Mechanisms preserving insulin action during high dietary fat intake

Annemarie Lundsgaard; Jacob Bak Holm; Kim Anker Sjøberg; Kirstine N Bojsen-Møller; Lene S Myrmel; Even Fjære; Benjamin Anderschou Holbech Jensen; Trine Sand Nicolaisen; Janne Rasmuss Hingst; Sine L Hansen; Sophia Doll; Philip E Geyer; Atul Shahaji Deshmukh; Jens Juul Holst; Lise Madsen; Karsten Kristiansen; Jørgen Wojtaszewski; Erik Richter; Bente Kiens

doi:10.1016/j.cmet.2018.08.022

Mechanisms preserving insulin action during high dietary fat intake

Annemarie Lundsgaard, Jacob Bak Holm, Kim Anker Sjøberg, Kirstine N Bojsen-Møller, Lene S Myrmel, Even Fjære, Benjamin Anderschou Holbech Jensen, Trine Sand Nicolaisen, Janne Rasmuss Hingst, Sine L Hansen, Sophia Doll, Philip E Geyer, Atul Shahaji Deshmukh, Jens Juul Holst, Lise Madsen, Karsten Kristiansen, Jørgen Wojtaszewski, Erik Richter, Bente Kiens

4 Citations (Scopus)

Abstract

Prolonged intervention studies investigating molecular metabolism are necessary for a deeper understanding of dietary effects on health. Here we provide mechanistic information about metabolic adaptation to fat-rich diets. Healthy, slightly overweight men ingested saturated or polyunsaturated fat-rich diets for 6 weeks during weight maintenance. Hyperinsulinemic clamps combined with leg balance technique revealed unchanged peripheral insulin sensitivity, independent of fatty acid type. Both diets increased fat oxidation potential in muscle. Hepatic insulin clearance increased, while glucose production, de novo lipogenesis, and plasma triacylglycerol decreased. High fat intake changed the plasma proteome in the immune-supporting direction and the gut microbiome displayed changes at taxonomical and functional level with polyunsaturated fatty acid (PUFA). In mice, eucaloric feeding of human PUFA and saturated fatty acid diets lowered hepatic triacylglycerol content compared with low-fat-fed control mice, and induced adaptations in the liver supportive of decreased gluconeogenesis and lipogenesis. Intake of fat-rich diets thus induces extensive metabolic adaptations enabling disposition of dietary fat without metabolic complications.

Original language	English
Journal	Cell Metabolism
Volume	29
Issue number	1
Pages (from-to)	50-63, e1-e4
Number of pages	19
ISSN	1550-4131
DOIs	https://doi.org/10.1016/j.cmet.2018.08.022
Publication status	Published - 2019

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10.1016/j.cmet.2018.08.022

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Lundsgaard, A., Holm, J. B., Sjøberg, K. A., Bojsen-Møller, K. N., Myrmel, L. S., Fjære, E., Jensen, B. A. H., Nicolaisen, T. S., Hingst, J. R., Hansen, S. L., Doll, S., Geyer, P. E., Deshmukh, A. S., Holst, J. J., Madsen, L., Kristiansen, K., Wojtaszewski, J., Richter, E., & Kiens, B. (2019). Mechanisms preserving insulin action during high dietary fat intake. Cell Metabolism, 29(1), 50-63, e1-e4. https://doi.org/10.1016/j.cmet.2018.08.022

Lundsgaard, A, Holm, JB, Sjøberg, KA, Bojsen-Møller, KN, Myrmel, LS, Fjære, E, Jensen, BAH , Nicolaisen, TS, Hingst, JR, Hansen, SL, Doll, S, Geyer, PE, Deshmukh, AS , Holst, JJ, Madsen, L, Kristiansen, K , Wojtaszewski, J , Richter, E & Kiens, B 2019, 'Mechanisms preserving insulin action during high dietary fat intake', Cell Metabolism, vol. 29, no. 1, pp. 50-63, e1-e4. https://doi.org/10.1016/j.cmet.2018.08.022

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title = "Mechanisms preserving insulin action during high dietary fat intake",

abstract = "Prolonged intervention studies investigating molecular metabolism are necessary for a deeper understanding of dietary effects on health. Here we provide mechanistic information about metabolic adaptation to fat-rich diets. Healthy, slightly overweight men ingested saturated or polyunsaturated fat-rich diets for 6 weeks during weight maintenance. Hyperinsulinemic clamps combined with leg balance technique revealed unchanged peripheral insulin sensitivity, independent of fatty acid type. Both diets increased fat oxidation potential in muscle. Hepatic insulin clearance increased, while glucose production, de novo lipogenesis, and plasma triacylglycerol decreased. High fat intake changed the plasma proteome in the immune-supporting direction and the gut microbiome displayed changes at taxonomical and functional level with polyunsaturated fatty acid (PUFA). In mice, eucaloric feeding of human PUFA and saturated fatty acid diets lowered hepatic triacylglycerol content compared with low-fat-fed control mice, and induced adaptations in the liver supportive of decreased gluconeogenesis and lipogenesis. Intake of fat-rich diets thus induces extensive metabolic adaptations enabling disposition of dietary fat without metabolic complications.",

author = "Annemarie Lundsgaard and Holm, {Jacob Bak} and Sj{\o}berg, {Kim Anker} and Bojsen-M{\o}ller, {Kirstine N} and Myrmel, {Lene S} and Even Fj{\ae}re and Jensen, {Benjamin Anderschou Holbech} and Nicolaisen, {Trine Sand} and Hingst, {Janne Rasmuss} and Hansen, {Sine L} and Sophia Doll and Geyer, {Philip E} and Deshmukh, {Atul Shahaji} and Holst, {Jens Juul} and Lise Madsen and Karsten Kristiansen and J{\o}rgen Wojtaszewski and Erik Richter and Bente Kiens",

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doi = "10.1016/j.cmet.2018.08.022",

language = "English",

volume = "29",

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T1 - Mechanisms preserving insulin action during high dietary fat intake

AU - Lundsgaard, Annemarie

AU - Holm, Jacob Bak

AU - Sjøberg, Kim Anker

AU - Bojsen-Møller, Kirstine N

AU - Myrmel, Lene S

AU - Fjære, Even

AU - Jensen, Benjamin Anderschou Holbech

AU - Nicolaisen, Trine Sand

AU - Hingst, Janne Rasmuss

AU - Hansen, Sine L

AU - Doll, Sophia

AU - Geyer, Philip E

AU - Deshmukh, Atul Shahaji

AU - Holst, Jens Juul

AU - Madsen, Lise

AU - Kristiansen, Karsten

AU - Wojtaszewski, Jørgen

AU - Richter, Erik

AU - Kiens, Bente

N1 - Correction to: Mechanisms preserving insulin action during high dietary fat intake

PY - 2019

Y1 - 2019

N2 - Prolonged intervention studies investigating molecular metabolism are necessary for a deeper understanding of dietary effects on health. Here we provide mechanistic information about metabolic adaptation to fat-rich diets. Healthy, slightly overweight men ingested saturated or polyunsaturated fat-rich diets for 6 weeks during weight maintenance. Hyperinsulinemic clamps combined with leg balance technique revealed unchanged peripheral insulin sensitivity, independent of fatty acid type. Both diets increased fat oxidation potential in muscle. Hepatic insulin clearance increased, while glucose production, de novo lipogenesis, and plasma triacylglycerol decreased. High fat intake changed the plasma proteome in the immune-supporting direction and the gut microbiome displayed changes at taxonomical and functional level with polyunsaturated fatty acid (PUFA). In mice, eucaloric feeding of human PUFA and saturated fatty acid diets lowered hepatic triacylglycerol content compared with low-fat-fed control mice, and induced adaptations in the liver supportive of decreased gluconeogenesis and lipogenesis. Intake of fat-rich diets thus induces extensive metabolic adaptations enabling disposition of dietary fat without metabolic complications.

AB - Prolonged intervention studies investigating molecular metabolism are necessary for a deeper understanding of dietary effects on health. Here we provide mechanistic information about metabolic adaptation to fat-rich diets. Healthy, slightly overweight men ingested saturated or polyunsaturated fat-rich diets for 6 weeks during weight maintenance. Hyperinsulinemic clamps combined with leg balance technique revealed unchanged peripheral insulin sensitivity, independent of fatty acid type. Both diets increased fat oxidation potential in muscle. Hepatic insulin clearance increased, while glucose production, de novo lipogenesis, and plasma triacylglycerol decreased. High fat intake changed the plasma proteome in the immune-supporting direction and the gut microbiome displayed changes at taxonomical and functional level with polyunsaturated fatty acid (PUFA). In mice, eucaloric feeding of human PUFA and saturated fatty acid diets lowered hepatic triacylglycerol content compared with low-fat-fed control mice, and induced adaptations in the liver supportive of decreased gluconeogenesis and lipogenesis. Intake of fat-rich diets thus induces extensive metabolic adaptations enabling disposition of dietary fat without metabolic complications.

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U2 - 10.1016/j.cmet.2018.08.022

DO - 10.1016/j.cmet.2018.08.022

M3 - Journal article

C2 - 30269983

SN - 1550-4131

VL - 29

SP - 50-63, e1-e4

JO - Cell Metabolism

JF - Cell Metabolism

IS - 1

ER -

Mechanisms preserving insulin action during high dietary fat intake

Abstract

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