Adipose tissue dysfunction in obesity. Gijs Goossens, PhD
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1 Adipose tissue dysfunction in obesity -The role of adipose tissue oxygenation - Gijs Goossens, PhD NUTRIM School of Nutrition and Translational Research in Metabolism Maastricht University Medical Centre + 2 Oct 2017 EASO s NIU Autumn School, Mallorca
2 Content of lecture Insulin resistance: a key factor in the pathophysiology of type 2 diabetes and cardiovascular diseases Fat mass, body fat distribution and adipose tissue function determine cardiometabolic health Adipose tissue oxygenation in obesity: a key player in adipose tissue dysfunction and insulin resistance? A gut microbiome adipose tissue axis?
3 Obesity: a major risk factor for chronic diseases Prevalence Overweight: >50% Obesity: 12% OBESITY Cardiovascular disease Type 2 diabetes Liver steatosis Cancer
4 Natural history of type 2 diabetes mellitus insulin resistance blood glucose β-cell dysfunction insulin secretion Normal Impaired glucose metabolism Type 2 diabetes Time (yrs) Adapted from Henry R., Am J Med, 1998
5 Natural history of type 2 diabetes mellitus insulin resistance blood glucose β-cell dysfunction insulin secretion Normal Impaired glucose metabolism Type 2 diabetes Time (yrs) Adapted from Henry R., Am J Med, 1998
6 Natural history of type 2 diabetes mellitus insulin resistance blood glucose β-cell dysfunction insulin secretion Normal Impaired glucose metabolism Type 2 diabetes Time (yrs) Adapted from Henry R., Am J Med, 1998
7 Natural history of type 2 diabetes mellitus Window of opportunity insulin resistance blood glucose insulin secretion β-cell dysfunction Normal Impaired glucose metabolism Type 2 diabetes Time (yrs) Adapted from Henry R., Am J Med, 1998
8 Body composition and metabolic health vs. similar BMI Body fat percentage is important metabolically unhealthy metabolically healthy
9 Fat mass is not necessarily related to insulin resistance at an individual level Weight gain insulin sensitivity Weight loss insulin sensitivity Healthy obese insulin sensitivity Liposuction insulin sensitivity TZD treatment insulin sensitivity despite BW gain Lipodystrophy severe insulin resistance
10 Body composition and metabolic health similar BMI Body fat percentage is important metabolically unhealthy metabolically healthy similar BMI similar fat% Body fat distribution is important metabolically unhealthy metabolically healthy similar BMI similar fat% similar waist Adipose tissue function is highly important metabolically unhealthy metabolically healthy
11 Healthy adipose tissue buffers the daily influx of dietary fatty acids HEALTHY ADIPOSE TISSUE dietary fat lipids of Human Biology Goossens GH, Physiol Behav, 2008
12 OBESITY excess adipose tissue Lipid overflow in obesity TAG lipid accumulation fatty acids ATGL HSL glycerol FFA insulin resistance LPL dietary fat lipids LIPODYSTROPHY adipose tissue deficiency impaired insulin secretion Goossens GH, Physiol Behav, 2008
13 Adipose tissue is an endocrine organ Lipid metabolism Insulin sensitivity Glucose homeostasis Appetite Energy balance Inflammation Immunity Angiogenesis Vascular homeostasis Blood pressure regulation Goossens et al. 2008, 2003; Trayhurn, 2013
14 The endocrine function of adipose tissue is disturbed in obesity and type 2 diabetes Lipid metabolism Insulin sensitivity Glucose homeostasis Appetite Energy balance Inflammation Immunity Angiogenesis Vascular homeostasis Blood pressure regulation Goossens et al. 2008, 2003; Trayhurn, 2013
15 Dynamic changes in immune cell populations during the development of obesity M2 macrophages T-regs Eosinphils M1 macrophages Mast cells Th1 cells Neutrophils Dendritic cells NK cells Rosen E, Cell, 2014
16 Fat cell enlargement in obesity is related to insulin resistance and type 2 diabetes Lean Obese Goossens et al., Circulation, 2011 Abdominal sc adipocyte enlargement is an independent marker of insulin resistance and predicts type 2 diabetes Goossens GH et al. 2011; Lundgren et al. 2007; Weyer et al. 2010
17 Obesity-induced alterations in adipose tissue function are linked to insulin resistance Normal adipocytes Excess energy intake Hypertrophic adipocytes Impaired lipid metabolism Altered adipokine secretion Immune cell infiltration Inflammation Insulin resistance Preadipocyte recruitment Preadipocytes of Human Biology Goossens GH, Front Endocrinol, 2015
18 Obesity-induced alterations in adipose tissue function are linked to insulin resistance Normal adipocytes Excess energy intake Hypertrophic adipocytes Impaired lipid metabolism Altered adipokine secretion Immune cell infiltration Inflammation Insulin resistance Preadipocyte recruitment Preadipocytes Liver Muscle Lipid accumulation Inflammation Insulin resistance Lipid accumulation Insulin resistance Lipid spill-over Systemic inflammation Goossens GH, Front Endocrinol, 2015
19 Adipose tissue function and body fat distribution determine cardiometabolic health METABOLICALLY HEALTHY OBESE METABOLICALLY UNHEALTHY OBESE Goossens GH, Obes Facts, 2017
20 Fat mass is not necessarily related to insulin resistance at an individual level Weight gain insulin sensitivity Weight loss insulin sensitivity Healthy obese insulin sensitivity Liposuction insulin sensitivity TZD treatment insulin sensitivity despite BW gain Lipodystrophy severe insulin resistance Fat cell size determines insulin sensitivity fat cell size ectopic fat storage inflammation insulin sensitivity
21 What is the trigger that instigates adipose tissue dysfunction in obesity?
22 Hypoxia hypothesis Normoxia Hypoxia Relative oxygen deficit Based on Trayhurn & Wood, Br J Nutr, 2004
23 Adipose tissue hypoxia in ob/ob mice po 2 in adipose tissue Hypoxia genes in fat Hypoxia probe Western blot against pimonidazole hydrochloride Immunostaining Ye et al., Am J Physiol, 2007
24 Miniaturized optochemical measurement system for continuous AT po 2 monitoring flow-through-cell Cover O 2 sensor Flow-through-cell microdialysis probe - Measurement range: mmhg - Temperature range: C - Accuracy: ~1 mmhg - Sample media: water, gas phase Čajlaković M, Bizzarri A, Goossens GH et al. Advances in Chemical Sensors, 2012
25 Adipose tissue oxygenation is increased in human obesity, despite lower ATBF 100 P=0.005 Fasting AT po 2 (mmhg) % O 2 3.2% O 2 0 Lean Obese 44.7±5.8 vs. 67.4±3.7 mmhg Goossens GH et al., Circulation, 2011
26 What is the underlying mechanism for increased abdominal sc AT po 2 in human obesity?
27 Determinants and putative effects of AT po 2 Goossens GH, Curr Opin Clin Nutr Metab Care, 2012
28 Acute exposure to extremely low and high oxygen tension evokes AT inflammation 1% 3% 11% 95% Adipose tissue inflammation Human physiological range? Adipose tissue oxygen tension (%) Goossens GH, Front Endocrinol, 2015
29 High physiologically O 2 tension may induce inflammation in human adipocytes 1% 3% 11% 95% Adipose tissue inflammation Human physiological range? Adipose tissue oxygen tension (%) Goossens GH, Front Endocrinol, 2015
30 AT po 2 was positively associated with inflammatory cell markers in human AT Chemoattraction Macrophage infiltration Inflammation 4 r=0.571, P= r=0.525, P= r=0.582, P=0.023 CCL5 mrna (a.u.) CD11b mrna (a.u.) TNFα mrna (a.u.) Fasting AT po2 (mmhg) Fasting AT po2 (mmhg) Fasting AT po2 (mmhg) lean (n=6) obese (n=9) of Human Biology Goossens GH et al., Circulation, 2011
31 AT po 2 was inversely associated with whole-body insulin sensitivity in humans Glucose infusion rate (µmol kg bw -1 min -1 ) 60 r=-0.609, P=0.012 lean (n=7) obese (n=9) Fasting AT po 2 (mmhg) of Human Biology Goossens GH et al., Circulation, 2011
32 Roel Vink What is the effect of diet-induced weight loss on adipose tissue oxygenation?
33 Diet-induced weight loss in humans 15 overweight/obese healthy subjects (18-65 yrs; kg/m 2 ) Dietary intervention 5-week VLCD (500 kcal/d) to achieve >8% weight loss (Modifast), followed by a 4-week weight-maintenance diet Body weight (-10.4%, P<0.001) Body fat % (-6.0%, P<0.001) Fat cell size (-6.2%, P=0.001) Vink R,..., Goossens GH, Int J Obes, 2017 (doi /ijo
34 Diet-induced weight loss decreased AT po 2 and improved insulin sensitivity in humans VLCD-induced weight loss decreased AT po 2 by ~20% (P=0.002), which was accompanied by improved insulin sensitivity (P<0.001) Vink RG et al., Int J Obes, 2017
35 Is adipose tissue oxygenation related to obesity and/or insulin sensitivity?
36 Adipose tissue oxygenation is higher in insulin resistant individuals Similar age, BMI (obese) and body fat percentage (obese) Goossens GH et al., submitted
37 Adipose tissue oxygenation is a major determinant of insulin sensitivity in humans Adipose tissue oxygenation is associated with insulin resistance, independent of age, sex and body fat percentage (standardized β = 0.494; p = 0.005). Goossens GH et al., submitted
38 Is there a difference in adipose tissue oxygenation between upper and lower adipose tissue depots? Max Vogel
39 Oxygen tension is higher in abdominal as compared to femoral sc adipose tissue Adipose tissue oxygen tension (mmhg) Abdominal Femoral Adipose tissue oxygen tension (mmhg) 80 * Abdominal Femoral Adipose tissue blood flow was comparable between depots Vogel M,, Goossens GH, submitted
40 Mechanistic experiments using human adipose tissue-derived stem cells Proliferation Differentiation D0 D7 D21 5% O 2 vs 10% O 2 vs 21% O 2 Gene expression, adipokine secretion, glucose uptake and mitochondrial oxygen consumption in abdominal and femoral adipocytes
41 Low physiological O 2 tension decreased inflammatory markers in human adipocytes abdominal femoral Vogel M,, Goossens GH, submitted
42 Mild hypoxia exposure: a novel treatment avenue to improve metabolic health? PARTICIPANTS - Obese insulin resistant men INTERVENTION - Exposure to mild intermittent hypoxia (3 x 2h per day; 15% or 21% O 2 ) for 7 days Rens van Meijel Max Vogel MEASUREMENTS - Systemic oxygen saturation - Adipose tissue and skeletal muscle oxygenation - Hepatic and peripheral insulin sensitivity - Energy expenditure and substrate metabolism - Ex vivo skeletal muscle mitochondrial function - Mechanistic cell culture experiments
43 Take home messages Body fat distribution and adipose tissue dysfunction are major determinants of cardiometabolic health in humans Adipose tissue hypoxia is present in rodent models of obesity, but adipose tissue oxygenation seems to be increased in human obesity and related to insulin resistance Adipose tissue oxygenation determines adipocyte functionality Prolonged exposure to low physiological AT po 2 seems to improve human adipocyte function Adipose tissue oxygenation may be a promising target to improve cardiometabolic health in humans
44 A gut microbiome - adipose tissue axis? Dorien Reijnders of Human Biology Reijnders D & Goossens GH et al., Cell Metab, 2016
45 A gut microbiome - adipose tissue axis? Emanuel Canfora of Human Biology Canfora E et al., Nat Rev Endocrinol, 2017
46 Maastricht University Medical Centre +, Maastricht, The Netherlands Prof. dr. E.E. Blaak Dr. J. Jocken Dr. D. Reijnders M. Vogel R. van Meijel Y. Essers N. Houbers Dr. R.G. Vink Prof. M. van Baak Prof. E. Mariman Dr. J.P. Cleutjens Joanneum Research Institute, Weiz, Austria Dr. M. Čajlaković Acknowledgments INSERM U872, UPMC University of Paris; ICAN, Pitié-Salpêtrière Hospital, Paris, France Prof. dr. K. Clément Innovative Pilot Research Grant (2008) EFSD Clinical Research Grant (2013) Senior Fellowship (2015) (Dr. G.H. Goossens) (Dr. G.H. Goossens)
47 Adipose tissue fatty acid trafficking is decreased in obesity AT absolute extraction of TG (nmol.100g -1.min -1 ) M1 M2 M3 lean obese AT transcapillary flux (nmol.100g -1.min -1 ) M1 M2 M3 lean obese % lean obese 13% 6% 35% 25% 47% 18% Removal of TAG from blood across adipose tissue Net movement of fatty acids across adipose tissue Relative quantity of meal fat stored in adipose tissue Impaired adipose tissue storage of dietary fat in obese individuals of Human Biology McQuaid et al, Diabetes, 2011
48 Mitochondria-related transcriptional signature is downregulated in adipocytes in obesity Affymetrix MZ twin pairs discordant for BMI qrt-pcr mtdna transcript levels OXPHOS protein content of Human Biology Heinonen et al., Diabetologia, 2017
49 Low physiological O 2 tension increased glucose uptake in human femoral adipocytes Glucose uptake Fold change (DPM) Abdominal Femoral * 0.0 INS - INS - INS - INS - INS - INS - 21% O 2 10% O 2 5% O 2 Vogel M,, Goossens GH, submitted
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