Incorporation of Omega-3 Fatty Acids Into Human Skeletal Muscle Sarcolemmal and Mitochondrial Membranes Following 12 Weeks of Fish Oil Supplementation.

Christopher J. Gerling,Kazutaka Mukai,Graham P. Holloway,George J. F. Heigenhauser,Sebastian Jannas-Vela,Lawrence L. Spriet,Adrian Chabowski

doi:10.3389/fphys.2019.00348

Abstract

Fish oil (FO) supplementation in humans results in the incorporation of omega-3 fatty acids (FAs) eicosapentaenoic acid (EPA; C20:5) and docosahexaenoic acid (DHA; C20:6) into skeletal muscle membranes. However, despite the importance of membrane composition in structure–function relationships, a paucity of information exists regarding how different muscle membranes/organelles respond to FO supplementation. Therefore, the purpose of the present study was to determine the effects 12 weeks of FO supplementation (3g EPA/2g DHA daily) on the phospholipid composition of sarcolemmal and mitochondrial fractions, as well as whole muscle responses, in healthy young males. FO supplementation increased the total phospholipid content in whole muscle (57%; p < 0.05) and the sarcolemma (38%; p = 0.05), but did not alter the content in mitochondria. The content of omega-3 FAs, EPA and DHA, were increased (+3-fold) in whole muscle, and mitochondrial membranes, and as a result the omega-6/omega-3 ratios were dramatically decreased (-3-fold), while conversely the unsaturation indexes were increased. Intriguingly, before supplementation the unsaturation index (UI) of sarcolemmal membranes was ∼3 times lower (p < 0.001) than either whole muscle or mitochondrial membranes. While supplementation also increased DHA within sarcolemmal membranes, EPA was not altered, and as a result the omega-6/omega-3 ratio and UI of these membranes were not altered. All together, these data revealed that mitochondrial and sarcolemmal membranes display unique phospholipid compositions and responses to FO supplementation.

Highlights

Phospholipids are the major constituents of cell membranes (Singer and Nicolson, 1972), and their composition determines the structure and function of the cell (McIntosh and Simon, 2006)
There is substantial evidence revealing that EPA and DHA are significantly incorporated into skeletal muscle membranes following omega-3 fatty acids (FAs) supplementation, at the expense of omega-6 FAs (Liu et al, 1994; Andersson et al, 2002; Haugaard et al, 2006; Tsalouhidou et al, 2006; Smith G.I. et al, 2011; Herbst et al, 2014; McGlory et al, 2014; Chorner et al, 2016)
The main findings of the present study were that: (1) a 12-week Fish oil (FO) supplementation period increased the total phospholipid content in whole muscle and sarcolemma, but did not affect the mitochondrial fraction, (2) omega-3 FAs were substantially increased in whole muscle, mitochondrial and sarcolemmal membrane fractions, and (3) sarcolemmal membranes had a lower unsaturation index (UI) and the FA composition was less responsive to omega-3 supplementation than whole muscle and mitochondria

Summary

Introduction

Phospholipids are the major constituents of cell membranes (Singer and Nicolson, 1972), and their composition determines the structure and function of the cell (McIntosh and Simon, 2006). The omega-3 fatty acids (FAs), eicosapentaenoic (EPA; C20:5) and docosahexaenoic (DHA; C20:6) acid, are characterized by their ability to modify the composition of biological membranes Incorporation of these FAs has been demonstrated to modify the activity of enzymes and proteins involved in the transport of substrates and ions across membranes (Liu et al, 1994; Hulbert, 2007; Herbst et al, 2014; Shaikh et al, 2015; Chorner et al, 2016), and to disrupt the formation of membrane rafts, thereby modulating multiple cellular and signaling events in different tissues (Wassall and Stillwell, 2008; Williams et al, 2012). Mitochondrial membranes are composed evenly of SFAs and PUFAs, and the omega-6 FAs are the major PUFA constituent (Fiehn et al, 1971; Stefanyk et al, 2010; Fajardo et al, 2013; Herbst et al, 2014) These differences may reflect the diverse roles that these compartments play in the cell. It remains unknown if sarcolemmal and mitochondrial membranes respond to omega-3 FA supplementation

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