Adipogenic progenitors from obese human skeletal muscle give rise to functional white adipocytes that contribute to insulin resistance

Background/Objectives: Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively correlated with aging, obesity and insulin resistance in humans. However, no molecular/cellular evidence is available to supp...

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Published inInternational Journal of Obesity Vol. 40; no. 3; pp. 497 - 506
Main Authors Laurens, C, Louche, K, Sengenes, C, Coué, M, Langin, D, Moro, C, Bourlier, V
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.03.2016
Nature Publishing Group
Subjects
13/31
14
14/34
14/63
38
38/77
631/443/319/1557
631/443/319/1642/2037
631/80/86/2367
692/4023/1671/1668/1973
692/699/2743/2037
692/699/2743/393
96
Adipocytes
Adipocytes, White - metabolism
Adipogenesis - physiology
Adipose tissue
Aging
Beads
Biopsy
Body fat
Body mass index
CD56 Antigen
Cell differentiation
Cell Differentiation - physiology
Cells (biology)
Cells, Cultured
Cytology
Development and progression
Epidemiology
Fascia
Fat cells
Female
Flow cytometry
Fucosyltransferases
Genotype & phenotype
Glucose
Health Promotion and Disease Prevention
Humans
Insulin
Insulin Resistance
Internal Medicine
Lewis X Antigen
Life Sciences
Male
Medicine
Medicine & Public Health
Metabolic Diseases
Metabolism
Middle age
Middle Aged
Muscle, Skeletal - cytology
Muscle, Skeletal - metabolism
Muscles
Musculoskeletal system
Myotubes
Obesity
Obesity - metabolism
original-article
Paracrine signalling
Phenotypes
Physiological aspects
Progenitor cells
Properties
Public Health
Risk factors
Satellite cells
Secretions
Signaling
Skeletal muscle
Stem cells
Stroma
France
Online AccessGet full text
ISSN0307-0565
1476-5497
0307-0565
DOI10.1038/ijo.2015.193

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Abstract Background/Objectives: Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively correlated with aging, obesity and insulin resistance in humans. However, no molecular/cellular evidence is available to support these interactions. The current study aimed to better characterize human skeletal muscle-derived adipogenic progenitors obtained from obese volunteers and investigate the impact of derived adipocytes on insulin action in primary skeletal muscle cells. Methods: Primary cultured stroma-vascular fraction (SVF) obtained from vastus lateralis muscle biopsies of middle-aged obese subjects was immunoseparated (magnetic beads or flow cytometry). The characteristics and/or metabolic phenotype of CD56 + , CD56 − and CD56 − CD15 + cellular fractions were investigated by complementary approaches (flow cytometry, cytology, quantitative PCR and metabolic assays). The effects of conditioned media from CD56 − CD15 + cells differentiated into adipocytes on insulin action and signaling in human primary myotubes was also examined. Results: Our data indicate that CD56 + and CD56 − cellular fractions isolated from cultured SVF of human muscle contain two distinct committed progenitors: CD56 + cells (that is, satellite cells) as myogenic progenitors and CD15 + cells as adipogenic progenitors, respectively. CD56 − CD15 + -derived adipocytes display the phenotype and metabolic properties of white adipocytes. Secretions of CD56 − CD15 + cells differentiated into functional white adipocytes reduced insulin-mediated non-oxidative glucose disposal ( P =0.0002) and insulin signaling. Conclusions: Using in - vitro models, we show for the first time that secretions of skeletal muscle adipocytes are able to impair insulin action and signaling of muscle fibers. This paracrine effect could explain, at least in part, the negative association between high levels of IMAT and insulin sensitivity in obesity and aging.
AbstractList Background/Objectives: Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively correlated with aging, obesity and insulin resistance in humans. However, no molecular/cellular evidence is available to support these interactions. The current study aimed to better characterize human skeletal muscle-derived adipogenic progenitors obtained from obese volunteers and investigate the impact of derived adipocytes on insulin action in primary skeletal muscle cells. Methods: Primary cultured stroma-vascular fraction (SVF) obtained from vastus lateralis muscle biopsies of middle-aged obese subjects was immunoseparated (magnetic beads or flow cytometry). The characteristics and/or metabolic phenotype of CD56 + , CD56 − and CD56 − CD15 + cellular fractions were investigated by complementary approaches (flow cytometry, cytology, quantitative PCR and metabolic assays). The effects of conditioned media from CD56 − CD15 + cells differentiated into adipocytes on insulin action and signaling in human primary myotubes was also examined. Results: Our data indicate that CD56 + and CD56 − cellular fractions isolated from cultured SVF of human muscle contain two distinct committed progenitors: CD56 + cells (that is, satellite cells) as myogenic progenitors and CD15 + cells as adipogenic progenitors, respectively. CD56 − CD15 + -derived adipocytes display the phenotype and metabolic properties of white adipocytes. Secretions of CD56 − CD15 + cells differentiated into functional white adipocytes reduced insulin-mediated non-oxidative glucose disposal ( P =0.0002) and insulin signaling. Conclusions: Using in - vitro models, we show for the first time that secretions of skeletal muscle adipocytes are able to impair insulin action and signaling of muscle fibers. This paracrine effect could explain, at least in part, the negative association between high levels of IMAT and insulin sensitivity in obesity and aging.
BACKGROUND/OBJECTIVESRecent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively correlated with aging, obesity and insulin resistance in humans. However, no molecular/cellular evidence is available to support these interactions. The current study aimed to better characterize human skeletal muscle-derived adipogenic progenitors obtained from obese volunteers and investigate the impact of derived adipocytes on insulin action in primary skeletal muscle cells.METHODSPrimary cultured stroma-vascular fraction (SVF) obtained from vastus lateralis muscle biopsies of middle-aged obese subjects was immunoseparated (magnetic beads or flow cytometry). The characteristics and/or metabolic phenotype of CD56(+), CD56(-) and CD56(-)CD15(+) cellular fractions were investigated by complementary approaches (flow cytometry, cytology, quantitative PCR and metabolic assays). The effects of conditioned media from CD56(-)CD15(+) cells differentiated into adipocytes on insulin action and signaling in human primary myotubes was also examined.RESULTSOur data indicate that CD56(+) and CD56(-) cellular fractions isolated from cultured SVF of human muscle contain two distinct committed progenitors: CD56(+) cells (that is, satellite cells) as myogenic progenitors and CD15(+) cells as adipogenic progenitors, respectively. CD56(-)CD15(+)-derived adipocytes display the phenotype and metabolic properties of white adipocytes. Secretions of CD56(-)CD15(+) cells differentiated into functional white adipocytes reduced insulin-mediated non-oxidative glucose disposal (P=0.0002) and insulin signaling.CONCLUSIONSUsing in-vitro models, we show for the first time that secretions of skeletal muscle adipocytes are able to impair insulin action and signaling of muscle fibers. This paracrine effect could explain, at least in part, the negative association between high levels of IMAT and insulin sensitivity in obesity and aging.
Background/ Objectives: Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively correlated with aging, obesity and insulin resistance in humans. However, no molecular/cellular evidence is available to support these interactions. The current study aimed to better characterize human skeletal muscle-derived adipogenic progenitors obtained from obese volunteers and investigate the impact of derived adipocytes on insulin action in primary skeletal muscle cells. Methods: Primary cultured stroma-vascular fraction (SVF) obtained from vastus lateralis muscle biopsies of middle-aged obese subjects was immunoseparated (magnetic beads or flow cytometry). The characteristics and/or metabolic phenotype of CD56 super(+), CD56 super(-) and CD56 super(-)CD15 super(+) cellular fractions were investigated by complementary approaches (flow cytometry, cytology, quantitative PCR and metabolic assays). The effects of conditioned media from CD56 super(-)CD15 super(+) cells differentiated into adipocytes on insulin action and signaling in human primary myotubes was also examined. Results: Our data indicate that CD56 super(+) and CD56 super(-) cellular fractions isolated from cultured SVF of human muscle contain two distinct committed progenitors: CD56 super(+) cells (that is, satellite cells) as myogenic progenitors and CD15 super(+) cells as adipogenic progenitors, respectively. CD56 super(-)CD15 super(+)-derived adipocytes display the phenotype and metabolic properties of white adipocytes. Secretions of CD56 super(-)CD15 super(+) cells differentiated into functional white adipocytes reduced insulin-mediated non-oxidative glucose disposal (P=0.0002) and insulin signaling. Conclusions: Using in-vitro models, we show for the first time that secretions of skeletal muscle adipocytes are able to impair insulin action and signaling of muscle fibers. This paracrine effect could explain, at least in part, the negative association between high levels of IMAT and insulin sensitivity in obesity and aging.
Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively correlated with aging, obesity and insulin resistance in humans. However, no molecular/cellular evidence is available to support these interactions. The current study aimed to better characterize human skeletal muscle-derived adipogenic progenitors obtained from obese volunteers and investigate the impact of derived adipocytes on insulin action in primary skeletal muscle cells. Primary cultured stroma-vascular fraction (SVF) obtained from vastus lateralis muscle biopsies of middle-aged obese subjects was immunoseparated (magnetic beads or flow cytometry). The characteristics and/or metabolic phenotype of CD56(+), CD56(-) and CD56(-)CD15(+) cellular fractions were investigated by complementary approaches (flow cytometry, cytology, quantitative PCR and metabolic assays). The effects of conditioned media from CD56(-)CD15(+) cells differentiated into adipocytes on insulin action and signaling in human primary myotubes was also examined. Our data indicate that CD56(+) and CD56(-) cellular fractions isolated from cultured SVF of human muscle contain two distinct committed progenitors: CD56(+) cells (that is, satellite cells) as myogenic progenitors and CD15(+) cells as adipogenic progenitors, respectively. CD56(-)CD15(+)-derived adipocytes display the phenotype and metabolic properties of white adipocytes. Secretions of CD56(-)CD15(+) cells differentiated into functional white adipocytes reduced insulin-mediated non-oxidative glucose disposal (P=0.0002) and insulin signaling. Using in-vitro models, we show for the first time that secretions of skeletal muscle adipocytes are able to impair insulin action and signaling of muscle fibers. This paracrine effect could explain, at least in part, the negative association between high levels of IMAT and insulin sensitivity in obesity and aging.
International Journal of Obesity (2016) 40, 497-506; doi: 10.1038/ijo.2015.193
BACKGROUND/OBJECTIVES: Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively correlated with aging, obesity and insulin resistance in humans. However, no molecular/cellular evidence is available to support these interactions. The current study aimed to better characterize human skeletal muscle-derived adipogenic progenitors obtained from obese volunteers and investigate the impact of derived adipocytes on insulin action in primary skeletal muscle cells. METHODS: Primary cultured stroma-vascular fraction (SVF) obtained from vastus lateralis muscle biopsies of middle-aged obese subjects was immunoseparated (magnetic beads or flow cytometry). The characteristics and/or metabolic phenotype of [CD56.sup.+], [CD56.sup.-] and [CD56.sup.-][CD15.sup.+] cellular fractions were investigated by complementary approaches (flow cytometry, cytology, quantitative PCR and metabolic assays). The effects of conditioned media from [CD56.sup.-][CD15.sup.+] cells differentiated into adipocytes on insulin action and signaling in human primary myotubes was also examined. RESULTS: Our data indicate that [CD56.sup.+] and [CD56.sup.-] cellular fractions isolated from cultured SVF of human muscle contain two distinct committed progenitors: [CD56.sup.+] cells (that is, satellite cells) as myogenic progenitors and [CD15.sup.+] cells as adipogenic progenitors, respectively. [CD56.sup.-][CD15.sup.+]-derived adipocytes display the phenotype and metabolic properties of white adipocytes. Secretions of [CD56.sup.-][CD15.sup.+] cells differentiated into functional white adipocytes reduced insulin-mediated non-oxidative glucose disposal (P = 0.0002) and insulin signaling. CONCLUSIONS: Using in-vitro models, we show for the first time that secretions of skeletal muscle adipocytes are able to impair insulin action and signaling of muscle fibers. This paracrine effect could explain, at least in part, the negative association between high levels of IMAT and insulin sensitivity in obesity and aging. International Journal of Obesity (2016) 40, 497-506; doi: 10.1038/ijo.2015.193
Background/Objectives:Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively correlated with aging, obesity and insulin resistance in humans. However, no molecular/cellular evidence is available to support these interactions. The current study aimed to better characterize human skeletal muscle-derived adipogenic progenitors obtained from obese volunteers and investigate the impact of derived adipocytes on insulin action in primary skeletal muscle cells.Methods:Primary cultured stroma-vascular fraction (SVF) obtained from vastus lateralis muscle biopsies of middle-aged obese subjects was immunoseparated (magnetic beads or flow cytometry). The characteristics and/or metabolic phenotype of CD56+, CD56− and CD56−CD15+ cellular fractions were investigated by complementary approaches (flow cytometry, cytology, quantitative PCR and metabolic assays). The effects of conditioned media from CD56−CD15+ cells differentiated into adipocytes on insulin action and signaling in human primary myotubes was also examined.Results:Our data indicate that CD56+ and CD56− cellular fractions isolated from cultured SVF of human muscle contain two distinct committed progenitors: CD56+ cells (that is, satellite cells) as myogenic progenitors and CD15+ cells as adipogenic progenitors, respectively. CD56−CD15+-derived adipocytes display the phenotype and metabolic properties of white adipocytes. Secretions of CD56−CD15+ cells differentiated into functional white adipocytes reduced insulin-mediated non-oxidative glucose disposal (P=0.0002) and insulin signaling.Conclusions:Using in-vitro models, we show for the first time that secretions of skeletal muscle adipocytes are able to impair insulin action and signaling of muscle fibers. This paracrine effect could explain, at least in part, the negative association between high levels of IMAT and insulin sensitivity in obesity and aging.
Background/Objectives:Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively correlated with aging, obesity and insulin resistance in humans. However, no molecular/cellular evidence is available to support these interactions. The current study aimed to better characterize human skeletal muscle-derived adipogenic progenitors obtained from obese volunteers and investigate the impact of derived adipocytes on insulin action in primary skeletal muscle cells.Methods:Primary cultured stroma-vascular fraction (SVF) obtained from vastus lateralis muscle biopsies of middle-aged obese subjects was immunoseparated (magnetic beads or flow cytometry). The characteristics and/or metabolic phenotype of CD56+ , CD56- and CD56- CD15+ cellular fractions were investigated by complementary approaches (flow cytometry, cytology, quantitative PCR and metabolic assays). The effects of conditioned media from CD56- CD15+ cells differentiated into adipocytes on insulin action and signaling in human primary myotubes was also examined.Results:Our data indicate that CD56+ and CD56- cellular fractions isolated from cultured SVF of human muscle contain two distinct committed progenitors: CD56+ cells (that is, satellite cells) as myogenic progenitors and CD15+ cells as adipogenic progenitors, respectively. CD56- CD15+ -derived adipocytes display the phenotype and metabolic properties of white adipocytes. Secretions of CD56- CD15+ cells differentiated into functional white adipocytes reduced insulin-mediated non-oxidative glucose disposal (P=0.0002) and insulin signaling.Conclusions:Using in-vitro models, we show for the first time that secretions of skeletal muscle adipocytes are able to impair insulin action and signaling of muscle fibers. This paracrine effect could explain, at least in part, the negative association between high levels of IMAT and insulin sensitivity in obesity and aging.
Audience Academic
Author Langin, D
Sengenes, C
Bourlier, V
Moro, C
Louche, K
Laurens, C
Coué, M
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Snippet Background/Objectives: Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the...
Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles, is positively...
BACKGROUND/OBJECTIVES: Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the...
International Journal of Obesity (2016) 40, 497-506; doi: 10.1038/ijo.2015.193
Background/Objectives:Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles,...
BACKGROUND/OBJECTIVESRecent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the muscles,...
Background/ Objectives: Recent reports indicate that inter/intramuscular adipose tissue (IMAT), composed by adipocytes underneath the deep fascia of the...
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96
Adipocytes
Adipocytes, White - metabolism
Adipogenesis - physiology
Adipose tissue
Aging
Beads
Biopsy
Body fat
Body mass index
CD56 Antigen
Cell differentiation
Cell Differentiation - physiology
Cells (biology)
Cells, Cultured
Cytology
Development and progression
Epidemiology
Fascia
Fat cells
Female
Flow cytometry
Fucosyltransferases
Genotype & phenotype
Glucose
Health Promotion and Disease Prevention
Humans
Insulin
Insulin Resistance
Internal Medicine
Lewis X Antigen
Life Sciences
Male
Medicine
Medicine & Public Health
Metabolic Diseases
Metabolism
Middle age
Middle Aged
Muscle, Skeletal - cytology
Muscle, Skeletal - metabolism
Muscles
Musculoskeletal system
Myotubes
Obesity
Obesity - metabolism
original-article
Paracrine signalling
Phenotypes
Physiological aspects
Progenitor cells
Properties
Public Health
Risk factors
Satellite cells
Secretions
Signaling
Skeletal muscle
Stem cells
Stroma
Title Adipogenic progenitors from obese human skeletal muscle give rise to functional white adipocytes that contribute to insulin resistance
URI https://link.springer.com/article/10.1038/ijo.2015.193
https://www.ncbi.nlm.nih.gov/pubmed/26395744
https://www.proquest.com/docview/1771229733
https://www.proquest.com/docview/2639130565
https://www.proquest.com/docview/1771723962
https://www.proquest.com/docview/1773837162
https://hal.inrae.fr/hal-05204307
Volume 40
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