Sucrose counteracts the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice

Tao Ma; Bjørn Liaset; Qin Hao; Rasmus Koefoed Petersen; Even Fjære; Ha Thi Ngo; Haldis Haukås Lillefosse; Stine Ringholm Jørgensen; Si Brask Sonne; Jonas Thue Treebak; Henriette Pilegaard; Livar Frøyland; Karsten Kristiansen; Lise Madsen

doi:10.1371/journal.pone.0021647

Sucrose counteracts the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice

Tao Ma, Bjørn Liaset, Qin Hao, Rasmus Koefoed Petersen, Even Fjære, Ha Thi Ngo, Haldis Haukås Lillefosse, Stine Ringholm Jørgensen, Si Brask Sonne, Jonas Thue Treebak, Henriette Pilegaard, Livar Frøyland, Karsten Kristiansen, Lise Madsen

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Abstract

Background: Polyunsaturated n-3 fatty acids (n-3 PUFAs) are reported to protect against high fat diet-induced obesity and inflammation in adipose tissue. Here we aimed to investigate if the amount of sucrose in the background diet influences the ability of n-3 PUFAs to protect against diet-induced obesity, adipose tissue inflammation and glucose intolerance. Methodology/Principal Findings: We fed C57BL/6J mice a protein- (casein) or sucrose-based high fat diet supplemented with fish oil or corn oil for 9 weeks. Irrespective of the fatty acid source, mice fed diets rich in sucrose became obese whereas mice fed high protein diets remained lean. Inclusion of sucrose in the diet also counteracted the well-known anti-inflammatory effect of fish oil in adipose tissue, but did not impair the ability of fish oil to prevent accumulation of fat in the liver. Calculation of HOMA-IR indicated that mice fed high levels of proteins remained insulin sensitive, whereas insulin sensitivity was reduced in the obese mice fed sucrose irrespectively of the fat source. We show that a high fat diet decreased glucose tolerance in the mice independently of both obesity and dietary levels of n-3 PUFAs and sucrose. Of note, increasing the protein:sucrose ratio in high fat diets decreased energy efficiency irrespective of fat source. This was accompanied by increased expression of Ppargc1a (peroxisome proliferator-activated receptor, gamma, coactivator 1 alpha) and increased gluconeogenesis in the fed state. Conclusions/Significance: The background diet influence the ability of n-3 PUFAs to protect against development of obesity, glucose intolerance and adipose tissue inflammation. High levels of dietary sucrose counteract the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice.

Original language	English
Journal	P L o S One
Volume	6
Issue number	6
Number of pages	12
ISSN	1932-6203
DOIs	https://doi.org/10.1371/journal.pone.0021647
Publication status	Published - 2011

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Ma, T., Liaset, B., Hao, Q., Petersen, R. K., Fjære, E., Ngo, H. T., Lillefosse, H. H., Jørgensen, S. R., Sonne, S. B., Treebak, J. T., Pilegaard, H., Frøyland, L., Kristiansen, K., & Madsen, L. (2011). Sucrose counteracts the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice. P L o S One, 6(6). https://doi.org/10.1371/journal.pone.0021647

Ma, T, Liaset, B, Hao, Q, Petersen, RK, Fjære, E, Ngo, HT, Lillefosse, HH, Jørgensen, SR, Sonne, SB, Treebak, JT , Pilegaard, H, Frøyland, L, Kristiansen, K & Madsen, L 2011, 'Sucrose counteracts the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice', P L o S One, vol. 6, no. 6. https://doi.org/10.1371/journal.pone.0021647

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title = "Sucrose counteracts the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice",

abstract = "Background: Polyunsaturated n-3 fatty acids (n-3 PUFAs) are reported to protect against high fat diet-induced obesity and inflammation in adipose tissue. Here we aimed to investigate if the amount of sucrose in the background diet influences the ability of n-3 PUFAs to protect against diet-induced obesity, adipose tissue inflammation and glucose intolerance. Methodology/Principal Findings: We fed C57BL/6J mice a protein- (casein) or sucrose-based high fat diet supplemented with fish oil or corn oil for 9 weeks. Irrespective of the fatty acid source, mice fed diets rich in sucrose became obese whereas mice fed high protein diets remained lean. Inclusion of sucrose in the diet also counteracted the well-known anti-inflammatory effect of fish oil in adipose tissue, but did not impair the ability of fish oil to prevent accumulation of fat in the liver. Calculation of HOMA-IR indicated that mice fed high levels of proteins remained insulin sensitive, whereas insulin sensitivity was reduced in the obese mice fed sucrose irrespectively of the fat source. We show that a high fat diet decreased glucose tolerance in the mice independently of both obesity and dietary levels of n-3 PUFAs and sucrose. Of note, increasing the protein:sucrose ratio in high fat diets decreased energy efficiency irrespective of fat source. This was accompanied by increased expression of Ppargc1a (peroxisome proliferator-activated receptor, gamma, coactivator 1 alpha) and increased gluconeogenesis in the fed state. Conclusions/Significance: The background diet influence the ability of n-3 PUFAs to protect against development of obesity, glucose intolerance and adipose tissue inflammation. High levels of dietary sucrose counteract the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice.",

author = "Tao Ma and Bj{\o}rn Liaset and Qin Hao and Petersen, {Rasmus Koefoed} and Even Fj{\ae}re and Ngo, {Ha Thi} and Lillefosse, {Haldis Hauk{\aa}s} and J{\o}rgensen, {Stine Ringholm} and Sonne, {Si Brask} and Treebak, {Jonas Thue} and Henriette Pilegaard and Livar Fr{\o}yland and Karsten Kristiansen and Lise Madsen",

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year = "2011",

doi = "10.1371/journal.pone.0021647",

language = "English",

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TY - JOUR

T1 - Sucrose counteracts the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice

AU - Ma, Tao

AU - Liaset, Bjørn

AU - Hao, Qin

AU - Petersen, Rasmus Koefoed

AU - Fjære, Even

AU - Ngo, Ha Thi

AU - Lillefosse, Haldis Haukås

AU - Jørgensen, Stine Ringholm

AU - Sonne, Si Brask

AU - Treebak, Jonas Thue

AU - Pilegaard, Henriette

AU - Frøyland, Livar

AU - Kristiansen, Karsten

AU - Madsen, Lise

N1 - Artikel ID: e21647

PY - 2011

Y1 - 2011

N2 - Background: Polyunsaturated n-3 fatty acids (n-3 PUFAs) are reported to protect against high fat diet-induced obesity and inflammation in adipose tissue. Here we aimed to investigate if the amount of sucrose in the background diet influences the ability of n-3 PUFAs to protect against diet-induced obesity, adipose tissue inflammation and glucose intolerance. Methodology/Principal Findings: We fed C57BL/6J mice a protein- (casein) or sucrose-based high fat diet supplemented with fish oil or corn oil for 9 weeks. Irrespective of the fatty acid source, mice fed diets rich in sucrose became obese whereas mice fed high protein diets remained lean. Inclusion of sucrose in the diet also counteracted the well-known anti-inflammatory effect of fish oil in adipose tissue, but did not impair the ability of fish oil to prevent accumulation of fat in the liver. Calculation of HOMA-IR indicated that mice fed high levels of proteins remained insulin sensitive, whereas insulin sensitivity was reduced in the obese mice fed sucrose irrespectively of the fat source. We show that a high fat diet decreased glucose tolerance in the mice independently of both obesity and dietary levels of n-3 PUFAs and sucrose. Of note, increasing the protein:sucrose ratio in high fat diets decreased energy efficiency irrespective of fat source. This was accompanied by increased expression of Ppargc1a (peroxisome proliferator-activated receptor, gamma, coactivator 1 alpha) and increased gluconeogenesis in the fed state. Conclusions/Significance: The background diet influence the ability of n-3 PUFAs to protect against development of obesity, glucose intolerance and adipose tissue inflammation. High levels of dietary sucrose counteract the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice.

AB - Background: Polyunsaturated n-3 fatty acids (n-3 PUFAs) are reported to protect against high fat diet-induced obesity and inflammation in adipose tissue. Here we aimed to investigate if the amount of sucrose in the background diet influences the ability of n-3 PUFAs to protect against diet-induced obesity, adipose tissue inflammation and glucose intolerance. Methodology/Principal Findings: We fed C57BL/6J mice a protein- (casein) or sucrose-based high fat diet supplemented with fish oil or corn oil for 9 weeks. Irrespective of the fatty acid source, mice fed diets rich in sucrose became obese whereas mice fed high protein diets remained lean. Inclusion of sucrose in the diet also counteracted the well-known anti-inflammatory effect of fish oil in adipose tissue, but did not impair the ability of fish oil to prevent accumulation of fat in the liver. Calculation of HOMA-IR indicated that mice fed high levels of proteins remained insulin sensitive, whereas insulin sensitivity was reduced in the obese mice fed sucrose irrespectively of the fat source. We show that a high fat diet decreased glucose tolerance in the mice independently of both obesity and dietary levels of n-3 PUFAs and sucrose. Of note, increasing the protein:sucrose ratio in high fat diets decreased energy efficiency irrespective of fat source. This was accompanied by increased expression of Ppargc1a (peroxisome proliferator-activated receptor, gamma, coactivator 1 alpha) and increased gluconeogenesis in the fed state. Conclusions/Significance: The background diet influence the ability of n-3 PUFAs to protect against development of obesity, glucose intolerance and adipose tissue inflammation. High levels of dietary sucrose counteract the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice.

U2 - 10.1371/journal.pone.0021647

DO - 10.1371/journal.pone.0021647

M3 - Journal article

C2 - 21738749

SN - 1932-6203

VL - 6

JO - PLoS Computational Biology

JF - PLoS Computational Biology

IS - 6

ER -

Sucrose counteracts the anti-inflammatory effect of fish oil in adipose tissue and increases obesity development in mice

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