High-fat diet results in postprandial insulin resistance that involves parasympathetic dysfunction

Ricardo A Afonso; W. Wayne Lautt; Joshua Schafer; Dallas J. Legare; António G Oliveira; M Paula  Macedo

doi:10.1017/S0007114510002400

High-fat diet results in postprandial insulin resistance that involves parasympathetic dysfunction

Ricardo A Afonso, W. Wayne Lautt, Joshua Schafer, Dallas J. Legare, António G Oliveira, M Paula Macedo

NOVA Medical School|Faculdade de Ciências Médicas (NMS|FCM)

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Abstract

Different diets have distinct impacts on glucose homoeostasis, for which insulin sensitivity (IS) after a meal (postprandial IS) is highly relevant. Postprandial IS depends upon hepatic parasympathetic activation and glutathione content elevation. We tested the hypothesis that postprandial IS is compromised in high-fat diet (HFD)-induced obesity. Sprague-Dawley rats were fed a standard diet (STD, n 10), 1-week HFD (n 9) or 4-week HFD (n 8). IS was tested in postprandial state using the rapid IS test (RIST) before and after the blockade of the parasympathetic nerves (atropine, 1 mg/kg); parasympathetic-dependent IS was obtained from the difference between control and post-atropine RIST. Fasting IS was also assessed in the STD-fed rats (n 4) and 4-week HFD-fed rats (n 3) using the RIST. Whole-body fat and regional fat pads were heavier in the 1-week HFD-fed rats (79.8 (SE 7.9) and 23.7 (SE 1.0) g, respectively) or 4-week HFD-fed rats (106.5 (SE 6.1) and 30.1 (SE 1.4) g, respectively) than in the STD-fed rats (32.5 (SE 3.7) and 13.7 (SE 1.0) g, respectively; P < 0.001). Fasted-state IS was similar between the groups studied. Postprandial IS was higher in the STD-fed rats (185.8 (SE 5.6) mg glucose/kg body weight (bw)) than in both the 1-week HFD-fed rats (108.8 (SE 2.9) mg glucose/kg bw; P < 0.001) and 4-week HFD-fed rats (69.3 (SE 2.6) mg glucose/kg bw; P < 0.001). Parasympathetic-dependent IS was impaired in both HFD-fed groups (STD, 108.9 (SE 3.9) mg glucose/kg bw; 1-week HFD, 38.6 (SE 4.2) mg glucose/kg bw; 4-week HFD, 5.4 (SE 1.7) mg glucose/kg bw; P < 0.001). Total (postprandial) and parasympathetic-dependent IS correlated negatively with whole-body fat (R-2 0.81 and 0.87) and regional adiposity (R-2 0.85 and 0.79). In conclusion, fat accumulation induced by HFD is associated with postprandial insulin resistance, but not with fasting insulin resistance. HFD-associated postprandial insulin resistance is largely mediated by impairment of parasympathetic-dependent insulin action, which correlates with adiposity. British Journal of Nutrition

Original language	Unknown
Pages (from-to)	1450-1459
Journal	British Journal Of Nutrition
Volume	104
Issue number	10
DOIs	https://doi.org/10.1017/S0007114510002400
Publication status	Published - 1 Jan 2010

Keywords

Obesity
High-fat diet
Insulin resistance
Parasympathetic nerves

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Cite this

@article{b0f4e48176404db7a607a026649b54a1,

title = "High-fat diet results in postprandial insulin resistance that involves parasympathetic dysfunction",

abstract = "Different diets have distinct impacts on glucose homoeostasis, for which insulin sensitivity (IS) after a meal (postprandial IS) is highly relevant. Postprandial IS depends upon hepatic parasympathetic activation and glutathione content elevation. We tested the hypothesis that postprandial IS is compromised in high-fat diet (HFD)-induced obesity. Sprague-Dawley rats were fed a standard diet (STD, n 10), 1-week HFD (n 9) or 4-week HFD (n 8). IS was tested in postprandial state using the rapid IS test (RIST) before and after the blockade of the parasympathetic nerves (atropine, 1 mg/kg); parasympathetic-dependent IS was obtained from the difference between control and post-atropine RIST. Fasting IS was also assessed in the STD-fed rats (n 4) and 4-week HFD-fed rats (n 3) using the RIST. Whole-body fat and regional fat pads were heavier in the 1-week HFD-fed rats (79.8 (SE 7.9) and 23.7 (SE 1.0) g, respectively) or 4-week HFD-fed rats (106.5 (SE 6.1) and 30.1 (SE 1.4) g, respectively) than in the STD-fed rats (32.5 (SE 3.7) and 13.7 (SE 1.0) g, respectively; P < 0.001). Fasted-state IS was similar between the groups studied. Postprandial IS was higher in the STD-fed rats (185.8 (SE 5.6) mg glucose/kg body weight (bw)) than in both the 1-week HFD-fed rats (108.8 (SE 2.9) mg glucose/kg bw; P < 0.001) and 4-week HFD-fed rats (69.3 (SE 2.6) mg glucose/kg bw; P < 0.001). Parasympathetic-dependent IS was impaired in both HFD-fed groups (STD, 108.9 (SE 3.9) mg glucose/kg bw; 1-week HFD, 38.6 (SE 4.2) mg glucose/kg bw; 4-week HFD, 5.4 (SE 1.7) mg glucose/kg bw; P < 0.001). Total (postprandial) and parasympathetic-dependent IS correlated negatively with whole-body fat (R-2 0.81 and 0.87) and regional adiposity (R-2 0.85 and 0.79). In conclusion, fat accumulation induced by HFD is associated with postprandial insulin resistance, but not with fasting insulin resistance. HFD-associated postprandial insulin resistance is largely mediated by impairment of parasympathetic-dependent insulin action, which correlates with adiposity. British Journal of Nutrition",

keywords = "Parasympathetic, nitric-oxide, visceral, adiposity, postmeal, adipose-tissue, obese, nerves, skeletal-muscle, white, blockade, oxidative, High-fat, diet, zucker, Obesity, stress, glucose, rat, test, Insulin, rist, resistance, nervous-system, synthase, sensitivity, Obesity, High-fat diet, Insulin resistance, Parasympathetic nerves",

author = "Afonso, {Ricardo A} and Lautt, {W. Wayne} and Joshua Schafer and Legare, {Dallas J.} and Oliveira, {Ant{\'o}nio G} and Macedo, {M Paula}",

note = "Funding information: info:eu-repo/grantAgreement/FCT/POCI/56716/PT# We are indebted to Dr Zhi Ming for sharing technical expertise and Gerald Nolette from the Central Animal Care Services of the University of Manitoba for animal care assistance. The present work was supported by the Portuguese Foundation for Science and Technology (FCT, grant POCI/ SAU-OBS/56 716/2004), the Portuguese Society of Endocrinology, Diabetes and Metabolism and the Canadian Diabetes Association and Canadian Institutes of Health Research (operating grants). M. P. M. and W. W. L. were involved in the conceptual work; R. A. A. was involved in all aspects of the work presented; D. J. L. and J. S. conducted insulin and GSH quantifications; A. G. O. was involved in data analysis. There are no conflicts of interests to report.",

year = "2010",

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doi = "10.1017/S0007114510002400",

language = "Unknown",

volume = "104",

pages = "1450--1459",

journal = "British Journal Of Nutrition",

issn = "0007-1145",

publisher = "Cambridge University Press",

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TY - JOUR

T1 - High-fat diet results in postprandial insulin resistance that involves parasympathetic dysfunction

AU - Afonso, Ricardo A

AU - Lautt, W. Wayne

AU - Schafer, Joshua

AU - Legare, Dallas J.

AU - Oliveira, António G

AU - Macedo, M Paula

N1 - Funding information: info:eu-repo/grantAgreement/FCT/POCI/56716/PT# We are indebted to Dr Zhi Ming for sharing technical expertise and Gerald Nolette from the Central Animal Care Services of the University of Manitoba for animal care assistance. The present work was supported by the Portuguese Foundation for Science and Technology (FCT, grant POCI/ SAU-OBS/56 716/2004), the Portuguese Society of Endocrinology, Diabetes and Metabolism and the Canadian Diabetes Association and Canadian Institutes of Health Research (operating grants). M. P. M. and W. W. L. were involved in the conceptual work; R. A. A. was involved in all aspects of the work presented; D. J. L. and J. S. conducted insulin and GSH quantifications; A. G. O. was involved in data analysis. There are no conflicts of interests to report.

PY - 2010/1/1

Y1 - 2010/1/1

N2 - Different diets have distinct impacts on glucose homoeostasis, for which insulin sensitivity (IS) after a meal (postprandial IS) is highly relevant. Postprandial IS depends upon hepatic parasympathetic activation and glutathione content elevation. We tested the hypothesis that postprandial IS is compromised in high-fat diet (HFD)-induced obesity. Sprague-Dawley rats were fed a standard diet (STD, n 10), 1-week HFD (n 9) or 4-week HFD (n 8). IS was tested in postprandial state using the rapid IS test (RIST) before and after the blockade of the parasympathetic nerves (atropine, 1 mg/kg); parasympathetic-dependent IS was obtained from the difference between control and post-atropine RIST. Fasting IS was also assessed in the STD-fed rats (n 4) and 4-week HFD-fed rats (n 3) using the RIST. Whole-body fat and regional fat pads were heavier in the 1-week HFD-fed rats (79.8 (SE 7.9) and 23.7 (SE 1.0) g, respectively) or 4-week HFD-fed rats (106.5 (SE 6.1) and 30.1 (SE 1.4) g, respectively) than in the STD-fed rats (32.5 (SE 3.7) and 13.7 (SE 1.0) g, respectively; P < 0.001). Fasted-state IS was similar between the groups studied. Postprandial IS was higher in the STD-fed rats (185.8 (SE 5.6) mg glucose/kg body weight (bw)) than in both the 1-week HFD-fed rats (108.8 (SE 2.9) mg glucose/kg bw; P < 0.001) and 4-week HFD-fed rats (69.3 (SE 2.6) mg glucose/kg bw; P < 0.001). Parasympathetic-dependent IS was impaired in both HFD-fed groups (STD, 108.9 (SE 3.9) mg glucose/kg bw; 1-week HFD, 38.6 (SE 4.2) mg glucose/kg bw; 4-week HFD, 5.4 (SE 1.7) mg glucose/kg bw; P < 0.001). Total (postprandial) and parasympathetic-dependent IS correlated negatively with whole-body fat (R-2 0.81 and 0.87) and regional adiposity (R-2 0.85 and 0.79). In conclusion, fat accumulation induced by HFD is associated with postprandial insulin resistance, but not with fasting insulin resistance. HFD-associated postprandial insulin resistance is largely mediated by impairment of parasympathetic-dependent insulin action, which correlates with adiposity. British Journal of Nutrition

AB - Different diets have distinct impacts on glucose homoeostasis, for which insulin sensitivity (IS) after a meal (postprandial IS) is highly relevant. Postprandial IS depends upon hepatic parasympathetic activation and glutathione content elevation. We tested the hypothesis that postprandial IS is compromised in high-fat diet (HFD)-induced obesity. Sprague-Dawley rats were fed a standard diet (STD, n 10), 1-week HFD (n 9) or 4-week HFD (n 8). IS was tested in postprandial state using the rapid IS test (RIST) before and after the blockade of the parasympathetic nerves (atropine, 1 mg/kg); parasympathetic-dependent IS was obtained from the difference between control and post-atropine RIST. Fasting IS was also assessed in the STD-fed rats (n 4) and 4-week HFD-fed rats (n 3) using the RIST. Whole-body fat and regional fat pads were heavier in the 1-week HFD-fed rats (79.8 (SE 7.9) and 23.7 (SE 1.0) g, respectively) or 4-week HFD-fed rats (106.5 (SE 6.1) and 30.1 (SE 1.4) g, respectively) than in the STD-fed rats (32.5 (SE 3.7) and 13.7 (SE 1.0) g, respectively; P < 0.001). Fasted-state IS was similar between the groups studied. Postprandial IS was higher in the STD-fed rats (185.8 (SE 5.6) mg glucose/kg body weight (bw)) than in both the 1-week HFD-fed rats (108.8 (SE 2.9) mg glucose/kg bw; P < 0.001) and 4-week HFD-fed rats (69.3 (SE 2.6) mg glucose/kg bw; P < 0.001). Parasympathetic-dependent IS was impaired in both HFD-fed groups (STD, 108.9 (SE 3.9) mg glucose/kg bw; 1-week HFD, 38.6 (SE 4.2) mg glucose/kg bw; 4-week HFD, 5.4 (SE 1.7) mg glucose/kg bw; P < 0.001). Total (postprandial) and parasympathetic-dependent IS correlated negatively with whole-body fat (R-2 0.81 and 0.87) and regional adiposity (R-2 0.85 and 0.79). In conclusion, fat accumulation induced by HFD is associated with postprandial insulin resistance, but not with fasting insulin resistance. HFD-associated postprandial insulin resistance is largely mediated by impairment of parasympathetic-dependent insulin action, which correlates with adiposity. British Journal of Nutrition

KW - Parasympathetic

KW - nitric-oxide

KW - visceral

KW - adiposity

KW - postmeal

KW - adipose-tissue

KW - obese

KW - nerves

KW - skeletal-muscle

KW - white

KW - blockade

KW - oxidative

KW - High-fat

KW - diet

KW - zucker

KW - Obesity

KW - stress

KW - glucose

KW - rat

KW - test

KW - Insulin

KW - rist

KW - resistance

KW - nervous-system

KW - synthase

KW - sensitivity

KW - Obesity

KW - High-fat diet

KW - Insulin resistance

KW - Parasympathetic nerves

U2 - 10.1017/S0007114510002400

DO - 10.1017/S0007114510002400

M3 - Article

C2 - 20594392

SN - 0007-1145

VL - 104

SP - 1450

EP - 1459

JO - British Journal Of Nutrition

JF - British Journal Of Nutrition

IS - 10

ER -