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Interactions Between Sex Steroid Hormones and Leptin in Women

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Interactions Between Sex Steroid Hormones and Leptin in Women International Journal of Obesity (2000) 24, 1438±1444 ß 2000 Macmillan Publishers Ltd All rights reserved 0307±0565/00 $15.00 www.nature.com/ijo Interactions between sex steroid hormones and leptin in women. Studies in vivo and in vitro K Kristensen1*, SB Pedersen1 and B Richelsen1 1Department of Endocrinology and Metabolism, Aarhus University Hospital, Aarhus Amtssygehus, DK-8000, Denmark OBJECTIVE: To investigate the associations between sex hormones and leptin. In addition, to investigate the direct effect of sex hormones by incubations of human subcutaneous adipose tissue explants, in vitro. DESIGN: Cross-sectional study and an experimental in vitro study. SUBJECTS: 36 women (age, 23 ± 65 y; body mass index, BMI, 19 ± 65 kg=m2) participated in the cross-sectional study. Subcutaneous abdominal biopsies were taken from nine women (age, 28 ± 46 y; BMI, 25.5 ± 36.0 kg=m2) for the in vitro study. MEASUREMENTS: Fat distribution parameters (by dual-energy X-ray absorptiometry and anthropometry), sex hormones, leptin and insulin. RESULTS: Leptin correlated signi®cantly with most estimates of adipose tissue mass (r 0.5 ± 0.9, P < 0.05). However, when the study group was divided in three equal groups (non-obese, obese, and very-obese) it revealed that the correlation predominantly was found in non-obese. In simple correlation analysis leptin was signi®cantly associated with estimates of adipose tissue, insulin and several sex hormones. However, in multiple regression analysis only insulin (partial correlation coef®cient 0.55, P < 0.004) and percentage fat mass (partial correlation coef®cient 0.72, P < 0.001) were signi®cantly and independently correlated with leptin without any independent effect of sex hormones. These ®ndings were in agreement with the in vitro studies where neither estrogen nor androgens (testosterone or DHT) affected subcutaneous adipose tissue leptin production. Dexamethasone (10 nM) stimulated adipose tissue leptin production 3-fold (P < 0.001). CONCLUSION: In regression analysis, where both insulin and measurements of fat mass were taken into account, androgens or estrogens did not independently contribute to the variation in leptin levels. Estrogens and androgens had no direct effects on adipose tissue leptin production in vitro. Thus, the sexual dimorphism evident in serum leptin is not likely to be due to a direct in¯uence of sex hormones on leptin production in females. International Journal of Obesity (2000) 24, 1438±1444 Keywords: leptin; anthropometric measurements; DEXA; sex steroid hormones; insulin Introduction is controlled for body mass index (BMI),10 percentage of body fat,11 total fat mass,12 different fat depots13 or A substantial variability in serum leptin concentra- skin-fold thickness. In addition, the sex difference is tions remains among subjects with equivalent amount evident at the ob mRNA level.14 In a study by of adipose tissue1,2 and obviously factors other than Wabitsch et al,15 the fat mass corrected leptin con- adipose tissue mass are important in the regulation of centrations were at the highest in boys during early serum leptin. In accordance, investigations have puberty and declined thereafter, whereas the leptin shown that prolonged fasting decreases serum leptin concentrations in girls increased during the whole of and leptin expression,3 whereas only excessive food puberty. In trans-sexual subjects, leptin concentrations intake increases serum leptin.4 Furthermore, hor- were reversed according to sex steroid-induced mones such as dexamethasone5,6 and insulin lead to change in phenotype, suggesting an in¯uence of sex an increase in leptin concentrations,7,8 and adrenergic hormones on plasma leptin.16 This had led to the agonists to a decrease in serum leptin.9 suggestion that sex hormones are important in regu- The majority of investigations indicate a gender lating serum leptin. Furthermore, some investigations difference in leptin concentrations. The increased have shown that the ¯uctuation in estrogen during the leptin concentration in females has been con®rmed menstrual cycle has an in¯uence on leptin concentra- in several large studies and persists even when leptin tions.17 However, other studies have not been able to con®rm any signi®cant difference during the men- strual cycle,18,19 in pre-or postmenopausal states20 or *Correspondence: K Kristensen, Departments of Endocrinology in postmenopausal women treated with hormone and Metabolism, Aarhus University Hospital, Aarhus replacement therapy.20 ± 22 Amtssygehus, DK-8000 Aarhus C, Denmark. The investigations regarding the effects of testos- E-mail: [email protected] Received 23 September 1999; revised 8 May 2000; accepted terone have been more convincing. In hypogonadal 12 June 2000 men, leptin concentrations adjusted for BMI, were Sex hormones and leptin in humans K Kristensen et al 1439 elevated when compared with those for healthy men, with underwater weighting and a reproducibility and normalized on testosterone substitution.23 How- of 98.7 ± 99.7%. Each scan can later be manipulated ever BMI is not a good estimate of adipose tissue to give body composition in speci®cally chosen mass and especially not when androgen hormones areas of interest. The following measurements were are administered because this is followed by used to evaluate the effects of adipose tissue distribu- changes in both lean mass and adipose tissue tion on leptin measurements: total fat mass (FMDEXA), 24 mass. However, association studies have con®rmed percentage fat tissue FMDEXA=body weightÂ100% a negative correlation between leptin and different (FM%), lean body mass (LBMDEXA), fat tissue 13 androgens. localized on the trunk (TFDEXA), percentage of In the present study we have investigated the fat localized on the trunk TFDEXA=FMDEXAÂ association between leptin and sex hormones in 100% (TF%), subcutaneous fat tissue localized 36 women. In addition, the direct effects of testo- on arms and legs (PERIFATDEXA) and percentage sterone, DHT and 17 b-estradiol were investigated of subcutaneous fat localized on arms and legs in female subcutaneous adipose tissue fragments (PERIFATDEXA%). in vitro. Finally, the correlation between leptin and estimates of body composition, evaluated by anthro- pometric measurements and by DEXA scans, was Incubation of adipose tissue investigated. Nine women (25.5 < BMI < 36.0 kg=m2) had a sub- cutaneous adipose tissue biopsy taken at the level of the umbilicus. The tissue was removed using sterile technique, placed in Medium 199 without phenol red Materials and methods and all subsequent procedures were carried out under a laminar air¯ow hood. The tissue was minced into Subjects fragments of less the 10 mg each. All samples were Thirty-six healthy adult women with an age span from washed free of blood clots and free lipid and placed in 23 to 65 y with a wide range of BMI (19.3 ± organ culture as previously described.22,25 In brief, 61.9 kg=m2) were selected to the study. Thirty-four 500 mg adipose tissue fragments ¯oated freely in were premenopausal and two were postmenopausal. 16 ml serum-free Medium 199 without phenol red in Twelve were considered as non-obese (BMI < 30), 12 50 ml plastic tubes. The cultures were placed in a as obese (30 < BMI < 40) and the last 12 as severely humidi®ed incubator and maintained at 37Cinan obese (BMI > 40). All the subjects were healthy apart atmosphere of 5% CO2 in O2. The medium was from being obese and none were diabetic. Body supplemented with 25 mM Hepes, 5% bovine albumin weight was stable for at least 2 months prior to the and 1 nM insulin (Novo Nordisk, Demark). The adi- study as indicated by history. The subjects were pose rissue inplants were incubated in duplicates, and included in the study after informed consent in accor- the medium collected at least every 24 h the medium dance with Helsinki Declaration II and the local was changed and the cumulative leptin secretion Ethics Committee approved the study. calculated. Because of the pronounced response to dexamethasone, all incubations with adipose tissue were made with dexamethasone as a control to assure Anthropometric measurements. the responsiveness of the cells. The culture medium Height and body weight were measured and body was kept at 720C until leptin was measured. All mass index (BMI weight in kg divided by the height reagents were obtained from Sigma Chemical Co., St in meters squared) was calculated. Waist circumfer- Louis, MO, USA. ence was measured in the supine position midway between the lower rib and the iliac crest. The hip circumference was measured at the widest part of the Blood parameters hip region and the waist ± hip ratio (WHR) was Leptin was measured as a single measurement calculated from the measurements. The sagittal dia- after fasting for 8 h in serum samples with a RIA meter (SD) was measured in maximal expiration with method from Linco Research Ltd., St Charles, a calliper halfway between the lower rib and the iliac MO. The range of the standard curve in this crest. assay was 0.5 ± 100 ng=ml. Intraassay coef®cient of variation was 3.7%. Full sex hormone status was measured at the Statens Serum Institute, Copen- Dual energy X-ray absorbtiometry (DEXA) scans hagen, Denmark. The following hormones were Body composition was evaluated using a QDR- measured: sexual hormone binding globulin 1000 densiometre (Hologic, Waltham, MA, USA). (SHBG), 17b-estradiol, free estradiol, estrone, Absorbance was measured in the patient alone and free testosterone, testosterone, dihydrotestosterone
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