Whole-body insulin resistance and energy expenditure indices, serum lipids, and skeletal muscle metabolome in a state of lipoprotein lipase overexpression View Full Text


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Article Info

DATE

2021-02-16

AUTHORS

Yuichiro Nishida, Kazutoshi Nishijima, Yosuke Yamada, Hiroaki Tanaka, Akiko Matsumoto, Jianglin Fan, Yoichi Uda, Hajime Tomatsu, Hiroyuki Yamamoto, Kenjiro Kami, Shuji Kitajima, Keitaro Tanaka

ABSTRACT

IntroductionOverexpression of lipoprotein lipase (LPL) protects against high-fat-diet (HFD)-induced obesity and insulin resistance in transgenic rabbits; however, the molecular mechanisms remain unclear. Skeletal muscle is a major organ responsible for insulin-stimulated glucose uptake and energy expenditure.ObjectivesThe main purpose of the current study was to examine the effects of the overexpression of LPL on the skeletal muscle metabolomic profiles to test our hypothesis that the mitochondrial oxidative metabolism would be activated in the skeletal muscle of LPL transgenic rabbits and that the higher mitochondrial oxidative metabolism activity would confer better phenotypic metabolic outcomes.MethodsUnder a HFD, insulin resistance index was measured using the intravenous glucose tolerance test, and total energy expenditure (TEE) was measured by doubly-labeled water in control and LPL transgenic rabbits (n = 12, each group). Serum lipids, such as triglycerides and free fatty acid, were also measured. The skeletal muscle metabolite profile was analyzed using capillary electrophoresis time-of flight mass spectrometry in the two groups (n = 9, each group). A metabolite set enrichment analysis (MSEA) with muscle metabolites and a false discovery rate q < 0.2 was performed to identify significantly different metabolic pathways between the 2 groups.ResultsThe triglycerides and free fatty acid levels and insulin resistance index were lower, whereas the TEE was higher in the LPL transgenic rabbits than in the control rabbits. Among 165 metabolites detected, the levels of 37 muscle metabolites were significantly different between the 2 groups after false discovery rate correction (q < 0.2). The MSEA revealed that the TCA cycle and proteinogenic amino acid metabolism pathways were significantly different between the 2 groups (P < 0.05). In the MSEA, all four selected metabolites for the TCA cycle (2-oxoglutaric acid, citric acid, malic acid, fumaric acid), as well as eight selected metabolites for proteinogenic amino acid metabolism (asparagine, proline, methionine, phenylalanine, histidine, arginine, leucine, isoleucine) were consistently increased in the transgenic rabbits compared with control rabbits, suggesting that these two metabolic pathways were activated in the transgenic rabbits. Some of the selected metabolites, such as citric acid and methionine, were significantly associated with serum lipids and insulin resistance (P < 0.05).ConclusionThe current results suggest that the overexpression of LPL may lead to increased activities of TCA cycle and proteinogenic amino acid metabolism pathways in the skeletal muscle, and these enhancements may play an important role in the biological mechanisms underlying the anti-obesity/anti-diabetes features of LPL overexpression. More... »

PAGES

26

Journal

TITLE

Metabolomics

ISSUE

3

VOLUME

17

Identifiers

URI

http://scigraph.springernature.com/pub.10.1007/s11306-021-01777-4

DOI

http://dx.doi.org/10.1007/s11306-021-01777-4

DIMENSIONS

https://app.dimensions.ai/details/publication/pub.1135412012

PUBMED

https://www.ncbi.nlm.nih.gov/pubmed/33594546


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31 schema:description IntroductionOverexpression of lipoprotein lipase (LPL) protects against high-fat-diet (HFD)-induced obesity and insulin resistance in transgenic rabbits; however, the molecular mechanisms remain unclear. Skeletal muscle is a major organ responsible for insulin-stimulated glucose uptake and energy expenditure.ObjectivesThe main purpose of the current study was to examine the effects of the overexpression of LPL on the skeletal muscle metabolomic profiles to test our hypothesis that the mitochondrial oxidative metabolism would be activated in the skeletal muscle of LPL transgenic rabbits and that the higher mitochondrial oxidative metabolism activity would confer better phenotypic metabolic outcomes.MethodsUnder a HFD, insulin resistance index was measured using the intravenous glucose tolerance test, and total energy expenditure (TEE) was measured by doubly-labeled water in control and LPL transgenic rabbits (n = 12, each group). Serum lipids, such as triglycerides and free fatty acid, were also measured. The skeletal muscle metabolite profile was analyzed using capillary electrophoresis time-of flight mass spectrometry in the two groups (n = 9, each group). A metabolite set enrichment analysis (MSEA) with muscle metabolites and a false discovery rate q < 0.2 was performed to identify significantly different metabolic pathways between the 2 groups.ResultsThe triglycerides and free fatty acid levels and insulin resistance index were lower, whereas the TEE was higher in the LPL transgenic rabbits than in the control rabbits. Among 165 metabolites detected, the levels of 37 muscle metabolites were significantly different between the 2 groups after false discovery rate correction (q < 0.2). The MSEA revealed that the TCA cycle and proteinogenic amino acid metabolism pathways were significantly different between the 2 groups (P < 0.05). In the MSEA, all four selected metabolites for the TCA cycle (2-oxoglutaric acid, citric acid, malic acid, fumaric acid), as well as eight selected metabolites for proteinogenic amino acid metabolism (asparagine, proline, methionine, phenylalanine, histidine, arginine, leucine, isoleucine) were consistently increased in the transgenic rabbits compared with control rabbits, suggesting that these two metabolic pathways were activated in the transgenic rabbits. Some of the selected metabolites, such as citric acid and methionine, were significantly associated with serum lipids and insulin resistance (P < 0.05).ConclusionThe current results suggest that the overexpression of LPL may lead to increased activities of TCA cycle and proteinogenic amino acid metabolism pathways in the skeletal muscle, and these enhancements may play an important role in the biological mechanisms underlying the anti-obesity/anti-diabetes features of LPL overexpression.
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38 LPL overexpression
39 MSeA
40 MethodsUnder
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42 TCA cycle
43 acid
44 acid levels
45 acid metabolism
46 activity
47 amino acid metabolism
48 amino acid metabolism pathways
49 analysis
50 biological mechanisms
51 capillary electrophoresis time
52 citric acid
53 control
54 control rabbits
55 correction
56 current results
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58 cycle
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60 different metabolic pathways
61 effect
62 electrophoresis time
63 energy expenditure
64 energy expenditure index
65 enhancement
66 enrichment analysis
67 expenditure
68 false discovery rate correction
69 false discovery rate q
70 fatty acid levels
71 fatty acids
72 features
73 flight mass spectrometry
74 free fatty acid levels
75 free fatty acids
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81 index
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83 insulin resistance index
84 insulin-stimulated glucose uptake
85 intravenous glucose tolerance test
86 levels
87 lipase
88 lipids
89 lipoprotein lipase
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91 major organs
92 mass spectrometry
93 mechanism
94 metabolic outcomes
95 metabolic pathways
96 metabolism
97 metabolism activity
98 metabolism pathways
99 metabolite profiles
100 metabolites
101 metabolome
102 metabolomic profiles
103 methionine
104 mitochondrial oxidative metabolism
105 molecular mechanisms
106 muscle
107 muscle metabolite profile
108 muscle metabolites
109 muscle metabolome
110 obesity
111 organs
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