Minor Contribution of Endogenous GLP-1 and GLP-2 to Postprandial Lipemia in Obese Men

Niina Matikainen; Elias Björnson; Sanni Söderlund; Christofer Borén; Björn Eliasson; Kirsi H Pietiläinen; Leonie H Bogl; Antti Hakkarainen; Nina Lundbom; Angela Rivellese; Gabriele Riccardi; Jean-Pierre Després; Natalie Alméras; Jens Juul Holst; Carolyn F Deacon; Jan Borén; Marja-Riitta Taskinen

doi:10.1371/journal.pone.0145890

Minor Contribution of Endogenous GLP-1 and GLP-2 to Postprandial Lipemia in Obese Men

Niina Matikainen, Elias Björnson, Sanni Söderlund, Christofer Borén, Björn Eliasson, Kirsi H Pietiläinen, Leonie H Bogl, Antti Hakkarainen, Nina Lundbom, Angela Rivellese, Gabriele Riccardi, Jean-Pierre Després, Natalie Alméras, Jens Juul Holst, Carolyn F Deacon, Jan Borén, Marja-Riitta Taskinen

Endocrinology and Metabolism

13 Citations (Scopus)

Abstract

Context. Glucose and lipids stimulate the gut-hormones glucagon-like peptide (GLP)-1, GLP-2 and glucose-dependent insulinotropic polypeptide (GIP) but the effect of these on human postprandial lipid metabolism is not fully clarified. Objective. To explore the responses of GLP-1, GLP-2 and GIP after a fat-rich meal compared to the same responses after an oral glucose tolerance test (OGTT) and to investigate possible relationships between incretin response and triglyceride-rich lipoprotein (TRL) response to a fat-rich meal. Design. Glucose, insulin, GLP-1, GLP-2 and GIP were measured after an OGTT and after a fat-rich meal in 65 healthy obese (BMI 26.5-40.2 kg/m²) male subjects. Triglycerides (TG), apoB48 and apoB100 in TG-rich lipoproteins (chylomicrons, VLDL₁ and VLDL₂) were measured after the fat-rich meal. Main Outcome Measures. Postprandial responses (area under the curve, AUC) for glucose, insulin, GLP-1, GLP-2, GIP in plasma, and TG, apoB48 and apoB100 in plasma and TG-rich lipoproteins. Results. The GLP-1, GLP-2 and GIP responses after the fat-rich meal and after the OGTT correlated strongly (r = 0.73, p<0.0001; r = 0.46, p<0.001 and r = 0.69, p<0.001, respectively). Glucose and insulin AUCs were lower, but the AUCs for GLP-1, GLP-2 and GIP were significantly higher after the fat-rich meal than after the OGTT. The peak value for all hormones appeared at 120 minutes after the fat-rich meal, compared to 30 minutes after the OGTT. After the fat-rich meal, the AUCs for GLP-1, GLP-2 and GIP correlated significantly with plasma TG- and apoB48 AUCs but the contribution was very modest. Conclusions. In obese males, GLP-1, GLP-2 and GIP responses to a fat-rich meal are greater than following an OGTT. However, the most important explanatory variable for postprandial TG excursion was fasting triglycerides. The contribution of endogenous GLP-1, GLP-2 and GIP to explaining the variance in postprandial TG excursion was minor.

Original language	English
Article number	e0145890
Journal	PLOS ONE
Volume	11
Issue number	1
Pages (from-to)	1-15
Number of pages	15
ISSN	1932-6203
DOIs	https://doi.org/10.1371/journal.pone.0145890
Publication status	Published - 11 Jan 2016

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Matikainen, N., Björnson, E., Söderlund, S., Borén, C., Eliasson, B., Pietiläinen, K. H., Bogl, L. H., Hakkarainen, A., Lundbom, N., Rivellese, A., Riccardi, G., Després, J-P., Alméras, N., Holst, J. J., Deacon, C. F., Borén, J., & Taskinen, M-R. (2016). Minor Contribution of Endogenous GLP-1 and GLP-2 to Postprandial Lipemia in Obese Men. PLOS ONE, 11(1), 1-15. [e0145890]. https://doi.org/10.1371/journal.pone.0145890

Matikainen, N, Björnson, E, Söderlund, S, Borén, C, Eliasson, B, Pietiläinen, KH, Bogl, LH, Hakkarainen, A, Lundbom, N, Rivellese, A, Riccardi, G, Després, J-P, Alméras, N, Holst, JJ , Deacon, CF, Borén, J & Taskinen, M-R 2016, 'Minor Contribution of Endogenous GLP-1 and GLP-2 to Postprandial Lipemia in Obese Men', PLOS ONE, vol. 11, no. 1, e0145890, pp. 1-15. https://doi.org/10.1371/journal.pone.0145890

@article{f4068775cace465cb825cdc935c2c843,

title = "Minor Contribution of Endogenous GLP-1 and GLP-2 to Postprandial Lipemia in Obese Men",

abstract = "Context. Glucose and lipids stimulate the gut-hormones glucagon-like peptide (GLP)-1, GLP-2 and glucose-dependent insulinotropic polypeptide (GIP) but the effect of these on human postprandial lipid metabolism is not fully clarified. Objective. To explore the responses of GLP-1, GLP-2 and GIP after a fat-rich meal compared to the same responses after an oral glucose tolerance test (OGTT) and to investigate possible relationships between incretin response and triglyceride-rich lipoprotein (TRL) response to a fat-rich meal. Design. Glucose, insulin, GLP-1, GLP-2 and GIP were measured after an OGTT and after a fat-rich meal in 65 healthy obese (BMI 26.5-40.2 kg/m2) male subjects. Triglycerides (TG), apoB48 and apoB100 in TG-rich lipoproteins (chylomicrons, VLDL1 and VLDL2) were measured after the fat-rich meal. Main Outcome Measures. Postprandial responses (area under the curve, AUC) for glucose, insulin, GLP-1, GLP-2, GIP in plasma, and TG, apoB48 and apoB100 in plasma and TG-rich lipoproteins. Results. The GLP-1, GLP-2 and GIP responses after the fat-rich meal and after the OGTT correlated strongly (r = 0.73, p<0.0001; r = 0.46, p<0.001 and r = 0.69, p<0.001, respectively). Glucose and insulin AUCs were lower, but the AUCs for GLP-1, GLP-2 and GIP were significantly higher after the fat-rich meal than after the OGTT. The peak value for all hormones appeared at 120 minutes after the fat-rich meal, compared to 30 minutes after the OGTT. After the fat-rich meal, the AUCs for GLP-1, GLP-2 and GIP correlated significantly with plasma TG- and apoB48 AUCs but the contribution was very modest. Conclusions. In obese males, GLP-1, GLP-2 and GIP responses to a fat-rich meal are greater than following an OGTT. However, the most important explanatory variable for postprandial TG excursion was fasting triglycerides. The contribution of endogenous GLP-1, GLP-2 and GIP to explaining the variance in postprandial TG excursion was minor.",

author = "Niina Matikainen and Elias Bj{\"o}rnson and Sanni S{\"o}derlund and Christofer Bor{\'e}n and Bj{\"o}rn Eliasson and Pietil{\"a}inen, {Kirsi H} and Bogl, {Leonie H} and Antti Hakkarainen and Nina Lundbom and Angela Rivellese and Gabriele Riccardi and Jean-Pierre Despr{\'e}s and Natalie Alm{\'e}ras and Holst, {Jens Juul} and Deacon, {Carolyn F} and Jan Bor{\'e}n and Marja-Riitta Taskinen",

year = "2016",

month = jan,

day = "11",

doi = "10.1371/journal.pone.0145890",

language = "English",

volume = "11",

pages = "1--15",

journal = "PLoS Computational Biology",

issn = "1932-6203",

publisher = "Public Library of Science",

number = "1",

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TY - JOUR

T1 - Minor Contribution of Endogenous GLP-1 and GLP-2 to Postprandial Lipemia in Obese Men

AU - Matikainen, Niina

AU - Björnson, Elias

AU - Söderlund, Sanni

AU - Borén, Christofer

AU - Eliasson, Björn

AU - Pietiläinen, Kirsi H

AU - Bogl, Leonie H

AU - Hakkarainen, Antti

AU - Lundbom, Nina

AU - Rivellese, Angela

AU - Riccardi, Gabriele

AU - Després, Jean-Pierre

AU - Alméras, Natalie

AU - Holst, Jens Juul

AU - Deacon, Carolyn F

AU - Borén, Jan

AU - Taskinen, Marja-Riitta

PY - 2016/1/11

Y1 - 2016/1/11

N2 - Context. Glucose and lipids stimulate the gut-hormones glucagon-like peptide (GLP)-1, GLP-2 and glucose-dependent insulinotropic polypeptide (GIP) but the effect of these on human postprandial lipid metabolism is not fully clarified. Objective. To explore the responses of GLP-1, GLP-2 and GIP after a fat-rich meal compared to the same responses after an oral glucose tolerance test (OGTT) and to investigate possible relationships between incretin response and triglyceride-rich lipoprotein (TRL) response to a fat-rich meal. Design. Glucose, insulin, GLP-1, GLP-2 and GIP were measured after an OGTT and after a fat-rich meal in 65 healthy obese (BMI 26.5-40.2 kg/m2) male subjects. Triglycerides (TG), apoB48 and apoB100 in TG-rich lipoproteins (chylomicrons, VLDL1 and VLDL2) were measured after the fat-rich meal. Main Outcome Measures. Postprandial responses (area under the curve, AUC) for glucose, insulin, GLP-1, GLP-2, GIP in plasma, and TG, apoB48 and apoB100 in plasma and TG-rich lipoproteins. Results. The GLP-1, GLP-2 and GIP responses after the fat-rich meal and after the OGTT correlated strongly (r = 0.73, p<0.0001; r = 0.46, p<0.001 and r = 0.69, p<0.001, respectively). Glucose and insulin AUCs were lower, but the AUCs for GLP-1, GLP-2 and GIP were significantly higher after the fat-rich meal than after the OGTT. The peak value for all hormones appeared at 120 minutes after the fat-rich meal, compared to 30 minutes after the OGTT. After the fat-rich meal, the AUCs for GLP-1, GLP-2 and GIP correlated significantly with plasma TG- and apoB48 AUCs but the contribution was very modest. Conclusions. In obese males, GLP-1, GLP-2 and GIP responses to a fat-rich meal are greater than following an OGTT. However, the most important explanatory variable for postprandial TG excursion was fasting triglycerides. The contribution of endogenous GLP-1, GLP-2 and GIP to explaining the variance in postprandial TG excursion was minor.

AB - Context. Glucose and lipids stimulate the gut-hormones glucagon-like peptide (GLP)-1, GLP-2 and glucose-dependent insulinotropic polypeptide (GIP) but the effect of these on human postprandial lipid metabolism is not fully clarified. Objective. To explore the responses of GLP-1, GLP-2 and GIP after a fat-rich meal compared to the same responses after an oral glucose tolerance test (OGTT) and to investigate possible relationships between incretin response and triglyceride-rich lipoprotein (TRL) response to a fat-rich meal. Design. Glucose, insulin, GLP-1, GLP-2 and GIP were measured after an OGTT and after a fat-rich meal in 65 healthy obese (BMI 26.5-40.2 kg/m2) male subjects. Triglycerides (TG), apoB48 and apoB100 in TG-rich lipoproteins (chylomicrons, VLDL1 and VLDL2) were measured after the fat-rich meal. Main Outcome Measures. Postprandial responses (area under the curve, AUC) for glucose, insulin, GLP-1, GLP-2, GIP in plasma, and TG, apoB48 and apoB100 in plasma and TG-rich lipoproteins. Results. The GLP-1, GLP-2 and GIP responses after the fat-rich meal and after the OGTT correlated strongly (r = 0.73, p<0.0001; r = 0.46, p<0.001 and r = 0.69, p<0.001, respectively). Glucose and insulin AUCs were lower, but the AUCs for GLP-1, GLP-2 and GIP were significantly higher after the fat-rich meal than after the OGTT. The peak value for all hormones appeared at 120 minutes after the fat-rich meal, compared to 30 minutes after the OGTT. After the fat-rich meal, the AUCs for GLP-1, GLP-2 and GIP correlated significantly with plasma TG- and apoB48 AUCs but the contribution was very modest. Conclusions. In obese males, GLP-1, GLP-2 and GIP responses to a fat-rich meal are greater than following an OGTT. However, the most important explanatory variable for postprandial TG excursion was fasting triglycerides. The contribution of endogenous GLP-1, GLP-2 and GIP to explaining the variance in postprandial TG excursion was minor.

U2 - 10.1371/journal.pone.0145890

DO - 10.1371/journal.pone.0145890

M3 - Journal article

C2 - 26752550

SN - 1932-6203

VL - 11

SP - 1

EP - 15

JO - PLoS Computational Biology

JF - PLoS Computational Biology

IS - 1

M1 - e0145890

ER -

Minor Contribution of Endogenous GLP-1 and GLP-2 to Postprandial Lipemia in Obese Men

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