Cardiolipin (CL) is a unique phospholipid that is almost exclusively localized at the level of the inner mitochondrial membrane (IMM), where it is biosynthesized. This phospholipid is associated with membranes which are designed to generate an electrochemical gradient that is used to produce ATP. Such membranes include the bacterial plasma membrane and IMM. This ubiquitous and intimate association between CL and energy-transducing membranes suggests an important role for CL in mitochondrial bioenergetic processes. CL has been shown to interact with a number of IMM proteins, including the respiratory chain complexes and substrate carriers. Moreover, CL is involved in different stages of the mitochondrial apoptosis process as well as in mitochondrial membrane stability and dynamics. Alterations in CL structure, content, and acyl chain composition have been associated with mitochondrial dysfunction in multiple tissues in several physiopathological conditions and aging. In this review, we provide an overview of the roles of CL in mitochondrial function and bioenergetics in health and disease. Antioxid. Redox Signal. 20, 1925–1953.
AcehanD, MalhotraA, XuY, RenM, StokesDL, and SchlameM. Cardiolipin affects the supramolecular organization of ATP synthase in mitochondria. Biophys J, 100: 2184–2192, 2011.
2.
AcehanD, VazF, HoutkooperRH, JamesJ, MooreV, TokunagaC, KulikW, WansapuraJ, TothMJ, StraussA, and KhuchuaZ. Cardiac and skeletal muscle defects in a mouse model of human Barth syndrome. J Biol Chem, 286: 899–908, 2011.
3.
Acín-PérezR, Fernández-SilvaP, PeleatoML, Pérez-MartosA, and EnriquezJA. Respiratory active mitochondrial supercomplexes. Mol Cell, 32: 529–539, 2008.
4.
AdamsJM and CoryS. The Bcl-2 protein family: arbiters of cell survival. Science, 281: 1322–1326, 1998.
5.
AldakkakM, StoweDF, DashRK, and CamaraAK. Mitochondrial handling of excess Ca2+ is substrate-dependent with implications for reactive oxygen species generation. Free Radic Biol Med, 56: 193–203, 2013.
6.
AllenRD, SchroederCC, and FokAK. An investigation of mitochondrial inner membranes by rapid-freeze deep-etch techniques. J Cell Biol, 108: 2233–2240, 1989.
7.
AmbrosioG, ZweierJL, and FlahertyJT. The relationship between oxygen radical generation and impairment of myocardial energy metabolism following post-ischemic reperfusion. J Mol Cell Cardiol, 12: 1359–1374, 1991.
8.
ArdailD, PrivatJP, Egret-CharlierM, LevratC, LermeF, and LouisotP. Mitochondrial contact sites. Lipid composition and dynamics. J Biol Chem, 265: 18797–18802, 1990.
9.
ArnoldI, PfeifferK, NeupertW, StuartRA, and SchäggerH. Yeast mitochondrial F1F0-ATP synthase exists as a dimer: identification of three dimer-specific subunits. EMBO J, 17: 7170–7178, 1998.
10.
BainesCP, KaiserRA, PurcellNH, BlairNS, OsinskaH, HambletonMA, BrunskillEW, SayenMR, GottliebRA, DornGW, RobbinsJ, and MolkentinJD. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature, 434: 658–662, 2005.
11.
BainesCP, KaiserRA, SheikoT, CraigenWJ, and MolkentinJD. Voltage-dependent anion channels are dispensable for mitochondrial-dependent cell death. Nat Cell Biol, 9: 550–555, 2007.
12.
BanT, HeymannJA, SongZ, HinshawJE, and ChanDC. OPA1 disease alleles causing dominant optic atrophy have defects in cardiolipin-stimulated GTP hydrolysis and membrane tubulation. Hum Mol Genet, 19: 2113–2122, 2010.
13.
BarthPG, ScholteHR, BerdenJA, Van der Klei-Van MoorselJM, Luyt-HouwenE, Van ’t Veer-KorthofET, Van der HartenJJ, and Sobotka-PlojharMA. An X-linked mitochondrial disease affecting cardiac muscle, skeletal muscle and neutrophil leucocytes. J Neurol Sci, 62: 327–355, 1983.
14.
BassoE, PetronilliV, ForteMA, and BernardiP. Phosphate is essential for inhibition of the mitochondrial permeability transition pore by cyclosporin A and by cyclophilin D ablation. J Biol Chem, 283: 26307–26311, 2008.
15.
BayirH, FadeelB, PalladinoMJ, WitaspE, KurnikovIV, TyurinaYY, TyurinVA, AmoscatoAA, JiangJ, KochanekPM, DeKoskyST, GreenbergerJS, ShvedovaAA, and KaganVE. Apoptotic interactions of cytochrome c: redox flirting with anionic phospholipids within and outside of mitochondria. Biochim Biophys Acta, 1757: 648–659, 2006.
16.
BayirH, KapralovAA, JiangJ, HuangZ, TyurinaYY, TyurinVA, ZhaoQ, BelikovaNA, VlasovaII, MaedaA, ZhuJ, NaHM, MastroberardinoPG, SparveroLJ, AmoscatoAA, ChuCT, GreenamyreJT, and KaganVE. Peroxidase mechanism of lipid-dependent cross-linking of synuclein with cytochrome C: protection against apoptosis versus delayed oxidative stress in Parkinson disease. J Biol Chem, 284: 15951–15969, 2009.
17.
BeckmanKB and AmesBN. The free radical theory of aging matures. Physiol Rev, 78: 547–581, 1998.
18.
BegricheK, IgoudjilA, PessayreD, and FromentyB. Mitochondrial dysfunction in NASH: causes, consequences and possible means to prevent it. Mitochondrion, 6: 1–28, 2006.
19.
BelikovaNA, VladimirovYA, OsipovAN, KapralovAA, TyurinVA, PotapovichMV, BasovaLV, PetersonJ, KurnikovIV, and KaganVE. Peroxidase activity and structural transitions of cytochrome c bound to cardiolipin-containing membranes. Biochemistry, 45: 4998–5009, 2006.
20.
BeranekA, RechbergerG, KnauerH, WolinskiH, KohlweinSD, and LeberR. Identification of a cardiolipin-specific phospholipase encoded by the gene CLD1 (YGR110W) in yeast. J Biol Chem, 284: 11572–11578, 2009.
21.
BeyerK and KlingenbergM. ADP/ATP carrier protein from beef heart mitochondria has high amounts of tightly bound cardiolipin, as revealed by 31P nuclear magnetic resonance. Biochemistry, 24: 3821–3826, 1985.
22.
BianchiC, GenovaML, Parenti CastelliG, and LenazG. The mitochondrial respiratory chain is partially organized in a supercomplex assembly: kinetic evidence using flux control analysis. J Biol Chem, 279: 36562–36569, 2004.
23.
BioneS, D'AdamoP, MaestriniE, GedeonAK, BolhuisPA, and TonioloD. A novel X-linked gene, G4.5. is responsible for Barth syndrome. Nat Genet, 12: 385–389, 1996.
24.
BisacciaF and PalmieriF. Specific elution from hydroxylapatite of the mitochondrial phosphate carrier by cardiolipin. Biochim Biophys Acta, 766: 386–394, 1984.
25.
BolhuisPA, HenselsGW, HulsebosTJ, BaasF, and BarthPG. Mapping of the locus for X-linked cardioskeletal myopathy with neutropenia and abnormal mitochondria (Barth syndrome) to Xq28. Am J Hum Genet, 48: 481–485, 1991.
26.
BoverisA and ChanceB. The mitochondrial generation of hydrogen peroxide: general properties and effect of hyperbaric oxygen. Biochem J, 134: 707–716, 1973.
27.
BrandnerK, MickDU, FrazierAE, TaylorRD, MeisingerC, and RehlingP. Taz1, an outer mitochondrial membrane protein, affects stability and assembly of inner membrane protein complexes: implications for Barth Syndrome. Mol Biol Cell, 16: 5202–5214, 2005.
28.
BrustovetskyN and KlingenbergM. Mitochondrial ADP/ATP carrier can be reversibly converted into a large channel by Ca2+. Biochemistry, 35: 8483–8488, 1996.
29.
BüelerH. Impaired mitochondrial dynamics and function in the pathogenesis of Parkinson's disease. Exp Neurol, 218: 235–246, 2009.
30.
ButlerJ, JaysonGG, and SwallowAJ. The reaction between the superoxide anion radical and cytochrome c. Biochim Biophys Acta, 408: 215–222, 1975.
31.
CamaraAK, BienengraeberM, and StoweDF. Mitochondrial approaches to protect against cardiac ischemia and reperfusion injury. Front Physiol, 2:13, 2011.
32.
CaoJ, LiuY, LockwoodJ, BurnP, and ShiY. 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: 31727–31734, 2004.
33.
CereghettiGM and ScorranoL. The many shapes of mitochondrial death. Oncogene, 25: 4717–4724, 2006.
34.
CervenyKL, TamuraY, ZhangZ, JensenRE, and SesakiH. Regulation of mitochondrial fusion and division. Trends Cell Biol, 17: 563–569, 2007.
35.
ChenD, ZhangXY, and ShiY. Identification and functional characterization of hCLS1, a human cardiolipin synthase localized in mitochondria. Biochem J, 398: 169–176, 2006.
36.
ChenS, HeQ, and GreenbergML. Loss of tafazzin in yeast leads to increased oxidative stress during respiratory growth. Mol Microbiol, 68: 1061–1072, 2008.
37.
ChiccoAJ and SparagnaGC. Role of cardiolipin alterations in mitochondrial dysfunction and disease. Am J Physiol Cell Physiol, 292: C33–C44, 2007.
38.
ChipukJE, Bouchier-HayesL, and GreenDR. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell Death Differ, 8: 1396–1402, 2006.
39.
ChitturiS and FarrellGC. Etiopathogenesis of nonalcoholic steatohepatitis. Semin Liver Dis, 21: 27–41, 2001.
40.
ChoiSY, HuangP, JenkinsGM, ChanDC, SchillerJ, and FrohmanMA. A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat Cell Biol, 11: 1255–1262, 2006.
41.
ChungS, DzejaPP, FaustinoRS, Perez-TerzicC, BehfarA, and TerzicA. Mitochondrial oxidative metabolism is required for the cardiac differentiation of stem cells. Nat Clin Pract Cardiovasc Med, 4Suppl 1: S60–S67, 2007.
42.
ClaypoolSM, McCafferyJM, and KoehlerCM. Mitochondrial mislocalization and altered assembly of a cluster of Barth syndrome mutant tafazzins. J Cell Biol, 174: 379–390, 2006.
43.
ClaypoolSM, OktayY, BoontheungP, LooJA, and KoehlerCM. Cardiolipin defines the interactome of the major ADP/ATP carrier protein of the mitochondrial inner membrane. J Cell Biol, 182: 937–950, 2008.
44.
ClaypoolSM. Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function. Biochim Biophys Acta, 1788: 2059–2068, 2009.
45.
ColeNB, DieuliisD, LeoP, MitchellDC, and NussbaumRL. Mitochondrial translocation of alpha-synuclein is promoted by intracellular acidification. Exp Cell Res, 314: 2076–2089, 2008.
46.
CromptonM, EllingerH, and CostiA. Inhibition by cyclosporin A of a Ca2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J, 255: 357–360, 1988.
47.
CromptonM. The mitochondrial permeability transition pore and its role in cell death. Biochem J, 341 (Pt 2): 233–249, 1999.
48.
CullisPR and de KruijffB. Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim Biophys Acta, 559: 399–420, 1979.
49.
DaumG. Lipids of mitochondria. Biochim Biophys Acta, 822: 1–42, 1985.
50.
de KroonAI, DolisD, MayerA, LillR, and de KruijffB. 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: 108–116, 1997.
51.
DeVayRM, Dominguez-RamirezL, LacknerLL, HoppinsS, StahlbergH, and NunnariJ. Coassembly of Mgm1 isoforms requires cardiolipin and mediates mitochondrial inner membrane fusion. J Cell Biol, 186: 793–803, 2009.
52.
DowhanW. Molecular basis for membrane phospholipid diversity: why are there so many lipids?. Annu Rev Biochem, 66: 199–232, 1997.
53.
EbleKS, ColemanWB, HantganRR, and CunninghamCC. Tightly associated cardiolipin in the bovine heart mitochondrial ATP synthase as analyzed by 31P nuclear magnetic resonance spectroscopy. J Biol Chem, 265: 19434–19440, 1990.
54.
EllisCE, MurphyEJ, MitchellDC, GolovkoMY, ScagliaF, Barceló-CoblijnGC, and NussbaumRL. Mitochondrial lipid abnormality and electron transport chain impairment in mice lacking alpha-synuclein. Mol Cell Biol, 25: 10190–10201, 2005.
55.
EpandRF, MartinouJC, Fornallaz-MulhauserM, HughesDW, and EpandRM. The apoptotic protein tBid promotes leakage by altering membrane curvature. J Biol Chem, 277: 32632–32639, 2002.
56.
EpandRF, SchlattnerU, WallimannT, LacombeML, and EpandRM. Novel lipid transfer property of two mitochondrial proteins that bridge the inner and outer membranes. Biophys J, 92: 126–137, 2007.
57.
EpandRF, Tokarska-SchlattnerM, SchlattnerU, WallimannT, and EpandRM. Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins. J Mol Biol, 365: 968–980, 2007.
58.
FrezzaC, CipolatS, Martins de BritoO, MicaroniM, BeznoussenkoGV, RudkaT, BartoliD, PolishuckRS, DanialNN, De StrooperB, and ScorranoL. OPA1 controls apoptotic cristae remodeling independently from mitochondrial fusion. Cell, 126: 177–189, 2006.
59.
FryM and GreenDE. Cardiolipin requirement for electron transfer in complex I and III of the mitochondrial respiratory chain. J Biol Chem, 256: 1874–1880, 1981.
60.
FyfePK, McAuleyKE, RoszakAW, IsaacsNW, CogdellRJ, and JonesMR. Probing the interface between membrane proteins and membrane lipids by X-ray crystallography. Trends Biochem Sci, 26: 106–112, 2001.
61.
GadicherlaAK, StoweDF, AntholineWE, YangM, and CamaraAK. Damage to mitochondrial complex I during cardiac ischemia reperfusion injury is reduced indirectly by anti-anginal drug ranolazine. Biochim Biophys Acta, 1817: 419–429, 2012.
62.
GallasMR, DienhartMK, StuartRA, and LongRM. Characterization of Mmp37p, a Saccharomyces cerevisiae mitochondrial matrix protein with a role in mitochondrial protein import. Mol Biol Cell, 17: 4051–4062, 2006.
63.
Garcia FernandezM, TroianoL, MorettiL, NasiM, PintiM, SalvioliS, DobruckiJ, and CossarizzaA. Early changes in intramitochondrial cardiolipin distribution during apoptosis. Cell Growth Differ, 13: 449–455, 2002.
64.
GiorgioV, von StockumS, AntonielM, FabbroA, FogolariF, ForteM, GlickGD, PetronilliV, ZorattiM, SzabóI, LippeG, and BernardiP. Dimers of mitochondrial ATP synthase form the permeability transition pore. Proc Natl Acad Sci U S A, 110: 5887–5892, 2013.
65.
GomezBJr., and RobinsonNC. Phospholipase digestion of bound cardiolipin reversibly inactivates bovine cytochrome bc1. Biochemistry, 38: 9031–9038, 1999.
66.
GómezLA, MonetteJS, ChavezJD, MaierCS, and HagenTM. Supercomplexes of the mitochondrial electron transport chain decline in the aging rat heart. Arch Biochem Biophys, 490: 30–35, 2009.
67.
GonzalvezF and GottliebE. Cardiolipin: setting the beat of apoptosis. Apoptosis, 12: 877–885, 2007.
68.
GonzalvezF, SchugZT, HoutkooperRH, MacKenzieED, BrooksDG, WandersRJ, PetitPX, VazFM, and GottliebE. Cardiolipin provides an essential activating platform for caspase-8 on mitochondria. J Cell Biol, 183: 681–696, 2008.
69.
GrijalbaMT, VercesiAE, and SchreierS. Ca2+-induced increased lipid packing and domain formation in submitochondrial particles. A possible early step in the mechanism of Ca2+-stimulated generation of reactive oxygen species by the respiratory chain. Biochemistry, 38: 13279–13287, 1999.
70.
GuZ, ValianpourF, ChenS, VazFM, HakkaartGA, WandersRJ, and GreenbergML. Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome. Mol Microbiol, 51: 149–158, 2004.
71.
HackenbrockCR, ChazotteB, and GupteSS. The random collision model and a critical assessment of diffusion and collision in mitochondrial electron transport. J Bioenerg Biomembr, 18: 331–368, 1986.
72.
HainesTH and DencherNA. Cardiolipin: a proton trap for oxidative phosphorylation. FEBS Lett, 528: 35–39, 2002.
73.
HalestrapAP, ClarkeSJ, and JavadovSA. Mitochondrial permeability transition pore opening during myocardial reperfusion—a target for cardioprotection. Cardiovasc Res, 61: 372–385, 2004.
74.
HalestrapAP and DavidsonAM. Inhibition of Ca2(+)-induced large-amplitude swelling of liver and heart mitochondria by cyclosporin is probably caused by the inhibitor binding to mitochondrial-matrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem J, 268: 153–160, 1990.
75.
HalestrapAP. Calcium, mitochondria and reperfusion injury: a pore way to die. Biochem Soc Trans, 34: 232–237, 2006.
76.
HalestrapAP. Mitochondrial permeability: dual role for the ADP/ATP translocator?. Nature, 430: 1 p following 983, 2004.
77.
HanX, AbendscheinDR, KelleyJG, and GrossRW. Diabetes-induced changes in specific lipid molecular species in rat myocardium. Biochem J, 15Pt 1: 79–89, 2000.
78.
HanX, YangJ, ChengH, YangK, AbendscheinDR, and GrossRW. Shotgun lipidomics identifies cardiolipin depletion in diabetic myocardium linking altered substrate utilization with mitochondrial dysfunction. Biochemistry, 44: 16684–16694, 2005.
79.
HanX, YangJ, YangK, ZhaoZ, AbendscheinDR, and GrossRW. Alterations in myocardial cardiolipin content and composition occur at the very earliest stages of diabetes: a shotgun lipidomics study. Biochemistry, 46: 6417–6428, 2007.
80.
HausenloyDJ and YellonDM. The mitochondrial permeability transition pore: its fundamental role in mediating cell death during ischaemia and reperfusion. J Mol Cell Cardiol, 35: 339–341, 2003.
81.
HeerdtPM, SchlameM, JehleR, BarboneA, BurkhoffD, and BlanckTJ. Disease-specific remodeling of cardiac mitochondria after a left ventricular assist device. Ann Thorac Surg, 73: 1216–1221, 2002.
82.
HerlanM, VogelF, BornhovdC, NeupertW, and ReichertAS. Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA. J Biol Chem, 278: 27781–27788, 2003.
83.
HigamiY and ShimokawaI. Apoptosis in the aging process. Cell Tissue Res, 301: 125–132, 2000.
HoffmannB, StöcklA, SchlameM, BeyerK, and KlingenbergM. The reconstituted ADP/ATP carrier activity has an absolute requirement for cardiolipin as shown in cysteine mutants. J Biol Chem, 269: 1940–1944, 1994.
86.
HoppinsS, LacknerL, and NunnariJ. The machines that divide and fuse mitochondria. Annu Rev Biochem, 76: 751–780, 2007.
87.
HostetlerKY. Effect of thyroxine on the activity of mitochondrial cardiolipin synthase in rat liver. Biochim Biophys Acta, 1086: 139–140, 1991.
88.
HoutkooperRH, TurkenburgM, Poll-TheBT, KarallD, Pérez-CerdáC, MorroneA, MalvagiaS, WandersRJ, KulikW, and VazFM. The enigmatic role of tafazzin in cardiolipin metabolism. Biochim Biophys Acta, 1788: 2003–2014, 2009.
89.
HoutkooperRH and VazFM. Cardiolipin, the heart of mitochondrial metabolism. Cell Mol Life Sci, 65: 2493–2506, 2008.
90.
HungT, SievenpiperJL, MarchieA, KendallCW, and JenkinsDJ. Fat versus carbohydrate in insulin resistance, obesity, diabetes and cardiovascular disease. Curr Opin Clin Nutr Metab Care, 6: 165–176, 2003.
91.
HüttemannM, PecinaP, RainboltM, SandersonTH, KaganVE, SamavatiL, DoanJW, and LeeI. The multiple functions of cytochrome c and their regulation in life and death decisions of the mammalian cell: from respiration to apoptosis. Mitochondrion, 11: 369–381, 2011.
92.
ImaiH, KoumuraT, NakajimaR, NomuraK, and NakagawaY. Protection from inactivation of the adenine nucleotide translocator during hypoglycaemia-induced apoptosis by mitochondrial phospholipid hydroperoxide glutathione peroxidase. Biochem J, 371: 799–809, 2003.
93.
KaganVE, BorisenkoGG, TyurinaYY, TyurinVA, JiangJ, PotapovichAI, KiniV, AmoscatoAA, and FujiiY. Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine. Free Radic Biol Med, 37: 1963–1985, 2004.
94.
KaganVE, TyurinVA, JiangJ, TyurinaYY, RitovVB, AmoscatoAA, OsipovAN, BelikovaNA, KapralovAA, KiniV, VlasovaII, ZhaoQ, ZouM, DiP, SvistunenkoDA, KurnikovIV, and BorisenkoGG. Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors. Nat Chem Biol, 1: 223–232, 2005.
95.
KajsturaJ, ChengW, SarangarajanR, LiP, LiB, NitaharaJA, ChapnickS, ReissK, OlivettiG, and AnversaP. Necrotic and apoptotic myocyte cell death in the aging heart of Fischer 344 rats. Am J Physiol, 271: H1215–H1228, 1996.
96.
KampF, ExnerN, LutzAK, WenderN, HegermannJ, BrunnerB, NuscherB, BartelsT, GieseA, BeyerK, EimerS, WinklhoferKF, and HaassC. Inhibition of mitochondrial fusion by α-synuclein is rescued by PINK1, Parkin and DJ-1. EMBO J, 29: 3571–3589, 2010.
97.
KapralovAA, KurnikovIV, VlasovaII, BelikovaNA, TyurinVA, BasovaLV, ZhaoQ, TyurinaYY, JiangJ, BayirH, VladimirovYA, and KaganVE. The hierarchy of structural transitions induced in cytochrome c by anionic phospholipids determines its peroxidase activation and selective peroxidation during apoptosis in cells. Biochemistry, 46: 14232–14244, 2007.
98.
KimTH, ZhaoY, DingWX, ShinJN, HeX, SeoYW, ChenJ, RabinowichH, AmoscatoAA, and YinXM. Bid-cardiolipin interaction at mitochondrial contact site contributes to mitochondrial cristae reorganization and cytochrome C release. Mol Biol Cell, 7: 3061–3072, 2004.
99.
KlingenAR, PalsdottirH, HunteC, and UllmannGM. Redox-linked protonation state changes in cytochrome bc1 identified by Poisson-Boltzmann electrostatics calculations. Biochim Biophys Acta, 1767: 204–221, 2007.
KokoszkaJE, WaymireKG, LevySE, SlighJE, CaiJ, JonesDP, MacGregorGR, and WallaceDC. The ADP/ATP translocator is not essential for the mitochondrial permeability transition pore. Nature, 427: 461–465, 2004.
102.
KroemerG, El-DeiryWS, GolsteinP, PeterME, VauxD, VandenabeeleP, ZhivotovskyB, BlagosklonnyMV, MalorniW, KnightRA, PiacentiniM, NagataS, MelinoG; Nomenclature Committee on Cell Death. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ, 12Suppl 2: 1463–1467, 2005.
103.
KulikW, van LentheH, StetFS, HoutkooperRH, KempH, StoneJE, StewardCG, WandersRJ, and VazFM. Bloodspot assay using HPLC-tandem mass spectrometry for detection of Barth syndrome. Clin Chem, 54: 371–378, 2008.
104.
KutikS, RisslerM, GuanXL, GuiardB, ShuiG, GebertN, HeacockPN, RehlingP, DowhanW, WenkMR, PfannerN, and WiedemannN. The translocator maintenance protein Tam41 is required for mitochondrial cardiolipin biosynthesis. J Cell Biol, 183: 1213–1221, 2008.
105.
LairdDM, EbleKS, and CunninghamCC. Reconstitution of mitochondrial F0.F1-ATPase with phosphatidylcholine using the nonionic detergent, octylglucoside. J Biol Chem, 261: 14844–14850, 1986.
106.
LangeC, NettJH, TrumpowerBL, and HunteC. Specific roles of protein-phospholipid interactions in the yeast cytochrome bc1 complex structure. EMBO J, 20: 6591–6600, 2001.
107.
LecocqJ and BallouCE. On the structure of cardiolipin. Biochemistry, 3: 976–980, 1964.
108.
LenazG, BovinaC, CastelluccioC, FatoR, FormigginiG, GenovaML, MarchettiM, PichMM, PallottiF, Parenti CastelliG, and BiaginiG. Mitochondrial complex I defects in aging. Mol Cell Biochem, 174: 329–333, 1997.
109.
LenazG and GenovaML. Structure and organization of mitochondrial respiratory complexes: a new understanding of an old subject. Antioxid Redox Signal, 12: 961–1008, 2010.
110.
LesnefskyEJ, SlabeTJ, StollMS, MinklerPE, and HoppelCL. Myocardial ischemia selectively depletes cardiolipin in rabbit heart subsarcolemmal mitochondria. Am J Physiol Heart Circ Physiol, 280: H2770–H2778, 2001.
111.
LetaiA, BassikMC, WalenskyLD, SorcinelliMD, WeilerS, and KorsmeyerSJ. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell, 3: 183–192, 2002.
112.
LeungAW, VaranyuwatanaP, and HalestrapAP. The mitochondrial phosphate carrier interacts with cyclophilin D and may play a key role in the permeability transition. J Biol Chem, 283: 26312–26323, 2008.
113.
LiuJ, DaiQ, ChenJ, DurrantD, FreemanA, LiuT, GrossmanD, and LeeRM. Phospholipid scramblase 3 controls mitochondrial structure, function, and apoptotic response. Mol Cancer Res, 12: 892–902, 2003.
114.
LiuX, KimCN, YangJ, JemmersonR, and WangX. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell, 86: 147–157, 1996.
115.
LuB, XuFY, JiangYJ, ChoyPC, HatchGM, GrunfeldC, and FeingoldKR. Cloning and characterization of a cDNA encoding human cardiolipin synthase (hCLS1). J Lipid Res, 47: 1140–1145, 2006.
LuoX, BudihardjoI, ZouH, SlaughterC, and WangX. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell, 94: 481–490, 1998.
118.
LutterM, FangM, LuoX, NishijimaM, XieX, and WangX. Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat Cell Biol, 2: 754–761, 2000.
119.
LutterM, PerkinsGA, and WangX. The pro-apoptotic Bcl-2 family member tBid localizes to mitochondrial contact sites. BMC Cell Biol, 2: 22, 2001.
120.
MaZA, ZhaoZ, and TurkJ. Mitochondrial dysfunction and β-cell failure in type 2 diabetes mellitus. Exp Diabetes Res, 2012: 703538, 2012.
121.
MalhotraA, XuY, RenM, and SchlameM. Formation of molecular species of mitochondrial cardiolipin. 1. A novel transacylation mechanism to shuttle fatty acids between sn-1 and sn-2 positions of multiple phospholipid species. Biochim Biophys Acta, 1791: 314–320, 2009.
122.
MancusoDJ, KotzbauerP, WozniakDF, SimsHF, JenkinsCM, GuanS, HanX, YangK, SunG, MalikI, ConyersS, GreenKG, SchmidtRE, and GrossRW. Genetic ablation of calcium-independent phospholipase A2{gamma} leads to alterations in hippocampal cardiolipin content and molecular species distribution, mitochondrial degeneration, autophagy, and cognitive dysfunction. J Biol Chem, 284: 35632–35644, 2009.
123.
MarchettiP, LupiR, Del GuerraS, BuglianiM, MarselliL, and BoggiU. The beta-cell in human type 2 diabetes. Adv Exp Med Biol, 654: 501–514, 2010.
124.
MaromM, SafonovR, AmramS, AvneonY, NachlielE, GutmanM, ZoharyK, AzemA, and TsfadiaY. Interaction of the Tim44 C-terminal domain with negatively charged phospholipids. Biochemistry, 48: 11185–11195, 2009.
125.
McAuleyKE, FyfePK, RidgeJP, IsaacsNW, CogdellRJ, and JonesMR. Structural details of an interaction between cardiolipin and an integral membrane protein. Proc Natl Acad Sci U S A, 96: 14706–14711, 1999.
126.
McCordJM. Free radicals and myocardial ischemia: overview and outlook. Free Radic Biol Med, 4: 9–14, 1988.
127.
McKenzieM, LazarouM, ThorburnDR, and RyanMT. Mitochondrial respiratory chain supercomplexes are destabilized in Barth Syndrome patients. J Mol Biol, 361: 462–469, 2006.
128.
MiquelJ, EconomosAC, FlemingJ, and JohnsonJEJr., Mitochondrial role in cell aging. Exp Gerontol, 15: 575–591, 1980.
129.
MiyataH, LakattaEG, SternMD, and SilvermanHS. Relation of mitochondrial and cytosolic free calcium to cardiac myocyte recovery after exposure to anoxia. Circ Res, 71: 605–613, 1992.
130.
MizunoY, OhtaS, TanakaM, TakamiyaS, SuzukiK, SatoT, OyaH, OzawaT, and KagawaY. Deficiencies in complex I subunits of the respiratory chain in Parkinson's disease. Biochem Biophys Res Commun, 163: 1450–1455, 1989.
131.
MizushimaT, YaoM, ImoueN, AoyamaH, YamashitaE, YamaguchiH, et al. Structure of phospholipids in a membrane protein complex, bovine heart cytochrome c oxidase. Acta Crystallogr A (Suppl), 55: P06.04.069, 1999.
132.
MulliganCM, SparagnaGC, LeCH, De MooyAB, RouthMA, HolmesMG, Hickson-BickDL, ZariniS, MurphyRC, XuFY, HatchGM, McCuneSA, MooreRL, and ChiccoAJ. Dietary linoleate preserves cardiolipin and attenuates mitochondrial dysfunction in the failing rat heart. Cardiovasc Res, 94: 460–468, 2012.
133.
MurphyMP. How mitochondria produce reactive oxygen species. Biochem J, 417: 1–13, 2009.
134.
MusatovA. Contribution of peroxidized cardiolipin to inactivation of bovine heart cytochrome c oxidase. Free Radic Biol Med, 41: 238–246, 2006.
135.
NakamuraK, NemaniVM, AzarbalF, SkibinskiG, LevyJM, EgamiK, MunishkinaL, ZhangJ, GardnerB, WakabayashiJ, SesakiH, ChengY, FinkbeinerS, NussbaumRL, MasliahE, and EdwardsRH. Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein. J Biol Chem, 286: 20710–20726, 2011.
136.
NałeczKA, KamińskaJ, NałeczMJ, and AzziA. The activity of pyruvate carrier in a reconstituted system: substrate specificity and inhibitor sensitivity. Arch Biochem Biophys, 297: 162–168, 1992.
137.
NavarroA and BoverisA. The mitochondrial energy transduction system and the aging process. Am J Physiol Cell Physiol, 292: C670–C686, 2007.
138.
NoëlH and PandeSV. An essential requirement of cardiolipin for mitochondrial carnitine acylcarnitine translocase activity. Lipid requirement of carnitine acylcarnitine translocase. Eur J Biochem, 155: 99–102, 1986.
139.
NohlH and StolzeK. Ubisemiquinones of the mitochondrial respiratory chain do not interact with molecular oxygen. Free Radic Res Commun, 16: 409–419, 1992.
140.
NovgorodovSA, GudzTI, KushnarevaYE, ZorovDB, and KudrjashovYB. Effect of ADP/ATP antiporter conformational state on the suppression of the nonspecific permeability of the inner mitochondrial membrane by cyclosporine A. FEBS Lett, 277: 123–126, 1990.
141.
NuryH, Dahout-GonzalezC, TrézéguetV, LauquinG, BrandolinG, and Pebay-PeyroulaE. Structural basis for lipid-mediated interactions between mitochondrial ADP/ATP carrier monomers. FEBS Lett, 579: 6031–6036, 2005.
142.
NuryH, Dahout-GonzalezC, TrézéguetV, LauquinGJ, BrandolinG, and Pebay-PeyroulaE. Relations between structure and function of the mitochondrial ADP/ATP carrier. Annu Rev Biochem, 75: 713–741, 2006.
143.
OliveiraCP, da Costa GayottoLC, TataiC, Della BinaBI, JaniszewskiM, LimaES, AbdallaDS, LopassoFP, LaurindoFR, and LaudannaAA. Oxidative stress in the pathogenesis of nonalcoholic fatty liver disease, in rats fed with a choline-deficient diet. J Cell Mol Med, 6: 399–406, 2002.
144.
O'RourkeB and ReibelDK. Effects of adrenoceptor blockade on cardiac hypertrophy and myocardial phospholipids. Proc Soc Exp Biol Med, 200: 95–100, 1992.
145.
OrreniusS, ZhivotovskyB, and NicoteraP. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol, 4: 552–565, 2003.
146.
OsmanC, HaagM, PottingC, RodenfelsJ, DipPV, WielandFT, BrüggerB, WestermannB, and LangerT. The genetic interactome of prohibitins: coordinated control of cardiolipin and phosphatidylethanolamine by conserved regulators in mitochondria. J Cell Biol, 184: 583–596, 2009.
147.
OsmanC, HaagM, WielandFT, BrüggerB, and LangerT. A mitochondrial phosphatase required for cardiolipin biosynthesis: the PGP phosphatase Gep4. EMBO J, 29: 1976–1987, 2010.
148.
OsteryoungKW and NunnariJ. The division of endosymbiotic organelles. Science, 302: 1698–1704, 2003.
149.
OttM, RobertsonJD, GogvadzeV, ZhivotovskyB, and OrreniusS. Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci U S A, 99: 1259–1263, 2002.
150.
PalmieriF. The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch, 447: 689–709, 2004.
151.
ParadiesG, ParadiesV, RuggieroFM, and PetrosilloG. Changes in the mitochondrial permeability transition pore in aging and age-associated diseases. Mech Ageing Dev, 134: 1–9, 2013.
152.
ParadiesG, PetrosilloG, ParadiesV, and RuggieroFM. Mitochondrial dysfunction in brain aging: role of oxidative stress and cardiolipin. Neurochem Int, 58: 447–457, 2011.
153.
ParadiesG, PetrosilloG, ParadiesV, and RuggieroFM. Oxidative stress, mitochondrial bioenergetics, and cardiolipin in aging. Free Radic Biol Med, 48: 1286–1295, 2010.
154.
ParadiesG, PetrosilloG, ParadiesV, and RuggieroFM. Role of cardiolipin peroxidation and Ca2+ in mitochondrial dysfunction and disease. Cell Calcium, 45: 643–650, 2009.
155.
ParadiesG, PetrosilloG, PistoleseM, Di VenosaN, FedericiA, and RuggieroFM. Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ Res, 94: 53–59, 2004.
156.
ParadiesG, PetrosilloG, PistoleseM, Di VenosaN, SerenaD, and RuggieroFM. Lipid peroxidation and alterations to oxidative metabolism in mitochondria isolated from rat heart subjected to ischemia and reperfusion. Free Radic Biol Med, 27: 42–50, 1999.
157.
ParadiesG, PetrosilloG, PistoleseM, and RuggieroFM. Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene, 286: 135–141, 2002.
158.
ParadiesG, PetrosilloG, PistoleseM, and RuggieroFM. Reactive oxygen species generated by the mitochondrial respiratory chain affect the complex III activity via cardiolipin peroxidation in beef-heart submitochondrial particles. Mitochondrion, 1: 151–159, 2001.
159.
ParadiesG, PetrosilloG, PistoleseM, and RuggieroFM. The effect of reactive oxygen species generated from the mitochondrial electron transport chain on the cytochrome c oxidase activity and on the cardiolipin content in bovine heart submitochondrial particles. FEBS Lett, 466: 323–326, 2000.
160.
ParadiesG, PetrosilloG, and RuggieroFM. Cardiolipin-dependent decrease of cytochrome c oxidase activity in heart mitochondria from hypothyroid rats. Biochim Biophys Acta, 1319: 5–8, 1997.
161.
ParadiesG, RuggieroFM, DinoiP, PetrosilloG, and QuagliarielloE. Decreased cytochrome oxidase activity and changes in phospholipids in heart mitochondria from hypothyroid rats. Arch Biochem Biophys, 307: 91–95, 1993.
162.
ParadiesG, RuggieroFM, and DinoiP. The influence of hypothyroidism on the transport of phosphate and on the lipid composition in rat-liver mitochondria. Biochim Biophys Acta, 1070: 180–186, 1991.
163.
ParadiesG, RuggieroFM, PetrosilloG, and QuagliarielloE. Alterations in carnitine-acylcarnitine translocase activity and in phospholipid composition in heart mitochondria from hypothyroid rats. Biochim Biophys Acta, 1362: 193–200, 1997.
164.
ParadiesG, RuggieroFM, PetrosilloG, and QuagliarielloE. Enhanced cytochrome oxidase activity and modification of lipids in heart mitochondria from hyperthyroid rats. Biochim Biophys Acta, 1225: 165–170, 1994.
165.
ParadiesG, RuggieroFM, PetrosilloG, and QuagliarielloE. Stimulation of carnitine acylcarnitine translocase activity in heart mitochondria from hyperthyroid rats. FEBS Lett, 397: 260–262, 1996.
166.
ParadiesG and RuggieroFM. Enhanced activity of the tricarboxylate carrier and modification of lipids in hepatic mitochondria from hyperthyroid rats. Arch Biochem Biophys, 278: 425–430, 1990.
167.
ParadiesG and RuggieroFM. Stimulation of phosphate transport in rat-liver mitochondria by thyroid hormones. Biochim Biophys Acta, 1019: 133–136, 1990.
168.
Pebay-PeyroulaE, Dahout-GonzalezC, KahnR, TrézéguetV, LauquinGJ, and BrandolinG. Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature, 426: 39–44, 2003.
169.
Pessayre D and Fromenty B NASH: a mitochondrial disease. J Hepatol, 42: 928–940, 2005.
170.
PeterME and KrammerPH. The CD95(APO-1/Fas) DISC and beyond. Cell Death Differ, 10: 26–35, 2003.
171.
PetrosilloG, CasanovaG, MateraM, RuggieroFM, and ParadiesG. Interaction of peroxidized cardiolipin with rat-heart mitochondrial membranes: induction of permeability transition and cytochrome c release. FEBS Lett, 580: 6311–6316, 2006.
172.
PetrosilloG, ColantuonoG, MoroN, RuggieroFM, TiravantiE, Di VenosaN, FioreT, and ParadiesG. Melatonin protects against heart ischemia-reperfusion injury by inhibiting mitochondrial permeability transition pore opening. Am J Physiol Heart Circ Physiol, 297: H1487–H1493, 2009.
173.
PetrosilloG, Di VenosaN, PistoleseM, CasanovaG, TiravantiE, ColantuonoG, FedericiA, ParadiesG, and RuggieroFM. Protective effect of melatonin against mitochondrial dysfunction associated with cardiac ischemia- reperfusion: role of cardiolipin. FASEB J, 20: 269–276, 2006.
174.
PetrosilloG, MateraM, CasanovaG, RuggieroFM, and ParadiesG. Mitochondrial dysfunction in rat brain with aging Involvement of complex I, reactive oxygen species and cardiolipin. Neurochem Int, 53: 126–131, 2008.
175.
PetrosilloG, MateraM, MoroN, RuggieroFM, and ParadiesG. Mitochondrial complex I dysfunction in rat heart with aging: critical role of reactive oxygen species and cardiolipin. Free Radic Biol Med, 46: 88–94, 2009.
176.
PetrosilloG, MoroN, ParadiesV, RuggieroFM, and ParadiesG. Increased susceptibility to Ca(2+)-induced permeability transition and to cytochrome c release in rat heart mitochondria with aging: effect of melatonin. J Pineal Res, 48: 340–346, 2010.
177.
PetrosilloG, MoroN, RuggieroFM, and ParadiesG. Melatonin inhibits cardiolipin peroxidation in mitochondria and prevents the mitochondrial permeability transition and cytochrome c release. Free Radic Biol Med, 47: 969–974, 2009.
178.
PetrosilloG, PortincasaP, GrattaglianoI, CasanovaG, MateraM, RuggieroFM, FerriD, and ParadiesG. Mitochondrial dysfunction in rat with nonalcoholic fatty liver Involvement of complex I, reactive oxygen species and cardiolipin. Biochim Biophys Acta, 1767: 1260–1267, 2007.
179.
PetrosilloG, RuggieroFM, Di VenosaN, and ParadiesG. Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin. FASEB J, 17: 714–716, 2003.
180.
PetrosilloG, RuggieroFM, PistoleseM, and ParadiesG. Reactive oxygen species generated from the mitochondrial electron transport chain induce cytochrome c dissociation from beef-heart submitochondrial particles via cardiolipin peroxidation. Possible role in the apoptosis. FEBS Lett, 509: 435–438, 2001.
PopC and SalvesenGS. Human caspases: activation, specificity, and regulation. J Biol Chem, 284: 21777–21781, 2009.
183.
PrankeIM, MorelloV, BigayJ, GibsonK, VerbavatzJM, AntonnyB, and JacksonCL. α-Synuclein and ALPS motifs are membrane curvature sensors whose contrasting chemistry mediates selective vesicle binding. J Cell Biol, 194: 89–103, 2011.
184.
ProtterD, LangC, and CooperAA. αSynuclein and mitochondrial dysfunction: a pathogenic partnership in Parkinson's disease?. Parkinsons Dis, 2012: 829207, 2012.
185.
RiccioP, AquilaH, and KlingenbergM. Purification of the carboxy-atractylate binding protein from mitochondria. FEBS Lett, 56: 133–138, 1975.
186.
RobinsonNC. Functional binding of cardiolipin to cytochrome c oxidase. J Bioenerg Biomembr, 25: 153–163, 1993.
187.
Saini-ChohanHK, HolmesMG, ChiccoAJ, TaylorWA, MooreRL, McCuneSA, Hickson-BickDL, HatchGM, and SparagnaGC. Cardiolipin biosynthesis and remodeling enzymes are altered during development of heart failure. J Lipid Res, 50: 1600–1608, 2009.
188.
ScaffidiC, FuldaS, SrinivasanA, FriesenC, LiF, TomaselliKJ, DebatinKM, KrammerPH, and PeterME. Two CD95 (APO-1/Fas) signaling pathways. EMBO J, 17: 1675–1687, 1998.
189.
SchäggerH and PfeifferK. Supercomplexes in the respiratory chains of yeast and mammalian mitochondria. EMBO J, 19: 1777–1783, 2000.
190.
SchäggerH. Respiratory chain supercomplexes of mitochondria and bacteria. Biochim Biophys Acta, 1555: 154–159, 2002.
191.
SchapiraAH, CooperJM, DexterD, ClarkJB, JennerP, and MarsdenCD. Mitochondrial complex I deficiency in Parkinson's disease. J Neurochem, 54: 823–827, 1990.
192.
SchlameM and HaldarD. Cardiolipin is synthesized on the matrix side of the inner membrane in rat liver mitochondria. J Biol Chem, 268: 74–79, 1993.
193.
SchlameM and HostetlerKY. Cardiolipin synthase from mammalian mitochondria. Biochim Biophys Acta, 1348: 207–213, 1997.
194.
SchlameM and HostetlerKY. Solubilization, purification, and characterization of cardiolipin synthase from rat liver mitochondria. Demonstration of its phospholipid requirement. J Biol Chem, 266: 22398–22403, 1991.
195.
SchlameM and RenM. Barth syndrome, a human disorder of cardiolipin metabolism. FEBS Lett, 580: 5450–5455, 2006.
196.
SchlameM and RenM. The role of cardiolipin in the structural organization of mitochondrial membranes. Biochim Biophys Acta, 1788: 2080–2083, 2009.
197.
SchlameM, RuaD, and GreenbergML. The biosynthesis and functional role of cardiolipin. Prog Lipid Res, 39: 257–288, 2000.
198.
SchlameM, TowbinJA, HeerdtPM, JehleR, DiMauroS, and BlanckTJ. Deficiency of tetralinoleoyl-cardiolipin in Barth syndrome. Ann Neurol, 51: 634–637, 2002.
199.
SchlameM, ZhaoM, RuaD, HaldarD, and GreenbergML. Kinetic analysis of cardiolipin synthase: a membrane enzyme with two glycerophospholipid substrates. Lipids, 30: 633–640, 1995.
200.
SchlameM. Cardiolipin remodeling and the function of tafazzin. Biochim Biophys Acta, 1831: 582–588, 2013.
201.
SchlameM. Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes. J Lipid Res, 49: 1607–1620, 2008.
202.
SchlattnerU, Tokarska-SchlattnerM, RamirezS, BrücknerA, KayL, PolgeC, EpandRF, LeeRM, LacombeML, and EpandRM. Mitochondrial kinases and their molecular interaction with cardiolipin. Biochim Biophys Acta, 1788: 2032–2047, 2009.
203.
SchlattnerU and WallimannT. Octamers of mitochondrial creatine kinase isoenzymes differ in stability and membrane binding. J Biol Chem, 275: 17314–17320, 2000.
204.
SchmidtO, PfannerN, and MeisingerC. Mitochondrial protein import: from proteomics to functional mechanisms. Nat Rev Mol Cell Biol, 11: 655–667, 2010.
205.
SchugZT and GottliebE. Cardiolipin acts as a mitochondrial signalling platform to launch apoptosis. Biochim Biophys Acta, 1788: 2022–2031, 2009.
206.
SchwallCT, GreenwoodVL, and AlderNN. The stability and activity of respiratory Complex II is cardiolipin-dependent. Biochim Biophys Acta, 1817: 1588–1596, 2012.
207.
ScorranoL, AshiyaM, ButtleK, WeilerS, OakesSA, MannellaCA, and KorsmeyerSJ. A distinct pathway remodels mitochondrial cristae and mobilizes cytochrome c during apoptosis. Dev Cell, 2: 55–67, 2002.
208.
SedlákE and RobinsonNC. Phospholipase A(2) digestion of cardiolipin bound to bovine cytochrome c oxidase alters both activity and quaternary structure. Biochemistry, 38: 14966–14972, 1999.
209.
SharpleyMS, ShannonRJ, DraghiF, and HirstJ. Interactions between phospholipids and NADH:ubiquinone oxidoreductase (complex I) from bovine mitochondria. Biochemistry, 45: 241–248, 2006.
210.
ShigenagaMK, HagenTM, and AmesBN. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci U S A, 91: 10771–10778, 1994.
211.
SinibaldiF, HowesBD, PiroMC, PolticelliF, BombelliC, FerriT, ColettaM, SmulevichG, and SantucciR. Extended cardiolipin anchorage to cytochrome c: a model for protein-mitochondrial membrane binding. J Biol Inorg Chem, 15: 689–700, 2010.
212.
SkulachevVP. Cytochrome c in the apoptotic and antioxidant cascades. FEBS Lett, 423: 275–280, 1998.
213.
SongZ, ChenH, FiketM, AlexanderC, and ChanDC. OPA1 processing controls mitochondrial fusion and is regulated by mRNA splicing, membrane potential, and Yme1L. J Cell Biol, 178: 749–755, 2007.
214.
SparagnaGC, ChiccoAJ, MurphyRC, BristowMR, JohnsonCA, ReesML, axeyML, McCuneSA, and MooreRL. Loss of cardiac tetralinoleoyl cardiolipin in human and experimental heart failure. J Lipid Res, 48: 1559–1570, 2007.
215.
SparagnaGC, JohnsonCA, McCuneSA, MooreRL, and MurphyRC. Quantitation of cardiolipin molecular species in spontaneously hypertensive heart failure rats using electrospray ionization mass spectrometry. J Lipid Res, 46: 1196–1204, 2005.
216.
StoweDF and CamaraAK. Mitochondrial reactive oxygen species production in excitable cells: modulators of mitochondrial and cell function. Antioxid Redox Signal, 11: 1373–1414, 2009.
217.
SzabóI and ZorattiM. The mitochondrial permeability transition pore may comprise VDAC molecules. I. Binary structure and voltage dependence of the pore. FEBS Lett, 330: 201–205, 1993.
218.
TaylorWA and HatchGM. Purification and characterization of monolysocardiolipin acyltransferase from pig liver mitochondria. J Biol Chem, 278: 12716–12721, 2003.
219.
TsukiharaT, AoyamaH, YamashitaE, TomizakiT, YamaguchiH, Shinzawa-ItohK, NakashimaR, YaonoR, and YoshikawaS. The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 A. Science, 272: 1136–1144, 1996.
220.
TuominenEK, WallaceCJ, and KinnunenPK. Phospholipid-cytochrome c interaction: evidence for the extended lipid anchorage. J Biol Chem, 277: 8822–8826, 2002.
221.
TuominenEK, ZhuK, WallaceCJ, Clark-LewisI, CraigDB, RytomaaM, and KinnunenPK. ATP induces a conformational change in lipid-bound cytochrome c. J Biol Chem, 276: 19356–19362, 2001.
222.
TurrensJF, AlexandreA, and LehningerAL. Ubisemiquinone is the electron donor for superoxide formation by complex III of heart mitochondria. Arch Biochem Biophys, 237: 408–414, 1985.
223.
TyurinVA, TyurinaYY, FengW, MnuskinA, JiangJ, TangM, ZhangX, ZhaoQ, KochanekPM, ClarkRS, BayirH, and KaganVE. Mass-spectrometric characterization of phospholipids and their primary peroxidation products in rat cortical neurons during staurosporine-induced apoptosis. J Neurochem, 107: 1614–1633, 2008.
224.
UngerRH. Lipotoxic diseases. Annu Rev Med, 53: 319–336, 2002.
225.
ValianpourF, MitsakosV, SchlemmerD, TowbinJA, TaylorJM, EkertPG, ThorburnDR, MunnichA, WandersRJ, BarthPG, and VazFM. Monolysocardiolipins accumulate in Barth syndrome but do not lead to enhanced apoptosis. J Lipid Res, 46: 1182–1195, 2005.
226.
Vanden HoekTL, BeckerLB, ShaoZ, LiC, and SchumackerPT. Reactive oxygen species released from mitochondria during brief hypoxia induce preconditioning in cardiomyocytes. J Biol Chem, 273: 18092–18098, 1998.
227.
Vanden HoekTL, LiC, ShaoZ, SchumackerPT, and BeckerLB. Significant levels of oxidants are generated by isolated cardiomyocytes during ischemia prior to reperfusion. J Mol Cell Cardiol, 29: 2571–2583, 1997.
228.
VrekenP, ValianpourF, NijtmansLG, GrivellLA, PleckoB, WandersRJ, and BarthPG. Defective remodeling of cardiolipin and phosphatidylglycerol in Barth syndrome. Biochem Biophys Res Commun, 279: 378–382, 2000.
229.
WalkerJE. The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains. Q Rev Biophys, 25: 253–324, 1992.
230.
WeissC, OppligerW, VergèresG, DemelR, JenöP, HorstM, de KruijffB, SchatzG, and AzemA. Domain structure and lipid interaction of recombinant yeast Tim44. Proc Natl Acad Sci U S A, 96: 8890–8894, 1999.
231.
WeissH, FriedrichT, HofhausG, and PreisD. The respiratory-chain NADH dehydrogenase (complex I) of mitochondria. Eur J Biochem, 197: 563–576, 1991.
232.
WittigI, CarrozzoR, SantorelliFM, and SchäggerH. Supercomplexes and subcomplexes of mitochondrial oxidative phosphorylation. Biochim Biophys Acta, 1757: 1066–1072, 2006.
233.
XuY, CondellM, PleskenH, Edelman-NovemskyI, MaJ, RenM, and SchlameM. A Drosophila model of Barth syndrome. Proc Natl Acad Sci U S A, 103: 11584–11588, 2006.
234.
XuY, MalhotraA, RenM, and SchlameM. The enzymatic function of tafazzin. J Biol Chem, 281: 39217–39224, 2006.
235.
YanLJ and SohalRS. Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. Proc Natl Acad Sci U S A, 95: 12896–12901, 1998.
236.
YinH and ZhuM. Free radical oxidation of cardiolipin: chemical mechanisms, detection and implication in apoptosis, mitochondrial dysfunction and human diseases. Free Radic Res, 46: 959–974, 2012.
237.
YouleRJ and KarbowskiM. Mitochondrial fission in apoptosis. Nat Rev Mol Cell Biol, 6: 657–663, 2005.
238.
ZambranoF, FleischerS, and FleischerB. Lipid composition of the Golgi apparatus of rat kidney and liver in comparison with other subcellular organelles. Biochim Biophys Acta, 380: 357–369, 1975.
239.
ZhangM, MileykovskayaE, and DowhanW. Cardiolipin is essential for organization of complexes III and IV into a supercomplex in intact yeast mitochondria. J Biol Chem, 280: 29403–29408, 2005.
240.
ZhangM, MileykovskayaE, and DowhanW. Gluing the respiratory chain together. Cardiolipin is required for supercomplex formation in the inner mitochondrial membrane. J Biol Chem, 277: 43553–43556, 2002.
241.
ZhaoM, SchlameM, RuaD, and GreenbergML. Cardiolipin synthase is associated with a large complex in yeast mitochondria. J Biol Chem, 273: 2402–2408, 1998.
242.
ZorattiM, SzabòI, and De MarchiU. Mitochondrial permeability transitions: how many doors to the house?. Biochim Biophys Acta, 1706: 40–52, 2005.