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 inNutrients Vol. 11; no. 11; p. 2566
Main Authors Martínez-García, M. Ángeles, Moncayo, Samuel, Insenser, María, Álvarez-Blasco, Francisco, Luque-Ramírez, Manuel, Escobar-Morreale, Héctor F.
Format Journal Article
LanguageEnglish
Published Switzerland MDPI AG 24.10.2019
MDPI
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ISSN2072-6643
2072-6643
DOI10.3390/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.
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
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  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
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  fullname: Álvarez-Blasco, Francisco
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  fullname: Luque-Ramírez, Manuel
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  givenname: Héctor F.
  orcidid: 0000-0002-6890-1644
  surname: Escobar-Morreale
  fullname: Escobar-Morreale, Héctor F.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31652917$$D View this record in MEDLINE/PubMed
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Issue 11
Keywords PCOS
adiposity
glucose
lipids
sex hormones
proteins
adipokines
oral loads
Language English
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PublicationDate 20191024
PublicationDateYYYYMMDD 2019-10-24
PublicationDate_xml – month: 10
  year: 2019
  text: 20191024
  day: 24
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PublicationTitle Nutrients
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MDPI
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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
URI https://www.ncbi.nlm.nih.gov/pubmed/31652917
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Volume 11
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