Accumulation of reactive oxygen species (ROS) is known to promote cellular damage in multiple cell types. In skeletal muscle, ROS has been implicated in disuse-induced muscle atrophy. However, the molecular origin and mechanism of how disuse promotes ROS and muscle dysfunction remains unclear.
Recent Advances:
Recently, we implicated membrane lipids of mitochondria to be a potential source of ROS to promote muscle atrophy.
Critical Issues:
In this review, we discuss evidence that changes in mitochondrial lipids represent a physiologically relevant process by which disuse promotes mitochondrial electron leak and oxidative stress.
Future Directions:
We further discuss lipid hydroperoxides as a potential downstream mediator of ROS to induce muscle atrophy. Antioxid. Redox Signal. 38, 338–351.
Get full access to this article
View all access options for this article.
References
1.
AhnB, RanjitR, PremkumarP, et al.Mitochondrial oxidative stress impairs contractile function but paradoxically increases muscle mass via fibre branching. J Cachexia Sarcopenia Muscle, 2019; 10(2):411–428; doi: 10.1002/jcsm.12375
2.
AldiniG, OrioliM, RossoniG, et al.The carbonyl scavenger carnosine ameliorates dyslipidaemia and renal function in Zucker obese rats. J Cell Mol Med, 2011; 15(6):1339–1354; doi: 10.1111/j.1582-4934.2010.01101.x
3.
AndersonEJ, VistoliG, KatungaLA, et al.A carnosine analog mitigates metabolic disorders of obesity by reducing carbonyl stress. J Clin Invest, 2018; 128(12):5280–5293; doi: 10.1172/JCI94307
4.
ArandaR, DoménechE, Diana RusA, et al.Age-related increase in xanthine oxidase activity in human plasma and rat tissues. Free Radic Res, 2007; 41(11):1195–1200; doi: 10.1080/10715760701481461
5.
ArikkethD, NelsonR, VanceJE. Defining the importance of phosphatidylserine synthase-1 (PSS1). J Biol Chem, 2008; 283(19):12888–12897; doi: 10.1074/jbc.m800714200
6.
BakerCD, Basu BallW, PryceEN, et al.Specific requirements of nonbilayer phospholipids in mitochondrial respiratory chain function and formation. Mol Biol Cell, 2016; 27(14):2161–2171; doi: 10.1091/mbc.E15-12-0865
7.
BarjaG. Mitochondrial oxygen radical generation and leak: Sites of production in states 4 and 3, organ specificity, and relation to aging and longevity. J Bioenerg Biomembr, 1999; 31(4):347–366; doi: 10.1023/a:1005427919188
BergoMO, GavinoBJ, SteenbergenR, et al.Defining the importance of phosphatidylserine synthase 2 in mice. J Biol Chem, 2002; 277(49):47701–47708; doi: 10.1074/jbc.m207734200
10.
BhattacharyaA, HamiltonR, JerniganA, et al.Genetic ablation of 12/15-lipoxygenase but not 5-lipoxygenase protects against denervation-induced muscle atrophy. Free Radic Biol Med, 2014; 67:30–40; doi: 10.1016/j.freeradbiomed.2013.10.002
BiletL, PhielixE, van de WeijerT, et al.One-leg inactivity induces a reduction in mitochondrial oxidative capacity, intramyocellular lipid accumulation and reduced insulin signalling upon lipid infusion: A human study with unilateral limb suspension. Diabetologia, 2020; 63(6):1211–1222; doi: 10.1007/s00125-020-05128-1
13.
BirkAV, ChaoWM, BrackenC, et al.Targeting mitochondrial cardiolipin and the cytochrome c/cardiolipin complex to promote electron transport and optimize mitochondrial ATP synthesis. Br J Pharmacol, 2014; 171(8):2017–2028; doi: 10.1111/bph.12468
14.
BottingerL, HorvathSE, KleinschrothT, et al.Phosphatidylethanolamine and cardiolipin differentially affect the stability of mitochondrial respiratory chain supercomplexes. J Mol Biol, 2012; 423(5):677–686; doi: 10.1016/j.jmb.2012.09.001
15.
BoverisA, CadenasE. Mitochondrial production of superoxide anions and its relationship to the antimycin insensitive respiration. FEBS Lett, 1975; 54(3):311–314; doi: 10.1016/0014-5793(75)80928-8
16.
BoverisA, ChanceB. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J, 1973; 134(3):707–716; doi: 10.1042/bj1340707
17.
BoverisA, OshinoN, ChanceB. The cellular production of hydrogen peroxide. Biochem J, 1972; 128(3):617–630; doi: 10.1042/bj1280617
18.
CadenasE, BoverisA, RaganCI, et al.Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch Biochem Biophys, 1977; 180(2):248–257; doi: 10.1016/0003-9861(77)90035-2
19.
CalzadaE, AveryE, SamPN, et al.Phosphatidylethanolamine made in the inner mitochondrial membrane is essential for yeast cytochrome bc1 complex function. Nat Commun, 2019; 10(1):1432; doi: 10.1038/s41467-019-09425-1
20.
ChenL, HambrightWS, NaR, et al.Ablation of the ferroptosis inhibitor glutathione peroxidase 4 in neurons results in rapid motor neuron degeneration and paralysis. J Biol Chem, 2015; 290(47):28097–28106; doi: 10.1074/jbc.m115.680090
21.
ConnerthM, TatsutaT, HaagM, et al.Intramitochondrial transport of phosphatidic acid in yeast by a lipid transfer protein. Science, 2012; 338(6108):815–818; doi: 10.1126/science.1225625
22.
CortieCH, HulbertAJ, HancockSE, et al.Of mice, pigs and humans: An analysis of mitochondrial phospholipids from mammals with very different maximal lifespans. Exp Gerontol, 2015; 70:135–143; doi: 10.1016/j.exger.2015.08.011
23.
DaumG, VanceJE. Import of lipids into mitochondria. Prog Lipid Res, 1997; 36(2):103–130; doi: 10.1016/S0163-7827(97)00006-4
24.
DixonSJ, PatelDN, WelschM, et al.Pharmacological inhibition of cystine-glutamate exchange induces endoplasmic reticulum stress and ferroptosis. Elife, 2014; 3:e02523; doi: 10.7554/eLife.02523
25.
Do VanB, GouelF, JonneauxA, et al.Ferroptosis, a newly characterized form of cell death in Parkinson's disease that is regulated by PKC. Neurobiol Dis, 2016; 94:169–178; doi: 10.1016/j.nbd.2016.05.011
26.
DoddSL, GagnonBJ, SenfSM, et al.Ros-mediated activation of NF-kappaB and Foxo during muscle disuse. Muscle Nerve, 2010; 41(1):110–113; doi: 10.1002/mus.21526
27.
Dupont-VersteegdenEE. Apoptosis in skeletal muscle and its relevance to atrophy. World J Gastroenterol, 2006; 12(46):7463–7466; doi: 10.3748/wjg.v12.i46.7463
28.
EshimaH, SiripoksupP, MahmassaniZS, et al.Neutralizing mitochondrial ROS does not rescue muscle atrophy induced by hindlimb unloading in female mice. J Appl Physiol (1985), 2020; 129(1):124–132; doi: 10.1152/japplphysiol.00456.2019
29.
EshimaH, SiripoksupP, ShahtoutJ, et al. Lipid hydroperoxides promote muscle atrophy through lysosomal amplification. BioRxiv 2021; [Epub ahead of print]; doi: 10.1101/2021.12.17.473200
30.
FajardoVA, MikhaeilJS, LeveilleCF, et al.Cardiolipin content, linoleic acid composition, and tafazzin expression in response to skeletal muscle overload and unload stimuli. Sci Rep, 2017; 7(1):2060; doi: 10.1038/s41598-017-02089-1
31.
FengG, ZhangZ, BaoQ, et al.Protective effect of chinonin in MPTP-induced C57BL/6 mouse model of Parkinson's Disease. Biol Pharm Bull, 2014; 37(8):1301–1307; doi: 10.1248/bpb.b14-00128
32.
FryM, GreenDE. Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. J Biol Chem, 1981; 256(4):1874–1880.
33.
FunaiK, LodhiIJ, SpearsLD, et al.Skeletal muscle phospholipid metabolism regulates insulin sensitivity and contractile function. Diabetes, 2016; 65(2):358–370; doi: 10.2337/db15-0659
34.
FunaiK, SummersSA, RutterJ. Reign in the membrane: How common lipids govern mitochondrial function. Curr Opin Cell Biol, 2020; 63:162–173; doi: 10.1016/j.ceb.2020.01.006
35.
GirishaKM, Von ElsnerL, NeethukrishnaK, et al.The homozygous variant c.797G>A/p.(Cys266Tyr) in PISD is associated with a Spondyloepimetaphyseal dysplasia with large epiphyses and disturbed mitochondrial function. Hum Mutat, 2019; 40(3):299–309; doi: 10.1002/humu.23693
36.
GoncalvesRLS, SchlameM, BarteltA, et al.Cardiolipin deficiency in Barth syndrome is not associated with increased superoxide/H2O2 production in heart and skeletal muscle mitochondria. FEBS Lett, 2021; 595(3):415–432; doi: 10.1002/1873-3468.13973
37.
GramM, VigelsoA, YokotaT, et al.Two weeks of one-leg immobilization decreases skeletal muscle respiratory capacity equally in young and elderly men. Exp Gerontol, 2014; 58:269–278; doi: 10.1016/j.exger.2014.08.013
38.
GuoJ, XuB, HanQ, et al.Ferroptosis: A novel anti-tumor action for cisplatin. Cancer Res Treat, 2018; 50(2):445–460; doi: 10.4143/crt.2016.572
39.
HambrightWS, FonsecaRS, ChenL, et al.Ablation of ferroptosis regulator glutathione peroxidase 4 in forebrain neurons promotes cognitive impairment and neurodegeneration. Redox Biol, 2017; 12:8–17; doi: 10.1016/j.redox.2017.01.021
40.
HedenT, JohnsonJ, FerraraP, et al.Mitochondrial PE potentiates respiratory enzymes to amplify skeletal muscle aerobic capacity. Sci Adv, 2019; 5(9):eaax8352; doi: 10.1126/sciadv.aax8352
HishikawaD, ShindouH, KobayashiS, et al.Discovery of a lysophospholipid acyltransferase family essential for membrane asymmetry and diversity. Proc Natl Acad Sci U S A, 2008; 105(8):2830–2835; doi: 10.1073/pnas.0712245105
43.
HoribataY, SugimotoH. StarD7 mediates the intracellular trafficking of phosphatidylcholine to mitochondria. J Biol Chem, 2010; 285(10):7358–7365; doi: 10.1074/jbc.M109.056960
HsuJ-L, HsiehY, TuC, et al.Catalytic properties of human manganese superoxide dismutase. J Biol Chem, 1996; 271(30):17687–17691; doi: 10.1074/jbc.271.30.17687
46.
HussainSN, MatarG, BarreiroE, et al.Modifications of proteins by 4-hydroxy-2-nonenal in the ventilatory muscles of rats. Am J Physiol Lung Cell Mol Physiol, 2006; 290(5):L996–L1003; doi: 10.1152/ajplung.00337.2005
47.
IadarolaDM, JoshiA, CaldwellCB, et al.Choline restores respiration in Psd1-deficient yeast by replenishing mitochondrial phosphatidylethanolamine. J Biol Chem, 2021; 296:100539; doi: 10.1016/j.jbc.2021.100539
JiangB, LeL, PanH, et al.Dihydromyricetin ameliorates the oxidative stress response induced by methylglyoxal via the AMPK/GLUT4 signaling pathway in PC12 cells. Brain Res Bull, 2014; 109:117–126; doi: 10.1016/j.brainresbull.2014.10.010
51.
JohnsonJM, FerraraPJ, VerkerkeARP, et al.Targeted overexpression of catalase to mitochondria does not prevent cardioskeletal myopathy in Barth syndrome. J Mol Cell Cardiol, 2018; 121:94–102; doi: 10.1016/j.yjmcc.2018.07.001
52.
KaganVE, MaoG, QuF, et al.Oxidized arachidonic and adrenic PEs navigate cells to ferroptosis. Nat Chem Biol, 2017; 13(1):81–90; doi: 10.1038/nchembio.2238
53.
KatungaLA, GudimellaP, EfirdJT, et al.Obesity in a model of gpx4 haploinsufficiency uncovers a causal role for lipid-derived aldehydes in human metabolic disease and cardiomyopathy. Mol Metab, 2015; 4(6):493–506; doi: 10.1016/j.molmet.2015.04.001
54.
KennedyEP, WeissSB. The function of cytidine coenzymes in the biosynthesis of phospholipides. J Biol Chem, 1956; 222(1):193–214.
55.
KonstorumA, TesfayL, PaulBT, et al.Systems biology of ferroptosis: A modeling approach. J Theor Biol, 2020; 493:110222; doi: 10.1016/j.jtbi.2020.110222
56.
LachaierE, LouandreC, GodinC, et al.Sorafenib induces ferroptosis in human cancer cell lines originating from different solid tumors. Anticancer Res, 2014; 34(11):6417–6422.
57.
LandsWE. Metabolism of glycerolipides; a comparison of lecithin and triglyceride synthesis. J Biol Chem, 1958; 231(2):883–888.
58.
LarsenS, NielsenJ, HansenCN, et al.Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects. J Physiol, 2012; 590(14):3349–3360; doi: 10.1113/jphysiol.2012.230185
59.
LawlerJM, HordJM, RyanP, et al.Nox2 inhibition regulates stress response and mitigates skeletal muscle fiber atrophy during simulated microgravity. Int J Mol Sci, 2021; 22(6):3252; doi: 10.3390/ijms22063252
60.
LeeH, HaTY, JungCH, et al.Mitochondrial dysfunction in skeletal muscle contributes to the development of acute insulin resistance in mice. J Cachexia Sarcopenia Muscle, 2021; 12(6):1925–1939; doi: 10.1002/jcsm.12794
61.
LeeS, NorheimF, GulsethHL, et al.Skeletal muscle phosphatidylcholine and phosphatidylethanolamine respond to exercise and influence insulin sensitivity in men. Sci Rep, 2018; 8(1):6531; doi: 10.1038/s41598-018-24976-x
62.
LeermakersPA, KneppersAEM, ScholsA, et al.Skeletal muscle unloading results in increased mitophagy and decreased mitochondrial biogenesis regulation. Muscle Nerve, 2019; 60(6):769–778; doi: 10.1002/mus.26702
63.
LouW, ReynoldsCA, LiY, et al.Loss of tafazzin results in decreased myoblast differentiation in C2C12 cells: A myoblast model of Barth syndrome and cardiolipin deficiency. Biochim Biophys Acta, 2018; 1863(8):857–865; doi: 10.1016/j.bbalip.2018.04.015
64.
MayrJA, HaackTB, GrafE, et al.Lack of the mitochondrial protein acylglycerol kinase causes Sengers syndrome. Am J Hum Genet, 2012; 90(2):314–320; doi: 10.1016/j.ajhg.2011.12.005
65.
McLeanJB, MoylanJS, AndradeFH. Mitochondria dysfunction in lung cancer-induced muscle wasting in C2C12 myotubes. Front Physiol, 2014; 5:503; doi: 10.3389/fphys.2014.00503
66.
MejiaEM, IbdahJA, SparagnaGC, et al.Differential reduction in cardiac and liver monolysocardiolipin acyltransferase-1 and reduction in cardiac and liver tetralinoleoyl-cardiolipin in the α-subunit of trifunctional protein heterozygous knockout mice. Biochem J, 2015; 471(1):123–129; doi: 10.1042/bj20150648
MendhamAE, GoedeckeJH, ZengY, et al.Exercise training improves mitochondrial respiration and is associated with an altered intramuscular phospholipid signature in women with obesity. Diabetologia, 2021; 64(7):1642–1659; doi: 10.1007/s00125-021-05430-6
69.
MeniniS, IacobiniC, RicciC, et al.D-Carnosine octylester attenuates atherosclerosis and renal disease in ApoE null mice fed a Western diet through reduction of carbonyl stress and inflammation. Br J Pharmacol, 2012; 166(4):1344–1356; doi: 10.1111/j.1476-5381.2012.01834.x
MiroO, CasademontJ, CasalsE, et al.Aging is associated with increased lipid peroxidation in human hearts, but not with mitochondrial respiratory chain enzyme defects. Cardiovasc Res, 2000;(47):624–631; doi: 10.1016/s0008-6363(00)00122-x
MullerFL, LiuY, Van RemmenH. Complex III releases superoxide to both sides of the inner mitochondrial membrane. J Biol Chem, 2004; 279(47):49064–49073; doi: 10.1074/jbc.M407715200
74.
MullerFL, SongW, JangYC, et al.Denervation-induced skeletal muscle atrophy is associated with increased mitochondrial ROS production. Am J Physiol Regul Integr Comp Physiol, 2007; 293(3):R1159–R1168; doi: 10.1152/ajpregu.00767.2006
75.
OhtsukaT, NishijimaM, SuzukiK, et al.Mitochondrial dysfunction of a cultured Chinese hamster ovary cell mutant deficient in cardiolipin. J Biol Chem, 1993; 268(30):22914–22919.
76.
PandeSV, MurthyMSR, NoëlH. Differential effects of phosphatidylcholine and cardiolipin on carnitine palmitoyltransferase activity. Biochim Biophys Acta, 1986; 877(2):223–230; doi: 10.1016/0005-2760(86)90298-5
77.
PangbornMC. Isolation and purification of a serologically active phospholipid from beef heart. J Biol Chem, 1942; 143(1):247–256; doi: 10.1016/s0021-9258(18)72683-5
78.
PenningtonER, FunaiK, BrownDA, et al.The role of cardiolipin concentration and acyl chain composition on mitochondrial inner membrane molecular organization and function. Biochim Biophys Acta, 2019; 1864(7):1039–1052; doi: 10.1016/j.bbalip.2019.03.012
79.
PereiraB, Costa RosaLFB, SafiDA, et al.Superoxide dismutase, catalase, and glutathione peroxidase activities in muscle and lymphoid organs of sedentary and exercise-trained rats. Physiol Behav, 1994; 56(5):1095–1099; doi: 10.1016/0031-9384(94)90349-2
80.
PeterVG, QuinodozM, Pinto-BastoJ, et al.The Liberfarb syndrome, a multisystem disorder affecting eye, ear, bone, and brain development, is caused by a founder pathogenic variant in the PISD gene. Gene Med, 2019; 21(12):2734–2743; doi: 10.1038/s41436-019-0595-x
81.
PharaohG, BrownJL, SataranatarajanK, et al.Targeting cPLA2 derived lipid hydroperoxides as a potential intervention for sarcopenia. Sci Reports, 2020; 10(1):13968; doi: 10.1038/s41598-020-70792-7
82.
PileggiCA, HedgesCP, D'SouzaRF, et al.Exercise recovery increases skeletal muscle H2O2 emission and mitochondrial respiratory capacity following two-weeks of limb immobilization. Free Radic Biol Med, 2018; 124:241–248; doi: 10.1016/j.freeradbiomed.2018.06.012
83.
PollardAK, OrtoriCA, StögerR, et al.Mouse mitochondrial lipid composition is defined by age in brain and muscle. Aging, 2017; 9(3):986–998; doi: 10.18632/aging.101204
RussoC, OlivieriO, GirelliD, et al.Anti-oxidant status and lipid peroxidation in patients with essential hypertension. J Hypertens, 1998; 16(9):1267–1271; doi: 10.1097/00004872-199816090-00007
88.
RyanMJ, JacksonJR, HaoY, et al.Inhibition of xanthine oxidase reduces oxidative stress and improves skeletal muscle function in response to electrically stimulated isometric contractions in aged mice. Free Radic Biol Med, 2011; 51(1):38–52; doi: 10.1016/j.freeradbiomed.2011.04.002
89.
SakellariouGK, PearsonT, LightfootAP, et al.Mitochondrial ROS regulate oxidative damage and mitophagy but not age-related muscle fiber atrophy. Sci Rep, 2016; 6:33944; doi: 10.1038/srep33944
90.
SamjooIA, SafdarA, HamadehMJ, et al.The effect of endurance exercise on both skeletal muscle and systemic oxidative stress in previously sedentary obese men. Nutr Diabetes, 2013; 3:e88; doi: 10.1038/nutd.2013.30
91.
ScalabrinM, PollockN, StauntonCA, et al.Redox responses in skeletal muscle following denervation. Redox Biol, 2019; 26:101294; doi: 10.1016/j.redox.2019.101294
92.
SchulerM-H, Di BartolomeoF, BöttingerL, et al.Phosphatidylcholine affects the role of the sorting and assembly machinery in the biogenesis of mitochondrial β-barrel proteins. J Biol Chem, 2015; 290(44):26523–26532; doi: 10.1074/jbc.m115.687921
93.
SchulerMH, Di BartolomeoF, MartenssonCU, et al.Phosphatidylcholine affects inner membrane protein translocases of mitochondria. J Biol Chem, 2016; 291(36):18718–18729; doi: 10.1074/jbc.M116.722694
94.
SelathuraiA, KowalskiGM, BurchML, et al.The CDP-ethanolamine pathway regulates skeletal muscle diacylglycerol content and mitochondrial biogenesis without altering insulin sensitivity. Cell Metab, 2015; 21(5):718–730; doi: 10.1016/j.cmet.2015.04.001
95.
SelathuraiA, KowalskiGM, MasonSA, et al.Phosphatidylserine decarboxylase is critical for the maintenance of skeletal muscle mitochondrial integrity and muscle mass. Mol Metab, 2019; 27:33–46; doi: 10.1016/j.molmet.2019.06.020
96.
SengersRC, TrijbelsJM, WillemsJL, et al.Congenital cataract and mitochondrial myopathy of skeletal and heart muscle associated with lactic acidosis after exercise. J Pediatr, 1975; 86(6):873–880; doi: 10.1016/s0022-3476(75)80217-4
97.
ShaikhSR, SullivanEM, AllemanRJ, et al.Increasing mitochondrial membrane phospholipid content lowers the enzymatic activity of electron transport complexes. Biochemistry, 2014; 53(35):5589–5591; doi: 10.1021/bi500868g
98.
SharpleyMS, ShannonRJ, DraghiF, et al.Interactions between phospholipids and NADH:Ubiquinone oxidoreductase (Complex I) from bovine mitochondria. Biochemistry, 2006; 45(1):241–248; doi: 10.1021/bi051809x
99.
SherRB, AoyamaC, HuebschKA, et al.A rostrocaudal muscular dystrophy caused by a defect in choline kinase beta, the first enzyme in phosphatidylcholine biosynthesis*. J Biol Chem, 2006; 281(8):4938–4948; doi: 10.1074/jbc.M512578200
100.
ShiaoY-J, LupoG, VanceJE. 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, 1995; 270(19):11190–11198; doi: 10.1074/jbc.270.19.11190
101.
Shinzawa-ItohK, AoyamaH, MuramotoK, et al.Structures and physiological roles of 13 integral lipids of bovine heart cytochrome c oxidase. EMBO J, 2007; 26(6):1713–1725; doi: 10.1038/sj.emboj.7601618
102.
SousaSB, JenkinsD, ChanudetE, et al.Gain-of-function mutations in the phosphatidylserine synthase 1 (PTDSS1) gene cause Lenz-Majewski syndrome. Nat Genet, 2014; 46(1):70–76; doi: 10.1038/ng.2829
103.
SpencerCT, ByrneBJ, BryantRM, et al.Impaired cardiac reserve and severely diminished skeletal muscle O(2) utilization mediate exercise intolerance in Barth syndrome. Am J Physiol Heart Circ Physiol, 2011; 301(5):H2122–H2129; doi: 10.1152/ajpheart.00479.2010
104.
SteenbergenR, NanowskiTS, BeigneuxA, et al.Disruption of the phosphatidylserine decarboxylase gene in mice causes embryonic lethality and mitochondrial defects. J Biol Chem, 2005; 280(48):40032–40040; doi: 10.1074/jbc.M506510200
105.
StefanykLE, CoverdaleN, RoyBD, et al.Skeletal muscle type comparison of subsarcolemmal mitochondrial membrane phospholipid fatty acid composition in rat. J Membr Biol, 2010; 234(3):207–215; doi: 10.1007/s00232-010-9247-4
106.
TaharaEB, NavareteFD, KowaltowskiAJ. Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radic Biol Med, 2009; 46(9):1283–1297; doi: 10.1016/j.freeradbiomed.2009.02.008
107.
TalbertEE, SmuderAJ, MinK, et al.Immobilization-induced activation of key proteolytic systems in skeletal muscles is prevented by a mitochondria-targeted antioxidant. J Appl Physiol (1985), 2013; 115(4):529–538; doi: 10.1152/japplphysiol.00471.2013
108.
TassevaG, BaiHD, DavidescuM, et al.Phosphatidylethanolamine deficiency in Mammalian mitochondria impairs oxidative phosphorylation and alters mitochondrial morphology. J Biol Chem, 2013; 288(6):4158–4173; doi: 10.1074/jbc.M112.434183
109.
TrevinoMB, ZhangX, StandleyRA, et al.Loss of mitochondrial energetics is associated with poor recovery of muscle function but not mass following disuse atrophy. Am J Physiol Endocrinol Metab, 2019; 317(5):E899–E910; doi: 10.1152/ajpendo.00161.2019
110.
TsalouhidouS, ArgyrouC, TheofilidisG, et al.Mitochondrial phospholipids of rat skeletal muscle are less polyunsaturated than whole tissue phospholipids: Implications for protection against oxidative stress. J Anim Sci, 2006; 84(10):2818–2825; doi: 10.2527/jas.2006-031
111.
ValianpourF, MitsakosV, SchlemmerD, et al.Monolysocardiolipins accumulate in Barth syndrome but do not lead to enhanced apoptosis. J Lipid Res, 2005; 46(6):1182–1195; doi: 10.1194/jlr.M500056-JLR200
112.
Van MeerG, VoelkerDR, FeigensonGW. Membrane lipids: Where they are and how they behave. Nat Rev Mol Cell Biol, 2008; 9(2):112–124; doi: 10.1038/nrm2330
113.
VanceJE. MAM (mitochondria-associated membranes) in mammalian cells: Lipids and beyond. Biochim Biophys Acta, 2014; 1841(4):595–609; doi: 10.1016/j.bbalip.2013.11.014
114.
VerkerkeARP, FerraraPJ, LinC-T, et al.Phospholipid methylation regulates muscle metabolic rate through Ca2+ transport efficiency. Nat Metab, 2019; 1(9):876–885; doi: 10.1038/s42255-019-0111-2
115.
WangL, MagdalenoS, TabasI, et al.Early embryonic lethality in mice with targeted deletion of the CTP:phosphocholine cytidylyltransferase α gene (Pcyt1a). Mol Cell Biol, 2005; 25(8):3357–3363; doi: 10.1128/MCB.25.8.3357-3363.2005
116.
WardWF, QiW, Van RemmenH, et al.Effects of age and caloric restriction on lipid peroxidation: Measurement of oxidative stress by F2-isoprostane levels. J Gerontol A Biol Sci Med Sci, 2005; 60(7):847–851; doi: 10.1093/gerona/60.7.847
117.
WatanabeY, TamuraY, KawanoS, et al.Structural and mechanistic insights into phospholipid transfer by Ups1–Mdm35 in mitochondria. Nat Commun, 2015; 6(1):1–12.
118.
WilkinsonJA, SilveraS, LeblancPJ. The effect of cardiolipin side chain composition on cytochrome c protein conformation and peroxidase activity. Physiol Reports, 2021; 9(5):e14772; doi: 10.14814/phy2.14772
119.
WuG, AoyamaC, YoungSG, et al.Early embryonic lethality caused by disruption of the gene for choline kinase α, the first enzyme in phosphatidylcholine biosynthesis. J Biol Chem, 2008; 283(3):1456–1462; doi: 10.1074/jbc.m708766200
120.
WuG, SherRB, CoxGA, et al.Understanding the muscular dystrophy caused by deletion of choline kinase beta in mice. Biochim Biophys Acta, 2009; 1791(5):347–356; doi: 10.1016/j.bbalip.2009.02.006
121.
WüllnerU, LöschmannPA, SchulzJB, et al.Glutathione depletion potentiates MPTP and MPP+ toxicity in nigral dopaminergic neurones. Neuroreport, 1996; 7(4):921–923; doi: 10.1097/00001756-199603220-00018
122.
XuY, MalhotraA, RenM, et al.The enzymatic function of tafazzin. J Biol Chem, 2006; 281(51):39217–39224; doi: 10.1074/jbc.m606100200
123.
YangWS, SriRamaratnamR, WelschME, et al.Regulation of ferroptotic cancer cell death by GPX4. Cell, 2014; 156(1–2):317–331; doi: 10.1016/j.cell.2013.12.010
124.
YangWS, StockwellBR. Synthetic lethal screening identifies compounds activating iron-dependent, nonapoptotic cell death in oncogenic-RAS-harboring cancer cells. Chem Biol, 2008; 15(3):234–245; doi: 10.1016/j.chembiol.2008.02.010
125.
YavuzerH, YavuzerS, CengizM, et al.Biomarkers of lipid peroxidation related to hypertension in aging. Hypertens Res, 2016; 39(5):342–348; doi: 10.1038/pj.2016.37
YoshiharaT, NatsumeT, TsuzukiT, et al.Long-term physical inactivity exacerbates hindlimb unloading-induced muscle atrophy in young rat soleus muscle. J Appl Physiol (1985), 2021; 130(4):1214–1225; doi: 10.1152/japplphysiol.00494.2020
128.
ZhangM, MileykovskayaE, DowhanW. Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J Biol Chem, 2002; 277(46):43553–43556; doi: 10.1074/jbc.C200551200
129.
ZhangX, TrevinoMB, WangM, et al.Impaired mitochondrial energetics characterize poor early recovery of muscle mass following hind limb unloading in old mice. J Gerontol A Biol Sci Med Sci, 2018; 73(10):1313–1322; doi: 10.1093/gerona/gly051
130.
ZhaoT, GoedhartCM, SamPN, et al.PISD is a mitochondrial disease gene causing skeletal dysplasia, cataracts, and white matter changes. Life Sci Alliance, 2019; 2(2):e201900353; doi: 10.26508/lsa.201900353
131.
ZhaoY, ChenYQ, BonacciTM, et al.Identification and characterization of a major liver lysophosphatidylcholine acyltransferase. J Biol Chem, 2008; 283(13):8258–8265; doi: 10.1074/jbc.M710422200
132.
ZhuangA, YangC, LiuY, et al.SOD2 in skeletal muscle: New insights from an inducible deletion model. Redox Biol, 2021; 47:102135; doi: 10.1016/j.redox.2021.102135
