Cardiolipin and its metabolites move from mitochondria to other cellular membranes during death receptor-mediated apoptosis

Cell Death and Differentiation

Volumn 11, Issue 10, 2004, Pages 1133-1145

  Sorice, Maurizio ^a   Circella, A ^a   Cristea, I M ^b   Garofalo, T ^a   Di Renzo, L ^a   Alessandri, C ^a   Valesini, G ^a   Degli Esposti, M ^b  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Bid; Cardiolipin; Mitochondria; Phospholipids

Indexed keywords

CARDIOLIPIN; FAS LIGAND; PROTEIN BID; PROTEIN P100;

APOPTOSIS; ARTICLE; CELL MEMBRANE; CELL ORGANELLE; CELL SURFACE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTRACELLULAR TRANSPORT; LIPID TRANSPORT; MASS SPECTROMETRY; METABOLITE; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANTIGENS, CD95; APOPTOSIS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; BIOLOGICAL TRANSPORT; CARDIOLIPINS; CARRIER PROTEINS; CELL MEMBRANE; HUMANS; IMMUNOPRECIPITATION; INTRACELLULAR MEMBRANES; MASS SPECTROMETRY; MITOCHONDRIA; SIGNAL TRANSDUCTION; U937 CELLS;

EID: 1842740658     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4401457     Document Type: Article

References (67)

1. Green DR, Droin N and Pinkoski M (2003) Activation-induced cell death in T cells. Immunol. Rev. 193: 70-81
2. Jaattela M and Tschopp J (2003) Caspase-independent cell death in T lymphocytes. Nat. Immunol. 4: 416-423
3. Boya P, Andreau K, Poncet D, Zamzami N, Perfettini JL, Metivier D, Ojcius DM, Jaattela M and Kroemer G (2003) Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J. Exp. Med. 197: 1323-1334
4. Peitsch MC, Mannhers HG and Tschopp J (1994) The apoptosis endonucleases: cleaning up after cell death? Trends Cell Biol. 4: 37-41
5. Martin SJ, Reutelinsperger CPM, McGahon AJ, Rader JA, van Schie RCAA, LaFace DM and Green DR (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. J. Exp. Med. 182: 1545-1556
6. Fadok VA and Henson PM (2003) Apoptosis: giving phosphatidylserine recognition an assist - with a twist. Curr. Biol. 13: 655-657
7. Verhoven B, Schlegel RA and Williamson P (1995) Mechanisms of phosphatidylserine exposure, a phagocyte recognition signal on apoptotic T lymphocytes. J. Exp. Med. 182: 1597-1601
8. Degli Esposti and M (2002) Lipids, cardiolipin and apoptosis: a greasy licence to kill. Cell Death Differ. 9: 234-236
9. Bretsche MS (1972) Asymmetrical lipid bilayer structure for biological membranes. Nature 236: 11-12
10. Schlame M, Rus D and Greenberg ML (2000) The biosynthesis and functional role of cardiolipin. Prog. Lipid Res. 39: 257-288
11. Fernandez MG, Troiano L, Moretti L, Nasi M, Pinti M, Salvioli S, Dobrucki J and Cossarizza A (2002) Early changes in intramitochondrial cardiolipin distribution during apoptosis. Cell Growth Differ. 13: 449-455
12. Sorice M, Circella A, Misasi R, Pittoni V, Garofalo T, Cirelli A, Pavan A, Pontieri GM and Valesini G (2000) Cardiolipin on the surface of apoptotic cells as possible trigger for antiphospholipid antibodies. Clin. Exp. Immunol. 122: 277-284
13. Luo X, Budihardjo I, Zou H, Slaughter C and Wang X (1998) Bid, a Bcl2 interacting protein, mediated cytochrome c release from mitochondria in response to activation of cell death receptors. Cell 94: 481-490
14. Wei MC, Lindsen T, Mootha VK, Eiler S, Gross A, Ashiya A, Thompson CB and Korsmeyer SJ (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev 10: 2060-2071
15. Yin XM, Wang K, Gross A, Zhao Y, Zinkel S, Klocke B, Roth KA and Korsmeyer SJ (1999) Bid-deficient mice are resistent to Fas-induced hepatocellular apoptosis. Nature 400: 886-891
16. Zha J, Weiler S, Oh K, Wei MC and Korsmeyer SJ (2000) Posttranslational N-myristoylation of BID as a molecular switch for targeting to mitochondria and apoptosis. Science 290: 1761-1765
17. Degli Esposti M, Erler JT, Hickman JA and Dive C (2001) Bid, a widely expressed proapoptotic protein of the Bcl-2 family, displays lipid transfer activity. Mol. Cell. Biol. 21: 7268-7276
18. Lutter M, Fang M, Luo X, Nashijima M, Xie X and Wang X (2000) Cardiolipin provides specificity for targeting of tBid to mitochondria. Nat. Cell Biol. 2: 754-756
19. Sorice M, Griggi T, Circella A, Garofalo T, d'Agostino F, Pittoni V, Pontieri GM, Lenti L and Valesini G (1994) Detection of antiphospholipid antibodies by immunostaining on thin layer chromatography plates. J. Immunol. Methods 173: 49-54
20. Matsko CM, Hunter OC, Rabinowich H, Lotz, MT and Amoscato AA (2001) Mitochondrial lipids alterations during Fas- and radiation-induced apoptosis. Biochem. Biophys. Res. Commun. 287: 1112-1120
21. Nomura K, Imai H, Koumura T, Kobayashi T and Nakagawa Y (2000) Mitochondrial phospholipid hydroperoxide glutathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem. J. 351: 183-193
22. Kirkland RA, Adibhatla RM, Hatcher JF and Franklin JL (2002) Loss of cardiolipin and mitochondria during programmed neuronal death: evidence for a role for lipid peroxidation and autophagy. Neuroscience 115: 587-602
23. McMillin JB and Dowhan W (2002) Cardiolipin and apoptosis. Biochim. Biophys. Acta 1585: 97-107
24. Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL and Korsmeyer SJ (1993) Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75: 241-251
25. Macho A, Castedo M, Marchetti P, Aguilar JJ, Decaudin D, Zamzami N, Girard PM, Uriel J and Kroemer G (1995) Mitochondrial dysfunctions in circulating T lymphocytes from human immunodeficiency virus 1 carriers. Blood 86: 2481-2487
26. Ott M, Robertson JD, Gogvadze V, Zhivotosky B and Orrenius S (2002) Cytochrome c release from mitochondria proceeds by a two-steps process. Proc. Natl. Acad. Sci. USA 99: 1259-1263
27. Degli Esposti M, Hatzinisiriou I, McLennan H and Ralph S (1999) Bcl-2 and mitochondrial oxygen radicals. New approaches with reactive oxygen species-sensitive probes. J. Biol. Chem. 274: 29831-29837
28. Degli Esposti M (2001) Assessing functional integrity of mitochondria in vitro and in vivo. Methods Cell. Biol. 65: 75-96
29. Schaffer C, Beckedorf AI, Scheberl A, Zayni S, Peter-Katalinic J and Messner P (2002) Isolation of glucocardiolipins from Geobacillus stearothermophilus NRS 2004/3a. J. Bacteriol. 184: 6709-6713
30. Fobker M, Voss R, Reinecke H, Corne C, Assmann G and Walter M (2001) Accumulation of cardiolipin and lysocardiolipin in fibroblasts from Tangier disease subjects. FEBS Lett. 500: 157-162
31. Degli Esposti M, Cristea IM, Gaskell SJ, Nakao Y and Dive C (2003) Pro-apoptotic Bid binds to monolysocardiolipin, a new molecular connection between mitochondrial membranes and cell death. Cell Death Differ. 10: 1300-1309
32. Eichberg J (1974) The reacylation of deacylated derivatives of diphosphatidylglycerol by microsomes and mitochondria from rat liver. J. Biol. Chem. 249: 3423-3429
33. Schlame M and Rustow B (1990) Lysocardiolipin formation and reacylation in isolated rat liver mitochondria. Biochem. J. 272: 589-595
34. Xu Y, Kelley RI, Blanck TJ and Schlame M 2003 Remodeling of cardiolipin by phospholipid transacylation. J. Biol. Chem. 278: 51380-51385
35. Morton R, Cunningham C, Jester R, Waite M, Miller N and Morris HP (1976) Alteration of mitochondrial function and lipid composition in Morris 7777 hepatoma. Cancer. Res. 36: 3246-3254
36. Wagenknecht B, Gulbins E, Lang F, Dichgans J and Weller M (1997) Lipoxygenase inhibitors block CD95 ligand-mediated apoptosis of human malignant glioma cells. FEBS Lett. 409: 17-23
37. Drecktrah D, de Figueiredo P, Mason RM and Brown WJ (1998) Retrograde trafficking of both Golgi complex and TGN markers to the ER induced by nordihydroguaiaretic acid and cyclofenil diphenol. J. Cell Sci. 111: 951-965
38. Ostrander DB, Sparagna GC, Amoscato AA, McMillin JB and Dowhan W (2001) Decreased cardiolipin synthesis corresponds with cytochrome c release in palmitate-induced cardiomiocyte apoptosis. J. Biol. Chem. 276: 38061-38067
39. Brotherus J and Renkonen O (1977) Phospholipids of subcellular organelles isolated from cultured BHK cells. Biochim. Biophys. Acta 486: 243-253
40. Somerharju P (1979) Subcellular localization of three degeneration-associated phospholipids in cultured hamster fibroblasts (BHK21 cells). Biochim. Biophys. Acta 574: 461-470
41. Kobayashi T, Beuchat MH, Chevallier J, Makino A, Mayran N, Escola JM, Lebrand C, Cosson P, Kobayashi T and Gruenberg J (2002) Separation and characterization of late endosomal membrane domains. J. Biol. Chem. 277: 32157-32164
42. Luquain C, Dolmazon R, Enderlin JM, Laugier C, Lagarde M and Pageaux JF (2000) Bis(monoacylglycerol) phosphate in rat uterine stromal cells: structural characterization and specific esterification of docosahexaenoic acid. Biochem. J. 351: 795-804
43. Han X, Abendschein DR, Kelley JG and Gross RW (2000) Diabetes-induced changes in specific lipid molecular species in rat myocardium. Biochem. J. 352: 79-89
44. Cifone MG, Roncaioli P, De Maria R, Camarda G, Santoni A, Ruberti G and Testi R (1995) Multiple pathways originate at the Fas/APO-1 (CD95) receptor: sequential involvement of phosphatidylcholine-specific phospholipase C and acidic sphingomyelinase in the propagation of the apoptotic signal. EMBO J. 14: 5859-5868
45. Degli Esposti M (2003) The mitochondrial battlefield and membrane lipids during cell death signalling. Ital. J. Biochem. 52: 43-50
46. Xu FY, Kelly SL, Taylor WA and Hatch GM (1998) On the mechanism of the phospholipase C-mediated attenuation of cardiolipin biosynthesis in H9c2 cardiac myoblast cells. Mol. Cell. Biochem. 188: 217-223
47. Wenk MR, Lucast L, Di Paolo G, Romanelli AJ, Suchy SF, Nussbaum RL, Cline GW, Shulman GI, McMurray W and De Camilli P (2003) Phosphoinositide profiling in complex lipid mixtures using electrospray ionization mass spectrometry. Nat. Biotechnol. 21: 813-817
48. Yague G, Segovia M and Valero-Guillen PL (1997) Acyl phosphatidylglycerol: a major phospholipid of Corynebacterium amycolatum. FEMS Microbiol. Lett. 151: 125-130
49. Cluett EB, Kuismanen E and Machamer CE (1997) Heterogeneous distribution of the unusual phospholipid semilysobisphosphatidic acid through the Golgi complex. Mol. Biol. Cell. 8: 2233-2240
50. Waite M, King L, Thornburg T, Osthoff G and Thuren TY (1990) Metabolisms of phosphatidylglycerol and bis(monoacylclycerol)-phosphate in macrophage subcellular fractions. J. Biol. Chem. 265: 21720-21726
51. Poorthuis BJ and Hostetler KY (1978) Conversion of diphosphatidylglycerol to bis(monoacylglyceryl)phosphate by lysosomes. J. Lipid Res. 19: 309-315
52. Algeciras-Schimnich A, Shen L, Barnhart BC, Murmann AE, Burkhardt JK and Peter ME (2002) Molecular ordering of the initial signaling events of CD95. Mol. Cell. Biol. 22: 207-220
53. Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR and Newmeyer DD (2002) Bid, bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell 111: 331-342
54. Liu J, Chen J, Dai Q and Lee RM (2003) Phospholipid scramblase 3 is the mitochondrial target of protein kinase C γ -induced apoptosis. Cancer Res. 63: 1153-1156
55. Epand RF, Martinou JC, Montessuit S and Epand RM (2003) Transbilayer lipid diffusion promoted by Bax: implications for apoptosis. Biochemistry 42: 14576-14582
56. Hambrey PN and Mellors A (1975) Cardiolipin degradation by rat liver lysosomes. Biochem. Biophys. Res. Commun. 62: 939-945
57. Arur S, Uche UE, Rezaul K, Fong M, Scranton V, Cowan AE, Mohler W and Han DK (2003) Annexin I is an endogenous ligand that mediates apoptotic cell death engulfment. Dev. Cell 4: 587-598
58. Galve-de Rochemonteix B, Kobayashi T, Rosnoblet O, Lindsay M, Parton RG, Reber G, de Maistre E, Wahl D, Kruithof EK, Gruenberg J and de Moerloose P (2000) Interaction of anti-phospholipid antibodies with late endosomes of human endothelial cells. Arterioscler. Thromb. Vasc. Biol. 20: 563-574
59. Mc Neil HP, Krillis SA and Chesterman CN (1988) Purification of antiphospholipid antibodies using a new affinity method. Thromb. Res. 52: 641-648
60. Tang DG, Chen YQ and Honn KV (1996) Arachidonate lipoxygenases as essential regulators of cell survival and apoptosis. Proc. Natl. Acad. Sci. USA 93: 5241-5246
61. Slee EA, Zhu H, Chow SC, MacFarlane M, Nicholson DW and Cohen GM (1996) Benzyloxycarbonyl-Val-Ala-Asp(O-Me) fluoromethyl ketone (z-VAD-FMK) inhibits apoptosis by blocking the processing CPP32. Biochem. J. 315: 21-24
62. Perdue JF (1974) The isolation and characterization of plasma membrane from cultured chicken embryo fibroblasts. Meth. Enzymol. 31: 162-168
63. Folch J, Lees M and Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497-509
64. Fischer K, Chatterjee D, Torrelles J, Brennan PJ, Kaufmann SH and Schaible UE (2001) Mycobacterial lysocardiolipin is exported from phagosomes upon cleavage of cardiolipin by a macrophage-derived lysosomal phospholipase A2. J. Immunol. 167: 2187-2192
65. Hsu FF, Ma Z, Wohltmann M, Bohrer A, Nowatzke W, Ramanadham S and Turk J (2000) Electrospray ionization/mass spectrometric analyses of human promonocytic U937 cell glycerolipids and evidence that differentiation is associated with membrane lipid composition changes that facilitate phospholipase A2 activation. J. Biol. Chem. 275: 16579-16589
66. Petkovic M, Schiller J, Muller M, Bernard S, Reichl S, Arnold K and Arnhold J (2001) Detection of individual phospholipids in lipid mixtures by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Anal. Biochem. 289: 202-216
67. Hancock K and Tsang VC (1983) India ink staining of proteins on nitrocellulose paper. Anal. Biochem. 133: 157-162