Metabolic Cytokines at Fasting and During Macronutrient Challenges: Influence of Obesity, Female Androgen Excess and Sex
Scope: Cytokines have pleiotropic functions within the organism and their levels may be influenced by obesity, visceral adiposity and sex hormones. Diet composition may also affect their systemic concentrations during fasting and in the postprandial period. Hence, we studied the influence of sex ste...
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Published in | Nutrients Vol. 11; no. 11; p. 2566 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
Switzerland
MDPI AG
24.10.2019
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Online Access | Get full text |
ISSN | 2072-6643 2072-6643 |
DOI | 10.3390/nu11112566 |
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Abstract | Scope: Cytokines have pleiotropic functions within the organism and their levels may be influenced by obesity, visceral adiposity and sex hormones. Diet composition may also affect their systemic concentrations during fasting and in the postprandial period. Hence, we studied the influence of sex steroids and obesity on the circulating levels of a panel of metabolic cytokines in the fasting state and after single macronutrient challenges. Methods: On alternate days we submitted 17 women with polycystic ovary syndrome (PCOS) (9 non-obese, 8 obese), 17 non-hyperandrogenic control women (9 non-obese, 8 obese) and 19 control men (10 non-obese, 9 obese) to isocaloric oral glucose, lipid and protein loads. Serum levels of omentin-1, vaspin, lipocalin-2, adipsin, PAI-1, chemerin, FGF-21 and FGF-23 were determined by Luminex multiplex technology. Results: During fasting, obese patients presented higher levels of PAI-1, chemerin and adipsin but decreased FGF-23 and omentin-1 compared with non-obese subjects. Vaspin showed sexual dimorphism with lower levels in men than women with PCOS and female controls. Following macronutrient ingestion, most metabolic cytokines presented a similar physiological response consisting of a decrease in circulating concentrations, which was inversely associated with the fasting levels of these molecules. Protein intake caused the major postprandial decrease whereas glucose did not significantly reduce PAI-1, FGF-23 and vaspin, and even increased FGF-21. Regardless of the macronutrient administered, vaspin levels showed a larger reduction in non-obese individuals while the decrease in PAI-1 was particularly noticeable in the obese subgroup. The postprandial reductions of omentin-1 and FGF-23 after glucose and protein loads were influenced by obesity. No major differences were found between patients with PCOS and male and female controls. Conclusions: Obesity, but not PCOS or sex, markedly influences metabolic cytokine levels at fasting and after macronutrient ingestion. The observed postprandial decrease in their circulating concentrations might represent a physiological compensatory mechanism against food-induced inflammation and oxidative stress. This mechanism is altered by obesity and is differently modulated by macronutrients, suggesting a larger contribution of glucose to stressful postprandial responses. |
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AbstractList | Scope: Cytokines have pleiotropic functions within the organism and their levels may be influenced by obesity, visceral adiposity and sex hormones. Diet composition may also affect their systemic concentrations during fasting and in the postprandial period. Hence, we studied the influence of sex steroids and obesity on the circulating levels of a panel of metabolic cytokines in the fasting state and after single macronutrient challenges. Methods: On alternate days we submitted 17 women with polycystic ovary syndrome (PCOS) (9 non-obese, 8 obese), 17 non-hyperandrogenic control women (9 non-obese, 8 obese) and 19 control men (10 non-obese, 9 obese) to isocaloric oral glucose, lipid and protein loads. Serum levels of omentin-1, vaspin, lipocalin-2, adipsin, PAI-1, chemerin, FGF-21 and FGF-23 were determined by Luminex multiplex technology. Results: During fasting, obese patients presented higher levels of PAI-1, chemerin and adipsin but decreased FGF-23 and omentin-1 compared with non-obese subjects. Vaspin showed sexual dimorphism with lower levels in men than women with PCOS and female controls. Following macronutrient ingestion, most metabolic cytokines presented a similar physiological response consisting of a decrease in circulating concentrations, which was inversely associated with the fasting levels of these molecules. Protein intake caused the major postprandial decrease whereas glucose did not significantly reduce PAI-1, FGF-23 and vaspin, and even increased FGF-21. Regardless of the macronutrient administered, vaspin levels showed a larger reduction in non-obese individuals while the decrease in PAI-1 was particularly noticeable in the obese subgroup. The postprandial reductions of omentin-1 and FGF-23 after glucose and protein loads were influenced by obesity. No major differences were found between patients with PCOS and male and female controls. Conclusions: Obesity, but not PCOS or sex, markedly influences metabolic cytokine levels at fasting and after macronutrient ingestion. The observed postprandial decrease in their circulating concentrations might represent a physiological compensatory mechanism against food-induced inflammation and oxidative stress. This mechanism is altered by obesity and is differently modulated by macronutrients, suggesting a larger contribution of glucose to stressful postprandial responses. Cytokines have pleiotropic functions within the organism and their levels may be influenced by obesity, visceral adiposity and sex hormones. Diet composition may also affect their systemic concentrations during fasting and in the postprandial period. Hence, we studied the influence of sex steroids and obesity on the circulating levels of a panel of metabolic cytokines in the fasting state and after single macronutrient challenges. On alternate days we submitted 17 women with polycystic ovary syndrome (PCOS) (9 non-obese, 8 obese), 17 non-hyperandrogenic control women (9 non-obese, 8 obese) and 19 control men (10 non-obese, 9 obese) to isocaloric oral glucose, lipid and protein loads. Serum levels of omentin-1, vaspin, lipocalin-2, adipsin, PAI-1, chemerin, FGF-21 and FGF-23 were determined by Luminex multiplex technology. During fasting, obese patients presented higher levels of PAI-1, chemerin and adipsin but decreased FGF-23 and omentin-1 compared with non-obese subjects. Vaspin showed sexual dimorphism with lower levels in men than women with PCOS and female controls. Following macronutrient ingestion, most metabolic cytokines presented a similar physiological response consisting of a decrease in circulating concentrations, which was inversely associated with the fasting levels of these molecules. Protein intake caused the major postprandial decrease whereas glucose did not significantly reduce PAI-1, FGF-23 and vaspin, and even increased FGF-21. Regardless of the macronutrient administered, vaspin levels showed a larger reduction in non-obese individuals while the decrease in PAI-1 was particularly noticeable in the obese subgroup. The postprandial reductions of omentin-1 and FGF-23 after glucose and protein loads were influenced by obesity. No major differences were found between patients with PCOS and male and female controls. Obesity, but not PCOS or sex, markedly influences metabolic cytokine levels at fasting and after macronutrient ingestion. The observed postprandial decrease in their circulating concentrations might represent a physiological compensatory mechanism against food-induced inflammation and oxidative stress. This mechanism is altered by obesity and is differently modulated by macronutrients, suggesting a larger contribution of glucose to stressful postprandial responses. Cytokines have pleiotropic functions within the organism and their levels may be influenced by obesity, visceral adiposity and sex hormones. Diet composition may also affect their systemic concentrations during fasting and in the postprandial period. Hence, we studied the influence of sex steroids and obesity on the circulating levels of a panel of metabolic cytokines in the fasting state and after single macronutrient challenges.SCOPECytokines have pleiotropic functions within the organism and their levels may be influenced by obesity, visceral adiposity and sex hormones. Diet composition may also affect their systemic concentrations during fasting and in the postprandial period. Hence, we studied the influence of sex steroids and obesity on the circulating levels of a panel of metabolic cytokines in the fasting state and after single macronutrient challenges.On alternate days we submitted 17 women with polycystic ovary syndrome (PCOS) (9 non-obese, 8 obese), 17 non-hyperandrogenic control women (9 non-obese, 8 obese) and 19 control men (10 non-obese, 9 obese) to isocaloric oral glucose, lipid and protein loads. Serum levels of omentin-1, vaspin, lipocalin-2, adipsin, PAI-1, chemerin, FGF-21 and FGF-23 were determined by Luminex multiplex technology.METHODSOn alternate days we submitted 17 women with polycystic ovary syndrome (PCOS) (9 non-obese, 8 obese), 17 non-hyperandrogenic control women (9 non-obese, 8 obese) and 19 control men (10 non-obese, 9 obese) to isocaloric oral glucose, lipid and protein loads. Serum levels of omentin-1, vaspin, lipocalin-2, adipsin, PAI-1, chemerin, FGF-21 and FGF-23 were determined by Luminex multiplex technology.During fasting, obese patients presented higher levels of PAI-1, chemerin and adipsin but decreased FGF-23 and omentin-1 compared with non-obese subjects. Vaspin showed sexual dimorphism with lower levels in men than women with PCOS and female controls. Following macronutrient ingestion, most metabolic cytokines presented a similar physiological response consisting of a decrease in circulating concentrations, which was inversely associated with the fasting levels of these molecules. Protein intake caused the major postprandial decrease whereas glucose did not significantly reduce PAI-1, FGF-23 and vaspin, and even increased FGF-21. Regardless of the macronutrient administered, vaspin levels showed a larger reduction in non-obese individuals while the decrease in PAI-1 was particularly noticeable in the obese subgroup. The postprandial reductions of omentin-1 and FGF-23 after glucose and protein loads were influenced by obesity. No major differences were found between patients with PCOS and male and female controls.RESULTSDuring fasting, obese patients presented higher levels of PAI-1, chemerin and adipsin but decreased FGF-23 and omentin-1 compared with non-obese subjects. Vaspin showed sexual dimorphism with lower levels in men than women with PCOS and female controls. Following macronutrient ingestion, most metabolic cytokines presented a similar physiological response consisting of a decrease in circulating concentrations, which was inversely associated with the fasting levels of these molecules. Protein intake caused the major postprandial decrease whereas glucose did not significantly reduce PAI-1, FGF-23 and vaspin, and even increased FGF-21. Regardless of the macronutrient administered, vaspin levels showed a larger reduction in non-obese individuals while the decrease in PAI-1 was particularly noticeable in the obese subgroup. The postprandial reductions of omentin-1 and FGF-23 after glucose and protein loads were influenced by obesity. No major differences were found between patients with PCOS and male and female controls.Obesity, but not PCOS or sex, markedly influences metabolic cytokine levels at fasting and after macronutrient ingestion. The observed postprandial decrease in their circulating concentrations might represent a physiological compensatory mechanism against food-induced inflammation and oxidative stress. This mechanism is altered by obesity and is differently modulated by macronutrients, suggesting a larger contribution of glucose to stressful postprandial responses.CONCLUSIONSObesity, but not PCOS or sex, markedly influences metabolic cytokine levels at fasting and after macronutrient ingestion. The observed postprandial decrease in their circulating concentrations might represent a physiological compensatory mechanism against food-induced inflammation and oxidative stress. This mechanism is altered by obesity and is differently modulated by macronutrients, suggesting a larger contribution of glucose to stressful postprandial responses. [...]we studied in a series of young healthy subjects, composed of non-obese and obese women with PCOS and appropriate male and female controls, the circulating levels of a panel of metabolic markers—including six adipokines and two members of the fibroblast growth factor (FGF) superfamily—during fasting and after glucose, lipid and protein oral challenges. 2. Briefly, patients with PCOS presented both clinical and biochemical hyperandrogenism but did not show higher waist circumference (WC), waist to hip ratio (WHR) or differences in metabolic parameters when compared with control women. Besides their higher T levels, men also presented increased WC and WHR but lower levels of high-density lipoprotein cholesterol (HDL) and SHBG compared with both groups of women. [...]we found no statistically significant differences between patients with PCOS and female and male controls in the responses of any metabolic cytokine (Figure 1C,F,I,L and Figure 2C,F,I,L), nor any interaction of the group of subjects with obesity or macronutrient intake (data not shown). [...]the smaller decrease observed for some cytokines after glucose load might be related to its triggering effect on inflammation and oxidative stress [3,10,11,18,19,21,27,28,40]. |
Author | Moncayo, Samuel Escobar-Morreale, Héctor F. Álvarez-Blasco, Francisco Insenser, María Luque-Ramírez, Manuel Martínez-García, M. Ángeles |
AuthorAffiliation | Diabetes, Obesity and Human Reproduction Research Group, Department of Endocrinology & Nutrition, Hospital Universitario Ramón y Cajal & Universidad de Alcalá & Instituto Ramón y Cajal de Investigación Sanitaria IRYCIS & Centro de Investigación Biomédica en Red Diabetes y Enfermedades Metabólicas Asociadas CIBERDEM, Madrid 28034, Spain; manitamg@yahoo.es (M.Á.M.-G.); samuel.moncayo@gmail.com (S.M.); mariarosa.insenser@salud.madrid.org (M.I.); fablas74@gmail.com (F.Á.-B.); manuluque@gmail.com (M.L.-R.) |
AuthorAffiliation_xml | – name: Diabetes, Obesity and Human Reproduction Research Group, Department of Endocrinology & Nutrition, Hospital Universitario Ramón y Cajal & Universidad de Alcalá & Instituto Ramón y Cajal de Investigación Sanitaria IRYCIS & Centro de Investigación Biomédica en Red Diabetes y Enfermedades Metabólicas Asociadas CIBERDEM, Madrid 28034, Spain; manitamg@yahoo.es (M.Á.M.-G.); samuel.moncayo@gmail.com (S.M.); mariarosa.insenser@salud.madrid.org (M.I.); fablas74@gmail.com (F.Á.-B.); manuluque@gmail.com (M.L.-R.) |
Author_xml | – sequence: 1 givenname: M. Ángeles orcidid: 0000-0002-8354-7284 surname: Martínez-García fullname: Martínez-García, M. Ángeles – sequence: 2 givenname: Samuel surname: Moncayo fullname: Moncayo, Samuel – sequence: 3 givenname: María orcidid: 0000-0003-3168-7856 surname: Insenser fullname: Insenser, María – sequence: 4 givenname: Francisco surname: Álvarez-Blasco fullname: Álvarez-Blasco, Francisco – sequence: 5 givenname: Manuel orcidid: 0000-0002-6002-4237 surname: Luque-Ramírez fullname: Luque-Ramírez, Manuel – sequence: 6 givenname: Héctor F. orcidid: 0000-0002-6890-1644 surname: Escobar-Morreale fullname: Escobar-Morreale, Héctor F. |
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Snippet | Scope: Cytokines have pleiotropic functions within the organism and their levels may be influenced by obesity, visceral adiposity and sex hormones. Diet... Cytokines have pleiotropic functions within the organism and their levels may be influenced by obesity, visceral adiposity and sex hormones. Diet composition... [...]we studied in a series of young healthy subjects, composed of non-obese and obese women with PCOS and appropriate male and female controls, the... |
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SubjectTerms | Abdomen adiposity Androgens Androgens - blood Androgens - metabolism animal ovaries blood serum Carbohydrates Cytokines Cytokines - genetics Cytokines - metabolism Diabetes Diet Dietary Proteins - administration & dosage Dietary Proteins - pharmacology Endocrinology fasting Female females Fibroblasts Food Deprivation Gene Expression Regulation - drug effects Gene Expression Regulation - physiology Glucose Glucose - administration & dosage Glucose - pharmacology Growth factors Homeostasis Hormones Humans Inflammation Insulin resistance Lipids Lipids - administration & dosage Lipids - pharmacology Load Male males Meals men Menstruation Metabolism Nutrition research Obesity Obesity - metabolism oxidative stress patients physiological response Physiology Polycystic ovary syndrome Polycystic Ovary Syndrome - metabolism protein intake Proteins Sex Characteristics sexual dimorphism women Young Adult |
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Title | Metabolic Cytokines at Fasting and During Macronutrient Challenges: Influence of Obesity, Female Androgen Excess and Sex |
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