < 0.05).
|
The dose-response curves of epinephrine and the -AR agonist
isoprenaline were significantly different, showing that the
-adrenergic lipolytic effect was higher after than before training
(Fig. 1, A and B).
The dose-response curves of the
1-AR agonist (dobutamine), but
not those of the
2-AR agonist
(procaterol) (not shown), were significantly different after training
(Fig. 1C).
|
The dose-response curves of epinephrine in the presence of propranolol
(expressed as a percentage of maximal inhibitory effect in the presence
of adenosine deaminase) were significantly different, indicating that
the antilipolytic 2-adrenergic
effect was decreased by training (Fig.
2A). The
antilipolytic action of insulin was also decreased after training (Fig.
2B).
|
To study the mechanism of the observed training-induced increase of
-adrenergic-mediated lipolysis stimulation in fat cells, the effect
of the agents acting at the postreceptor level of lipolysis stimulation
was evaluated. After subtraction of basal lipolysis values, the
lipolytic effects of forskolin, cAMP, IBMX, and theophylline were not
modified by training (Table 3).
To investigate whether the changes in lipolytic activity are mediated by changes in body fat mass, the correlation (Pearson's product-moment correlation coefficient using linear regression) between the training-induced change of maximal response to isoprenaline stimulation and the training-induced change of body fat mass was calculated. No correlation was found.
![]() |
DISCUSSION |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Previous cross-sectional studies (8, 9) from our group showed a clear training-induced enhancement of the lipolytic responsiveness of adipose tissue in nonobese subjects. The main interest of this study was to investigate whether the changes in regulation of lipolysis that were previously reported in these and other studies (10) in nonobese subjects also occur in obese subjects submitted to a training program. To take into account the gender-specific effect of training on in vitro lipolysis (9, 11), we limited our investigation to obese male subjects.
The main finding of the present longitudinal study is that aerobic training (corresponding in frequency and intensity to that routinely prescribed for obese subjects in clinical practice) promotes an increase in catecholamine-induced lipolytic activity of subcutaneous adipose tissue.
In fact, in our subjects, this kind of aerobic training produced a minor, although significant, change in physical fitness (assessed by maximum aerobic capacity). It did not produce a change in body weight, whereas there was a slight decrease of fat mass and a small but not significant increase in fat-free mass. The modest effects of this type of training are in agreement with other reports on the effects of moderate training in obese subjects (1, 16). The metabolic changes detected in plasma were mild in accordance with other studies in nonobese and obese subjects with comparable training programs (1, 6, 30).
The training did not induce a change in fat cell volume, which is in agreement with the small change in total body fatness. Other longitudinal studies have not found a decrease in fat cell weight; this was the case in nonobese male subjects (10) and in obese women (21). However, in the latter group, the training was coupled with hypocaloric diet. Moreover, most cross-sectional studies found a significantly lower fat cell volume in trained subjects, but in most of these studies, groups with very different training status and body fatness were compared (8, 9, 20).
In this study, we found a decrease in basal lipolysis after training. However, basal lipolysis changes by training remain controversial. In fact, our results are in agreement with previous data (24, 29) in cross-sectional studies but in disagreement with others (12, 20). In a longitudinal study, Després et al. (10) did not find any difference in basal lipolysis after training. Similarly, discrepancies in the effects of training on lipolysis at rest occurred in studies examining lipolysis in vivo with labeled NEFA and glycerol; higher as well as lower lipolytic rates were reported in trained compared with untrained subjects (7, 26). These differences probably came from training volume, duration, mode of exercise, and the moment when the investigations were made. In the present study, the decrease of basal lipolysis was associated with a decrease of HSL expression. HSL catalyzes the rate-limiting step in adipose tissue lipolysis; therefore, the decrease of basal lipolysis during training may be caused by the decrease of HSL expression. This is supported by observations during very-low-calorie diet in obese subjects, which report a concomitant increase (28) or decrease (23) of HSL and basal lipolysis during very-low-calorie diet or after a weight-maintenance period, respectively.
The most important result of the study is the finding that training
enhances the lipolytic response of adipocytes to catecholamine stimulation. This confirms that the training-induced sensitization of
adipose tissue found previously in vitro in nonobese subjects (10) also
occurs in obese subjects and that this sensitization can be achieved
with training volumes feasible in routine practice. The present study
shows, in agreement with previous studies (8, 9), that the
-adrenergic pathway is responsible for this sensitization phenomenon. The obese subjects have been shown to present decreased
-adrenergic stimulation of lipolysis (4, 19, 22), and the data
reported here suggest that the decrease in the
-adrenergic responsiveness of lipolysis seen in obese subjects could be partially improved by exercise training. Furthermore, in an attempt to understand which subpopulations of
-AR mediate the training-induced effect, we
explored the stimulatory effects of selective
1- and
2-AR agonists (dobutamine and
procaterol, respectively) on lipolysis. A significant training-induced
enhancement was found for the
1-adrenergic and not for the
2-adrenergic
pathway; this suggests that training selectively increases
1-adrenergic activity.
In obese subjects, the
2-AR-mediated antilipolytic
effect of catecholamines is high (19), and the present study suggests that endurance training can decrease
2-adrenergic sensitivity. This
lower
2-adrenergic
antilipolytic effect might contribute to the training-induced rise of
the lipolytic effect of epinephrine (Fig.
1A).
Besides catecholamines, insulin is a powerful hormone in the control of lipolysis in adipocytes. Therefore, the influence of training on the antilipolytic action of insulin was assessed. The training resulted in its decrease. The only study known to date which deals with training effects on insulin antilipolytic activity in vitro in adipose tissue in obese subjects (women) did not find any change due to training (16). Whereas the duration and volume of training were identical in this study, gender differences could explain the different results (similar to gender-dependent effects of training on the lipolytic action of catecholamines). It is noteworthy that the effect of training on the action of insulin differs with respect to the target tissue: whereas the sensitivity to insulin action on glucose transport in muscle is enhanced in obese subjects (1, 16), the antilipolytic effect in adipose tissue appears to be decreased.
When lipolysis was stimulated with agents acting at a postreceptor level (forskolin, cAMP, IBMX, theophylline), no differences in pre- and posttraining status were found. This is in contrast to our previous results (9) and other results (20) in nonobese subjects. The reason may be the very different training status of the groups in other studies, which contrasts with the mild training-induced increase in physical capacity in the present study.
It is important to note that the results of this study are specific to the gender of the subjects and the region of adipose tissue deposit. The gender-specific effect of exercise training on lipolysis (9, 11) and body fat reduction (1) has been repeatedly demonstrated. Regional differences have also been reported in the training-induced lipolysis modifications (20). The variability of exercise-induced lipolysis with respect to region and gender has also been demonstrated during a single bout of exercise (2). Therefore, it remains to be shown whether the beneficial effect of exercise is preserved in obese women and in other fat depots.
In conclusion, the present study demonstrates that 12 wk of aerobic
training induces an enhancement of in vitro catecholamine-stimulated lipolysis in abdominal subcutaneous tissue of obese male subjects, without substantially changing body fat mass. The basal rates of
lipolysis and HSL activity were decreased after 12 wk of training. The
increase in lipolytic response seems to be related to an increased response of the -adrenergic pathway. Decreases in the antilipolytic action of
2-AR and insulin also
contribute to the improvement of the lipolytic activity of adipose
tissue in trained states.
![]() |
ACKNOWLEDGEMENTS |
---|
This work was partially supported by Grant 3611-2 of Czech Ministry of Health.
![]() |
FOOTNOTES |
---|
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. §1734 solely to indicate this fact.
Address for reprint requests: D. Rivière, Service d'Exploration de la Fonction Respiratoire et de Médecine du Sport, CHU Purpan, 31059 Toulouse Cedex, France.
Received 19 March 1998; accepted in final form 1 September 1998.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
1.
Andersson, B.,
W. F. Xy,
M. Rebuffe-Scrive,
K. Terning,
M. Krotkiewski,
and
P. Bjorntorp.
The effects of exercise training on body composition and metabolism in men and women.
Int. J. Obes.
15:
75-81,
1991[Medline].
2.
Arner, P.,
E. Kriegholm,
P. Engfeldt,
and
J. Bolinder.
Adrenergic regulation of lipolysis in situ at rest and during exercise.
J. Clin. Invest.
85:
893-898,
1990[Medline].
3.
Ballor, D. L.,
and
E. T. Poehlmann.
Exercise training enhances fat-free mass preservation during diet-induced weight loss: a meta-analytical finding.
Int. J. Obes.
18:
35-40,
1994.
4.
Blaak, E. E.,
M. A. Van Baak,
A. D. Kester,
and
W. H. M. Saris.
-adrenergically mediated thermogenic and heart rate response: effect of obesity and weight loss.
Metabolism
44:
520-524,
1995[Medline].
5.
Bradley, D. C.,
and
H. R. Kaslow.
Radiometric assays for glycerol, glucose and glycogen.
Anal. Biochem.
180:
11-16,
1989[Medline].
6.
Buemann, B.,
and
A. Tremblay.
Effects of exercise on abdominal obesity and related metabolic complications.
Sports Med.
21:
191-212,
1996[Medline].
7.
Calles-Escandon, J.,
and
P. Driscoll.
Free fatty acid metabolism in aerobically fit individuals.
J. Appl. Physiol.
77:
2374-2379,
1994
8.
Crampes, F.,
M. Beauville,
D. Rivière,
and
M. Garrigues.
Effect of physical training in humans on the response of isolated fat cells to epinephrine.
J. Appl. Physiol.
61:
25-29,
1986
9.
Crampes, F.,
D. Rivière,
M. Beauville,
M. Marceron,
and
M. Garrigues.
Lipolytic response of adipocytes to epinephrine in sedentary and exercise-trained subjects: sex-related differences.
Eur. J. Appl. Physiol.
59:
249-255,
1989.
10.
Després, J. P.,
C. Bouchard,
R. Savard,
A. Tremblay,
M. Marcotte,
and
G. Theriault.
The effect of 20-week endurance training program on adipose tissue morphology and lipolysis in men and women.
Metabolism
33:
235-239,
1984[Medline].
11.
Després, J. P.,
C. Bouchard,
R. Savard,
A. Tremblay,
M. Marcotte,
and
G. Theriault.
Effects of exercise-training and detraining on fat cell lipolysis in men and women.
Eur. J. Appl. Physiol.
53:
25-30,
1984.
12.
Després, J. P.,
C. Bouchard,
R. Savard,
A. Tremblay,
M. Marcotte,
and
G. Theriault.
Level of physical fitness and adipocyte lipolysis in humans.
J. Appl. Physiol.
56:
1157-1161,
1984
13.
Frayn, K. N.,
D. Langin,
C. Holm,
and
P. Belfrage.
Hormone-sensitive lipase: quantitation of enzyme activity and mRNA level in small biopsies of human adipose tissue.
Clin. Chim. Acta
216:
183-189,
1993[Medline].
14.
Karvonen, M.,
K. Kentala,
and
O. Musta.
The effects of training on heart rate.
Ann. Med. Exp. Biol. Fenn.
35:
307-315,
1957.
15.
Kather, H.,
F. Schroder,
and
B. Simon.
Microdetermination of glycerol using bacterial NADH-linked luciferase.
Clin. Chim. Acta
120:
295-300,
1982[Medline].
16.
Krotkiewski, M.,
P. Lönnroth,
K. Mandroukas,
Z. Wroblewski,
M. Rebuffe-Scrive,
G. Holm,
U. Smith,
and
P. Bjorntorp.
The effects of physical training on insulin secretion and effectiveness and on glucose metabolism in obesity and type 2 (non-insulin-dependent) diabetes mellitus.
Diabetologia
28:
881-890,
1985[Medline].
17.
Lafontan, M.,
and
M. Berlan.
Fat cell adrenergic receptors and the control of white and brown fat cell function.
J. Lipid Res.
34:
1057-1091,
1993[Abstract].
18.
Lowry, O. H.,
N. J. Rosebrough,
A. L. Farr,
and
N. J. Randall.
Protein measurement with the Folin phenol reagent.
J. Biol. Chem.
193:
265-275,
1951
19.
Mauriège, P.,
J. P. Després,
D. Prud'homme,
M. C. Pouliot,
M. Marcotte,
A. Tremblay,
and
C. Bouchard.
Regional variation in adipose tissue lipolysis in lean and obese men.
J. Lipid Res.
32:
1625-1633,
1991[Abstract].
20.
Mauriège, P.,
D. Prud'Homme,
M. Marcotte,
M. Yoshioka,
A. Tremblay,
C. Bouchard,
A. Nadeau,
and
J. P. Després.
Regional differences in adipose tissue metabolism between sedentary and endurance-trained women.
Am. J. Physiol.
273 (Endocrinol. Metab. 36):
E497-E506,
1997
21.
Nicklas, B. J.,
E. M. Rogus,
and
A. P. Goldberg.
Exercise blunts declines in lipolysis and fat oxidation after dietary-induced weight loss in obese older women.
Am. J. Physiol.
273 (Endocrinol. Metab. 36):
E149-E155,
1997
22.
Reynisdottir, S.
Catecholamine resistance in fat cells of women with upper-body obesity due to decreased expression of beta 2-adrenoceptors.
Diabetologia
37:
428-435,
1994[Medline].
23.
Reynisdottir, S.,
D. Langin,
K. Carlstrom,
C. Holm,
S. Rossner,
and
P. Arner.
Effects of weight reduction on the regulation of lipolysis in adipocytes of women with upper-body obesity.
Clin. Sci. (Colch.)
89:
421-429,
1995[Medline].
24.
Rivière, D.,
F. Crampes,
M. Beauville,
and
M. Garrigues.
Lipolytic response of fat cells to catecholamines in sedentary and exercise-trained women.
J. Appl. Physiol.
66:
330-335,
1989
25.
Rodbell, M.
Metabolism of isolated fat cells. I. Effects of hormones on glucose metabolism and lipolysis.
J. Biol. Chem.
29:
375-380,
1964.
26.
Romijn, J. A.,
S. Klein,
E. F. Coyle,
L. S. Sidossis,
and
R. R. Wolfe.
Strenuous endurance training increase lipolysis and triglyceride-fatty acid cycling at rest.
J. Appl. Physiol.
75:
108-113,
1993[Abstract].
27.
Siri, W. E.
Body composition from fluid spaces and density: analysis of methods.
In: Techniques for Measuring Body Composition, edited by J. Brozek,
and A. Henschel. Washington, DC: National Academy of Sciences, 1961, p. 223-244.
28.
Stich, V.,
I. Harant,
I. De Glisezinski,
F. Crampes,
M. Berlan,
M. Kunesova,
V. Hainer,
M. Dauzats,
D. Rivière,
M. Garrigues,
C. Holm,
M. Lafontan,
and
D. Langin.
Adipose tissue lipolysis and hormone-sensitive lipase expression during very-low-calorie diet in obese female identical twins.
J. Clin. Endocrinol. Metab.
82:
739-744,
1997
29.
Toode, K.,
A. Viru,
and
A. Eller.
Lipolytic actions of hormones on adipocytes in exercise-trained organisms.
Jpn. J. Physiol.
43:
253-258,
1993[Medline].
30.
Tremblay, A.,
J. P. Després,
and
C. Bouchard.
The effects of exercise-training on energy balance and adipose tissue morphology and metabolism.
Sports Med.
2:
223-233,
1985[Medline].