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. 2017 Feb 7;18(6):1558-1572.
doi: 10.1016/j.celrep.2017.01.038.

Lipidomic Adaptations in White and Brown Adipose Tissue in Response to Exercise Demonstrate Molecular Species-Specific Remodeling

Francis J May  1 , Lisa A Baer  1 , Adam C Lehnig  1 , Kawai So  2 , Emily Y Chen  3 , Fei Gao  3 , Niven R Narain  3 , Liubov Gushchina  1 , Aubrey Rose  1 , Andrea I Doseff  1 , Michael A Kiebish  3 , Laurie J Goodyear  4 , Kristin I Stanford  5
Affiliations

Lipidomic Adaptations in White and Brown Adipose Tissue in Response to Exercise Demonstrate Molecular Species-Specific Remodeling

Francis J May et al. Cell Rep. .

Abstract

Exercise improves whole-body metabolic health through adaptations to various tissues, including adipose tissue, but the effects of exercise training on the lipidome of white adipose tissue (WAT) and brown adipose tissue (BAT) are unknown. Here, we utilize MS/MSALL shotgun lipidomics to determine the molecular signatures of exercise-induced adaptations to subcutaneous WAT (scWAT) and BAT. Three weeks of exercise training decrease specific molecular species of phosphatidic acid (PA), phosphatidylcholines (PC), phosphatidylethanolamines (PE), and phosphatidylserines (PS) in scWAT and increase specific molecular species of PC and PE in BAT. Exercise also decreases most triacylglycerols (TAGs) in scWAT and BAT. In summary, exercise-induced changes to the scWAT and BAT lipidome are highly specific to certain molecular lipid species, indicating that changes in tissue lipid content reflect selective remodeling in scWAT and BAT of both phospholipids and glycerol lipids in response to exercise training, thus providing a comprehensive resource for future studies of lipid metabolism pathways.

Keywords: adipose tissue; exercise; lipidomics.

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Figures

Figure 1
Figure 1. Changes in Lipid Composition of scWAT after Chronic Exercise
(A) Quantified lipid classes and their abbreviations. (B–D) Concentration of quantified lipid classes in scWAT of sedentary vs. exercise-trained mice. Data are presented as means ± S.E.M. (n=6/group; *P<0.05). (E) The relative percentage difference in concentration of quantified lipid species between sedentary and exercise-trained mice. Each circle represents a significantly changed particular species of lipid within the indicated lipid class. Size of circle indicates level of significance (n=6/group; P<0.05, increasing size with increasing significance).
Figure 2
Figure 2. Changes in Lipid Composition of BAT after Chronic Exercise
(A–C) Concentration of quantified lipid classes in scWAT of sedentary vs. exercise-trained mice. Data are presented as means ± S.E.M. (n=6/group; *P<0.05). (D) The relative percentage difference in concentration of quantified lipid species between sedentary and exercise-trained mice. Each circle represents a significantly changed particular species of lipid within the indicated lipid class. Size of circle indicates level of significance (n=6/group; P<0.05, increasing size with increasing significance).
Figure 3
Figure 3. Exercise-Induced Changes in Phospholipid Species, Acyl Chain Composition, and Gene Expression in scWAT
(A) Concentration of phospholipid species significantly changed in scWAT after 3 wks of exercise. The concentration of acyl chains associated with (B) PE and (C) PS/LPS phospholipids. Data are means ± S.E.M. (n=6/group; *P<0.05). (D) Expression of genes involved in phospholipid metabolism by qPCR in mouse scWAT after 3 wks of exercise training. Data are presented as means ± S.E.M. (n=6/group; *P<0.05). (E) Microarray analysis of genes involved in phospholipid metabolism and fatty acid elongation after 11 days of exercise training in mice, n=7/group.
Figure 4
Figure 4. Exercise-Induced Changes in Phospholipid Species, Acyl Chain Composition, and Gene Expression in BAT
(A) Concentration of phospholipid species significantly changed in BAT after 3 wks of exercise. The concentration of acyl chains associated with (B) PC and (C) PE phospholipids. Data are presented as mean ± S.E.M. (n=6/group; *P<0.05; **P<0.01). (D) Expression of genes involved in phospholipid metabolism by qPCR in mouse BAT after 3 wks of exercise training. Data are presented as means ± S.E.M. (n=6/group; *P<0.05).
Figure 5
Figure 5. Exercise-Induced Changes in TAG Species, Acyl Chain Composition, and Gene Expression in scWAT
The concentration of (A) highly abundant, (B) moderately abundant, and (C) low abundance TAG species significantly altered by exercise in scWAT. (D) The concentration of acyl chains associated with TAG in scWAT from sedentary and exercise-trained mice. Data are presented as means ± S.E.M. (n=6/group; *P<0.05; **P<0.01; ***P<0.001). (E) Expression of genes involved in fatty acid biosynthesis and elongation measured by qPCR. (F) Western blots of pHSL/HSL ratio in scWAT. Data are presented as means ± S.E.M. (n=6/group; *P<0.05).
Figure 6
Figure 6. Exercise-Induced Changes in TAG Species, Acyl Chain Composition, and Gene Expression in BAT
The concentration of (A) highly abundant, (B) moderately abundant, and (C) low abundance TAG species significantly altered by exercise in BAT. (D) The concentration of acyl chains associated with TAG in BAT from sedentary and exercise-trained mice. Data are presented as means ± S.E.M. (n=6/group; *P<0.05; **P<0.01). (E) Expression of genes involved in fatty acid biosynthesis and elongation measured by qPCR. Data are presented as means ± S.E.M. (n=6/group; *P<0.05).
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