Mitochondrial respiration in subcutaneous and visceral adipose tissue from patients with morbid obesity

Regitze Kraunsøe; Robert Christopher Boushel; Christina Neigaard Hansen; Peter Schjerling; Klaus Qvortrup; Mikael Støckel; Kári J Mikines; Flemming Dela

doi:10.1113/jphysiol.2009.184754

Mitochondrial respiration in subcutaneous and visceral adipose tissue from patients with morbid obesity

Regitze Kraunsøe, Robert Christopher Boushel, Christina Neigaard Hansen, Peter Schjerling, Klaus Qvortrup, Mikael Støckel, Kári J Mikines, Flemming Dela

80 Citations (Scopus)

Abstract

Adipose tissue exerts important endocrine and metabolic functions in health and disease. Yet the bioenergetics of this tissue is not characterized in humans and possible regional differences are not elucidated. Using high resolution respirometry, mitochondrial respiration was quantified in human abdominal subcutaneous and intra-abdominal visceral (omentum majus) adipose tissue from biopsies obtained in 20 obese patients undergoing bariatric surgery. Mitochondrial DNA (mtDNA) and genomic DNA (gDNA) were determined by the PCR technique for estimation of mitochondrial density. Adipose tissue samples were permeabilized and respirometric measurements were performed in duplicate at 37°C. Substrates (glutamate (G) + malate (M) + octanoyl carnitine (O) + succinate (S)) were added sequentially to provide electrons to complex I + II. ADP (_D) for state 3 respiration was added after GM. Uncoupled respiration was measured after addition of FCCP. Visceral fat contained more mitochondria per milligram of tissue than subcutaneous fat, but the cells were smaller. Robust, stable oxygen fluxes were found in both tissues, and coupled state 3 (GMOS_D) and uncoupled respiration were significantly (P < 0.05) higher in visceral (0.95 ± 0.05 and 1.15 ± 0.06 pmol O₂ s^-1 mg^-1, respectively) compared with subcutaneous (0.76 ± 0.04 and 0.98 ± 0.05 pmol O₂ s^-1 mg^-1, respectively) adipose tissue. Expressed per mtDNA, visceral adipose tissue had significantly (P < 0.05) lower mitochondrial respiration. Substrate control ratios were higher and uncoupling control ratio lower (P < 0.05) in visceral compared with subcutaneous adipose tissue. We conclude that visceral fat is bioenergetically more active and more sensitive to mitochondrial substrate supply than subcutaneous fat. Oxidative phosphorylation has a higher relative activity in visceral compared with subcutaneous adipose tissue.

Original language	English
Journal	Journal of Physiology
Volume	588
Issue number	12
Pages (from-to)	2023-2032
Number of pages	10
ISSN	0022-3751
DOIs	https://doi.org/10.1113/jphysiol.2009.184754
Publication status	Published - Jun 2010

Keywords

Adult
Biopsy
Carbonyl Cyanide p-Trifluoromethoxyphenylhydrazone
Carnitine
Cell Respiration
DNA, Mitochondrial
Energy Metabolism
Female
Glutamic Acid
Humans
Intra-Abdominal Fat
Malates
Male
Microscopy, Electron, Transmission
Mitochondria
Obesity, Morbid
Omentum
Oxidative Phosphorylation
Subcutaneous Fat, Abdominal
Succinic Acid
Time Factors
Uncoupling Agents

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1113/jphysiol.2009.184754

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@article{0ad55350d9db447e9559bf9d210606a3,

title = "Mitochondrial respiration in subcutaneous and visceral adipose tissue from patients with morbid obesity",

abstract = "Adipose tissue exerts important endocrine and metabolic functions in health and disease. Yet the bioenergetics of this tissue is not characterized in humans and possible regional differences are not elucidated. Using high resolution respirometry, mitochondrial respiration was quantified in human abdominal subcutaneous and intra-abdominal visceral (omentum majus) adipose tissue from biopsies obtained in 20 obese patients undergoing bariatric surgery. Mitochondrial DNA (mtDNA) and genomic DNA (gDNA) were determined by the PCR technique for estimation of mitochondrial density. Adipose tissue samples were permeabilized and respirometric measurements were performed in duplicate at 37°C. Substrates (glutamate (G) + malate (M) + octanoyl carnitine (O) + succinate (S)) were added sequentially to provide electrons to complex I + II. ADP (D) for state 3 respiration was added after GM. Uncoupled respiration was measured after addition of FCCP. Visceral fat contained more mitochondria per milligram of tissue than subcutaneous fat, but the cells were smaller. Robust, stable oxygen fluxes were found in both tissues, and coupled state 3 (GMOSD) and uncoupled respiration were significantly (P < 0.05) higher in visceral (0.95 ± 0.05 and 1.15 ± 0.06 pmol O2 s-1 mg-1, respectively) compared with subcutaneous (0.76 ± 0.04 and 0.98 ± 0.05 pmol O2 s-1 mg-1, respectively) adipose tissue. Expressed per mtDNA, visceral adipose tissue had significantly (P < 0.05) lower mitochondrial respiration. Substrate control ratios were higher and uncoupling control ratio lower (P < 0.05) in visceral compared with subcutaneous adipose tissue. We conclude that visceral fat is bioenergetically more active and more sensitive to mitochondrial substrate supply than subcutaneous fat. Oxidative phosphorylation has a higher relative activity in visceral compared with subcutaneous adipose tissue.",

keywords = "Adult, Biopsy, Carbonyl Cyanide p-Trifluoromethoxyphenylhydrazone, Carnitine, Cell Respiration, DNA, Mitochondrial, Energy Metabolism, Female, Glutamic Acid, Humans, Intra-Abdominal Fat, Malates, Male, Microscopy, Electron, Transmission, Mitochondria, Obesity, Morbid, Omentum, Oxidative Phosphorylation, Subcutaneous Fat, Abdominal, Succinic Acid, Time Factors, Uncoupling Agents",

author = "Regitze Krauns{\o}e and Boushel, {Robert Christopher} and Hansen, {Christina Neigaard} and Peter Schjerling and Klaus Qvortrup and Mikael St{\o}ckel and Mikines, {K{\'a}ri J} and Flemming Dela",

year = "2010",

month = jun,

doi = "10.1113/jphysiol.2009.184754",

language = "English",

volume = "588",

pages = "2023--2032",

journal = "The Journal of Physiology",

issn = "0022-3751",

publisher = "Wiley-Blackwell",

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TY - JOUR

T1 - Mitochondrial respiration in subcutaneous and visceral adipose tissue from patients with morbid obesity

AU - Kraunsøe, Regitze

AU - Boushel, Robert Christopher

AU - Hansen, Christina Neigaard

AU - Schjerling, Peter

AU - Qvortrup, Klaus

AU - Støckel, Mikael

AU - Mikines, Kári J

AU - Dela, Flemming

PY - 2010/6

Y1 - 2010/6

N2 - Adipose tissue exerts important endocrine and metabolic functions in health and disease. Yet the bioenergetics of this tissue is not characterized in humans and possible regional differences are not elucidated. Using high resolution respirometry, mitochondrial respiration was quantified in human abdominal subcutaneous and intra-abdominal visceral (omentum majus) adipose tissue from biopsies obtained in 20 obese patients undergoing bariatric surgery. Mitochondrial DNA (mtDNA) and genomic DNA (gDNA) were determined by the PCR technique for estimation of mitochondrial density. Adipose tissue samples were permeabilized and respirometric measurements were performed in duplicate at 37°C. Substrates (glutamate (G) + malate (M) + octanoyl carnitine (O) + succinate (S)) were added sequentially to provide electrons to complex I + II. ADP (D) for state 3 respiration was added after GM. Uncoupled respiration was measured after addition of FCCP. Visceral fat contained more mitochondria per milligram of tissue than subcutaneous fat, but the cells were smaller. Robust, stable oxygen fluxes were found in both tissues, and coupled state 3 (GMOSD) and uncoupled respiration were significantly (P < 0.05) higher in visceral (0.95 ± 0.05 and 1.15 ± 0.06 pmol O2 s-1 mg-1, respectively) compared with subcutaneous (0.76 ± 0.04 and 0.98 ± 0.05 pmol O2 s-1 mg-1, respectively) adipose tissue. Expressed per mtDNA, visceral adipose tissue had significantly (P < 0.05) lower mitochondrial respiration. Substrate control ratios were higher and uncoupling control ratio lower (P < 0.05) in visceral compared with subcutaneous adipose tissue. We conclude that visceral fat is bioenergetically more active and more sensitive to mitochondrial substrate supply than subcutaneous fat. Oxidative phosphorylation has a higher relative activity in visceral compared with subcutaneous adipose tissue.

AB - Adipose tissue exerts important endocrine and metabolic functions in health and disease. Yet the bioenergetics of this tissue is not characterized in humans and possible regional differences are not elucidated. Using high resolution respirometry, mitochondrial respiration was quantified in human abdominal subcutaneous and intra-abdominal visceral (omentum majus) adipose tissue from biopsies obtained in 20 obese patients undergoing bariatric surgery. Mitochondrial DNA (mtDNA) and genomic DNA (gDNA) were determined by the PCR technique for estimation of mitochondrial density. Adipose tissue samples were permeabilized and respirometric measurements were performed in duplicate at 37°C. Substrates (glutamate (G) + malate (M) + octanoyl carnitine (O) + succinate (S)) were added sequentially to provide electrons to complex I + II. ADP (D) for state 3 respiration was added after GM. Uncoupled respiration was measured after addition of FCCP. Visceral fat contained more mitochondria per milligram of tissue than subcutaneous fat, but the cells were smaller. Robust, stable oxygen fluxes were found in both tissues, and coupled state 3 (GMOSD) and uncoupled respiration were significantly (P < 0.05) higher in visceral (0.95 ± 0.05 and 1.15 ± 0.06 pmol O2 s-1 mg-1, respectively) compared with subcutaneous (0.76 ± 0.04 and 0.98 ± 0.05 pmol O2 s-1 mg-1, respectively) adipose tissue. Expressed per mtDNA, visceral adipose tissue had significantly (P < 0.05) lower mitochondrial respiration. Substrate control ratios were higher and uncoupling control ratio lower (P < 0.05) in visceral compared with subcutaneous adipose tissue. We conclude that visceral fat is bioenergetically more active and more sensitive to mitochondrial substrate supply than subcutaneous fat. Oxidative phosphorylation has a higher relative activity in visceral compared with subcutaneous adipose tissue.

KW - Adult

KW - Biopsy

KW - Carbonyl Cyanide p-Trifluoromethoxyphenylhydrazone

KW - Carnitine

KW - Cell Respiration

KW - DNA, Mitochondrial

KW - Energy Metabolism

KW - Female

KW - Glutamic Acid

KW - Humans

KW - Intra-Abdominal Fat

KW - Malates

KW - Male

KW - Microscopy, Electron, Transmission

KW - Mitochondria

KW - Obesity, Morbid

KW - Omentum

KW - Oxidative Phosphorylation

KW - Subcutaneous Fat, Abdominal

KW - Succinic Acid

KW - Time Factors

KW - Uncoupling Agents

U2 - 10.1113/jphysiol.2009.184754

DO - 10.1113/jphysiol.2009.184754

M3 - Journal article

C2 - 20421291

SN - 0022-3751

VL - 588

SP - 2023

EP - 2032

JO - The Journal of Physiology

JF - The Journal of Physiology

IS - 12

ER -

Mitochondrial respiration in subcutaneous and visceral adipose tissue from patients with morbid obesity

Abstract

Keywords

UN SDGs

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