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The Journal of Clinical Endocrinology & Metabolism Vol. 85, No. 2 799-803
Copyright © 2000 by The Endocrine Society

Original Studies

Effects of Cortisol and Growth Hormone on Lipolysis in Human Adipose Tissue1

Malin Ottosson, Peter Lönnroth, Per Björntorp and Staffan Edén

Wallenberg Laboratory for Cardiovascular Research, Department of Physiology and Pharmacology, Endocrine Unit (M.O., S.E.), Department of Internal Medicine (P.L.), and Department of Heart and Lung Diseases (P.B.), Sahlgrenska University Hospital, Goteborg University, Goteborg, Sweden

Address all correspondence and requests for reprints to: Malin Ottosson, Ph.D., Wallenberg Laboratory for Cardiovascular Research, Sahlgrenska University Hospital, S-413 45 Goteborg, Sweden. E-mail: malin.ottosson{at}wlab.wall.gu.se


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
The in vitro effects of cortisol and GH on basal and stimulated lipolysis in human adipose tissue were studied using a tissue incubation technique. After preincubation for 3 days in control medium containing insulin, adipose tissue pieces were exposed to cortisol for 3 days. GH was added to the cortisol-containing medium during the last 24 h (day 6). Adipocytes were then isolated, and lipolysis was studied in the absence and presence of isoprenaline, noradrenaline, forskolin, and N-6-monobutyryl-cAMP.

Cortisol reduced the basal rate of lipolysis (P < 0.01) and the sensitivity to isoprenaline compared to the control values (P < 0.01). Addition of GH to the cortisol-containing medium increased the basal rate of lipolysis (P < 0.01) and the sensitivity to isoprenaline (P < 0.01) to the control level and increased the maximum isoprenaline--induced lipolytic activity (P < 0.01). Similar effects were obtained in the presence of noradrenaline.

Maximum forskolin-induced lipolytic activity was reduced after exposure of the tissue to cortisol (P < 0.05), whereas addition of GH antagonized this effect (P < 0.01). Induction of the maximum lipolytic activity with N-6-monobutyryl-cAMP was not influenced by the preceding hormone exposure. Addition of GH alone during the last 24 h of incubation increased the basal rate of lipolysis (P < 0.05) and resulted in a borderline significant increase in the maximum isoprenaline-induced lipolytic activity (P = 0.055), suggesting that GH induces lipolysis also in the absence of glucocorticoids.

Thus, cortisol and GH have opposite effects on the basal lipolytic activity in human adipose tissue in vitro as well as on the sensitivity to catecholamines, GH being the lipolytic and cortisol the antilipolytic agent. The present findings are in agreement with in vivo observations.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
BOTH GLUCOCORTICOIDS and GH are known to have profound effects on body composition, including body fat mass (1, 2, 3, 4, 5). Glucocorticoids favor lipid accumulation, at least partly by stimulation of lipoprotein lipase (LPL) activity (6). However, the effects of glucocorticoids on lipid mobilization are still controversial. In vivo studies suggest that glucocorticoids have no effect (7) or stimulate (8, 9, 10) lipolysis, whereas other report an inhibiting effect of glucocorticoids on the lipolytic activity in vivo in man (11, 12). The long term in vitro effects of glucocorticoids on human adipose tissue lipolysis have not been fully evaluated. Cigolini and Smith suggested that hydrocortisone, in the presence of insulin, reduces both basal and noradrenaline-stimulated lipolysis, but no data were shown (13). In rat adipose tissue, however, glucocorticoids seem to increase the ability of lipolytic agents to activate triglyceride lipolysis (reviewed in Ref. 14).

In animals, GH has been reported to have direct lipolytic effects on adipose tissue, i.e. stimulates basal lipolysis, and also to influence lipolysis indirectly by altering the ability of adipocytes to respond to lipolytic factors such as catecholamines. However, some reports appear conflicting (reviewed in Ref. 15). In man, GH is known to reduce adipose tissue mass (4, 5) and to increase the release of free fatty acids (16). GH treatment of GH-deficient adults has been reported to increase the sensitivity of isolated adipocytes to catecholamines, whereas basal lipolysis was not affected (17). Evaluation of the lipolytic effect of GH in human adipose tissue in vitro has given contradictory results. Incubation of biopsies of human sc adipose tissue for 1 week with various concentrations of GH, with or without cortisol, was not followed by altered basal or noradrenaline-stimulated lipolysis (18). In a study by Marcus et al., GH had no direct lipolytic effect on human fat cells exposed to GH during a few hours, but GH markedly increased the catecholamine sensitivity without any change in maximal lipolysis (19). GH exposure of adipocytes from GH-deficient adults for 4 h has been reported to produce a direct lipolytic effect, and the effect was increased after the administration of recombinant human GH for 6 months (20).

We previously studied the regulation of LPL activity by cortisol and GH in human adipose tissue in vitro using a tissue incubation technique allowing standardized conditions for several days (21, 22). As the tissue incubation technique has proven useful to study the effects of cortisol and GH on adipose tissue metabolism, the present work was designed to evaluate the effects of these hormones on basal and stimulated lipolysis in human adipose tissue using this technique.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Source of tissue

Subcutaneous abdominal adipose tissue was obtained from 21 subjects, 3 men and 18 women (4 postmenopausal), aged 23–76 (45.5 ± 2.9) yr. Surgical biopsies were taken from 9 patients undergoing abdominal surgery for nonmalignant conditions and from 5 healthy volunteers. Needle aspirations were obtained from 7 healthy volunteers. The body mass index was 22.1–37.3 (27.7 ± 0.9) kg/m2. None was diabetic. Surgery was performed under general or local anesthesia, and aspiration was performed under local anesthesia. As differences in age, sex, body mass index, and the technique used to obtain the biopsies had no apparent influence on the results, the data were pooled.

A part of the tissue incubations performed in the present work was also used to study the regulation of LPL activity as described previously (22). The study was approved by the ethics committee of the University of Goteborg.

Incubation system

Pieces of adipose tissue (5–20 mg each) were prepared under sterile conditions and used for incubations in 50-mL plastic tubes (500 mg tissue/20 mL medium). Connective tissue and blood vessels were removed. For each incubation experiment, adipose tissue from one subject was used. Initial (immediately after excision of the tissue) cell size was determined as indicated.

The incubation schedule was as follows. The tissue was first preincubated for 3 days in a control medium containing 7175 pmol/L insulin as described previously (21, 22). During the next 3 days, the tissue was incubated in the control medium with and without 1000 nmol/L cortisol (hydrocortisone, Sigma, St. Louis, MO). During the last 24 h (day 6), GH (2.3 nmol/L; Norditropin, Novo Nordisk, Gentofte, Denmark) was added to half of the control tubes and to half of the tubes with cortisol medium. After the 6 days of incubation, basal and stimulated lipolytic activities as well as fat cell size were determined in isolated adipocytes from adipose tissue incubated in the different media. Incubations were performed at 37 C at 90% humidity and 4.0–5.0% CO2 in an incubator (Forma Scientific, Division of Mallinckrodt, Inc., Marietta, OH), and media were changed daily.

Lipolysis

Lipolytic measurements were performed on cells isolated from the stroma by incubating the tissue from the different media in Parker medium 199 (SBL, Stockholm, Sweden) supplemented with 4% (wt/vol) albumin and 0.8 mg/mL collagenase (Sigma) at 37 C for 60 min as described by Smith et al. (23). After filtration through a nylon mesh (250 µm), the cells were washed three times and suspended in fresh medium. One hundred-microliter aliquots in duplicate of the cell suspension (lipocrit, 20–25%) were added to plastic vials containing 2 mL Parker medium 199 supplemented with 4% albumin with or without a lipolytic agent as indicated (final lipocrit, 1–2%). The lipolytic agents (all from Sigma) were the nonselective ß-adrenergic agonist isoprenaline (10-9-10-6 mol/L); the physiological catecholamine noradrenaline (10-8-10-5 mol/L); forskolin, which stimulates the adenylate cyclase (10-6 mol/L); and the phosphodiesterase-resistant cAMP analog N-6-monobutyryl-cAMP (4 mmol/L). After 2-h incubation at 37 C and pH 7.4, cells and medium were transferred to soft plastic tubes and centrifuged through silicone oil to separate the cells and the incubation medium as described by Gammeltoft and Gliemann (24). The glycerol content of the medium was analyzed enzymatically (25) and was taken as an index of lipolysis. The amount of triglycerides in the fat cell suspension was measured after extraction according to the method of Dole and Meinertz (26) and weighing after evaporation of solvents. The fat cell diameter was measured microscopically (23), and the lipolytic activity was expressed as nanomoles of glycerol released per 104 cells.

Cell size

Adipocyte size was determined before and after incubation in all media as indicated. Fat cell diameter was measured microscopically according to Smith et al. (23).

Statistical analysis

The dose-response values for the effect of catecholamines on glycerol release in adipose tissue from the different media were fitted by nonlinear regression to the four-parametric curve: y = (a - b)/(1 + (x/c)d) + b, where the response variable y (glycerol release) is expressed in terms of the four calculated parameters a through d, where a is the basal level, b is the maximal response to the catecholamine, c is the ED50, d is the slope factor, and x is the hormone concentration (27).

Results are expressed as the mean ± SEM. Significance of differences were calculated with Student’s paired t test or one-way ANOVA for repeated measures followed by Student-Newman-Keuls multiple range test. P < 0.05 was regarded as significant.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
The dose-response curves for isoprenaline-induced lipolysis (10-9-10-6 mol/L) are depicted in Fig. 1Go. Exposure of the tissue to cortisol for 3 days reduced both the basal rate of lipolysis (P < 0.01) and the sensitivity to isoprenaline, demonstrated by an increase in the ED50 value compared to the control value (P < 0.01). The maximum isoprenaline-induced lipolytic activity was not affected by cortisol. Addition of GH (2.3 nmol/L) to the cortisol-containing medium during the last 24 h of incubation (day 6), increased the basal rate of lipolysis (P < 0.01) and reduced the ED50 value (P < 0.01) to the control level. The maximum isoprenaline-induced lipolytic activity after exposure of the tissue to both cortisol and GH was significantly increased (P < 0.01) compared to the maximum lipolytic activity after incubating the tissue in the control or cortisol medium. Similar dose-response curves were obtained with noradrenaline (10-8-10-5 mol/L; Fig. 2Go). The effects of exposure of the tissue to cortisol and cortisol plus GH on noradrenaline-stimulated lipolysis were the same as those on isoprenaline-stimulated lipolysis, except for significantly different ED50 values in the three groups (control, cortisol, and cortisol plus GH; P < 0.01). Basal and maximum lipolysis rates and ED50 values for isoprenaline and noradrenaline are shown in Table 1Go. Adipocyte mean diameter did not change during incubation in the different media, as demonstrated previously (22).



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  		Figure 1. Mean dose-response curves for lipolysis stimulated by isoprenaline. Adipose tissue was preincubated for 3 days in control medium and was then incubated in the control medium with addition of cortisol (1000 nmol/L) for 3 days (Cortisol). GH (2.3 nmol/L) was added to the cortisol-containing medium during the last 24 h, day 6 (Cort. + GH). Tissue was also incubated in the control medium for 6 days (Control). Six incubations were performed. Isolated fat cells from the different media were incubated with or without the indicated concentrations of isoprenaline, and glycerol release was measured and used as an index of lipolysis.

 


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  		Figure 2. Mean dose-response curves for lipolysis stimulated by noradrenaline. The incubations and methods used were the same as described in Fig. 1Go.

 

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  		Table 1. Lipolysis rates and ED50 values of isolated fat cells

 
Lipolysis was also stimulated at a postreceptor level with forskolin (10-6 mol/L) and N-6-monobutyryl-cAMP (4 mmol/L; Fig. 3Go). Maximum forskolin-induced lipolytic activity was reduced after exposure of the tissue to cortisol compared to the control value (P < 0.05), and the addition of GH to the cortisol-containing medium during the last 24 h of incubation significantly antagonized this effect (P < 0.01). Addition of GH increased maximum forskolin-induced lipolytic activity compared to the control value (P < 0.05). The maximum lipolytic activity induced by N-6-monobutyryl-cAMP was not influenced by the preceding hormone exposure.



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  		Figure 3. Basal lipolysis and the lipolytic effect of forskolin (10-6 mol/L) and N-6-monobutyryl-cAMP (4 mmol/L). Adipose tissue incubations and glycerol measurements were as described in Fig. 1Go. Nine incubations were performed. +, P < 0.01, cortisol vs. control and cortisol plus GH. *, P < 0.05, cortisol vs. control; P < 0.01, cortisol vs. cortisol plus GH. #, P < 0.05, cortisol plus GH vs. control.

 
Figure 4Go shows that addition of GH alone during the last 24 h of incubation to adipose tissue incubated in the control medium for 6 days resulted in a mean increase of 32.6 ± 9.91% of the basal rate of lipolysis (P < 0.05). The maximum isoprenaline-induced lipolytic activity was increased 14.2 ± 6.11% after GH exposure compared to the control value (P = 0.055; Fig. 4Go). The diameter of the adipocytes did not differ among the media, as demonstrated previously (22).



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  		Figure 4. Basal lipolysis and the lipolytic effect of isoprenaline (10-7 mol/L). Adipose tissue was incubated for 6 days in control medium (Control). GH (2.3 nmol/L) was added to the control medium during the last 24 h, day 6 (GH). Twelve incubations were performed. Isolated fat cells from the different media were incubated with or without isoprenaline, and glycerol release was measured and used as an index of lipolysis. *, P < 0.05; (*), P < 0.1 (control vs. GH).

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The main findings in the these studies were that in the presence of insulin, cortisol and GH had opposite effects on lipolytic activity, with cortisol inhibiting and GH stimulating. In line with the fact that both glucocorticoid and GH receptors are expressed in human adipose tissue (28, 29), the findings indicate that cortisol and GH act directly on adipose tissue to exert their physiological influences. Furthermore, the present results suggest that the lipolytic effect of GH is strengthened in the presence of cortisol.

We have developed an experimental protocol, including a tissue incubation technique, for the study of hormonal regulation of LPL activity, the key enzyme for lipid accumulation, in human adipose tissue (21, 22). This protocol was now used to explore the effects of cortisol and GH on the other major determinant of the turnover of intracellular triglyceride, i.e. lipolytic activity. Thus, the conditions used during these incubations regarding hormone concentrations and times of exposure were chosen with the guidance of previous information on hormonal responsiveness in this system. It cannot therefore be excluded that optimal lipolytic effects of cortisol and GH can be observed under somewhat modified conditions.

In this study the mechanisms by which cortisol and GH influenced lipolysis were only partially investigated. The effects of GH may be mediated via an effect on ß-adrenoceptors as previously suggested (17, 19, 30, 31). The influence of cortisol on the sensitivity to catecholamines could also be compatible with changes in ß-adrenoceptor number or functional coupling to the Gs protein. In fact, in 3T3-F442A adipocytes dexamethasone down-regulates ß3-adrenoceptor protein expression and ß3-adrenoceptor-mediated adenylate cyclase activity (32). However, postreceptor effects of the hormones are also most likely involved, as forskolin-stimulated lipolysis was affected by the preceding hormone exposure of the tissue. Cortisol exposure of the tissue reduced the maximum lipolytic activity induced by forskolin, which activates adenylate cyclase (33), but had no effect on maximum lipolytic activity stimulated by N-6-monobutyryl-cAMP, a phosphodiesterase-resistant cAMP analog (34). This observation suggests that cortisol affects the cAMP production rate at the adenylate cyclase level or, alternatively, alters the cAMP elimination rate by stimulating phosphodiesterase activity. Addition of GH to the cortisol-containing medium antagonized the inhibiting effect of cortisol on maximum forskolin-induced lipolytic activity and increased this activity compared to the control value, indicating that GH may also affect the adenylate cyclase and/or phosphodiesterase activities. Clearly, further studies are needed to clarify the mechanisms by which glucocorticoids and GH participate in the regulation of lipolysis.

The suggestion by Cigolini and Smith that exposure of human adipose tissue to hydrocortisone in the presence of insulin reduces basal and noradrenaline-stimulated lipolysis (13) is in agreement with the present results. Four publications address differing effects of GH on lipolysis in human adipose tissue in vitro (18, 19, 20, 35). One important difference between the previous (18) and the present study that could explain the discrepant results is the presence of insulin in the incubation medium during our tissue incubations. It has previously been reported that human adipose tissue explants in tissue culture medium exposed to various concentrations of insulin for 1 week released more glycerol than explants that were not treated with insulin (36). The simultaneous presence of GH and insulin during a 16-h culture of rat adipocytes increased the basal lipolytic rate compared with that found when cells were incubated with GH alone. Additionally, the response to isoprenaline was greater in cells cultured with both hormones than the responses of cells cultured with each hormone alone (37). Together, previous and the present findings indicate that chronic exposure of adipocytes to insulin results in alterations in basal lipolytic activity and in their response to subsequent stimulation with other hormones. Thus, it is possible that the presence of insulin in the incubation medium during long term tissue or cell culture is necessary for the effects of cortisol and GH on lipolysis to appear.

In agreement with our findings, a direct lipolytic effect of GH was observed after exposure of human adipocytes to GH immediately after excision of the tissue and subsequent isolation of the cells (20). In support of this, Wabitsch et al. (35) observed direct lipolytic effects of GH in cultured newly differentiated human adipocytes, whereas Marcus et al. (19) did not observe any direct lipolytic effect in response to short term GH exposure of human adipocytes. Differences in methods, such as different GH concentrations and exposure times, could be the reason for this discrepancy. In our hands, the inhibitory effect of GH on LPL activity in human adipose tissue in vitro occurs at the earliest after 4 h of GH exposure (Ottosson, M., unpublished observation), suggesting that the antilipogenic effects of GH take several hours of exposure to be expressed.

Together with previous results on cortisol and GH regulation of human adipose tissue LPL activity in vitro (21, 22), the present study indicates opposite effects of cortisol and GH on both lipid uptake and lipid mobilization in human adipose tissue. On the one hand, cortisol in the presence of insulin favors lipid accumulation by stimulation of LPL activity and by inhibition of basal and catecholamine-stimulated lipolysis; on the other hand, GH attenuates cortisol-induced LPL activity and stimulates basal and catecholamine-stimulated lipolysis. These results are in line with the effects of the two hormones observed in clinical conditions (1, 2, 3, 4, 5). Also, it may be suggested that the tissue incubation technique may be a useful tool in further studies of the mechanisms by which glucocorticoids and GH affect adipose tissue metabolism.


   Acknowledgments
 
We thank Anna Nilsson, Birgitta Odén, and Carolina Simonsson for excellent technical assistance.


   Footnotes
 
1 This work was supported by grants from the Swedish Medical Research Council (00251, 08269, and 10864), the Handlaren Hjalmar Svenson’s Foundation, and the Nordisk Insulin Foundation. Back

Received December 4, 1998.

Revised September 22, 1999.

Accepted October 27, 1999.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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Gene deletion reveals roles for annexin A1 in the regulation of lipolysis and IL-6 release in epididymal adipose tissue
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N. Hiscock, C. P. Fischer, M. Sacchetti, G. van Hall, M. A. Febbraio, and B. K. Pedersen
Recombinant human interleukin-6 infusion during low-intensity exercise does not enhance whole body lipolysis or fat oxidation in humans
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M. Misra, K. K. Miller, C. Almazan, M. Worley, D. B. Herzog, and A. Klibanski
Hormonal Determinants of Regional Body Composition in Adolescent Girls with Anorexia Nervosa and Controls
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A. G. Holmes, M. J. Watt, and M. A. Febbraio
Suppressing lipolysis increases interleukin-6 at rest and during prolonged moderate-intensity exercise in humans
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C. B. Djurhuus, C. H. Gravholt, S. Nielsen, S. B. Pedersen, N. Moller, and O. Schmitz
Additive effects of cortisol and growth hormone on regional and systemic lipolysis in humans
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G. Engstrom, B. Hedblad, L. Stavenow, P. Lind, L. Janzon, and F. Lindgarde
Inflammation-Sensitive Plasma Proteins Are Associated With Future Weight Gain
Diabetes, August 1, 2003; 52(8): 2097 - 2101.
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G. van Hall, A. Steensberg, M. Sacchetti, C. Fischer, C. Keller, P. Schjerling, N. Hiscock, K. Moller, B. Saltin, M. A. Febbraio, et al.
Interleukin-6 Stimulates Lipolysis and Fat Oxidation in Humans
J. Clin. Endocrinol. Metab., July 1, 2003; 88(7): 3005 - 3010.
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J. W. Tomlinson, N. Crabtree, P. M. S. Clark, G. Holder, A. A. Toogood, C. H. L. Shackleton, and P. M. Stewart
Low-Dose Growth Hormone Inhibits 11{beta}-Hydroxysteroid Dehydrogenase Type 1 but Has No Effect upon Fat Mass in Patients with Simple Obesity
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M. M Buijs, J. Burggraaf, C. Wijbrandts, M. L de Kam, M. Frolich, A. F Cohen, J. A Romijn, H. P Sauerwein, A E. Meinders, and H. Pijl
Blunted lipolytic response to fasting in abdominally obese women: evidence for involvement of hyposomatotropism
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T. Dimitriou, C. Maser-Gluth, and T. Remer
Adrenocortical activity in healthy children is associated with fat mass
Am. J. Clinical Nutrition, March 1, 2003; 77(3): 731 - 736.
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Y. Appiagyei-Dankah, C. D. Tapiador, J. F. Evans, M. Castro-Magana, J. F. Aloia, and J. K. Yeh
Influence of growth hormone on bone marrow adipogenesis in hypophysectomized rats
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S. Nielsen, N. Moller, S. B. Pedersen, J. S. Christiansen, and J. O. L. Jorgensen
The Effect of Long-Term Pharmacological Antilipolysis on Substrate Metabolism in Growth Hormone (GH)-Substituted GH-Deficient Adults
J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3274 - 3278.
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C. B. Djurhuus, C. H. Gravholt, S. Nielsen, A. Mengel, J. S. Christiansen, O. E. Schmitz, and N. Moller
Effects of cortisol on lipolysis and regional interstitial glycerol levels in humans
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R. J. Saad, B. S. Keenan, K. Danadian, V. D. Lewy, and S. A. Arslanian
Dihydrotestosterone Treatment in Adolescents with Delayed Puberty: Does it Explain Insulin Resistance of Puberty?
J. Clin. Endocrinol. Metab., October 1, 2001; 86(10): 4881 - 4886.
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S. Meijssen, M. C. Cabezas, C. G. M. Ballieux, R. J. Derksen, S. Bilecen, and D. W. Erkelens
Insulin Mediated Inhibition of Hormone Sensitive Lipase Activity in Vivo in Relation to Endogenous Catecholamines in Healthy Subjects
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