Mechanisms by Which Dietary Fatty Acids Regulate Mitochondrial Structure-Function in Health and Disease

Nikaido, 1983, Proteins forming large channels from bacterial and mitochondrial outer membranes: porins and phage lambda receptor protein, Methods Enzymol, 97, 85, 10.1016/0076-6879(83)97122-7 Mihara, 1985, Molecular cloning and sequencing of cDNA for yeast porin, an outer mitochondrial membrane protein: a search for targeting signal in the primary structure, EMBO J, 4, 769, 10.1002/j.1460-2075.1985.tb03695.x Vander Heiden, 2000, Outer mitochondrial membrane permeability can regulate coupled respiration and cell survival, Proc Natl Acad Sci USA, 97, 4666, 10.1073/pnas.090082297 Mayer, 1995, Mitochondrial protein import: reversible binding of the presequence at the trans side of the outer membrane drives partial translocation and unfolding, Cell, 80, 127, 10.1016/0092-8674(95)90457-3 Meisinger, 2001, Protein import channel of the outer mitochondrial membrane: a highly stable Tom40-Tom22 core structure differentially interacts with preproteins, small tom proteins, and import receptors, Mol Cell Biol, 21, 2337, 10.1128/MCB.21.7.2337-2348.2001 Künkele, 1998, The preprotein translocation channel of the outer membrane of mitochondria, Cell, 93, 1009, 10.1016/S0092-8674(00)81206-4 Krauss, 2001, Mitochondria: structure and role in respiration de Kroon, 1997, Phospholipid composition of highly purified mitochondrial outer membranes of rat liver and Neurospora crassa: is cardiolipin present in the mitochondrial outer membrane?, Biochim Biophys Acta, 1325, 108, 10.1016/S0005-2736(96)00240-4 Comte, 1976, Lipid composition and protein profiles of outer and inner membranes from pig heart mitochondria: comparison with microsomes, Biochim Biophys Acta, 419, 271, 10.1016/0005-2736(76)90353-9 Sperka-Gottlieb, 1988, Lipid topology and physical properties of the outer mitochondrial membrane of the yeast, Saccharomyces cerevisiae, Biochim Biophys Acta, 946, 227, 10.1016/0005-2736(88)90397-5 Ott, 2007, Role of cardiolipin in cytochrome c release from mitochondria, Cell Death Differ, 14, 1243, 10.1038/sj.cdd.4402135 Petrosillo, 2003, Role of reactive oxygen species and cardiolipin in the release of cytochrome c from mitochondria, FASEB J, 17, 2202, 10.1096/fj.03-0012com Fernandez, 2002, Early changes in intramitochondrial cardiolipin distribution during apoptosis, Cell Growth Differ, 13, 449 Schug, 2009, Cardiolipin acts as a mitochondrial signaling platform to launch apoptosis, Biochim Biophys Acta, 1788, 2022, 10.1016/j.bbamem.2009.05.004 Sorice, 2009, Cardiolipin-enriched raft-like microdomains are essential activating platforms for apoptotic signals on mitochondria, FEBS Lett, 583, 2447, 10.1016/j.febslet.2009.07.018 Gonzalvez, 2008, Cardiolipin provides an essential activating platform for caspase-8 on mitochondria, J Cell Biol, 183, 681, 10.1083/jcb.200803129 Colli, 1969, Characterization of the fatty acid elongation system in soluble extracts and membrane preparations of rat liver mitochondria, J Biol Chem, 244, 6432, 10.1016/S0021-9258(18)63482-9 Howard, 1970, Synthesis of fatty acids in outer and inner membranes of mitochondria, J Biol Chem, 245, 462, 10.1016/S0021-9258(18)63356-3 Raturi, 2013, Where the endoplasmic reticulum and the mitochondrion tie the knot: the mitochondria-associated membrane (MAM), Biochim Biophys Acta, 1833, 213, 10.1016/j.bbamcr.2012.04.013 Rusiñol, 1994, A unique mitochondria-associated membrane fraction from rat liver has a high capacity for lipid synthesis and contains pre-Golgi secretory proteins including nascent lipoproteins, J Biol Chem, 269, 27494, 10.1016/S0021-9258(18)47012-3 Stone, 2000, Phosphatidylserine synthase-1 and -2 are localized to mitochondria-associated membranes, J Biol Chem, 275, 34534, 10.1074/jbc.M002865200 Vance, 2014, MAM (mitochondria-associated membranes) in mammalian cells: lipids and beyond, Biochim Biophys Acta, 1841, 595, 10.1016/j.bbalip.2013.11.014 de Brito, 2008, Mitofusin 2 tethers endoplasmic reticulum to mitochondria, Nature, 456, 605, 10.1038/nature07534 Kornmann, 2013, The molecular hug between the ER and the mitochondria, Curr Opin Cell Biol, 25, 443, 10.1016/j.ceb.2013.02.010 Patergnani, 2011, Calcium signaling around mitochondria associated membranes (MAMs), Cell Commun Signal, 9, 19, 10.1186/1478-811X-9-19 van Vliet, 2014, New functions of mitochondria associated membranes in cellular signaling, Biochim Biophys Acta, 1843, 2253, 10.1016/j.bbamcr.2014.03.009 Hayashi, 2017, MAM: more than just a housekeeper, Trends Cell Biol, 19, 81, 10.1016/j.tcb.2008.12.002 Rizzuto, 2004, Flirting in little space: the ER/mitochondria Ca2+ liaison, Sci STKE, 2004, re1, 10.1126/stke.2152004re1 Vance, 1990, Phospholipid synthesis in a membrane fraction associated with mitochondria, J Biol Chem, 265, 7248, 10.1016/S0021-9258(19)39106-9 Shiao, 1995, Evidence that phosphatidylserine is imported into mitochondria via a mitochondria-associated membrane and that the majority of mitochondrial phosphatidylethanolamine is derived from decarboxylation of phosphatidylserine, J Biol Chem, 270, 11190, 10.1074/jbc.270.19.11190 Holthuis, 2005, Lipid traffic: floppy drives and a superhighway, Nat Rev Mol Cell Biol, 6, 209, 10.1038/nrm1591 Achleitner, 1999, Association between the endoplasmic reticulum and mitochondria of yeast facilitates interorganelle transport of phospholipids through membrane contact, Eur J Biochem, 264, 545, 10.1046/j.1432-1327.1999.00658.x Tatsuta, 2017, Mitochondrial lipid trafficking, Trends Cell Biol, 24, 44, 10.1016/j.tcb.2013.07.011 Cao, 2004, A novel cardiolipin-remodeling pathway revealed by a gene encoding an endoplasmic reticulum-associated acyl-CoA:lysocardiolipin acyltransferase (ALCAT1) in mouse, J Biol Chem, 279, 31727, 10.1074/jbc.M402930200 Li, 2010, Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity, Cell Metab, 12, 154, 10.1016/j.cmet.2010.07.003 Murphy, 1999, Mechanisms of lipid-body formation, Trends Biochem Sci, 24, 109, 10.1016/S0968-0004(98)01349-8 Yao, 2012, Apolipoprotein C-III and hepatic triglyceride-rich lipoprotein production, Curr Opin Lipidol, 23, 206, 10.1097/MOL.0b013e328352dc70 Nishimaki-Mogami, 2002, Inhibition of phosphatidylcholine synthesis via the phosphatidylethanolamine methylation pathway impairs incorporation of bulk lipids into VLDL in cultured rat hepatocytes, J Lipid Res, 43, 1035, 10.1194/jlr.M100354-JLR200 Fernie, 2004, Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport, Curr Opin Plant Biol, 7, 254, 10.1016/j.pbi.2004.03.007 Strauss, 2008, Dimer ribbons of ATP synthase shape the inner mitochondrial membrane, EMBO J, 27, 1154, 10.1038/emboj.2008.35 Vonck, 2009, Supramolecular organization of protein complexes in the mitochondrial inner membrane, Biochim Biophys Acta, 1793, 117, 10.1016/j.bbamcr.2008.05.019 Horvath, 2013, Lipids of mitochondria, Prog Lipid Res, 52, 590, 10.1016/j.plipres.2013.07.002 Schlame, 2009, The role of cardiolipin in the structural organization of mitochondrial membranes, Biochim Biophys Acta, 1788, 2080, 10.1016/j.bbamem.2009.04.019 Verkman, 2002, Solute and macromolecule diffusion in cellular aqueous compartments, Trends Biochem Sci, 27, 27, 10.1016/S0968-0004(01)02003-5 Calamita, 2005, The inner mitochondrial membrane has aquaporin-8 water channels and is highly permeable to water, J Biol Chem, 280, 17149, 10.1074/jbc.C400595200 Gnaiger, 1998, Mitochondrial oxygen affinity, respiratory flux control and excess capacity of cytochrome c oxidase, J Exp Biol, 201, 1129, 10.1242/jeb.201.8.1129 Nicholls, 1974, The influence of respiration and ATP hydrolysis on the proton-electrochemical gradient across the inner membrane of rat-liver mitochondria as determined by ion distribution, Eur J Biochem, 50, 305, 10.1111/j.1432-1033.1974.tb03899.x Saraste, 1999, Oxidative phosphorylation at the fin de siecle, Science, 283, 1488, 10.1126/science.283.5407.1488 Shaikh, 2012, Models of plasma membrane organization can be applied to mitochondrial membranes to target human health and disease with polyunsaturated fatty acids, Prostaglandins Leukot Essent Fatty Acids, 88, 21, 10.1016/j.plefa.2012.03.004 Palade, 1952, The fine structure of mitochondria, Anat Rec, 114, 427, 10.1002/ar.1091140304 Sjostrand, 1953, Electron microscopy of mitochondria and cytoplasmic double membranes: ultra-structure of rod-shaped mitochondria, Nature, 171, 30, 10.1038/171030a0 Rasmussen, 1995, Mitochondrial structure and the practice of cell biology in the 1950s, J Hist Biol, 28, 381, 10.1007/BF01059387 Mannella, 2006, Structure and dynamics of the mitochondrial inner membrane cristae, Biochim Biophys Acta, 1763, 542, 10.1016/j.bbamcr.2006.04.006 Zick, 2009, Cristae formation—linking ultrastructure and function of mitochondria, Biochim Biophys Acta, 1793, 5, 10.1016/j.bbamcr.2008.06.013 Cogliati, 2016, Mitochondrial cristae: where beauty meets functionality, Trends Biochem Sci, 41, 261, 10.1016/j.tibs.2016.01.001 Palade, 1953, An electron microscope study of the mitochondrial structure, J Histochem Cytochem, 1, 188, 10.1177/1.4.188 Sjöstrand, 1956, The ultrastructure of cells as revealed by the electron microscope, Int Rev Cytol, 5, 455, 10.1016/S0074-7696(08)62578-4 Mannella, 1994, The internal compartmentation of rat-liver mitochondria: tomographic study using the high-voltage transmission electron microscope, Microsc Res Tech, 27, 278, 10.1002/jemt.1070270403 Mannella, 2017, Reconsidering mitochondrial structure: new views of an old organelle, Trends Biochem Sci, 22, 37, 10.1016/S0968-0004(96)30050-9 Frey, 2000, The internal structure of mitochondria, Trends Biochem Sci, 25, 319, 10.1016/S0968-0004(00)01609-1 Mannella, 2001, Topology of the mitochondrial inner membrane: dynamics and bioenergetic implications, IUBMB Life, 52, 93, 10.1080/15216540152845885 Frey, 2002, Insight into mitochondrial structure and function from electron tomography, Biochim Biophys Acta, 1555, 196, 10.1016/S0005-2728(02)00278-5 Olofsson, 2013, Ionization constants pKa of cardiolipin, PLoS One, 8, e73040, 10.1371/journal.pone.0073040 Kates, 1993, pH-dissociation characteristics of cardiolipin and its 2'-deoxy analogue, Lipids, 28, 877, 10.1007/BF02537494 Lewis, 2009, The physicochemical properties of cardiolipin bilayers and cardiolipin-containing lipid membranes, Biochim Biophys Acta, 1788, 2069, 10.1016/j.bbamem.2009.03.014 Haines, 2002, Cardiolipin: a proton trap for oxidative phosphorylation, FEBS Lett, 528, 35, 10.1016/S0014-5793(02)03292-1 Mileykovskaya, 2009, Cardiolipin membrane domains in prokaryotes and eukaryotes, Biochim Biophys Acta, 1788, 2084, 10.1016/j.bbamem.2009.04.003 Paradies, 2014, Cardiolipin and mitochondrial function in health and disease, Antioxid Redox Signal, 20, 1925, 10.1089/ars.2013.5280 Claypool, 2016, The complexity of cardiolipin in health and disease, Trends Biochem Sci, 37, 32, 10.1016/j.tibs.2011.09.003 Paradies, 2014, Functional role of cardiolipin in mitochondrial bioenergetics, Biochim Biophys Acta, 1837, 408, 10.1016/j.bbabio.2013.10.006 Klingenberg, 2009, Cardiolipin and mitochondrial carriers, Biochim Biophys Acta, 1788, 2048, 10.1016/j.bbamem.2009.06.007 Shen, 2015, The role of cardiolipin in cardiovascular health, BioMed Res Int, 2015, 10.1155/2015/891707 Brown, 2013, Mitochondrial inner membrane lipids and proteins as targets for decreasing cardiac ischemia/reperfusion injury, Pharmacol Ther, 140, 258, 10.1016/j.pharmthera.2013.07.005 Genova, 2014, Functional role of mitochondrial respiratory supercomplexes, Biochim Biophys Acta, 1837, 427, 10.1016/j.bbabio.2013.11.002 Mileykovskaya, 2014, Cardiolipin-dependent formation of mitochondrial respiratory supercomplexes, Chem Phys Lipids, 179, 42, 10.1016/j.chemphyslip.2013.10.012 Schwall, 2012, The stability and activity of respiratory complex II is cardiolipin-dependent, Biochim Biophys Acta, 1817, 1588, 10.1016/j.bbabio.2012.04.015 Bazán, 2013, Cardiolipin-dependent reconstitution of respiratory supercomplexes from purified saccharomyces cerevisiae complexes III and IV, J Biol Chem, 288, 401, 10.1074/jbc.M112.425876 Chicco, 2007, Role of cardiolipin alterations in mitochondrial dysfunction and disease, Am J Phys Cell Phys, 292, C33 Eble, 1990, Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by 31P nuclear magnetic resonance spectroscopy, J Biol Chem, 265, 19434, 10.1016/S0021-9258(17)45391-9 Arnarez, 2013, Identification of cardiolipin binding sites on cytochrome c oxidase at the entrance of proton channels, Sci Rep, 3, 1263, 10.1038/srep01263 Arnarez, 2013, Evidence for cardiolipin binding sites on the membrane-exposed surface of the cytochrome bc1, J Am Chem Soc, 135, 3112, 10.1021/ja310577u Planas-Iglesias, 2015, Cardiolipin interactions with proteins, Biophys J, 109, 1282, 10.1016/j.bpj.2015.07.034 Paradies, 2014, Oxidative stress, cardiolipin and mitochondrial dysfunction in nonalcoholic fatty liver disease, World J Gastroenterol, 20, 14205, 10.3748/wjg.v20.i39.14205 Iverson, 2004, The cardiolipin–cytochrome c interaction and the mitochondrial regulation of apoptosis, Arch Biochem Biophys, 423, 37, 10.1016/j.abb.2003.12.002 Zhang, 2002, Gluing the respiratory chain together: cardiolipin is required for supercomplex formation in the inner mitochondrial membrane, J Biol Chem, 277, 43553, 10.1074/jbc.C200551200 Zhang, 2005, Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria, J Biol Chem, 280, 29403, 10.1074/jbc.M504955200 Mejia, 2014, Mammalian cardiolipin biosynthesis, Chem Phys Lipids, 179, 11, 10.1016/j.chemphyslip.2013.10.001 Sullivan, 2017, Murine diet-induced obesity remodels cardiac and liver mitochondrial phospholipid acyl chains with differential effects on respiratory enzyme activity, J Nutr Biochem, 45, 94, 10.1016/j.jnutbio.2017.04.004 Schlame, 2006, Barth syndrome, a human disorder of cardiolipin metabolism, FEBS Lett, 580, 5450, 10.1016/j.febslet.2006.07.022 Simons, 2004, Model systems, lipid rafts, and cell membranes, Annu Rev Biophys Biomol Struct, 33, 269, 10.1146/annurev.biophys.32.110601.141803 Soula, 2012, Membrane microdomains emergence through non-homogeneous diffusion, BMC Biophys, 5, 6, 10.1186/2046-1682-5-6 Lingwood, 2010, Lipid rafts as a membrane-organizing principle, Science, 327, 46, 10.1126/science.1174621 Jessup, 2005, Membrane microdomain signaling: lipid rafts in biology and medicine, Immunol Cell Biol, 83, 10.1111/j.1440-1711.2005.01355.x Fan, 2010, Formation and regulation of lipid microdomains in cell membranes: theory, modeling, and speculation, FEBS Lett, 584, 1678, 10.1016/j.febslet.2009.10.051 Zheng, 2009, Mitochondria do not contain lipid rafts, and lipid rafts do not contain mitochondrial proteins, J Lipid Res, 50, 988, 10.1194/jlr.M800658-JLR200 Osman, 2011, Making heads or tails of phospholipids in mitochondria, J Cell Biol, 192, 7, 10.1083/jcb.201006159 Renner, 2011, Cardiolipin microdomains localize to negatively curved regions of Escherichia coli membranes, Proc Natl Acad Sci USA, 108, 6264, 10.1073/pnas.1015757108 Jouhet, 2013, Importance of the hexagonal lipid phase in biological membrane organization, Front Plant Sci, 4, 494, 10.3389/fpls.2013.00494 de Kruijff, 1981, Non-bilayer lipids and the inner mitochondrial membrane, Cell Biol Int, 559 Stepanyants, 2015, Cardiolipin's propensity for phase transition and its reorganization by dynamin-related protein 1 form a basis for mitochondrial membrane fission, Mol Biol Cell, 26, 3104, 10.1091/mbc.E15-06-0330 Beales, 2011, Single vesicle observations of the cardiolipin-cytochrome c interaction: induction of membrane morphology changes, Langmuir, 27, 6107, 10.1021/la104924c Maniti, 2008, Mitochondrial creatine kinase binding to phospholipid monolayers induces cardiolipin segregation, Biophys J, 96, 2428, 10.1016/j.bpj.2008.12.3911 Epand, 2007, Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins, J Mol Biol, 365, 968, 10.1016/j.jmb.2006.10.028 Trusova, 2010, Cytochrome c-lipid interactions: new insights from resonance energy transfer, Biophys J, 99, 1754, 10.1016/j.bpj.2010.06.017 Bogdanov, 2008, Lipids in the assembly of membrane proteins and organization of protein supercomplexes: implications for lipid-linked disorders, Subcell Biochem, 49, 197, 10.1007/978-1-4020-8831-5_8 Kuhlbrandt, 2015, Structure and function of mitochondrial membrane protein complexes, BMC Biol, 13, 1, 10.1186/s12915-015-0201-x Andersson, 2002, Fatty acid composition of skeletal muscle reflects dietary fat composition in humans, Am J Clin Nutr, 76, 1222, 10.1093/ajcn/76.6.1222 Schumann, 2011, Fatty acid and peptide profiles in plasma membrane and membrane rafts of PUFA supplemented RAW264.7 macrophages, PLoS One, 6, e24066, 10.1371/journal.pone.0024066 Huang, 2012, Saturated fatty acids activate TLR-mediated proinflammatory signaling pathways, J Lipid Res, 53, 2002, 10.1194/jlr.D029546 Almeida, 2005, Thermodynamics of membrane domains, Biochem Biophys Acta, 1720, 1, 10.1016/j.bbamem.2005.12.004 Pitman, 2004, Molecular-level organization of saturated and polyunsaturated fatty acids in a phosphatidylcholine bilayer containing cholesterol, Biochemistry, 43, 15318, 10.1021/bi048231w Simons, 2010, Revitalizing membrane rafts: new tools and insights, Nat Rev Mol Cell Biol, 11, 688, 10.1038/nrm2977 Crescenzo, 2015, Fat quality influences the obesogenic effect of high fat diets, Nutrients, 7, 9475, 10.3390/nu7115480 Ruiz-Ramirez, 2015, Cytochrome c release from rat liver mitochondria is compromised by increased saturated cardiolipin species induced by sucrose feeding, Am J Physiol Endocrinol Metab, 309, E777, 10.1152/ajpendo.00617.2014 Rajamoorthi, 2005, Packing and viscoelasticity of polyunsaturated ω-3 and ω-6 lipid bilayers as seen by 2H NMR and X-ray diffraction, J Am Chem Soc, 127, 1576, 10.1021/ja046453b Rockett, 2011, Membrane raft organization is more sensitive to disruption by (n-3) PUFA than nonraft organization in EL4 and B cells, J Nutr, 141, 1041, 10.3945/jn.111.138750 Claypool, 2008, Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane, J Cell Biol, 182, 937, 10.1083/jcb.200801152 Jiang, 2000, Absence of cardiolipin in the crd1 null mutant results in decreased mitochondrial membrane potential and reduced mitochondrial function, J Biol Chem, 275, 22387, 10.1074/jbc.M909868199 Gohil, 2004, Cardiolipin biosynthesis and mitochondrial respiratory chain function are interdependent, J Biol Chem, 279, 42612, 10.1074/jbc.M402545200 Dudek, 2013, Cardiolipin deficiency affects respiratory chain function and organization in an induced pluripotent stem cell model of Barth syndrome, Stem Cell Res, 11, 806, 10.1016/j.scr.2013.05.005 Kiebish, 2013, Dysfunctional cardiac mitochondrial bioenergetic, lipidomic, and signaling in a murine model of Barth syndrome, J Lipid Res, 54, 1312, 10.1194/jlr.M034728 Baile, 2014, Unremodeled and remodeled cardiolipin are functionally indistinguishable in yeast, J Biol Chem, 289, 1768, 10.1074/jbc.M113.525733 Ye, 2016, Cardiolipin remodeling: a regulatory hub for modulating cardiolipin metabolism and function, J Bioenerg Biomembr, 48, 113, 10.1007/s10863-014-9591-7 Cocco, 1999, Arachidonic acid interaction with the mitochondrial electron transport chain promotes reactive oxygen species generation, Free Radic Biol Med, 27, 51, 10.1016/S0891-5849(99)00034-9 Khairallah, 2012, Improved mitochondrial function with diet-induced increase in either docosahexaenoic acid or arachidonic acid in membrane phospholipids, PLoS One, 7, e34402, 10.1371/journal.pone.0034402 Scorrano, 2001, Arachidonic acid causes cell death through the mitochondrial permeability transition: implications for tumor necrosis factor-a apoptotic signaling, J Biol Chem, 276, 12035, 10.1074/jbc.M010603200 Simopoulos, 2016, An increase in the omega-6/omega-3 fatty acid ratio increases the risk for obesity, Nutrients, 8, 128, 10.3390/nu8030128 Liu, 2013, A high ratio of dietary n-3/n-6 polyunsaturated fatty acids improves obesity-linked inflammation and insulin resistance through suppressing activation of TLR4 in SD rats, Nutr Res, 33, 849, 10.1016/j.nutres.2013.07.004 Russo, 2009, Dietary n−6 and n−3 polyunsaturated fatty acids: from biochemistry to clinical implications in cardiovascular prevention, Biochem Pharmacol, 77, 937, 10.1016/j.bcp.2008.10.020 Shaikh, 2015, How polyunsaturated fatty acids modify molecular organization in membranes: insight from NMR studies of model systems, Biochem Biophys Acta, 1848, 211, 10.1016/j.bbamem.2014.04.020 Stulnig, 2001, Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition, J Biol Chem, 276, 37335, 10.1074/jbc.M106193200 Schley, 2007, (n-3) PUFAs alter raft lipid composition and decrease epidermal growth factor receptor levels in lipid rafts of human breast cancer cells, J Nutr, 137, 548, 10.1093/jn/137.3.548 Shaikh, 2012, Biophysical and biochemical mechanisms by which dietary n-3 polyunsaturated fatty acids from fish oil disrupt membrane lipid rafts, J Nutr Biochem, 23, 101, 10.1016/j.jnutbio.2011.07.001 Kucerka, 2010, Cholesterol in bilayers with PUFA chains: doping with DMPC or POPC results in sterol reorientation and membrane-domain formation, Biochemistry, 49, 7485, 10.1021/bi100891z Li, 2005, Docosahexaenoic acid changes lipid composition and interleukin-2 receptor signaling in membrane rafts, J Lipid Res, 46, 1904, 10.1194/jlr.M500033-JLR200 Turk, 2013, Membrane lipid raft organization is uniquely modified by n-3 polyunsaturated fatty acids, Prostaglandins Leukot Essent Fatty Acids, 88, 43, 10.1016/j.plefa.2012.03.008 Ting, 2015, Polyunsaturated fatty acids incorporation into cardiolipin in H9c2 cardiac myoblast, J Nutr Biochem, 26, 769, 10.1016/j.jnutbio.2015.02.005 Forman, 1997, Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta, Proc Natl Acad Sci USA, 94, 4312, 10.1073/pnas.94.9.4312 Varga, 2011, PPARs are a unique set of fatty acid regulated transcription factors controlling both lipid metabolism and inflammation, Biochim Biophys Acta, 1812, 1007, 10.1016/j.bbadis.2011.02.014 Tanaka, 2003, Activation of peroxisome proliferator-activated receptor delta induces fatty acid beta-oxidation in skeletal muscle and attenuates metabolic syndrome, Proc Natl Acad Sci USA, 100, 15924, 10.1073/pnas.0306981100 Braissant, 1996, Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha, -beta, and -gamma in the adult rat, Endocrinology, 137, 354, 10.1210/endo.137.1.8536636 Brun, 1996, Differential activation of adipogenesis by multiple PPAR isoforms, Genes Dev, 10, 974, 10.1101/gad.10.8.974 Széles, 2007, PPARγ in immunity and inflammation: cell types and diseases, Biochim Biophys Acta, 1771, 1014, 10.1016/j.bbalip.2007.02.005 Mandard, 2004, Peroxisome proliferator-activated receptor alpha target genes, Cell Mol Life Sci, 61, 393, 10.1007/s00018-003-3216-3 Hancock, 2008, High-fat diets cause insulin resistance despite an increase in muscle mitochondria, Proc Natl Acad Sci USA, 105, 7815, 10.1073/pnas.0802057105 Jorgensen, 2015, One-year high fat diet affects muscle-but not brain mitochondria, J Cereb Blood Flow Metab, 35, 943, 10.1038/jcbfm.2015.27 Kakimoto, 2016, Effects of high fat diets on rodent liver bioenergetics and oxidative imbalance, Redox Biol, 8, 216, 10.1016/j.redox.2016.01.009 Stillwell, 1997, Effect of docosahexaenoic acid on mouse mitochondrial membrane properties, Lipids, 32, 497, 10.1007/s11745-997-0064-6 Pennington, 2017, Distinct membrane properties are differentially influenced by cardiolipin content and acyl chain composition in biomimetic membranes, Biochim Biophys Acta, 1859, 257, 10.1016/j.bbamem.2016.11.012 Sullivan, 2018, Docosahexaenoic acid lowers cardiac mitochondrial enzyme activity by replacing linoleic acid in the phospholipidome, J Biol Chem, 293, 466, 10.1074/jbc.M117.812834 Herbst, 2014, Omega-3 supplementation alters mitochondrial membrane composition and respiration kinetics in human skeletal muscle, J Physiol, 592, 1341, 10.1113/jphysiol.2013.267336 Khairallah, 2010, Dietary supplementation with docosahexaenoic acid, but not eicosapentaenoic acid, dramatically alters cardiac mitochondrial phospholipid fatty acid composition and prevents permeability transition, Biochim Biophys Acta, 1797, 1555, 10.1016/j.bbabio.2010.05.007 Hong, 2002, Fish oil increases mitochondrial phospholipid unsaturation, upregulating reactive oxygen species and apoptosis in rat colonocytes, Carcinogenesis, 23, 1919, 10.1093/carcin/23.11.1919 Malis, 1990, Incorporation of marine lipids into mitochondrial membranes increases susceptibility to damage by calcium and reactive oxygen species: evidence for enhanced activation of phospholipase A2 in mitochondria enriched with n-3 fatty acids, Proc Natl Acad Sci USA, 87, 8845, 10.1073/pnas.87.22.8845 Chapkin, 2002, Dietary n-3 PUFA alter colonocyte mitochondrial membrane composition and function, Lipids, 37, 193, 10.1007/s11745-002-0880-8 Aoun, 2012, Rat liver mitochondrial membrane characteristics and mitochondrial functions are more profoundly altered by dietary lipid quantity than by dietary lipid quality: effect of different nutritional lipid patterns, Br J Nutr, 107, 647, 10.1017/S000711451100331X Chen, 2003, Production of reactive oxygen species by mitochondria: central role of complex III, J Biol Chem, 278, 36027, 10.1074/jbc.M304854200 Brand, 2004, Mitochondrial superoxide: production, biological effects, and activation of uncoupling proteins, Free Radic Biol Med, 37, 755, 10.1016/j.freeradbiomed.2004.05.034 Watkins, 1998, Docosahexaenoic acid accumulates in cardiolipin and enhances HT-29 cell oxidant production, J Lipid Res, 39, 1583, 10.1016/S0022-2275(20)32186-6 McLean, 1993, Role of lipid structure in the activation of phospholipase A2 by peroxidized phospholipids, Lipids, 28, 505, 10.1007/BF02536081 Abdukeyum, 2016, Up-regulation of mitochondrial antioxidant superoxide dismutase underpins persistent cardiac nutritional-preconditioning by long chain n-3 polyunsaturated fatty acids in the rat, J Clin Med, 5, 10.3390/jcm5030032 Di Nunzio, 2011, Pro- and anti-oxidant effects of polyunsaturated fatty acid supplementation in HepG2 cells, Prostaglandins Leukot Essent Fatty Acids, 85, 121, 10.1016/j.plefa.2011.07.005 Anderson, 2011, Aldehyde stress and up-regulation of Nrf2-mediated antioxidant systems accompany functional adaptations in cardiac mitochondria from mice fed n-3 polyunsaturated fatty acids, Biochem J, 441, 359, 10.1042/BJ20110626 Giordano, 2014, Long-chain omega 3 fatty acids: molecular bases of potential antioxidant actions, Prostaglandins Leukot Essent Fatty Acids, 90, 1, 10.1016/j.plefa.2013.11.002 Richard, 2009, Docosahexaenoic acid down-regulates endothelial Nox 4 through a sPLA2 signalling pathway, Biochem Biophys Res Commun, 389, 516, 10.1016/j.bbrc.2009.09.013 Fry, 1981, Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain, J Biol Chem, 256, 1874, 10.1016/S0021-9258(19)69888-1 Hunte, 2003, Protonmotive pathways and mechanisms in the cytochrome bc1 complex, FEBS Lett, 545, 39, 10.1016/S0014-5793(03)00391-0 Robinson, 1982, Specificity and binding affinity of phospholipids to the high-affinity cardiolipin sites of beef heart cytochrome c oxidase, Biochemistry, 21, 184, 10.1021/bi00530a031 Robinson, 1993, Functional binding of cardiolipin to cytochrome c oxidase, J Bioenerg Biomembr, 25, 153, 10.1007/BF00762857 Sedlak, 1999, Phospholipase A2 digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure, Biochemistry, 38, 14966, 10.1021/bi9914053 Sedlak, 2006, Photolabeling of cardiolipin binding subunits within bovine heart cytochrome c oxidase, Biochemistry, 45, 746, 10.1021/bi050870z Paumard, 2002, The ATP synthase is involved in generating mitochondrial cristae morphology, EMBO J, 21, 221, 10.1093/emboj/21.3.221 Acehan, 2011, Cardiolipin affects the supramolecular organization of ATP synthase in mitochondria, Biophys J, 100, 2184, 10.1016/j.bpj.2011.03.031 Milenkovic, 2017, The enigma of the respiratory chain supercomplex, Cell Metab, 25, 765, 10.1016/j.cmet.2017.03.009 Gonzalvez, 2013, Barth syndrome: cellular compensation of mitochondrial dysfunction and apoptosis inhibition due to changes in cardiolipin remodeling linked to tafazzin (TAZ) gene mutation, Biochim Biophys Acta, 1832, 1194, 10.1016/j.bbadis.2013.03.005 McKenzie, 2006, Mitochondrial respiratory chain supercomplexes are destabilized in Barth syndrome patients, J Mol Biol, 361, 462, 10.1016/j.jmb.2006.06.057 Luo, 2009, c-Jun DNAzymes inhibit myocardial inflammation, ROS generation, infarct size, and improve cardiac function after ischemia-reperfusion injury, Arterioscler Thromb Vasc Biol, 29, 1836, 10.1161/ATVBAHA.109.189753 Hu, 2015, Protective effects of tanshinone IIA on myocardial ischemia reperfusion injury by reducing oxidative stress, HMGB1 expression, and inflammatory reaction, Pharm Biol, 53, 1752, 10.3109/13880209.2015.1005753 Asada, 2016, Tolerance to ischemia reperfusion injury in a congenital heart disease model, Pediatr Int, 58, 1266, 10.1111/ped.13022 Farias, 2017, Polyunsaturated fatty acid induces cardioprotection against ischemia-reperfusion through the inhibition of NF-kappaB and induction of Nrf2, Exp Biol Med, 242, 1104, 10.1177/1535370216649263 Madingou, 2016, Comparison of the effects of EPA and DHA alone or in combination in a murine model of myocardial infarction, Prostaglandins Leukot Essent Fatty Acids, 111, 11, 10.1016/j.plefa.2016.06.001 McMillin, 1992, Influence of dietary fish oil on mitochondrial function and response to ischemia, Am J Physiol Heart Circ Physiol, 263, H1479, 10.1152/ajpheart.1992.263.5.H1479 Castillo, 2014, Omega 3 chronic supplementation attenuates myocardial ischaemia-reperfusion injury through reinforcement of antioxidant defense system in rats, Cell Biochem Funct, 32, 274, 10.1002/cbf.3012 Gao, 2015, Marine n-3 PUFA protects hearts from I/R injury via restoration of mitochondrial function, Scand Cardiovasc J, 49, 264, 10.3109/14017431.2015.1071873 Burban, 2016, An intravenous bolus of EPA:DHA 6:1 protects against myocardial ischemia-reperfusion-induced shock, Shock, 46, 549, 10.1097/SHK.0000000000000624 Richard, 2014, Infusion of docosahexaenoic acid protects against myocardial infarction, Prostaglandins Leukot Essent Fatty Acids, 90, 139, 10.1016/j.plefa.2014.01.001 Stanley, 2012, Update on lipids and mitochondrial function: impact of dietary n-3 polyunsaturated fatty acids, Curr Opin Clin Nutr Metab Care, 15, 122, 10.1097/MCO.0b013e32834fdaf7 O'Shea, 2009, Dietary ω-3 fatty acids alter cardiac mitochondrial phospholipid composition and delay Ca2+-induced permeability transition, J Mol Cell Cardiol, 47, 819, 10.1016/j.yjmcc.2009.08.014 Michas, 2014, Dietary fats and cardiovascular disease: putting together the pieces of a complicated puzzle, Atherosclerosis, 234, 320, 10.1016/j.atherosclerosis.2014.03.013 Pinel, 2016, EPA prevents fat mass expansion and metabolic disturbances in mice fed with a Western diet, J Lipid Res, 57, 1382, 10.1194/jlr.M065458 Pinel, 2014, n-3 Polyunsaturated fatty acids modulate metabolism of insulin-sensitive tissues: implication for the prevention of type 2 diabetes, J Physiol Biochem, 70, 647, 10.1007/s13105-013-0303-2 Lorente-Cebrian, 2013, Role of omega-3 fatty acids in obesity, metabolic syndrome, and cardiovascular diseases: a review of the evidence, J Physiol Biochem, 69, 633, 10.1007/s13105-013-0265-4 Ovide-Bordeaux, 2004, Docosahexaenoic acid affects insulin deficiency- and insulin resistance-induced alterations in cardiac mitochondria, Am J Physiol Regul Integr Comp Physiol, 286, R519, 10.1152/ajpregu.00303.2003 Janovská, 2013, Anti-obesity effect of n-3 polyunsaturated fatty acids in mice fed high-fat diet is independent of cold-induced thermogenesis, Physiol Res, 62, 153, 10.33549/physiolres.932464 Ruzickova, 2004, Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue, Lipids, 39, 1177, 10.1007/s11745-004-1345-9 Damsgaard, 2013, n-3 PUFA status in school children is associated with beneficial lipid profile, reduced physical activity and increased blood pressure in boys, Br J Nutr, 110, 1304, 10.1017/S0007114513000585 Rockett, 2012, High dose of an n-3 polyunsaturated fatty acid diet lowers activity of C57BL/6 mice, Prostaglandins Leukot Essent Fatty Acids, 86, 137, 10.1016/j.plefa.2011.12.001 Han, 2005, Shotgun lipidomics identifies cardiolipin depletion in diabetic myocardium linking altered substrate utilization with mitochondrial dysfunction, Biochemistry, 44, 16684, 10.1021/bi051908a Han, 2007, Alterations in myocardial cardiolipin content and composition occur at the very earliest stages of diabetes: a shotgun lipidomics study, Biochemistry, 46, 6417, 10.1021/bi7004015 Rinella, 2015, Nonalcoholic fatty liver disease: a systematic review, J Am Med Assoc, 313, 2263, 10.1001/jama.2015.5370 Nair, 2003, Hepatic ATP reserve and efficiency of replenishing, Am J Gastroenterol, 98, 466 Pessayre, 2007, Role of mitochondria in non-alcoholic fatty liver disease, J Gastroenterol Hepatol, 22, S20, 10.1111/j.1440-1746.2006.04640.x Rector, 2010, Mitochondrial dysfunction precedes insulin resistance and hepatic steatosis and contributes to the natural history of non-alcoholic fatty liver disease in an obese rodent model, J Hepatol, 52, 727, 10.1016/j.jhep.2009.11.030 Sanyal, 2001, Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities, Gastroenterology, 120, 1183, 10.1053/gast.2001.23256 Seki, 2002, In situ detection of lipid peroxidation and oxidative DNA damage in non-alcoholic fatty liver diseases, J Hepatol, 37, 56, 10.1016/S0168-8278(02)00073-9 Pérez-Carreras, 2003, Defective hepatic mitochondrial respiratory chain in patients with nonalcoholic steatohepatitis, Hepatology, 38, 999, 10.1002/hep.1840380426 Fromenty, 2004, The ins and outs of mitochondrial dysfunction in NASH, Diabetes Metab, 30, 121, 10.1016/S1262-3636(07)70098-8 Capanni, 2006, Prolonged n-3 polyunsaturated fatty acid supplementation ameliorates hepatic steatosis in patients with non-alcoholic fatty liver disease: a pilot study, Aliment Pharmacol Ther, 23, 1143, 10.1111/j.1365-2036.2006.02885.x de Castro, 2018, Non-alcoholic fatty liver disease and its treatment with n-3 polyunsaturated fatty acids, Clin Nutr, 37, 37, 10.1016/j.clnu.2017.01.006 Di Minno, 2012, Omega-3 fatty acids for the treatment of non-alcoholic fatty liver disease, World J Gastroenterol, 18, 5839, 10.3748/wjg.v18.i41.5839 Dongiovanni, 2016, Nutritional therapy for nonalcoholic fatty liver disease, J Nutr Biochem, 29, 1, 10.1016/j.jnutbio.2015.08.024 Masterton, 2010, Review article: omega-3 fatty acids—a promising novel therapy for non-alcoholic fatty liver disease, Aliment Pharmacol Ther, 31, 679, 10.1111/j.1365-2036.2009.04230.x Scorletti, 2013, Omega-3 fatty acids, hepatic lipid metabolism, and nonalcoholic fatty liver disease, Annu Rev Nutr, 33, 231, 10.1146/annurev-nutr-071812-161230 Shapiro, 2011, The therapeutic potential of long-chain omega-3 fatty acids in nonalcoholic fatty liver disease, Clin Nutr, 30, 6, 10.1016/j.clnu.2010.06.001 Spadaro, 2008, Effects of n-3 polyunsaturated fatty acids in subjects with nonalcoholic fatty liver disease, Dig Liver Dis, 40, 194, 10.1016/j.dld.2007.10.003 Tapia, 2014, n-3 Long-chain PUFA supplementation prevents high fat diet induced mouse liver steatosis and inflammation in relation to PPAR-α upregulation and NF-κB DNA binding abrogation, Mol Nutr Food Res, 58, 1333, 10.1002/mnfr.201300458 Valenzuela, 2011, The importance of the long-chain polyunsaturated fatty acid n-6/n-3 ratio in development of non-alcoholic fatty liver associated with obesity, Food Funct, 2, 644, 10.1039/c1fo10133a Nogueira, 2016, Omega-3 polyunsaturated fatty acids in treating non-alcoholic steatohepatitis: a randomized, double-blind, placebo-controlled trial, Clin Nutr, 35, 578, 10.1016/j.clnu.2015.05.001 Kelley, 2016, Treatment of nonalcoholic fatty liver disease with long-chain n-3 polyunsaturated fatty acids in humans, Metab Syndr Relat Disord, 14, 417, 10.1089/met.2016.0051 Zhang, 2011, Mitochondrial dysfunction during in vitro hepatocyte steatosis is reversed by omega-3 fatty acid–induced up-regulation of mitofusin 2, Metabolism, 60, 767, 10.1016/j.metabol.2010.07.026 Kolar, 2007, Docosahexaenoic acid and butyrate synergistically induce colonocyte apoptosis by enhancing mitochondrial Ca2+ accumulation, Cancer Res, 67, 5561, 10.1158/0008-5472.CAN-06-4716 Fan, 2003, Dietary (n-3) polyunsaturated fatty acids remodel mouse T-cell lipid rafts, J Nutr, 133, 1913, 10.1093/jn/133.6.1913 Arita, 2001, Mechanism of apoptosis in HL-60 cells induced by n-3 and n-6 polyunsaturated fatty acids, Biochem Pharmacol, 62, 821, 10.1016/S0006-2952(01)00723-7 Larsson, 2004, Dietary long-chain n-3 fatty acids for the prevention of cancer: a review of potential mechanisms, Am J Clin Nutr, 79, 935, 10.1093/ajcn/79.6.935 Harris, 2016, Membrane disordering by eicosapentaenoic acid in B lymphomas is reduced by elongation to docosapentaenoic acid as revealed with solid-state nuclear magnetic resonance spectroscopy of model membranes, J Nutr, 146, 1283, 10.3945/jn.116.231639 Davidson, 2004, Chemopreventive n-3 polyunsaturated fatty acids reprogram genetic signatures during colon cancer initiation and progression in the rat, Cancer Res, 64, 6797, 10.1158/0008-5472.CAN-04-1068 Schley, 2005, Mechanisms of omega-3 fatty acid-induced growth inhibition in MDA-MB-231 human breast cancer cells, Breast Cancer Res Treat, 92, 187, 10.1007/s10549-005-2415-z Ng, 2005, The role of docosahexaenoic acid in mediating mitochondrial membrane lipid oxidation and apoptosis in colonocytes, Carcinogenesis, 26, 1914, 10.1093/carcin/bgi163 Giros, 2009, Regulation of colorectal cancer cell apoptosis by the n-3 polyunsaturated fatty acids docosahexaenoic and eicosapentaenoic, Cancer Prev Res, 2, 732, 10.1158/1940-6207.CAPR-08-0197 Khatib, 2016, Reducing the burden of obesity-associated cancers with anti-inflammatory long-chain omega-3 polyunsaturated fatty acids, Prostaglandins Other Lipid Mediat, 125, 100, 10.1016/j.prostaglandins.2016.07.011 Serhan, 2015, The resolution code of acute inflammation: novel pro-resolving lipid mediators in resolution, Semin Immunol, 27, 200, 10.1016/j.smim.2015.03.004