Cardiolipin and Its Different Properties in Mitophagy and Apoptosis

Journal of Histochemistry and Cytochemistry

Volumn 63, Issue 5, 2015, Pages 301-311

  Li, Xiao Xiao ^a   Tsoi, Bun ^a   Li, Yi Fang ^a   Kurihara, Hiroshi ^a   He, Rong Rong ^a  

^a JINAN UNIVERSITY   (China)

Author keywords

apoptosis; cardiolipin; mitophagy; oxidation; translocation

Indexed keywords

CARDIOLIPIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PHOSPHOLIPID SCRAMBLASE 3; SCRAMBLASE; UNCLASSIFIED DRUG;

APOPTOSIS; AUTOPHAGOSOME; HUMAN; LIPID PEROXIDATION; MITOCHONDRIAL MEMBRANE; MITOPHAGY; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW; ANIMAL; AUTOPHAGY; CHEMISTRY; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PROTEIN TRANSPORT;

EUKARYOTA;

ANIMALS; APOPTOSIS; AUTOPHAGY; CARDIOLIPINS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; OXIDATION-REDUCTION; PROTEIN TRANSPORT;

EID: 84930659018     PISSN: 00221554     EISSN: 15515044     Source Type: Journal    
DOI: 10.1369/0022155415574818     Document Type: Review

References (119)

1. Acehan D,Khuchua Z,Houtkooper RH,Malhotra A,Kaufman J,Vaz FM,Ren M,Rockman HA,Stokes DL,Schlame M.Distinct effects of tafazzin deletion in differentiated and undifferentiated mitochondria.Mitochondrion. 2009;9:86-95
2. Acehan D,Vaz F,Houtkooper RH,James J,Moore V,Tokunaga C,Kulik W,Wansapura J,Toth MJ,Strauss A.Cardiac and skeletal muscle defects in a mouse model of human Barth syndrome.J Biol Chem. 2011;286:899-908
3. Annis MG,Soucie EL,Dlugosz PJ,Cruz-Aguado JA,Penn LZ,Leber B,Andrews DW.Bax forms multispanning monomers that oligomerize to permeabilize membranes during apoptosis.EMBO J. 2005;24:2096-2103
4. Antonsson B,Montessuit S,Sanchez B,Martinou J-C.Bax is present as a high molecular weight oligomer/complex in the mitochondrial membrane of apoptotic cells.J Biol Chem. 2001;276:11615-11623
5. Ardail D,Privat J,Egret-Charlier M,Levrat C,Lerme F,Louisot P.Mitochondrial contact sites. Lipid composition and dynamics.J Biol Chem. 1990;265:18797-18802
6. Ashrafi G,Schwarz T.The pathways of mitophagy for quality control and clearance of mitochondria.Cell Death Differ. 2012;20:31-42
7. Basañez G,Sharpe JC,Galanis J,Brandt TB,Hardwick JM,Zimmerberg J.Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature.J Biol Chem. 2002;277:49360-49365
8. Bayir H,Tyurin VA,Tyurina YY,Viner R,Ritov V,Amoscato AA,Zhao Q,Zhang XJ,Janesko-Feldman KL,Alexander H.Selective early cardiolipin peroxidation after traumatic brain injury: an oxidative lipidomics analysis. Ann Neurol. 2007;62:154-169
9. Belikova NA,Vladimirov YA,Osipov AN,Kapralov AA,Tyurin VA,Potapovich MV,Basova LV,Peterson J,Kurnikov IV,Kagan VE.Peroxidase activity and structural transitions of cytochrome c bound to cardiolipin-containing membranes.Biochemistry (Mosc). 2006;45:4998-5009
10. Camberg JL,Johnson TL,Patrick M,Abendroth J,Hol WG,Sandkvist M.Synergistic stimulation of EpsE ATP hydrolysis by EpsL and acidic phospholipids.EMBO J. 2007;26:19-27
11. Cao J,Liu Y,Lockwood J,Burn P,Shi Y.A novel cardiolipin-remodeling pathway revealed by a gene encoding an endoplasmic reticulum-associated acyl-CoA: lysocardiolipin acyltransferase (ALCAT1) in mouse.J Biol Chem. 2004;279:31727-31734
12. Cassidy-Stone A,Chipuk JE,Ingerman E,Song C,Yoo C,Kuwana T,Kurth MJ,Shaw JT,Hinshaw JE,Green DR.Chemical inhibition of the mitochondrial division dynamin reveals its role in Bax/Bak-dependent mitochondrial outer membrane permeabilization.Dev Cell. 2008;14:193-204
13. Cereghetti G,Costa V,Scorrano L.Inhibition of Drp1-dependent mitochondrial fragmentation and apoptosis by a polypeptide antagonist of calcineurin.Cell Death Differ. 2010;17:1785-1794
14. Cereghetti G,Scorrano L.The many shapes of mitochondrial death.Oncogene. 2006;25:4717-4724
15. Chang S-C,Heacock PN,Clancey CJ,Dowhan W.The PEL1 Gene (Renamed PGS1) Encodes the Phosphatidylglycero-phosphate Synthase ofSaccharomyces cerevisiae.J Biol Chem. 1998;273:9829-9836
16. Chicco AJ,Sparagna GC.Role of cardiolipin alterations in mitochondrial dysfunction and disease.Am J Physiol Cell Physiol. 2007;292:C33-C44
17. Choi S,Swanson JM.Interaction of cytochrome c with cardiolipin: an infrared spectroscopic study.Biophys Chem. 1995;54:271-278
18. Chu CT,Ji J,Dagda RK,Jiang JF,Tyurina YY,Kapralov AA,Tyurin VA,Yanamala N,Shrivastava IH,Mohammadyani D.Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells.Nat Cell Biol. 2013;15:1197-1205
19. Claypool SM.Cardiolipin, a critical determinant of mitochondrial carrier protein assembly and function.Biochim Biophys Acta. 2009;1788:2059-2068
20. Danos M,Taylor WA,Hatch GM.Mitochondrial monolysocardiolipin acyltransferase is elevated in the surviving population of H9c2 cardiac myoblast cells exposed to 2-deoxyglucose-induced apoptosis.Biochem Cell Biol. 2008;86:11-20
21. Daum G.Lipids of mitochondria.Biochim Biophys Acta. 1985;822:1-42
22. Daum G,Vance JE.Import of lipids into mitochondria.Prog Lipid Res. 1997;36:103-130
23. de Arriba G,Calvino M,Benito S,Parra T.Cyclosporine A-induced apoptosis in renal tubular cells is related to oxidative damage and mitochondrial fission.Toxicol Lett. 2013;218:30-38
24. Dickerson RE,Takano T,Eisenberg D,Kallai OB,Samson L,Cooper A,Margoliash E.Ferricytochrome c I. General features of the horse and bonito proteins at 2.8 A resolution.J Biol Chem. 1971;246:1511-1535
25. Eichberg J.The reacylation of deacylated derivatives of diphosphatidylglycerol by microsomes and mitochondria from rat liver.J Biol Chem. 1974;249:3423-3429
26. Epand RF,Martinou J-C,Fornallaz-Mulhauser M,Hughes DW,Epand RM.The apoptotic protein tBid promotes leakage by altering membrane curvature.J Biol Chem. 2002;277:32632-32639
27. Epand RF,Schlattner U,Wallimann T,Lacombe M-L,Epand RM.Novel lipid transfer property of two mitochondrial proteins that bridge the inner and outer membranes.Biophys J. 2007a;92:126-137
28. Epand RF,Tokarska-Schlattner M,Schlattner U,Wallimann T,Epand RM.Cardiolipin clusters and membrane domain formation induced by mitochondrial proteins.J Mol Biol. 2007b;365:968-980
29. Estaquier J,Arnoult D.Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis.Cell Death Differ. 2007;14:1086-1094
30. Füllgrabe J,Klionsky DJ,Joseph B.The return of the nucleus: transcriptional and epigenetic control of autophagy.Nature Reviews Molecular Cell Biology. 2013;15:65-74
31. Fernandez MG,Troiano L,Moretti L,Nasi M,Pinti M,Salvioli S,Dobrucki J,Cossarizza A.Early changes in intramitochondrial cardiolipin distribution during apoptosis.Cell Growth Differ. 2002;13:449-455
32. Frank S,Gaume B,Bergmann-Leitner ES,Leitner WW,Robert EG,Catez F,Smith CL,Youle RJ.The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis.Dev Cell. 2001;1:515-525
33. Fujita N,Morita E,Itoh T,Tanaka A,Nakaoka M,Osada Y,Umemoto T,Saitoh T,Nakatogawa H,Kobayashi S,Haraguchi T,Guan JL,Iwai K,Tokunaga F,Saito K,Ishibashi K,Akira S,Fukuda M,Noda T,Yoshimori T.Recruitment of the autophagic machinery to endosomes during infection is mediated by ubiquitin.The Journal of Cell Biology. 2013;203:115-128
34. Gawrisch K.Lipids: Tafazzin senses curvature.Nat Chem Biol. 2012;8:811-812
35. Gonzalvez F,Pariselli F,Dupaigne P,Budihardjo I,Lutter M,Antonsson B,Diolez P,Manon S,Martinou J,Goubern M.tBid interaction with cardiolipin primarily orchestrates mitochondrial dysfunctions and subsequently activates Bax and Bak.Cell Death Differ. 2005;12:614-626
36. Gu Z,Valianpour F,Chen S,Vaz FM,Hakkaart GA,Wanders RJ,Greenberg ML.Aberrant cardiolipin metabolism in the yeast taz1 mutant: a model for Barth syndrome.Mol Microbiol. 2004;51:149-158
37. Haines TH,Dencher NA.Cardiolipin: a proton trap for oxidative phosphorylation.FEBS Lett. 2002;528:35-39
38. Hamasaki M,Furuta N,Matsuda A,Nezu A,Yamamoto A,Fujita N,Oomori H,Noda T,Haraguchi T,Hiraoka Y.Autophagosomes form at ER-mitochondria contact sites.Nature. 2013;495:389-393
39. Han X,Yang J,Yang K,Zhao Z,Abendschein DR,Gross RW.Alterations in myocardial cardiolipin content and composition occur at the very earliest stages of diabetes: a shotgun lipidomics study.Biochemistry (Mosc). 2007;46:6417-6428
40. Hatch GM.Cardiolipin: biosynthesis, remodeling and trafficking in the heart and mammalian cells (Review).Int J Mol Med. 1998;1:33-74
41. He Y,Liu J,Grossman D,Durrant D,Sweatman T,Lothstein L,Epand RF,Epand RM,Lee RM.Phosphorylation of mitochondrial phospholipid scramblase 3 by protein kinase C-δ induces its activation and facilitates mitochondrial targeting of tBid.J Cell Biochem. 2007;101:1210-1221
42. Houtkooper R,Vaz F.Cardiolipin, the heart of mitochondrial metabolism.Cell Mol Life Sci. 2008;65:2493-2506
43. Huang W,Choi W,Hu W,Mi N,Guo Q,Ma M,Liu M,Tian Y,Lu P,Wang F-L.Crystal structure and biochemical analyses reveal Beclin 1 as a novel membrane binding protein.Cell Res. 2012;22:473-489
44. Jiang J,Huang Z,Zhao Q,Feng W,Belikova NA,Kagan VE.Interplay between bax, reactive oxygen species production, and cardiolipin oxidation during apoptosis.Biochem Biophys Res Commun. 2008;368:145-150
45. Kagan V,Tyurina Y,Bayir H,Chu C,Kapralov A,Vlasova I,Belikova N,Tyurin V,Amoscato A,Epperly M.The “pro-apoptotic genies” get out of mitochondria: Oxidative lipidomics and redox activity of cytochrome c/cardiolipin complexes.Chem Biol Interact. 2006;163:15-28
46. Kagan VE,Bayir A,Bayir H,Stoyanovsky D,Borisenko GG,Tyurina YY,Wipf P,Atkinson J,Greenberger JS,Chapkin RS.Mitochondria-targeted disruptors and inhibitors of cytochrome c/cardiolipin peroxidase complexes: A new strategy in anti-apoptotic drug discovery.Mol Nutr Food Res. 2009a;53:104-114
47. Kagan VE,Bayır HA,Belikova NA,Kapralov O,Tyurina YY,Tyurin VA,Jiang J,Stoyanovsky DA,Wipf P,Kochanek PM.Cytochrome c/cardiolipin relations in mitochondria: a kiss of death.Free Radic Biol Med. 2009b;46:1439-1453
48. Kagan VE,Borisenko GG,Tyurina YY,Tyurin VA,Jiang J,Potapovich AI,Kini V,Amoscato AA,Fujii Y.Oxidative lipidomics of apoptosis: redox catalytic interactions of cytochrome c with cardiolipin and phosphatidylserine.Free Radic Biol Med. 2004;37:1963-1985
49. Kagan VE,Chu CT,Tyurina YY,Cheikhi A,Bayir H.Cardiolipin asymmetry, oxidation and signaling.Chem Phys Lipids. 2014;179:64-69
50. Kagan VE,Tyurin VA,Jiang J,Tyurina YY,Ritov VB,Amoscato AA,Osipov AN,Belikova NA,Kapralov AA,Kini V.Cytochrome c acts as a cardiolipin oxygenase required for release of proapoptotic factors.Nat Chem Biol. 2005;1:223-232
51. Kapralov AA,Yanamala N,Tyurina YY,Castro L,Samhan-Arias A,Vladimirov YA,Maeda A,Weitz AA,Peterson J,Mylnikov D.Topography of tyrosine residues and their involvement in peroxidation of polyunsaturated cardiolipin in cytochrome c/cardiolipin peroxidase complexes.Biochim Biophys Acta. 2011;1808:2147-2155
52. Kawai C,Prado FM,Nunes GL,Di Mascio P,Carmona-Ribeiro AM,Nantes IL.pH-dependent interaction of cytochrome c with mitochondrial mimetic membranes The role of an array of positively charged amino acids.J Biol Chem. 2005;280:34709-34717
53. Kim T-H,Zhao Y,Ding W-X,Shin JN,He X,Seo Y-W,Chen J,Rabinowich H,Amoscato AA,Yin X-M.Bid-cardiolipin interaction at mitochondrial contact site contributes to mitochondrial cristae reorganization and cytochrome c release.Mol Biol Cell. 2004;15:3061-3072
54. Kirkland RA,Windelborn JA,Kasprzak JM,Franklin JL.A Bax-induced pro-oxidant state is critical for cytochrome c release during programmed neuronal death.J Neurosci. 2002;22:6480-6490
55. Kishi-Itakura C,Koyama-Honda I,Itakura E,Mizushima N.Ultrastructural analysis of autophagosome organization using mammalian autophagy-deficient cells.J Cell Sci. 2014;127:4089-4102
56. Klionsky DJ,Schulman BA.Dynamic regulation of macroautophagy by distinctive ubiquitin-like proteins.Nat Struct Mol Biol. 2014;21:336-345
57. Korytowski W,Basova LV,Pilat A,Kernstock RM,Girotti AW.Permeabilization of the mitochondrial outer membrane by Bax/Truncated Bid (Tbid) proteins as sensitized by cardiolipin hydroperoxide translocation mechanistic implications for the intrinsic pathway of oxidative apoptosis.J Biol Chem. 2011;286:26334-26343
58. Kraft C,Peter M,Hofmann K.Selective autophagy: ubiquitin-mediated recognition and beyond.Nat Cell Biol. 2010;12:836-841
59. Krebs J,Hauser H,Carafoli E.Asymmetric distribution of phospholipids in the inner membrane of beef heart mitochondria.J Biol Chem. 1979;254:5308-5316
60. Kroemer G,Galluzzi L,Brenner C.Mitochondrial membrane permeabilization in cell death.Physiol Rev. 2007;87:99-163
61. Kuwana T,Mackey MR,Perkins G,Ellisman MH,Latterich M,Schneiter R,Green DR,Newmeyer DD.Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane.Cell. 2002;111:331-342
62. Labrousse AM,Zappaterra MD,Rube DA,van der Bliek AM.C. elegans Dynamin-Related Protein DRP-1 Controls Severing of the Mitochondrial Outer Membrane.Mol Cell. 1999;4:815-826
63. Lee Y,Lee H-Y,Hanna RA,Gustafsson ÅB.Mitochondrial autophagy by Bnip3 involves Drp1-mediated mitochondrial fission and recruitment of Parkin in cardiac myocytes.Am J Physiol Heart Circ Physiol. 2011;301:H1924-H1931
64. Legesse-Miller A,Massol RH,Kirchhausen T.Constriction and Dnm1p recruitment are distinct processes in mitochondrial fission.Mol Biol Cell. 2003;14:1953-1963
65. Lemasters JJ.Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging.Rejuvenation Res. 2005;8:3-5
66. Li H,Zhu H,Xu C-j,Yuan J.Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis.Cell. 1998;94:491-501
67. Li J,Romestaing C,Han X,Li Y,Hao X,Wu Y,Sun C,Liu X,Jefferson LS,Xiong J.Cardiolipin remodeling by ALCAT1 links oxidative stress and mitochondrial dysfunction to obesity.Cell Metab. 2010;12:154-165
68. Li P,Nijhawan D,Budihardjo I,Srinivasula SM,Ahmad M,Alnemri ES,Wang X.Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade.Cell. 1997;91:479-489
69. Liu J,Dai Q,Chen J,Durrant D,Freeman A,Liu T,Grossman D,Lee RM.Phospholipid Scramblase 3 Controls Mitochondrial Structure, Function, and Apoptotic Response.Mol Cancer Res. 2003;1:892-902
70. Liu J,Epand RF,Durrant D,Grossman D,Chi N-w,Epand RM,Lee RM.Role of Phospholipid Scramblase 3 in the Regulation of Tumor Necrosis Factor-α-Induced Apoptosis†.Biochemistry (Mosc). 2008;47:4518-4529
71. Lu B,Xu FY,Jiang YJ,Choy PC,Hatch GM,Grunfeld C,Feingold KR.Cloning and characterization of a cDNA encoding human cardiolipin synthase (hCLS1).J Lipid Res. 2006;47:1140-1145
72. Lucken-Ardjomande S,Montessuit S,Martinou J-C.Contributions to Bax insertion and oligomerization of lipids of the mitochondrial outer membrane.Cell Death Differ. 2008;15:929-937
73. Lutter M,Fang M,Luo X,Nishijima M,Xie X-s,Wang X.Cardiolipin provides specificity for targeting of tBid to mitochondria.Nat Cell Biol. 2000;2:754-761
74. Ma BJ,Taylor WA,Dolinsky VW,Hatch GM.Acylation of monolysocardiolipin in rat heart.J Lipid Res. 1999;40:1837-1845
75. Manon S.Utilization of yeast to investigate the role of lipid oxidation in cell death.Antioxid Redox Signal. 2004;6:259-267
76. Mileykovskaya E,Dowhan W,Birke RL,Zheng D,Lutterodt L,Haines TH.Cardiolipin binds nonyl acridine orange by aggregating the dye at exposed hydrophobic domains on bilayer surfaces.FEBS Lett. 2001;507:187-190
77. Montessuit S,Somasekharan SP,Terrones O,Lucken-Ardjomande S,Herzig S,Schwarzenbacher R,Manstein DJ,Bossy-Wetzel E,Basañez G,Meda P.Membrane remodeling induced by the dynamin-related protein Drp1 stimulates Bax oligomerization.Cell. 2010;142:889-901
78. Narendra DP,Youle RJ.Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control.Antioxid Redox Signal. 2011;14:1929-1938
79. Orrenius S,Zhivotovsky B.Cardiolipin oxidation sets cytochrome c free.Nat Chem Biol. 2005;1:188-189
80. Pangborn MC.Isolation and purification of a serologically active phospholipid from beef heart.J Biol Chem. 1942;143:247-256
81. Paradies G,Paradies V,De Benedictis V,Ruggiero FM,Petrosillo G.Functional role of cardiolipin in mitochondrial bioenergetics.Biochim Biophys Acta. 2014;1837:408-417
82. Paradies G,Petrosillo G,Pistolese M,Di Venosa N,Federici A,Ruggiero FM.Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart involvement of reactive oxygen species and cardiolipin.Circ Res. 2004;94:53-59
83. Park SJ,Shin JH,Kim ES,Jo YK,Kim JH,Hwang JJ,Kim JC,Cho D-H.Mitochondrial fragmentation caused by phenanthroline promotes mitophagy.FEBS Lett. 2012;586:4303-4310
84. Petrosillo G,De Benedictis V,Ruggiero FM,Paradies G.Decline in cytochrome c oxidase activity in rat-brain mitochondria with aging. Role of peroxidized cardiolipin and beneficial effect of melatonin.J Bioenerg Biomembr. 2013;45:431-440
85. Petrosillo G,Ruggiero FM,Di Venosa N,Paradies G.Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin.FASEB J. 2003;17:714-716
86. Russell RC,Tian Y,Yuan H,Park HW,Chang Y-Y,Kim J,Kim H,Neufeld TP,Dillin A,Guan K-L.ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase.Nat Cell Biol. 2013;15:741-750
87. Rytömaa M,Kinnunen P.Evidence for two distinct acidic phospholipid-binding sites in cytochrome c.J Biol Chem. 1994;269:1770-1774
88. Sani M-A,Dufourc EJ,Gröbner G.How does the Bax-α1 targeting sequence interact with mitochondrial membranes? The role of cardiolipin.Biochim Biophys Acta. 2009;1788:623-631
89. Scarffe LA,Stevens DA,Dawson VL,Dawson TM.Parkin and PINK1: much more than mitophagy.Trends Neurosci. 2014;37:315-324
90. Schinzel A,Kaufmann T,Borner C.Bcl-2 family members: intracellular targeting, membrane-insertion, and changes in subcellular localization.Biochim Biophys Acta. 2004;1644:95-105
91. Schlame M.Cardiolipin remodeling and the function of tafazzin.Biochim Biophys Acta. 2012;183:582-588
92. Schlame M.Thematic Review Series: Glycerolipids. Cardiolipin synthesis for the assembly of bacterial and mitochondrial membranes.J Lipid Res. 2008;49:1607-1620
93. Schlame M,Acehan D,Berno B,Xu Y,Valvo S,Ren M,Stokes DL,Epand RM.The physical state of lipid substrates provides transacylation specificity for tafazzin.Nat Chem Biol. 2012;8:862-869
94. Schlame M,Rua D,Greenberg ML.The biosynthesis and functional role of cardiolipin.Prog Lipid Res. 2000;39:257-288
95. Schlame M,Rustow B.Lysocardiolipin formation and reacylation in isolated rat liver mitochondria.Biochem J. 1990;272:589-595
96. Schlattner U,Tokarska-Schlattner M,Ramirez S,Brückner A,Kay L,Polge C,Epand RF,Lee RM,Lacombe M-L,Epand RM.Mitochondrial kinases and their molecular interaction with cardiolipin.Biochim Biophys Acta. 2009;1788:2032-2047
97. Schlattner U,Tokarska-Schlattner M,Ramirez S,Tyurina YY,Amoscato AA,Mohammadyani D,Huang Z,Jiang J,Yanamala N,Seffouh A.Dual function of mitochondrial Nm23-H4 protein in phosphotransfer and intermembrane lipid transfer: a cardiolipin-dependent switch.J Biol Chem. 2013;288:111-121
98. Shamas-Din A,Bindner S,Zhu W,Zaltsman Y,Campbell C,Gross A,Leber B,Andrews DW,Fradin C.tBid undergoes multiple conformational changes at the membrane required for Bax activation.J Biol Chem. 2013;288:22111-22127
99. Singh SB,Ornatowski W,Vergne I,Naylor J,Delgado M,Roberts E,Ponpuak M,Master S,Pilli M,White E.Human IRGM regulates autophagy and cell-autonomous immunity functions through mitochondria.Nat Cell Biol. 2010;12:1154-1165
100. Smirnova E,Griparic L,Shurland D-L,Van Der Bliek AM.Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells.Mol Biol Cell. 2001;12:2245-2256
101. Sorice M,Circella A,Cristea I,Garofalo T,Di Renzo L,Alessandri C,Valesini G,Degli Esposti M.Cardiolipin and its metabolites move from mitochondria to other cellular membranes during death receptor-mediated apoptosis.Cell Death Differ. 2004;11:1133-1145
102. Sparagna GC,Lesnefsky EJ.Cardiolipin remodeling in the heart.J Cardiovasc Pharmacol. 2009;53:290-301
103. Springer W,Kahle PJ.Regulation of PINK1-Parkin-mediated mitophagy.Autophagy. 2011;7:266-278
104. Stanacev NZ,Chang Y-Y,Kennedy EP.Biosynthesis of cardiolipin in Escherichia coli.J Biol Chem. 1967;242:3018-3019
105. Tanida I,Ueno T,Kominami EAutophagosome and Phagosome. Deretic V, ed. New York: Humana Press Inc.; 2008:77-88.
106. Taylor WA,Hatch GM.Identification of the human mitochondrial linoleoyl-coenzyme A monolysocardiolipin acyltransferase (MLCL AT-1).J Biol Chem. 2009;284:30360-30371
107. Taylor WA,Hatch GM.Purification and characterization of monolysocardiolipin acyltransferase from pig liver mitochondria.J Biol Chem. 2003;278:12716-12721
108. Thomas KJ,Jacobson MR.Defects in mitochondrial fission protein dynamin-related protein 1 are linked to apoptotic resistance and autophagy in a lung cancer model.PLoS ONE. 2012;7:e45319
109. Tooze SA,Yoshimori T.The origin of the autophagosomal membrane.Nat Cell Biol. 2010;12:831-835
110. Tuominen EK,Wallace CJ,Kinnunen PK.Phospholipid-cytochrome c interaction evidence for the extended lipid anchorage.J Biol Chem. 2002;277:8822-8826
111. Twig G,Elorza A,Molina AJ,Mohamed H,Wikstrom JD,Walzer G,Stiles L,Haigh SE,Katz S,Las G.Fission and selective fusion govern mitochondrial segregation and elimination by autophagy.EMBO J. 2008;27:433-446
112. Tyurin V,Tyurina Y,Osipov A,Belikova N,Basova L,Kapralov A,Bayir H,Kagan V.Interactions of cardiolipin and lyso-cardiolipins with cytochrome c and tBid: conflict or assistance in apoptosis.Cell Death Differ. 2006;14:872-875
113. Uemura T,Yamamoto M,Kametaka A,Sou YS,Yabashi A,Yamada A,Annoh H,Kametaka S,Komatsu M,Waguri S.A cluster of thin tubular structures mediates transformation of the endoplasmic reticulum to autophagic isolation membrane.Mol Cell Biol. 2014;34:1695-1706
114. Ushmorov A,Ratter F,Lehmann V,Droge W,Schirrmacher V,Umansky V.Nitric-oxide-induced apoptosis in human leukemic lines requires mitochondrial lipid degradation and cytochrome C release.Blood. 1999;93:2342-2352
115. Van Q,Liu J,Lu B,Feingold K,Shi Y,Lee R,Hatch G.Phospholipid scramblase-3 regulates cardiolipin de novo biosynthesis and its resynthesis in growing HeLa cells.Biochem J. 2007;401:103-109
116. Xu Y,Condell M,Plesken H,Edelman-Novemsky I,Ma J,Ren M,Schlame M.A Drosophila model of Barth syndrome.Proc Natl Acad Sci U S A. 2006a;103:11584-11588
117. Xu Y,Malhotra A,Ren M,Schlame M.The enzymatic function of tafazzin.J Biol Chem. 2006b;281:39217-39224
118. Youle RJ,Karbowski M.Mitochondrial fission in apoptosis.Nat Rev Mol Cell Biol. 2005;6:657-663
119. Youle RJ,Strasser A.The BCL-2 protein family: opposing activities that mediate cell death.Nat Rev Mol Cell Biol. 2008;9:47-59