Training status diverges muscle diacylglycerol accumulation during free fatty acid elevation

Lisa S. Chow, Douglas G. Mashek, Erin Austin, Lynn E. Eberly, Xuan Mai Persson, Mara T. Mashek, Elizabeth R. Seaquist, Michael Dennis Jensen

Research output: Contribution to journalArticle

20 Citations (Scopus)

Abstract

How endurance training alters muscle lipid metabolism while preserving insulin sensitivity remains unclear. Because acute free fatty acid (FFA) elevation by lipid infusion reduces insulin sensitivity, we hypothesized that training status would alter accumulation of muscle triacylglycerol (TAG), diacylglycerol (DAG), ceramide, and acylcarnitine during acute FFA elevation. Trained (n = 15) and sedentary (n = 13) participants matched for age, sex, and BMI received either a 6-h infusion of lipid (20% Intralipid at 90 ml/h) or glycerol (2.25 g/100 ml at 90 ml/h) during a hyperinsulinemic euglycemic clamp. Muscle biopsies were taken at 0, 120, and 360 min after infusion initiation to measure intramyocellular concentrations of TAG, DAG, ceramides, and acylcarnitines by liquid chromatography-tandem mass spectrometry. Trained participants had a higher V̇O2 max and insulin sensitivity than sedentary participants. The lipid infusion produced a comparable elevation of FFA (594 ± 90 μmol/l in trained, 721 ± 30 μmol/l in sedentary, P = 0.4) and a decline in insulin sensitivity (-44.7% trained vs. -47.2% sedentary, P = 0.89). In both groups, lipid infusion increased the linoleic and linolenic acid content of TAG without changing total TAG. In the sedentary group, lipid infusion increased total, oleic, and linoleic acid and linolenic acid content of DAG. Regardless of training status, lipid infusion did not alter total ceramide, saturated ceramide, palmitoyl-carnitine, or oleoyl-carnitine. We conclude that during acute FFA elevation, trained adults have a similar decline in insulin sensitivity with less accumulation of muscle DAG than sedentary adults, suggesting that lipid-induced insulin resistance can occur without elevation of total muscle DAG.

Original languageEnglish (US)
JournalAmerican Journal of Physiology - Endocrinology and Metabolism
Volume307
Issue number1
DOIs
StatePublished - Jul 1 2014

Fingerprint

Diglycerides
Nonesterified Fatty Acids
Insulin Resistance
Lipids
Ceramides
Muscles
Triglycerides
alpha-Linolenic Acid
Carnitine
Linoleic Acid
Glucose Clamp Technique
Oleic Acid
Tandem Mass Spectrometry
Lipid Metabolism
Liquid Chromatography
Glycerol
Biopsy

Keywords

  • Diacylglycerol
  • Free fatty acids
  • Insulin sensitivity
  • Intramyocellular lipid
  • Training

ASJC Scopus subject areas

  • Physiology
  • Physiology (medical)
  • Endocrinology, Diabetes and Metabolism

Cite this

Training status diverges muscle diacylglycerol accumulation during free fatty acid elevation. / Chow, Lisa S.; Mashek, Douglas G.; Austin, Erin; Eberly, Lynn E.; Persson, Xuan Mai; Mashek, Mara T.; Seaquist, Elizabeth R.; Jensen, Michael Dennis.

In: American Journal of Physiology - Endocrinology and Metabolism, Vol. 307, No. 1, 01.07.2014.

Research output: Contribution to journalArticle

Chow, Lisa S. ; Mashek, Douglas G. ; Austin, Erin ; Eberly, Lynn E. ; Persson, Xuan Mai ; Mashek, Mara T. ; Seaquist, Elizabeth R. ; Jensen, Michael Dennis. / Training status diverges muscle diacylglycerol accumulation during free fatty acid elevation. In: American Journal of Physiology - Endocrinology and Metabolism. 2014 ; Vol. 307, No. 1.
@article{1be08d16289049c3b6f3f14ce0cabcf8,
title = "Training status diverges muscle diacylglycerol accumulation during free fatty acid elevation",
abstract = "How endurance training alters muscle lipid metabolism while preserving insulin sensitivity remains unclear. Because acute free fatty acid (FFA) elevation by lipid infusion reduces insulin sensitivity, we hypothesized that training status would alter accumulation of muscle triacylglycerol (TAG), diacylglycerol (DAG), ceramide, and acylcarnitine during acute FFA elevation. Trained (n = 15) and sedentary (n = 13) participants matched for age, sex, and BMI received either a 6-h infusion of lipid (20{\%} Intralipid at 90 ml/h) or glycerol (2.25 g/100 ml at 90 ml/h) during a hyperinsulinemic euglycemic clamp. Muscle biopsies were taken at 0, 120, and 360 min after infusion initiation to measure intramyocellular concentrations of TAG, DAG, ceramides, and acylcarnitines by liquid chromatography-tandem mass spectrometry. Trained participants had a higher V̇O2 max and insulin sensitivity than sedentary participants. The lipid infusion produced a comparable elevation of FFA (594 ± 90 μmol/l in trained, 721 ± 30 μmol/l in sedentary, P = 0.4) and a decline in insulin sensitivity (-44.7{\%} trained vs. -47.2{\%} sedentary, P = 0.89). In both groups, lipid infusion increased the linoleic and linolenic acid content of TAG without changing total TAG. In the sedentary group, lipid infusion increased total, oleic, and linoleic acid and linolenic acid content of DAG. Regardless of training status, lipid infusion did not alter total ceramide, saturated ceramide, palmitoyl-carnitine, or oleoyl-carnitine. We conclude that during acute FFA elevation, trained adults have a similar decline in insulin sensitivity with less accumulation of muscle DAG than sedentary adults, suggesting that lipid-induced insulin resistance can occur without elevation of total muscle DAG.",
keywords = "Diacylglycerol, Free fatty acids, Insulin sensitivity, Intramyocellular lipid, Training",
author = "Chow, {Lisa S.} and Mashek, {Douglas G.} and Erin Austin and Eberly, {Lynn E.} and Persson, {Xuan Mai} and Mashek, {Mara T.} and Seaquist, {Elizabeth R.} and Jensen, {Michael Dennis}",
year = "2014",
month = "7",
day = "1",
doi = "10.1152/ajpendo.00166.2014",
language = "English (US)",
volume = "307",
journal = "American Journal of Physiology - Renal Fluid and Electrolyte Physiology",
issn = "1931-857X",
publisher = "American Physiological Society",
number = "1",

}

TY - JOUR

T1 - Training status diverges muscle diacylglycerol accumulation during free fatty acid elevation

AU - Chow, Lisa S.

AU - Mashek, Douglas G.

AU - Austin, Erin

AU - Eberly, Lynn E.

AU - Persson, Xuan Mai

AU - Mashek, Mara T.

AU - Seaquist, Elizabeth R.

AU - Jensen, Michael Dennis

PY - 2014/7/1

Y1 - 2014/7/1

N2 - How endurance training alters muscle lipid metabolism while preserving insulin sensitivity remains unclear. Because acute free fatty acid (FFA) elevation by lipid infusion reduces insulin sensitivity, we hypothesized that training status would alter accumulation of muscle triacylglycerol (TAG), diacylglycerol (DAG), ceramide, and acylcarnitine during acute FFA elevation. Trained (n = 15) and sedentary (n = 13) participants matched for age, sex, and BMI received either a 6-h infusion of lipid (20% Intralipid at 90 ml/h) or glycerol (2.25 g/100 ml at 90 ml/h) during a hyperinsulinemic euglycemic clamp. Muscle biopsies were taken at 0, 120, and 360 min after infusion initiation to measure intramyocellular concentrations of TAG, DAG, ceramides, and acylcarnitines by liquid chromatography-tandem mass spectrometry. Trained participants had a higher V̇O2 max and insulin sensitivity than sedentary participants. The lipid infusion produced a comparable elevation of FFA (594 ± 90 μmol/l in trained, 721 ± 30 μmol/l in sedentary, P = 0.4) and a decline in insulin sensitivity (-44.7% trained vs. -47.2% sedentary, P = 0.89). In both groups, lipid infusion increased the linoleic and linolenic acid content of TAG without changing total TAG. In the sedentary group, lipid infusion increased total, oleic, and linoleic acid and linolenic acid content of DAG. Regardless of training status, lipid infusion did not alter total ceramide, saturated ceramide, palmitoyl-carnitine, or oleoyl-carnitine. We conclude that during acute FFA elevation, trained adults have a similar decline in insulin sensitivity with less accumulation of muscle DAG than sedentary adults, suggesting that lipid-induced insulin resistance can occur without elevation of total muscle DAG.

AB - How endurance training alters muscle lipid metabolism while preserving insulin sensitivity remains unclear. Because acute free fatty acid (FFA) elevation by lipid infusion reduces insulin sensitivity, we hypothesized that training status would alter accumulation of muscle triacylglycerol (TAG), diacylglycerol (DAG), ceramide, and acylcarnitine during acute FFA elevation. Trained (n = 15) and sedentary (n = 13) participants matched for age, sex, and BMI received either a 6-h infusion of lipid (20% Intralipid at 90 ml/h) or glycerol (2.25 g/100 ml at 90 ml/h) during a hyperinsulinemic euglycemic clamp. Muscle biopsies were taken at 0, 120, and 360 min after infusion initiation to measure intramyocellular concentrations of TAG, DAG, ceramides, and acylcarnitines by liquid chromatography-tandem mass spectrometry. Trained participants had a higher V̇O2 max and insulin sensitivity than sedentary participants. The lipid infusion produced a comparable elevation of FFA (594 ± 90 μmol/l in trained, 721 ± 30 μmol/l in sedentary, P = 0.4) and a decline in insulin sensitivity (-44.7% trained vs. -47.2% sedentary, P = 0.89). In both groups, lipid infusion increased the linoleic and linolenic acid content of TAG without changing total TAG. In the sedentary group, lipid infusion increased total, oleic, and linoleic acid and linolenic acid content of DAG. Regardless of training status, lipid infusion did not alter total ceramide, saturated ceramide, palmitoyl-carnitine, or oleoyl-carnitine. We conclude that during acute FFA elevation, trained adults have a similar decline in insulin sensitivity with less accumulation of muscle DAG than sedentary adults, suggesting that lipid-induced insulin resistance can occur without elevation of total muscle DAG.

KW - Diacylglycerol

KW - Free fatty acids

KW - Insulin sensitivity

KW - Intramyocellular lipid

KW - Training

UR - http://www.scopus.com/inward/record.url?scp=84903596011&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84903596011&partnerID=8YFLogxK

U2 - 10.1152/ajpendo.00166.2014

DO - 10.1152/ajpendo.00166.2014

M3 - Article

C2 - 24844260

AN - SCOPUS:84903596011

VL - 307

JO - American Journal of Physiology - Renal Fluid and Electrolyte Physiology

JF - American Journal of Physiology - Renal Fluid and Electrolyte Physiology

SN - 1931-857X

IS - 1

ER -