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Specific skeletal muscle sphingolipid compounds in energy expenditure regulation and weight gain in Native Americans of Southwestern heritage.

ABSTRACT: BACKGROUND/OBJECTIVES:In animal models, a role in the regulation of energy expenditure (EE) has been ascribed to sphingolipids, active components of cell membranes participating in cellular signaling. In humans, it is unknown whether sphingolipids have a role in the modulation of EE and, consequently, influence weight gain. The present study investigated the putative association of EE and weight gain with sphingolipid levels in the human skeletal muscle, a component of fat-free mass (the strongest determinant of EE), in adipose tissue and plasma. SUBJECTS/METHODS:Twenty-four-hour EE, sleeping metabolic rate (SMR) and resting metabolic rate (RMR) were assessed in 35 healthy Native Americans of Southwestern heritage (24 male; 30.2±7.73 years). Sphingolipid (ceramide, C; sphingomyelin, SM) concentrations were measured in skeletal muscle tissue, subcutaneous adipose tissue and plasma samples. After 6.68 years (0.26-12.4 years), follow-up weights were determined in 16 participants (4 females). RESULTS:Concentrations of C24:0, SM18:1/26:1 and SM18:0/24:1 in muscle were associated with 24-h EE (r=-0.47, P=0.01), SMR (r=-0.59, P=0.0008) and RMR (r=-0.44, P=0.01), respectively. Certain muscle sphingomyelins also predicted weight gain (for example, SM18:1/23:1, r=0.74, P=0.004). For specific muscle sphingomyelins that correlated with weight gain and EE (SM18:1/23:0, SM18:1/23:1 and SMR, r=-0.51, r=-0.41, respectively, all P<0.03; SM18:1/24:2 and RMR, r=-0.36, P=0.03), associations could be reproduced with SMR in adipose tissue (all r<-0.46, all P<0.04), though not in plasma. CONCLUSIONS:This study provides preliminary, novel evidence, that specific muscle and adipose tissue sphingolipid compounds are associated with EE and weight gain in Native Americans of Southwestern heritage. Further studies are warranted to investigate whether sphingolipids of different body compartments act in concert to modulate energy balance in humans.

SUBMITTER: Heinitz S

PROVIDER: S-EPMC5626585 | biostudies-literature | 2017 Oct

REPOSITORIES: biostudies-literature

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Specific skeletal muscle sphingolipid compounds in energy expenditure regulation and weight gain in Native Americans of Southwestern heritage.

Heinitz S S Piaggi P P Vinales K L KL Basolo A A Spranger J J Piomelli D D Krakoff J J Jumpertz von Schwartzenberg R R

International journal of obesity (2005) 20170613 10

<h4>Background/objectives</h4>In animal models, a role in the regulation of energy expenditure (EE) has been ascribed to sphingolipids, active components of cell membranes participating in cellular signaling. In humans, it is unknown whether sphingolipids have a role in the modulation of EE and, consequently, influence weight gain. The present study investigated the putative association of EE and weight gain with sphingolipid levels in the human skeletal muscle, a component of fat-free mass (the ...[more]

PMID: 28607453

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Project description:BACKGROUND:There are significant variations in gestational weight gain, with many women gaining in excess of the Institute of Medicine guidelines. Unfortunately, efforts to improve appropriate gestational weight gain have had only limited success. To date, interventions have focused primarily on decreasing energy intake and/or increasing physical activity. Maternal resting energy expenditure, which comprises ?60% of total energy expenditure compared with the ?20% that comes from physical activity, may be an important consideration in understanding variations in gestational weight gain. OBJECTIVE:Our objective was to quantify the changes in resting energy expenditure during pregnancy and their relationship to gestational weight gain and body composition changes among healthy women. We hypothesized that greater gestational weight gain, and fat mass accrual in particular, are inversely related to variations in resting energy expenditure. STUDY DESIGN:We conducted a secondary analysis of a prospective cohort studied before conception and late pregnancy (34-36 weeks). Body composition (estimated using hydrodensitometry) and resting energy expenditure (estimated using indirect calorimetry) were measured. The relationship between the changes in resting energy expenditure and gestational weight gain and the change in fat mass and fat-free mass were quantified. Resting energy expenditure was expressed as kilocalories per kilogram of fat-free mass per day (kilocalories per kilogram of fat-free mass-1/day-1) and kilocalories per day. Correlations are reported as r. RESULTS:Among 51 women, preconception body mass index was 23.0 (4.7) kg/m2; gestational weight gain was 12.8 (4.7) kg. Preconception and late pregnancy resting energy expenditure (kilocalories per day) correlated positively with the change in fat-free mass (r = 0.37, P = .008; r = 0.51, P = .001). Late-pregnancy resting energy expenditure (kilocalories per kilogram of fat-free mass-1/day-1) was inversely associated with the change in fat mass (r = -0.34, P = .02) and gestational weight gain (r = -0.29, P = .04). From before pregnancy through late gestation, the increase in resting energy expenditure (kilocalories per day) correlated positively with the change in fat-free mass (r = 0.44, P = .002) and negatively with the change in fat mass (r = -0.27, P = .06). CONCLUSION:The change in resting energy expenditure from before conception through late gestation correlated positively with changes in fat-free mass but negatively with fat mass accrual. Women with smaller increases in resting energy expenditure across pregnancy had greater gestational weight gain, specifically more adipose tissue. These data suggest that resting energy expenditure is an important factor in gestational weight gain, particularly excess fat mass accrual. Future lifestyle intervention studies need to consider clinically feasible means of estimating resting energy expenditure and, in response, tailor nutrient intake and composition recommendations. Implementing and testing such interventions would be a novel approach to improve compliance with gestational weight gain guidelines.

Project description:Background/objectivesEnergy expenditure (EE), as reflective of body energy demand, has been proposed to be the key driver of food intake, possibly influencing weight change in humans. Variation in this energy-sensing link (overeating relative to weight-maintaining energy requirements) may lead to weight gain over time.Subjects/methodsSixty-one overweight otherwise healthy Native Americans (age: 34.0 ± 7.9 years, body fat: 39.7 ± 9.5%, 36 males) were admitted to our clinical research unit for measurements of body composition by dual-energy X-ray absorptiometry, and 24-h EE and respiratory quotient (RQ) in a whole-room indirect calorimeter during energy balance and weight stability. Following this, ad libitum food intake was assessed for three days using computerized vending machines. Body weight change under unrestricted free-living conditions was assessed at an outpatient follow-up visit (median follow-up time = 1.7 years).ResultsTotal ad libitum food intake (3-day average) was positively associated with 24-h EE (r = 0.44, p < 0.001), RQ (r = 0.34, p = 0.007), and fat free mass (r = 0.38, p = 0.002). A relatively greater food intake after accounting for 24-h EE, but not for RQ (p = 0.30) or for fat free mass (p = 0.23) nor total food intake (p = 0.16), predicted weight gain at the outpatient follow-up visit (r = 0.26, p = 0.04), such that overeating 100 Kcal/d above the food intake predicted by 24-h EE at baseline was associated with an average weight gain of 0.22 Kg over the follow-up period (95% CI: 0.01 to 0.42 Kg). This was due to relatively greater dietary fat intake (r = 0.32, p = 0.01), but not carbohydrate (p = 0.27) or protein (p = 0.06) intake.ConclusionThe individual propensity to overeating, particularly fat, in excess of the weight-maintaining energy requirements can be assessed and predicts long-term weight gain, suggesting that variation in energy sensing may influence appetite by favoring overeating thus promoting obesity development.

Dataset Information

Specific skeletal muscle sphingolipid compounds in energy expenditure regulation and weight gain in Native Americans of Southwestern heritage.

Publications

Specific skeletal muscle sphingolipid compounds in energy expenditure regulation and weight gain in Native Americans of Southwestern heritage.

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